integrative taxonomy reveals the chortÍs block of
TRANSCRIPT
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INTEGRATIVE TAXONOMY REVEALS THE CHORTÍS BLOCK OF CENTRAL AMERICA AS AN UNDERESTIMATED HOTSPOT OF AMPHIBIAN DIVERSITY
By
JOSIAH HAROLD TOWNSEND
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
2011
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© 2011 Josiah Harold Townsend
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Para Ileana
And in loving memory of my grandfather, Vernon Lynn Boyd
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ACKNOWLEDGMENTS
I want to begin by expressing my gratitude for the support shown by my advisory
committee during the course of preparing this dissertation. My Chair, James Austin,
supported me both academically and personally throughout this process; his leadership
and steadfast support was instrumental in my success. I want to thank my committee
members, Rob Fletcher, Mike Miyamoto, Rick Stepp, and Larry David Wilson, for their
guidance, advice, and support through the process of researching and writing this
dissertation.
Writing a dissertation must be both a singularly selfish act and one that relies on
the extended patience and support of loved ones, labmates, and colleagues. This
certainly was the case for me. To the one person who is literally all three of those
things, my wife Ileana Luque-Montes, I cannot adequately express the amazement with
which I have watched you begin your own graduate studies over the past four months;
maintaining a rigorous field schedule and supervising undergraduates, while I was of
minimal help and fully focused on writing the following document. I simply would not
have completed this without your remarkable dedication and support, and my gratitude
will be best expressed by giving you the same degree of support as you pursue your
own goals. I am blessed with the devoted support and seemingly endless patience and
understanding of a wonderful and inspirational family, my parents Steve and Terri Boyd
Townsend, my sister Katielynn, and my grandparents Vernon Lynn and Norma Jean
Boyd and Willa Parker Townsend, who are largely responsible for any past and future
successes I may have.
In many ways, I am who I am today thanks to the mentorship of Larry David
Wilson. As a mentor, colleague, and friend, Larry introduced me to Honduras in 1999
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and guided my developing research interests there throughout my community college
and undergraduate years, becoming my colleague and supporter as I progressed
through my graduate studies.
I owe no small debt of gratitude to my friends and colleagues in the Austin Lab,
and, in particular, for actively assisting with my labwork and providing countless
impromptu instructional sessions, I want to thank Jason Butler, John Hargrove, Nathan
Johnson, Emily Saarinen, Matt Shirley, and Aria (Johnson) St. Louis. I also benefited
from the dedicated work of a series of undergraduate researchers and volunteers:
Teresa Burlingame, Dania Gutierrez, Jaclyn Irwin, Rachel Shapiro, Vicki Villanova, and
Lauryn Walter.
My work for the past six years has benefited greatly from the support of the
Section of Protected Areas and Wildlife, Instituto Nacional de Conservación y Desarrollo
Forestal, Áreas Protegidas y Vida Silvestre, and particularly Iris Acosta, Carla Cárcamo,
Saíd Lainez O., Andrés Alegria, Ramón Alvarez L., Wilson Zúniga D., Sonia Martínez
Moreno, and Wendy Aronne (Instituto Nacional de Conservación y Desarrollo Forestal,
Áreas Protegidas y Vida Silvestre [ICF]). Fieldwork was carried out under a series of
research permits issued by ICF, most recently Resolución DE-MP-086-2010 and
Dictamen DVS-ICF-045-2010. In Honduras, my work would not have been possible
without the hard work and support variously given by Ileana Luque-Montes (UNAH),
Melissa Medina-Flores (UNAH, UNA), Luis A. Herrera (UNAH), Allan J. Fuentes and
Eduardo J. Zavala (PROLANSATE), Alcalde Adolfo Pagoada-Saybe (Municipalidad de
Arizona), Alcadesa Teresa Espinosa Aguilar (Municipalidad de Marale), Oliver Komar,
Jose Mora, Jorge Iván Restrepo, and Fredy Membreño (Centro Zamorano de
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Biodiversidad), Efrain Aguilar (San José de Texíguat), Alfonso Contreras (Mezapita),
Alionso Portillo (Jilamito Nuevo), J. Dubón (La Liberación), Mario Orellana Leiva (El
Playon), Leonel Erazo Chávez (El Cedral), Rafael Ulloa (Municipalidad de Gualaco),
Eduardo Rico (ICF-Gualaco), Carlos Perdomo (Aldea Global), Paul House (UNAH,
Herbario TEFH), Robert Dale (Los Naranjos), and Alicia Ward (Santa Bárbara). I would
like to acknowledge the following people for their work in the field in support of this
project: Carlos Andino, Ben K. Atkinson, James D. Austin, Christopher Begley, Mark
Bonta, Jason M. Butler, Brian Campesano, César A. Cerrato, Gabriela Diaz, Anne
Donnelly, Matthew Donnelly, Yensi Flores, Sergio C. Gonzalez, Levi Gray, Vladlen
Henriquez, Luis A. Herrera, Paul House, Robert Hyman, Lorraine Ketzler, Ileana Luque,
Christina Martin, David Medina, Melissa Medina-Flores, Mayron Mckewy-Mejía, Aaron
Mendoza, Wendy Naira, Ciro Navarro, Lenin Obando, Sandy Pereira, Onán A. Reyes,
John Slapcinsky, Mario Solís, Fito Steiner, Nathaniel Stewart, Alexander Stubbs,
Katielynn Townsend, Steve Townsend, Scott L. Travers, Rony Valle, Hermes Vega,
Alicia Ward, and Christopher Wolf.
I am very grateful for the support of Amy Driscoll, Dan Mulcahy, Andrea Ormos,
and the SI Barcoding Project (Smithsonian Institution Laboratory of Analytical Biology),
and Roy McDiarmid (USNM) for supporting my ―Barcoding the Herpetofauna of Eastern
Nuclear Central America‖ initiative. Deposition of voucher specimens and timely
acquisition of catalog numbers was facilitated by: Jim McGuire, Ted Papenfuss, Sean
Rovito, Carol Spencer, and David Wake (MVZ), Jose Rosado (MCZ), and Steve Gotte,
Jeremy Jacobs, John Poindexter, and Robert Wilson (USNM). Jason Butler, Ileana
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Luque, Javier Sunyer, and Scott Travers kindly contributed photographs for use in this
dissertation.
Various portions of this dissertation was funded by Critical Ecosystem Partnership
Fund (CEPF), a Summer Research Grant from the Working Forests in the Tropics
IGERT Program (National Science Foundation DGE–0221599) at the University of
Florida, a grant to Kirsten E. Nicholson (Central Michigan University; National Science
Foundation DEB-0949359), and the Explorer’s Club (via Robert Hyman; Flag #93).
During my dissertation studies, I was supported by a 2007–09 NSF GK-12 Fellowship
from the UF SPICE Program, and as much as any experience during my graduate
education, my participation in this program was truly formative and help to shape the
conceptual framework within which I propose to carry out research. I am especially
grateful to Doug Levey and Suzan Smith, my partner-teacher Nate Stewart, and fellow
fellows Jackson Frechette, Rachel Naumann, and Tom Tidyman, for helping to make
SPICE a truly great experience. Following SPICE, my work with the UFTeach Program
as an instructor for their core Research Methods class was key during the final two
years of my dissertation, and I thank Alan Dorsey, Dimple Flesner, Griff Jones, Linda
Jones, Katrina Short, Gloria Weber, and our RM students for making these last two
spring semesters so enjoyable.
Finally, I want to take this opportunity to dedicate my work in the past and future to
the memory of three friends that I lost while completing this degree. I met Thad Owens
as a student in my Herpetology class at UF and we quickly became friends, as he did
with just about everyone who knew him. Thad was one of the most honest, unreserved,
and enthusiastic people I will ever have the pleasure of knowing, and rarely a day
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passes since he was lost in May 2009 that I do not think about him or find inspiration in
his memory. Wade Wassenberg was a good friend since high school, and was one of
the most loyal friends anyone could hope to have. After losing track of him for years, I
learned that Wade had joined the US Army and served in the elite 1st Battalion of the
75th Ranger Regiment, surviving four tours of duty in Afghanistan and two more in Iraq
from 2002 to 2008. After retiring to rejoin life with his beautiful young family, he was
suddenly diagnosed with brain cancer and passed soon thereafter at the VA Hospital in
Gainesville, walking distance from my office. I will always regret that while my friend
suffered and passed literally minutes away from my home, I was unaware and in the
field in Honduras. Finally, Don Mario Guiffaro of Olancho, Honduras, was an influential
and remarkable man whose legendary life story included being a feared pistolero, a
frontier gold miner, a jaguar hunter, and in his later years, and outstanding advocate
and conservationist in the Patuca region. In 2007, Don Mario’s forceful opposition to
illegal logging and drug trafficking in the Mosquitia was ultimately answered by violence,
and he was gunned down in front of his son and friends. The memories of, and
examples set, by these three friends, to each of whom I would not have hesitated to
entrust with my life, and in some cases did just that, will always be my compass and my
motivation as I continue through life’s journey.
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TABLE OF CONTENTS page
ACKNOWLEDGMENTS .................................................................................................. 4
LIST OF TABLES .......................................................................................................... 14
LIST OF FIGURES ........................................................................................................ 15
ABSTRACT ................................................................................................................... 18
CHAPTER
1 INTRODUCTION .................................................................................................... 20
2 BIOGEOGRAPHIC DELIMITATION OF THE CHORTÍS BLOCK: GEOLOGICAL HISTORY, PHYSIOGRAPHY, AND ECOLOGICAL ASSOCIATIONS .................... 25
Geological History ................................................................................................... 27
Contemporary Ecophysiography ............................................................................. 34
Characterizing Ecological Associations: Holdridge Forest Formations ................... 46
Characterizing Ecological Associations: Updating and Operationalizing the Carr (1950) System for Classifying Honduran Ecosystems ......................................... 50
Lowland-associated Habitats ............................................................................ 51
Habitats Shared Between Lowlands and the Chortís Highlands ...................... 57
Habitats of the Chortís Highlands ..................................................................... 61
Introduction to Biodiversity of the Chortís Block ...................................................... 70
3 TAXONOMIC DIVERSITY, DISTRIBUTIONAL PATTERNS, AND CONSERVATION STATUS OF THE CHORTÍS BLOCK HERPETOFAUNA ......... 72
Methods and Materials ............................................................................................ 74
Field Sampling .................................................................................................. 74
Taxonomic Scope and Standards .................................................................... 74
Evaluating Conservation Status ....................................................................... 77
Results .................................................................................................................... 78
Composition of the Herpetofauna ..................................................................... 78
Patterns of Distribution and Endemism within the Chortís Block ...................... 79
Distribution of Chortís Highland Endemics ....................................................... 79
Conservation Status ......................................................................................... 80
Sampling Results by Locality .................................................................................. 80
Parque Nacional Celaque ................................................................................. 81
Parque Nacional Cerro Azul Copán ................................................................. 82
Parque Nacional Cerro Azul Meámbar ............................................................. 83
Parque Nacional Cusuco .................................................................................. 86
Parque Nacional La Tigra ................................................................................. 87
Parque Nacional Montaña de Botaderos .......................................................... 87
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Parque Nacional Montaña de Comayagua ....................................................... 90
Parque Nacional Montaña de Santa Bárbara ................................................... 91
Parque Nacional Montaña de Yoro .................................................................. 94
Parque Nacional Pico Bonito ............................................................................ 95
Parque Nacional Pico Pijol ............................................................................... 95
Parque Nacional Sierra de Agalta .................................................................... 96
Refugio de Vida Silvestre Texiguat .................................................................. 97
Reserva Biológica Cerro Uyuca ....................................................................... 98
Reserva Biológica Guajiquiro ......................................................................... 100
Reserva Biológica Güisayote ......................................................................... 101
Reserva Biológica Yerbabuena ...................................................................... 102
Reserva de la Biosfera Bosawas .................................................................... 102
Jardín Botánico Lancetilla .............................................................................. 104
Área de Uso Multíple Isla del Tigre ................................................................ 106
Non-Protected Areas ...................................................................................... 107
Cerro El Zarciadero .................................................................................. 107
Highlands surround the Meseta de La Esperanza ................................... 107
Los Naranjos ............................................................................................ 108
Montaña de Jacaleapa ............................................................................. 109
Montaña Macuzal ..................................................................................... 109
Saguay ..................................................................................................... 112
San José de Texíguat .............................................................................. 112
Selva Negra ............................................................................................. 113
Yeguare Valley ......................................................................................... 113
Discussion ............................................................................................................ 116
Baseline Herpetological Inventory of Parque Nacional Montaña de Yoro ............. 116
A New Species of Anole ................................................................................. 118
Salamanders of Uncertain Taxonomic Assignment ........................................ 119
Hotspot within a Hotspot: the Special Case of Refugio de Vida Silvestre Texíguat ............................................................................................................. 120
Discovery of Plectrohyla chrysospleura .......................................................... 122
Underestimated Salamander Diversity? ......................................................... 124
Highly Endemic and Highly Endangered ........................................................ 125
Cryptozoic Snake Diversity ................................................................................... 126
A New Species of Centipede Snake (genus Tantilla) from La Liberación ...... 127
A Large New Species of Blindsnake (Typhlops tycherus) .............................. 128
Geophis damiani at La Liberación .................................................................. 130
Noteworthy Ninia ............................................................................................ 131
Unidentified Salamander Populations ................................................................... 133
4 THE CHORTIS BLOCK IS AN UNDERESTIMATED HOTSPOT OF AMPHIBIAN DIVERSITY AND ENDEMISM ......................................................... 166
Methods and Materials .......................................................................................... 172
Sampling and Sample Identification ............................................................... 172
Extraction, Amplification, and Sequencing ..................................................... 173
Sequence Evaluation and Alignment .............................................................. 174
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Distance-Based Barcode Metrics ................................................................... 175
Phylogenetic Analysis .................................................................................... 176
Species Delimitation and Candidate Species ................................................. 176
Results .................................................................................................................. 177
Broad Results for Distance-based Analyses .................................................. 177
Identification of Potential Candidate Species of Anura ................................... 179
BLASTN Results for Unassigned Salamander Sequences ............................ 187
Distance-Based Analyses of Caudata ............................................................ 187
Phylogenetic Analysis of Caudata .................................................................. 191
Discussion ............................................................................................................ 196
Candidates for Further Taxonomic Study Among Anurans ............................ 196
Incilius coccifer/ibarrai/porteri ................................................................... 197
Incilius coniferus ...................................................................................... 198
Rhaebo haematiticus ............................................................................... 200
Craugastor aurilegulus ............................................................................. 200
Craugastor laevissimus ............................................................................ 200
Craugastor sp. inquirenda 1 & 2 .............................................................. 201
Diasporus diastema ................................................................................. 201
Plectrohyla cf. guatemalensis .................................................................. 201
Ptychohyla hypomykter ............................................................................ 202
Ptychohyla spinipollex .............................................................................. 202
Smilisca baudinii ...................................................................................... 203
Leptodactylus fragilis ............................................................................... 204
Lithobates brownorum X forreri ................................................................ 204
Lithobates brownorum ............................................................................. 205
Lithobates forreri ...................................................................................... 205
Lithobates maculatus ............................................................................... 208
Lithobates taylori ...................................................................................... 209
Lithobates warszewitschii......................................................................... 209
Pristimantis ridens .................................................................................... 209
Candidate Species and Allopatric Populations of Salamanders ..................... 210
Bolitoglossa (Magnadigita) sp. inquirenda 1 ............................................ 210
Bolitoglossa (Magnadigita) oresbia / sp. inquirenda 2 .............................. 211
Bolitoglossa (Magnadigita) celaque ......................................................... 214
Bolitoglossa (Magnadigita) conanti .......................................................... 214
Bolitoglossa (Magnadigita) porrasorum ................................................... 215
Bolitoglossa (Nanotriton) rufescens/nympha ............................................ 215
Nototriton barbouri ................................................................................... 217
Nototriton sp. inquirenda 1 ....................................................................... 217
Nototriton sp. inquirenda 2 ....................................................................... 218
Nototriton sp. inquirenda 3 ....................................................................... 218
Nototriton lignicola / sp. inquirenda 4 ....................................................... 218
Nototriton limnospectator / sp. inquirenda 5 ............................................. 219
Oedipina kasios / sp. inquirenda 1 ........................................................... 219
Oedipina nica / sp. inquirenda 2 ............................................................... 220
Oedipina koehleri / sp. inquirenda 3 ......................................................... 220
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Oedipina gephyra ..................................................................................... 222
Amphibian Endemism and Conservation Priorities in the Chortís Block ............... 223
Iterative Taxonomic Approaches to Biodiversity Inventory.................................... 224
5 CRYPTIC DIVERSITY AND REVISIONARY SYSTEMATICS OF CHORTÍS HIGHLAND MOSS SALAMANDERS (CAUDATA: PLETHODONTIDAE) ............. 250
Salamanders as Models for Evolutionary Study ................................................... 250
Salamander Diversity in the Chortís Block ............................................................ 252
Methods and Materials .......................................................................................... 256
Sampling ........................................................................................................ 256
DNA Extraction, PCR Amplification, and Sequencing .................................... 257
Sequence Alignment and Model Selection ..................................................... 258
Sequence Analyses ........................................................................................ 259
Bayesian Inference and Maximum Likelihood Phylogenetic Analyses ........... 260
Comparative Morphology ............................................................................... 260
Results .................................................................................................................. 261
Discussion ............................................................................................................ 266
DNA Barcode Identification of Chortís Highland Moss Salamanders ............. 266
Influence of Substitution Saturation in Cytochrome B Dataset ....................... 267
Phylogenetic Systematics and Candidate Species ......................................... 268
Systematics .......................................................................................................... 269
A Divergent New Lineage from Refugio de Vida Silvestre Texíguat ............... 269
Nototriton tomamorum Townsend, Butler, Wilson, & Austin 2010a .......... 270
A New Species from the Sierra de Agalta ...................................................... 275
Nototriton picucha Townsend, Medina-Flores, Murillo, and Austin 2011 . 275
Restriction of the taxon Nototriton barbouri (Schmidt, 1936) .......................... 281
Nototriton barbouri (Schmidt 1936) .......................................................... 282
Description of unassigned populations from the Cordillera Nombre de Dios .. 284
Nototriton sp. A, sp. nov. .......................................................................... 284
Nototriton sp. B, sp. nov. .......................................................................... 285
Review of the Remaining Species of Nototriton from the Chortís Highlands .. 286
Nototriton brodiei Campbell & Smith 1998 ............................................... 287
Nototriton lignicola McCranie & Wilson 1997 ........................................... 287
Nototriton limnospectator McCranie, Wilson, & Polisar 1998 ................... 289
Nototriton stuarti Wake & Campbell 2000 ................................................ 290
6 INTEGRATING RESEARCH, EDUCATION, AND OUTREACH IN SUPPORT OF CONSERVATION IN THE CHORTÍS HIGHLANDS ........................................ 294
Taxonomic Inventories in Promotion of Education and Extension ........................ 295
Opportunities for Training and Education .............................................................. 298
Pilot Project: Parque Nacional Montaña de Yoro .................................................. 299
Concluding Statement........................................................................................... 303
APPENDIX: TAXONOMIC REVIEW OF CAUDATA FROM THE CHORTÍS BLOCK .. 304
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REFERENCES ............................................................................................................ 326
BIOGRAPHICAL SKETCH .......................................................................................... 350
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LIST OF TABLES
Table page 3-1 Summary of fieldwork undertaken in the Chortís Block, 2006–2011. ............... 135
3-2 Conservation status and physiographic distribution of the native non-marine herpetofauna of the Chortís Highlands ............................................................. 137
3-3 Composition of the Chortís Block herpetofauna. .............................................. 159
3-4 Broad distributional patterns of herpetofaunal diversity in the Chortís Block. ... 160
3-5 Endemic and conservation priority herpetofaunal diversity from the Chortís Block ................................................................................................................. 160
3-6 Distribution by mountain ranges of the endemic amphibians and reptiles of the Chortís Highlands ....................................................................................... 161
4-1 Voucher information for samples used in this study ......................................... 228
4-2 Average nucleotide compositions of various taxonomic groups ....................... 244
4-3 Potential candidate species identified through this study ................................. 245
4-4 Results of BLASTN searches of the NCBI database for 16S consensus sequences representing 10 populations of taxonomically-unassigned salamanders ..................................................................................................... 249
5-1 Samples used in sequence divergence and phylogenetic analyses ................. 291
5-2 Models of nucleotide substitution chosen for phylogenetic analyses of Chortís Highland taxa using Akaike Information Criterion values. ................................. 292
5-3 Within and between species sequence divergence (uncorrected p-distance) for Chortís Highland moss salamanders ........................................................... 292
5-4 Morphological and morphometric comparison of species of Nototriton ............ 293
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LIST OF FIGURES
Figure page 1-1 Map showing present-day location of the Chortís Block ..................................... 21
2-1 Political divisions of the Chortís Block ................................................................ 26
2-2 Tectonic plate reconstructions showing the relative position and movement of the Chortís Block during the Cenozoic ............................................................... 30
2-3 Physiographic regions of the Chortís Block ........................................................ 35
2-4 Map showing mountain ranges of the Chortís Block ........................................... 36
2-5 Mountain ranges of the Chortís Block I ............................................................... 37
2-6 Mountain ranges of the Chortís Block II .............................................................. 39
2-7 Ecological associations of the Chortís Block I .................................................... 52
2-8 Ecological associations of the Chortís Block II ................................................... 58
2-9 Ecological associations of the Chortís Highlands ............................................... 64
3-1 Map showing sampling localities in the Chortís Block ........................................ 75
3-2 Sampling in the Chortís Block I ........................................................................... 84
3-3 Sampling in the Chortís Block II .......................................................................... 88
3-4 Sampling in the Chortís Block III ......................................................................... 92
3-5 Sampling in the Chortís Block IV ........................................................................ 98
3-6 Sampling in the Chortís Block V ....................................................................... 104
3-7 Sampling in the Chortís Block VI ...................................................................... 110
3-8 Sampling in the Chortís Block VII ..................................................................... 114
3-9 Exemplar paratypes and habitats from Parque Nacional Montaña de Yoro ..... 117
3-10 La Liberación de Texíguat ................................................................................ 121
3-11 Plectrohyla chrysopleura (Hylidae) from La Liberación .................................... 123
3-12 New species of Tantilla (Colubridae) and Typhlops (Typhlopidae) ................... 129
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3-13 Noteworthy cryptozoic snakes .......................................................................... 132
4-1 Radial phylogram showing coverage of higher-level taxonomic groups ........... 178
4-2 Maximum likelihood phylogram of COI data showing generic and subgeneric relationships of salamander samples ............................................................... 180
4-3 COI (left) and 16S (right) neighbor-joining trees for Bufonidae ......................... 182
4-4 COI (left) and 16S (right) neighbor-joining trees for Craugastoridae, Eleutherodactylidae, Leptodactylidae, and Strabomantidae ............................. 183
4-5 COI (left) and 16S (right) neighbor-joining trees for Hylidae ............................. 185
4-6 COI (left) and 16S (right) neighbor-joining trees for Ranidae ........................... 186
4-7 COI (left) and 16S (right) neighbor-joining trees for Bolitoglossa ...................... 188
4-8 COI (left) and 16S (right) neighbor-joining trees for Cryptotriton, Dendrotriton, Nototriton, and Oedipina ................................................................................... 190
4-9 Maximum likelihood phylogram for the genus Bolitoglossa .............................. 192
4-10 Maximum likelihood phylogram for the genera Nototriton, Oedipina, Dendrotriton, and Cryptotriton .......................................................................... 194
4-11 Candidate Species I: Bufonidae and Craugastoridae ....................................... 199
4-12 Candidate Species II: Eleutherodactylidae and Hylidae ................................... 203
4-13 Candidate Species III: Ranidae and Strabomantidae ....................................... 206
4-14 Candidate Species IV: Bolitoglossa .................................................................. 213
4-15 Candidate Species V: Bolitoglossa cf. porrasorum ........................................... 216
4-16 Candidate Species VI: Oedipina ....................................................................... 221
4-17 Candidate Species VII: Oedipina cf. gephyra (= O. petiola) ............................. 221
5-1 Distribution of Nototriton in the Chortís Highlands ............................................ 255
5-2 Comparison of ―barcoding gaps‖ for three mitochondrial genes used to delimit species boundaries in Nototriton ........................................................... 262
5-3 Bayesian phylograms showing discordance between combined mtDNA phylogenies due to saturation at the third codon position for cytochrome b ..... 265
5-4 Nototriton tomamorum ...................................................................................... 271
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5-5 Nototriton picucha ............................................................................................. 277
5-6 Nototriton barbouri sensu stricto ....................................................................... 283
5-7 Nototriton sp. B ................................................................................................. 286
5-8 Nototriton lignicola ............................................................................................ 288
5-9 Nototriton limnospectator .................................................................................. 289
6-1 Print media coverage of the discovery of new endemic species during 2008 and 2009. ......................................................................................................... 297
6-2 Examples of public outreach and dissemination of results from taxonomic inventories ........................................................................................................ 300
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Abstract of Dissertation Presented to the Graduate School of the University of Florida, in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy
INTEGRATIVE TAXONOMY REVEALS THE CHORTÍS BLOCK OF CENTRAL
AMERICA AS AN UNDERESTIMATED HOTSPOT OF AMPHIBIAN DIVERSITY
By
Josiah Harold Townsend
December 2011
Chair: James D. Austin Major: Interdisciplinary Ecology
Central America has a remarkably complex geological history, has served as the
biological dispersal route between North and South America, and is the site of extensive
in situ evolution. Nuclear Central America is recognized as a region of high biodiversity,
and the eastern portion of Nuclear Central America (the Chortís Block) has largely been
overlooked as a biodiversity hotspot. In this dissertation, I use an integrative systematic
approach to examine evolutionary patterns in a group with high diversity of endemic
species that is also of global conservation priority: amphibians. I carried out 17
expeditions to over 60 localities in the Chortís Block for this dissertation, results from
which are synthesized with existing data on regional herpetofaunal diversity,
distribution, and conservation status. The Chortís herpetofauna is characterized by a
high degree of endemism (35% of all species are endemic) and equally high extinction
risk (41% threatened, including 96% of endemic species). Endemism is highest among
salamanders (86% of species are endemic). A total of 456 amphibian samples
representing 52 species were sequenced for two genes (16S and COI) and analyzed
using distance-based and phylogenetic methods. I identify at least 36 unnamed
―candidate‖ across eight families of amphibians, while confirming that four
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taxonomically-uncertain salamander populations represented new allopatric populations
of endangered species previously assumed to be single-site endemics. These results
reveal a regional amphibian fauna, already recognized as being of global conservation
priority, with species diversity underestimated by 26% (47% in salamanders),
highlighting the critical role molecular systematics plays in endangered species
conservation and management. To directly address the systematics a poorly-known
group with multiple candidate species, I present an integrative taxonomic revision of the
genus Nototriton using data from three genes, external morphology, and osteology. I
restrict the taxon N. barbouri to populations from the Sierra de Sulaco, describe three
new species from the Chortís Highlands, and a review of the remaining regional
species. In light of these findings, I present my vision for using systematic biology as the
basis for integrating research, education, and outreach in support of biodiversity
conservation in the Chortís Block.
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CHAPTER 1 INTRODUCTION
The formation of the Central American land bridge, with subsequent interchange of
previously-isolated organisms of Laurasian and Gondwanian origin, has been a source
of inquiry for biogeographers since the founding of the discipline (Wallace 1876; Stehli
and Webb 1985). Central America has had a remarkably complex geological history,
owing in large part to its position as the contact zone for five of the world’s 14 major
tectonic plates: the Caribbean, Cocos, Nazca, North American, and South American
plates (Figure 1-1; Bird 2003). Central America has not only served as the dispersal
route between North and South America, but the region’s extreme topographical and
ecological heterogeneity has also fuelled significant in situ diversification, particularly
associated with the disjunct highland areas of Nuclear Central America and southern
Central America (Savage 1966, 1983; Wake 1987).
Whereas Nuclear Central America has long been accepted as a region of high
biodiversity, some observers have further recognized the western and eastern portions
of this highland block as distinct biogeographic entities (Johnson 1989; Campbell 1999;
Townsend 2006, 2009). Eastern Nuclear Central America, corresponding to the Chortís
Block tectonic formation (Figure 1), has been shown to have a distinctive component of
endemic biodiversity, particularly in amphibians and reptiles (Wilson & Johnson 2010),
however molecular characterization of evolutionary patterns of diversification in this
region has been limited to a few studies of a restricted taxonomic breadth and broader
geographic focus (e.g. Castoe et al. 2009).
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Figure 1-1. Map showing present-day location of the Chortís Block. Relative present-day positions of four major tectonic plates and selected elements of the Central American Isthmus are indicated, with the contemporary Chortís Block highlighted in green (map generated using ODSN Plate Tectonic Reconstruction Service1 and modified by author).
My principal goal is to broadly initiate molecular systematics research and studies
in evolutionary biogeography in the Chortís Block (Figure 1-1), a distinctive
biogeographic region with a complex and unique geomorphological history and highly
variable contemporary ecophysiographic landscape. This region has a largely
unrealized biogeographic importance as the first fragment of proto-Central America to
contact the North American plate; furthermore, it is characterized by a high degree of in-
situ endemism and evolutionary diversification in its extant biota. As a group with the
highest documented endemism and highest risk for extinction, amphibians, and
1 http://www.odsn.de/odsn/services/paleomap/paleomap.html
22
particularly salamanders, make excellent taxa upon which to base studies of
systematics and evolution.
I begin in Chapter 2 by providing a synthesis of relevant characteristics of the
Chortís Block, in order to support a working definition for use in this dissertation and
beyond. I begin by summarizing the geological history of the Chortís Block, providing a
comprehensive account of the contemporary physiographic and ecological landscape,
and finally presenting an operationalized version of Carr’s (1950) outline of a system for
characterizing Honduran animal habitats.
In Chapter 3, I provide an assessment of the diversity, conservation status, and
distribution of amphibians and reptiles in the Chortís Block. This assessment is based
on over 12,560 person-hours of fieldwork conducted since 2006 (over 2,577 person-
hours logged myself), and existing data on distribution and conservation status of
amphibians and reptiles from the region. The Chortís Block herpetofauna is
characterized by a high degree of endemism that is faced with an equally high degree of
extinction risk. Thirty-five percent of the Chortís Block herpetofauna is endemic, and
41% of those species are conservation priority (i.e. listed in the IUCN Red List’s three
highest threat categories, Critically Endangered, Endangered, and Vulnerable),
including an alarming 96% of endemic species. Endemism is by far highest among the
salamanders (86% of species are endemic); while 75% of salamander species are
considered conservation priority by the IUCN (2011). This figure likely is underestimated
significantly.
As a result of the fieldwork detailed in Chapter 3, a comprehensive sample set of
taxa and localities was assembled for Chortís Block amphibians, with particularly good
23
representation of salamanders (Caudata). In Chapter 4, take an integrative taxonomic
approach involving genetic distance-based analysis (i.e., DNA barcoding) and model-
based phylogenetic analysis to identify and characterize cryptic amphibian diversity in
the Chortís Block. Analysis of 456 individual samples representing 52 named species in
eight families of amphibians indicate that there are at least 36 unnamed ―candidate‖
species (20 anurans and 16 salamanders) in the Chortís Block, while confirming that
four taxonomically-uncertain salamander populations actually represented new
allopatric populations of endangered species previously assumed to be single-site
endemics. These results reveal a regional amphibian fauna, already recognized as
being of global conservation priority, to be underestimated by 26% (47% in
salamanders) in terms of species diversity, highlighting the critical role molecular
systematics plays in endangered species conservation and management.
In Chapter 5, I further utilize an integrative approach to delineate and estimate
species-level phylogenetic relationships among and endemic radiation of highly cryptic
moss salamanders (genus Nototriton) in the Chortís Highlands. Using data from three
mitochondrial DNA loci, I examine the utility of each gene in a distance-based DNA
barcoding approach for determining species diversity. The evolutionary relationships of
diagnosed lineages are inferred using model-based phylogenetic analyses. My results
indicate that species-level diversity in Nototriton is underestimated in the Chortís Block.
Three undescribed species of Nototriton were identified: one from the Sierra de Agalta
in Departamento de Olancho, and one each from Pico Bonito and Texíguat in the
Cordillera Nombre de Dios. Finally, the taxonomy of this clade of Nototriton is reviewed
and revised, with a restriction of the taxon N. barbouri (Schmidt) to populations from the
24
Sierra de Sulaco, formal description of the three new species, and a review of the
remaining species.
Finally, Chapter 6 presents my long-term vision for scientific exploration, research,
education, and outreach in support of herpetofaunal conservation in Honduras, the
country containing the bulk of the Chortís Highlands and the majority of the Chortís
Block’s endemic species. I then provide a closing synthesis of the dissertation,
reviewing the results within a context of their regional and global significance.
25
CHAPTER 2 BIOGEOGRAPHIC DELIMITATION OF THE CHORTÍS BLOCK: GEOLOGICAL
HISTORY, PHYSIOGRAPHY, AND ECOLOGICAL ASSOCIATIONS
My enthusiasm for the topic of Chortís Block biogeography grew from the
realization that patterns of endemism observed over the course of my studies in
Honduras and northern Nicaragua seemed to be largely a reflection of emerging
patterns in tectonic plate dynamics that have shaped the complex geomorphological
history of the region. In previous works, I have favored use of the ―Eastern Nuclear
Central America‖ biogeographic province (Townsend 2006, 2009; Townsend & Wilson
2010a) in order to set this region apart, in recognition of its distinctiveness from proximal
regions. This region is geographically analogous to the Chortís Block, an allochthonous1
geological formation that today forms the only modern continental portion of the
Caribbean Tectonic Plate and the largest terrestrial segment of the contemporary
Central American land bridge (Rogers 2003; Marshall 2007). The Chortís Block has a
challengingly complex history, and has recently been the subject of increased focus,
and sometimes contentious debate, within the geological research community (James
2007; Mann et al. 2007; Ortega-Gutiérrez et al. 2007; Silva-Romo 2008; Morán-Zenteno
et al. 2009).
Politically, the contemporary region I refer to as the Chortís Block includes all of
the country of Honduras, the northern portion of El Salvador, eastern Guatemala, and
northern Nicaragua (Figure 2-1). As a working delimitation of the biogeographic region, I
consider the Chortís Block to be nearly homologous with Campbell’s (1999: 116)
concept of an Eastern Nuclear Central American biogeographic province. I include the
1 Allochthonous – referencing an independent geological structure that has moved from its site of origin.
26
Figure 2-1. Political divisions of the Chortís Block. Countries are shaded differently and labeled in all capital letters, while
departments are labeled in sentence-case in a smaller font size.
27
associated coastal plains, with the western extent of the Chortís Block at the edge of the
Río Motagua Valley (the eastern edge of the Polochic-Motagua fault complex) to a
north-south line roughly running through Zacapa, Chiquimula, Concepcíon Las Minas,
and the Guatemalan-El Salvador border at the Pacific Coast. It extends eastward to
include all of Honduras and El Salvador, and south to a line roughly between Lago
Xolotlán (= Lago de Managua) and Lago Colcibolca (= Lago de Nicaragua) in northern
Nicaragua (Figure 2-1). Without including the associated lowlands, Campbell’s Eastern
Nuclear Central America is homologous with the highlands of the Chortís Block, referred
to collectively as the Chortís Highlands (Marshall 2007) or the serranía (Carr 1950).
An integrative definition of the Chortís Block Biogeographic Province, as presented
here, combines an ecological and biodiversity-based framework, as used to delineate
Eastern Nuclear Central America, with that of a physiographically and tectonically-
defined Chortís Block.
Geological History
The history of the Chortís Block is in large part characterized by its eastward
movement along a series of strike-slip faults on the southern margin of the North
American Plate (Figure 2-2; Dengo 1969; Donnelly et al. 1990; Gordon 1992; Rogers et
al. 2007). As recently as the K-T Boundary (65 million years before present [mybp];
Figure 2-2), the Chortís Block was located somewhere south of modern south-central
México, having moved along a west-to-east trajectory around 200 km into its current
position as the principal surface area of the Central American land bridge and the
modern territory of Honduras, El Salvador, eastern Guatemala and northern Nicaragua
(Figure 2-1; Rogers 2003; Ortega-Gutiérrez et al. 2007).
28
Origin and Cenozoic development of the Chortís Block. The Chortís Block
represents the only exposed Precambrian and early Paleozoic continental crust on the
contemporary Caribbean Plate (DeMets et al. 2007). The oldest exposed geological
formation of the Chortís Block is Precambrian in age and of Rodinian2 derivation,
originating during the Grenville orogeny (1,017 ± 20 mybp or 1400 mybp, depending on
dating methods) contemporaneously with the Appalachian and Adirondack mountains of
eastern North America and the Llano Plateau of Texas and northeastern México
(Mandon 1996; Gordon et al. 2010). Today, this ancient formation is visible as a 60 km-
long series of exposed outcrops along the Jocotán-Ceiba Fault in the Departamento de
Yoro, Honduras (Gordon et al. 2010). While it is generally accepted among geologists
that the Chortís Block originated approximately 1,100 km west of its current position and
became detached during the Eocene, sliding and rotating along the Motagua-Polochic
Fault Complex at the southern margin of the stationary North American Plate, there are
two competing hypotheses regarding the Chortís Block’s origin (reviewed by Rogers et
al. 2007). The first hypothesis places the Chortís Block along the southwestern margin
of the North American Plate and physically contiguous with México, and is supported by
the existence of similarly aged Precambrian and Paleozoic rock formations, potential
aligned fault systems in present day Honduras and southwestern México, and
geological evidence that the Chortís Block rotated 30–40° counterclockwise while
sliding eastward (Figure 2-2; Gose 1985, Silva-Romo 2008). The second hypothesis
places the Chortís Block’s original position some 700–800 km south of México, with it
moving northeastwardly while rotating 40° clockwise (Keppie & Moran-Zenteno 2005). A
2 Rodinia was a paleo-supercontinent that contained most of Earth’s landmass and existed between
approximately 2,000 mybp and 750 mybp
29
third, less accepted hypothesis holds that the Chortís Block has remained in virtually the
same position relative to the North American Plate, and that structures and evidence to
the contrary have essentially been misinterpreted (James 2007).
The relatively dramatic Cenozoic tectonic history of the Chortís Block was
dominated by what can only be described as catastrophic, prolonged, and repeated
volcanism as the block slid and rotated its way eastward. The beginning of this
extended period was the mid-Eocene (approximately 55 mybp), following initial
detachment of the Chortís Block from its parent structure (Jordan et al. 2008). A second
flare-up took place during the mid-Oligocene (around 40 mybp), and the third, and
largest, flare-up took place during the early to middle Miocene (Jordan et al. 2008).
Miocene Ignimbrite Flare-up and subsequent uplift. The Mesozoic history of
the Chortís Block features an approximately 10 million year period of intense explosive
volcanism along the margins of the Chortís Block and Central American Volcanic Front,
considered the second largest ignimbrite1 event in the known geological history of Earth
(Jordan et al. 2008). During the mid-Miocene over 5,000 km3 of ignimbrites up to 2,000
m thick were deposited on top of the low-relief surface of the southern and western
Chortís Block and tens of thousands of square kilometers were repeatedly covered in
thick layers of ash (Williams & McBirney 1969; Rogers et al. 2002; Jordan et al. 2008).
The most intense period of the ignimbrite flare-up lasted from around 20 mybp to 15
mybp, with activity ceasing approximately 10.5 mybp (Gordon & Muehlberger 1994).
This period is well documented by a series of deep-sea sediment cores from sites in the
western Caribbean Sea (Jordan et al. 2008). The site of a fissure-like volcano that was
3 Ignimbrite – hard rock formed from the deposition of super-heated pyroclastic flow
30
Figure 2-2. Tectonic plate reconstructions showing the relative position and movement
of the Chortís Block (shaded green) during the Cenozoic. Follows the generally accepted tectonic model of Hay et al. (1999; alternative models reviewed in Rogers et al. 2007), with black lines represent tectonic boundaries and gray shading delineates modern-day shorelines and landmasses (maps generated using ODSN Plate Tectonic Reconstruction Service2 and modified by author).
4 http://www.odsn.de/odsn/services/paleomap/paleomap.html
31
―ground zero‖ for the Miocene Ignimbrite Flare-up is represented today by the Padre
Miguel Group geological formation in southwestern Honduras and peripherally in El
Salvador and Guatemala (Rogers 2003). Under these circumstances, it would seem
unlikely that extant terrestrial organisms and ecosystems on the Chortís Block are
survivors of this extreme volcanism, and more likely that the extant biota represents the
product of post-volcanic colonization and diversification. Following the Miocene flare-up
and up and until approximately 3.8 mybp, the Chortís Block went through a period of
rapid uplift driven by the detachment and subsequent subduction of a portion of the
Cocos Plate, which induced upwelling in the mantle that raised the Chortís Block up to
1,100 m (Rogers et al. 2002).
The contemporary Chortís Block. The Chortís Block presently continues its
eastward movement along the strike-slip faults of the Motagua-Polochic Fault Zone and
Swan Island Fault Zone, interacting in the continental context with the Maya Block of the
North American Plate to the north and the Chorotega Block to the south, albeit
interrupted by the Nicaraguan Depression (Figure 1-1, 2-2; Rogers 2003, Marshall
2007). Marshall (2007) defined 15 physiographic provinces in Central America, four of
which (the Chortís Highlands, Chortís Volcanic Front, Chortís Fore Arc, and Mosquitia
Coast Lowlands) are geomorphological associates of the Chortís Block.
The Chortís Highlands Province consists of a large dissected plateau that forms
the greater part of the Chortís Block and includes the majority of the territory of the
countries of Honduras and El Salvador, as well as western Guatemala and northern
Nicaragua (Marshall 2007). The Chortís Highlands Province is subdivided into four
regions: the Western Rifted Highlands, the Central Chortís Plateau, the Eastern
32
Dissected Highlands, and the Honduran Borderlands. The Chortís Volcanic Front
Province is an active volcanic front that borders the southern margins of the Chortís
Highlands Province, and includes two regions: the Guatemalan Cordillera, which
borders the western margin of the Chortís Highlands Province; and the Salvadoran
Cordillera, which borders the Median Trough, an elongate graben that extends along
the boundary faults at the margin of the active Nicaraguan Volcanic Front (Marshall
2007). The Chortís Volcanic Front Province represents part of the proverbial ―Ring of
Fire.‖ a loose chain of active volcanoes and tectonic plate subduction that rings the
Pacific Ocean. The Chortís Fore Arc Province encompasses the Pacific coastal plain of
the Chortís Volcanic Front Province, and is similarly subdivided into the Guatemalan
Coastal Plain and Salvadoran Coastal Plain (Marshall 2007). The Mosquito Coast
Lowlands Province is the wide alluvial plain along the eastern Caribbean slope of
Honduras and Nicaragua, a region also referred to as La Mosquitia. The Mosquito
Coast Lowlands Province is dominated by a massive paleo-Coco/Patuca river delta built
up during the glacial cycles of the Pliocene-Pleistocene (Marshall 2007).
The aforementioned Chortís Highlands Province and its four constituent
subregions are of principal interest for this dissertation, and these subregions are
described in detail below.
The Western Rifted Highlands region of southeastern Guatemala, southwestern
Honduras, and northern El Salvador is a west-to-east oriented plateau, generally
exceeding 1,000 m elevation, which is interrupted by a series of independent, north-to-
south oriented rift valleys featuring flat, xeric valley floors (Marshall 2007). The rift
valleys, or grabens, of the Western Rifted Highlands include the contemporary
33
Comayagua Valley and Otoro Valley. This region corresponds to the Padre Miguel
Group, a 1,000–2,000 m thick layer of mid-Miocene ignimbrites laid down during the
super-volcanic eruptions along the margin of the Chortís Highlands and Chortís
Volcanic Front. Those super-eruptions essentially reset the landscape, allowing the
development of new meandering river drainages as the rift valleys began spreading
following the end of the Miocene ignimbrite flare-up around 10.5 mybp (Gordon &
Muehlberger 1994; Rogers et al. 2002).
The Central Chortís Plateau region of the Honduran interior represents the most
tectonically stable portion of the Chortís Highlands, forming an essentially level plateau
with little dissection or embedding by rivers (Marshall 2007). The Central Chortís
Plateau lies atop of Paleozoic bedrock overlain with layered Cretaceous-aged
sedimentary deposits (Rogers et al. 2002; Marshall 2007).
The Eastern Dissected Highlands region of eastern Honduras and Nicaragua
includes the lower elevation, higher relief mountains bordering the Mosquito Coast
Lowlands, and features three large, deeply embedded river drainages that drain a large
portion of the Chortís Highlands Province (Marshall 2007).
The Honduran Borderlands region lies along the northern margin of the Chortís
Highlands, and is characterized by five major west-to-east trending faults that border
major mountain ranges, including the Cordillera Nombre de Dios in northern Honduras
(Rogers 2003, Marshall 2007). One large graben valley, the Sula Graben, extends
north-to-south from the Caribbean coast to the north end of Lago de Yojoa, and today
contains the lower courses of two of the largest watersheds in the Chortís Block: the Río
Chamelecón and the Río Ulua.
34
Contemporary Ecophysiography
Carr (1950), in his pioneering classification of Honduran ecological associations,
recognized three principal ecophysiographic components that make up the Chortís
Block: the Caribbean versant lowlands, the Pacific versant lowlands, and the
mountainous interior region known as the serranía (Figure 2-3). Carr’s
ecophysiographic regions correspond well with the geologically-based physiographic
provinces of Marshall (2007; described in the previous section), with the serranía being
congruent with the Marshall’s Chortís Highlands Physiographic Province. Subsequently,
from this point forward I use the name ―Chortís Highlands‖ analogously with serranía.
Carr (1950) further subdivided the Chortís Highlands into the Northern Cordillera, the
Southern Cordillera, and the Pacific Colinas. This arrangement was also used by Wilson
& Meyer (1985), McCranie & Wilson (2002), and others. Mejía-Ordóñez & House (2002)
introduced a modified arrangement, based on their comprehensive evaluation of the
ecosystems of Honduras using the UNESCO system of Physiognomic-Ecological
Classification of Plant Formations of the Earth (Mueller-Dombois & Ellenberg 1974),
which recognized a Cordillera del Norte, Cordillera Central, and Cordillera del Sur. This
arrangement is preferable and is used here as the basis for describing the
ecophysiography of the Chortís Block, which I divide into three principal regions: the
Caribbean Lowlands, the Pacific Lowlands, and the Chortís Highlands, which itself is
subsequently subdivided into the Northern, Central, and Southern Cordilleras.
Northern Cordillera of the Serranía. As first defined by Mejía-Ordóñez & House
(2002) and expanded here, the Northern Cordillera consists of the following mountain
ranges and groups of ranges:
35
Figure 2-3. Physiographic regions of the Chortís Block. After Carr (1950).
The Cordillera (or Sierra) Nombre de Dios (Figure 2-4) stretches west-to-east across the departments of Atlántida, Colón, and Yoro, Honduras, and includes the cloud forest protected areas Refugio de Vida Silvestre (RVS) Texíguat (maximum elevation 2,208 m) at the western end and Parque Nacional (PN) Pico Bonito (2,435 m) and PN Nombre de Dios (1,725 m) in the central portion, with a few scattered low peaks extending to the east, terminating with PN Capiro y Calentura (1,235 m) near Trujillo. Based on my preliminary observations, I consider the Sierra de Mico Quemado, a north-to-south oriented range in western Yoro, to be the western terminus of the Cordillera Nombre de Dios. This range, which includes Zona de Reserva Ecológica (ZRE) Montaña de Mico Quemado y Las Guanchias, was considered part of the Central Cordillera by Mejía-Ordóñez & House (2002).
The Sierra de Omoa (Figure 2-4) in the departments of Cortés and Santa Bárbara, Honduras, with the cloud forest protected area PN Cusuco (2,242 m), as well as the Área de Producción de Agua Merendón (1,749 m).
The Sierra de Espíritu Santo (Figure 2-4) in the departments of Copán and Santa Bárbara, in Honduras and Izabal and Zacapa in Guatemala, which includes the cloud forest reserve PN Cerro Azul Copán (2,285 m), as well as unprotected highland forests at Río Amarillo (1,479 m) in Copán, Honduras, and Cerro del Mono (1,653 m) in Zacapa, Guatemala.
While these mountain ranges appear disjunct and isolated (Figure 2-4), particularly
with respect to the Sula Graben, their herpetofaunal composition and patterns of
36
Figure 2-4. Map showing mountain ranges of the Chortís Block. Green outlines correspond to the Northern Cordillera,
blue to the Central Cordillera, red to the Southern Cordillera, and black to ranges extralimital to this study. 1 = Sierra Nombre de Dios, 2 = Sierra de Omoa, 3 = Sierra de Espíritu Santo, 4 = Sierra de Joconal, 5 = Montaña de Santa Bárbara, 6 = Montañas de Meámbar, 7 = Sierra de Montecillos, 8 = Sierra de Comayagua, 9 = Sierra de Sulaco, 10 = Cordillera de La Flor-La Muralla, 11 = Sierra de Agalta, 12 = Sierra de Botaderos, 13 = Sierra Punta Piedra, 14 = Montañas de Patuca, 15 = Sierra de Montecristo, 16 = Sierra del Merendón, 17 = Sierra de Celaque, 18 = Sierra de Erandique, 19 = Sierra de Puca-Opalaca, 20 = Montaña de la Sierra, 21 = Sierra de Lepaterique, 22 = Sierra de Dipilto, 23 = Montaña de Colón, 24 = Cordillera Dariense, 25 = Salvadoran Cordillera, 26 = Cordillera de Las Marabios.
37
Figure 2-5. Mountain ranges of the Chortís Block I. A) Cordillera Nombre de Dios, seen
from offshore looking south; Cerro Búfalo is the tallest mountain on the left (east) side, and Pico Bonito is the sharp peak on the right (west) side. B) Sierra de Omoa, seen from near Buenos Aires de Bañaderos looking east-northeast. C) Southern slopes of Cerro Azul de Copán in the Sierra de Espíritu Santo, seen from Quebrada Grande. D) Montaña de Santa Bárbara, seen from the road west of Peñas Blancas looking south-southwest. E) Montañas de Meámbar, seen from the road south of Santa Elena looking south. F) Sierra de Comayagua, seen from road south of San Jerónimo looking south. (Photos © J.H. Townsend).
distribution reflect a greater shared evolutionary history among these mountains than
any of them share with other ranges (as evidenced in Chapter 4).
38
Central Cordillera of the Serranía. I follow Mejía-Ordóñez & House (2002) in
recognizing a Central Cordillera made up of the remaining Caribbean versant serranía,
otherwise included in Carr’s (1950) Northern Cordillera.
The Sierra de Joconal (1,688 m; Figure 2-4) extends to the roughly west-to-east from eastern Departamento de Copán (municipalities Nueva Arcadia and San Nicolás), across Departamento de Santa Bárbara and into western Departamento de Cortés (municipality of Villanueva).
Montaña de Santa Bárbara (2,744 m; Figure 2-4) is an isolated karstic massif rising from the southern terminus of the Ulúa-Chamelecón Plain to the west of Lago de Yojoa, its unique ecological communities wholly contained within the boundaries of PN Montaña de Santa Bárbara.
The Montañas de Meámbar (2,080 m; Figure 2-4), also called the Montañas de Yule, are a rugged set of peaks on the eastern side of Lago de Yojoa on the border between the departments of Cortés and Comayagua, primarily contained within PN Cerro Azul Meámbar. Mejía-Ordóñez & House (2002) apparently included this group of mountains in the Sierra de Montecillos; however I consider it to be a separate formation.
The Sierra de Montecillos (Figure 2-4) is one of two roughly parallel mountain ranges that are oriented northwest-southeast and form the margins of the ―Honduran Depression‖ in central Honduras. Some of the highest portions of this mountain range, which straddles the border between the departments of Comayagua and Intibucá, make up RB Montecillos (2,459 m).
The Sierra de Comayagua (Figure 2-4) runs roughly parallel to the Sierra de Montecillos, separated by the dry intermontane Comayagua Valley, and extends over 130 km north-to-south along the border between the departments of Comayagua and Francisco Morazán. The highest portions of this range are found within PN Montaña de Comayagua (2,407 m) and RVS Corralitos (2,117 m).
The Sierra de Sulaco (Figure 2-4) runs roughly west-to-east in the southwestern part of the Departamento de Yoro, and includes the highlands of PN Pico Pijol (2,282 m) at the western end of the range and Montaña Macuzal (1,945 m) at the eastern end.
The Cordillera de La Flor-La Muralla (Figure 2-4) stretches across northern Departamento de Francisco Morazán, southern Departamento de Yoro, and into western Departamento de Olancho, with highland forest protected areas PN Montaña de Yoro (2,245 m), RVS La Muralla (2,064 m), Reserva Forestal Anthropológica (RFA) Montaña de la Flor (1,637 m), RB El Cipresal (1,930 m), and RB Misoco (2,153 m).
39
Figure 2-6. Mountain ranges of the Chortís Block II. A) Looking west along the spine of
the Sierra de Sulaco, taken from the top of Montaña Macuzal, with Pico Pijol being the largest peak in the distance. B) Southeastern reaches of the highest peak in the Sierra de Botaderos. C) The Sierra de Celaque viewed from the east, with the tallest peak in the Chortís Block, Cerro de la Minas, visible as the peak in the middle of the photograph. (Photos © J.H. Townsend).
40
The Sierra de Agalta (Figure 2-4) in central Olancho is a long, relatively narrow and steep range that includes, from west to east, the protected areas Monumento Natural Boquerón (1,261 m), PN Sierra de Agalta (2,335 m), Reserva Anthropológica El Carbón (1,817 m), and PN Sierra de Río Tinto (1,925 m).
The Sierra de Botaderos (Figure 2-4) is located in northern Olancho along the border with the department of Colón, and includes Cerro Ulloa (1,735 m) and Cerro Azul (1,433 m) within the highland reserve PN Montaña de Botaderos, as well as the lower mountains of the Sierra de La Esperanza.
The Sierra Punta Piedra (Figure 2-4) is a relatively low elevation range in the departments of Colón and Gracias a Dios, and includes Montaña Punta Piedra (1,500 m), Cerro Antílope (1,075 m), Cerro Mirador (1,200 m), and Cerro Baltimór (1,082 m). These mountains are found in Reserva de Hombre y la Biosfera Río Plátano.
The Montañas de Patuca (1,155 m; Figure 2-4) in Olancho are located between the Río Guayape, which flows directly southwest to meet the Río Guayambre and form the Río Patuca, and a lower course of the Río Patuca that flows northeast to the Caribbean Sea. The southeastern portion of this range is found within PN Patuca.
Southern Cordillera of the Serranía. The Southern Cordillera is a
geomorphologically linked series of mountain ranges extending from the vicinity of the
El Salvador-Guatemala-Honduras border region east-southeast into northern
Nicaragua.
The Sierra de Montecristo (Figure 2-4) has its highest elevations at the point where El Salvador, Guatemala, and Honduras meet, in a tri-nationally managed protected area called Montecristo Trifinio (2,419 m). Most of this range is found in Guatemala, where it extends northward into the department of Chiquimula.
The Sierra del Merendón (Figure 2-4) is a north-south oriented range that extends from Guatemala (Chiquimula, Zacapa) across Honduras (Copán, Ocotepeque, Lempira) and into El Salvador (Chalatenango), and includes the following cloud forest areas: RVS Erapuca (2,380 m), Cerro El Pital (2,730 m), Cerro Sumpul (2,167 m), and Reserva Biológica (RB) Güisayote (2,310 m),
The Sierra de Celaque (Figure 2-4) is a north-south oriented range located in Lempira and easternmost Ocotepeque, and contains the highest elevations in the Chortís Highlands in PN Celaque (including peaks of 2,849 m, 2,825 m, and 2,804 m elevation) and RB Volcán Pacayita (2,516 m).
41
The Sierra de Erandique (2,134 m; Figure 2-4) is a north-south oriented range in southeastern Lempira, extending from the municipality of La Campa at the northern end to the municipality of Piraera in the south.
The Sierra de Puca-Opalaca (Figure 2-4) is located in Intibucá, northeastern Lempira, and extreme southern Santa Bárbara, and includes cloud forest areas found in RC Cordillera de Opalaca (2,390 m), RVS Puca (2,234 m), RVS Mixcure (2,312 m), and RVS Montana Verde (2,127 m).
The Montaña de la Sierra (Figure 2-4) is found in the department of La Paz and extreme southern Intibucá, and includes a number of peaks and high plateaus, including a number within RB Guajiquiro (2,265 m), RB El Chiflador (1,811 m), RB El Pacayal (1,955 m), RB Mogola (1,648 m), RB Sabanetas (2,047 m), RB San Pablo (1,741 m), and RB San Pedro (1,719 m).
The Sierra de Lepaterique (Figure 2-4) is the roughly U-shaped range that circles the southern side of the upper Choluteca valley, which is also the valley containing the Honduran capital, Tegucigalpa. This range includes PN La Tigra (2,290 m), RB Yerba Buena (2,243 m), RB Cerro Uyuca (2,006 m), RB El Chile (2,190 m), and RB Monserrat-Yuscarán (1,825 m).
The Sierra de Dipilto (Figure 2-4) extends over 300 km west-to-east from PN La Botija (1,710 m) in Choluteca, to the Cordillera Entre Ríos in PN Patuca, straddling
the Honduras-Nicaragua border and including Reserva Natural (RN) Cerro Mogotón (2,106 m), the highest point in Nicaragua.
The Montaña de Colón (Figure 2-4) is a low (maximum elevation 941 m), isolated karstic range located in southeastern Olancho and adjacent Gracias a Dios, and is found primarily within the Reserva de Biosfera Tawahka-Asangni.
The Cordillera Dariense (Figure 2-4) is a collection of cloud forested peaks and highland areas in northern Nicaragua, in the departments of Jinotega, Matagalpa, and Región Autónoma Atlántico Norte, including Reserva Natural (RN) Apante (1,442 m), RN Cerro Musún (1,438 m), RN Dantalí-El Diablo (1,680 m), RN Kilambé (1,755 m), RN Peñas Blancas (1,744 m), RN Saslaya (1,658 m), and RN Volcán Yali (1,709 m).
Intermontane Valleys and Plains. The Chortís Highlands can be characterized
as well for its valleys as it can be for its mountains; the isolated mountains form
―islands‖ of cool mesic habitat and the subhumid intermontane valleys represent
isolated areas of hot, dry habitat. Aspects of the physiography, ecological associations,
and biogeography of these subhumid valleys were the subject of study by Stuart (1954),
42
Johannessen (1963), Wilson & McCranie (1998), Sasa & Bolaños (2004), and
Townsend & Wilson (2010b).
The Middle Motagua Valley is among the driest areas in Central America, along with the Middle Aguán Valley in Honduras. This valley lies between the Sierra de las Minas (extralimital to the Chortís Highlands) and the Sierra Espíritu Santo.
The Sula Valley in northwestern Honduras is formed from combined drainages of two large watersheds, the Río Chamelecón and Río Ulúa, which have courses that flow closely together in their lower reaches into the Caribbean Sea. The Sula Valley is a north-to-south oriented graben valley that has been spreading since the late Miocene.
The Otoro Valley is a moderately high elevation subhumid graben valley (lowest elevations 500–600 m) lying in a narrow upper portion of the Sula Valley, possessing an ecological character distinctive from that of the broader middle Sula Valley.
The Comayagua Valley is a relatively high subhumid graben valley (lowest elevations 580–680 m) that forms a principal portion of the Honduran Depression, lying between the Sierra de Montecillos to the west and the Sierra de Comayagua to the east. This valley, like the Otoro Valley to the west, is actually a narrow upper portion of the Sula Valley, distinctive enough in character to warrant recognition.
The Middle Aguán Valley is a west-to-east oriented fault valley that lies in the rain-shadow of the Cordillera Nombre de Dios in Yoro and is one of the driest areas in the Chortís Block.
The Siria-Talanga Valley is a high plain (lowest elevations 620–720 m) in central Francisco Morazán that is the headwaters of two of the largest watersheds in the Chortís Highlands, the Río Guayambre/Río Patuca and the Río Ulúa.
The Olancho Valley (or Guayape–Guayambre Valley) is a large valley in central Olancho surrounded by several mountain ranges, including the Sierra de Agalta, Cordillera de La Flor-La Muralla, and Montañas de Patuca, to form the headwaters of the Río Patuca.
The Agalta Valley, also referred to as the ―San Esteban Valley‖ by various authors (Wilson & McCranie 1998, McCranie & Wilson 2002, Townsend & Wilson 2010b), is found between the Sierra de Botaderos and Sierra de Agalta in central Olancho. The lowest elevations of the relatively high subhumid intermontane valley, formed by the Río Grande (a river whose name changes to Río Sico, Tinto, and Negro downstream), are 550–650 m.
The Middle Lempa Valley lies on a west-to-east orientation in central El Salvador between the Southern Cordillera of the Serranía and the Salvadoran Cordillera.
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The Upper Segovia Valley in Nicaragua is a subhumid region in the headwaters of the Río Coco (the upper reaches are also called the Río Segovia, and the lower river is called the Wangki by the indigenous Miskitu).
The Choluteca Valley is the only major subhumid intermontane valley on the Pacific versant, and is initially oriented south-to-north from the headwaters of the Río Choluteca in the Sierra de Lepaterique, before curving around the north side of the mountains protected within PN La Tigra and turning south and then southwest on its path to the Pacific Ocean.
The Meseta de La Esperanza is the highest plain in the Chortís Highlands, extending 12 km in length across central Intibucá at elevations ranging between 1800 and 2000 m.
The Meseta de Siguatepeque is located in Comayagua between the Sierra de Comayagua, Sierra de Montecillos, and Montañas de Meámbar at around 1,100 m elevation.
The Meseta de Santa Rosa is a wide plain on a plateau at about 1,100 m elevation in western Copán.
Caribbean Lowlands. Corresponding to the Mosquito Coast Lowlands
Physiographic Province of Marshall (2007), the major ecophysiographic regions of the
Caribbean lowlands include (McCranie & Wilson 2002, Wilson & Townsend 2006): the
Motagua Plain (lower alluvial plain of the Río Motagua, east of the river and northwest
and west of the Sierra de Omoa and Sierra de Espíritu Santo), the Ulúa-Chamelecón
Plain (large alluvial plain formed by Chamelecón and Ulúa rivers, which drain close to
half of the physical territory of Honduras), the Nombre de Dios Piedmont (the narrow
strip of coastal plain backed by the Cordillera Nombre de Dios), the Aguán-Negro Plain,
and the wide expanse of the Mosquitia (broad alluvial plain essentially lying between the
Sico-Paulaya watershed in Honduras and the Río Grande de Matagalpa watershed in
Nicaragua). Two climatic regimes are present in the Caribbean Lowlands (McCranie
and Wilson 2002, Wilson & Townsend 2006): the Lowland Wet climate is found on the
Caribbean coastal plain from sea level to about 600 m elevation, with mean annual
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precipitation exceeding 2000 mm and mean annual temperature exceeding 24°C.
Important protected areas for Caribbean Lowlands ecosystems include: Parque
Nacional (PN) Cuyamel-Omoa, PN Jeannette Kawas, Refugio de Vida Silvestre (RVS)
Cuero y Salado, PN Punto Izopo, Jardín Botánico Lancetilla, RVS Laguna de
Guaymoreto, Reserva de Hombre y la Biosfera Río Plátano, PN Patuca, PN Warunta,
Reserva Biológica (RB) Rus Rus, RB Laguna de Karataska, PN Río Kruta, Reserva de
Biosfera Tawahka-Asangni, Reserva de Biosfera Bosawas, Reserva Natural (RN) Cabo
Viejo-Tela Sulumas, RN Laguna Bismuna-Raya, and RN Laguna Pahara.
Pacific Lowlands. Corresponding to the Salvadoran Coastal Plain of the Chortís
Fore Arc Physiographic Province of Marshall (2007), the Pacific versant lowlands
consist of a relatively broad coastal plain extending from the western to the southern
limits of the Chortís Highlands province, becoming narrowest around the Gulf of
Fonseca. These lowlands constitute a single ecophysiographic region with a relatively
homogenized biota (Wilson & McCranie 1998; Sasa & Bolaños 2004; Townsend &
Wilson 2010b). The Pacific Lowlands are subject to the Lowland Dry climate regime
(Wilson & Meyer 1985), found from sea level to about 600 m elevation, with mean
annual precipitation below 2000 mm and mean annual temperature exceeding 24°C.
Important protected areas for Pacific Lowlands ecosystems include: Área Protegida con
Recursos Manejados Barra de Santiago, Parque Privada Walter T. Deininger, Área de
Protección y Restauración (APR) Nancuchiname, Área de Manejo Laguna El Jocotal,
APR Conchagua, Área de Manejo de Habitát de Especie (AMHE) Bahía de Chismuyo,
AMHE Bahía de San Lorenzo, AMHE Las Iguanas-Punta Condega, AMHE Los
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Delgaditos, AMHE El Jicarito, AMHE La Berbería, AMHE San Bernardo, and RN Delta
de Estero Real.
Salvadoran Cordillera. The Salvadoran Cordillera is not geomorphologically part
of the the Chortís Highlands, instead constituting the Chortís Volcanic Front and being
dominated by more recent Pliocene and Quaternary volcanic deposits (Marshall 2007). I
include the Salvadoran Cordillera for the sake of completeness in this discussion, given
its position across the Pacific Lowlands of El Salvador and putative inclusion in the
Eastern Nuclear Central America biogeographic province of Campbell (1999; as
expanded upon by Townsend 2006). This west-to-east oriented range is a continuation
of the Guatemalan Cordillera, and is made up of several dozen volcanic cones and
peaks, including Santa Ana (2,365 m), San Vincente (2,182 m), and San Miguel (2,130
m).
Cordillera Los Marabios. Like the Salvadoran Cordillera, this range not
geomorphologically part of the Chortís Highlands, and is represented by a string of
northwest-to-southeast oriented Quaternary (and in some cases active) volcanic cones
arising from the Pacific Lowlands of northwestern Nicaragua. Volcanoes in this
cordillera include Cosigüina (858 m), San Cristóbal (1,745 m), Casita (1,405 m), Telica
(1,060 m), Cerro Negro (726 m), El Hoyo (1,079 m), and Momotombo (1,279 m).
Watersheds. Major river systems on the Caribbean versant of the Chortís Block
include: Motagua (485 km), Chamelecón (200 km), Ulúa (300 km), Leán (60 km), Aguán
(225 km), Sico or Tinto or Negro or Grande (215 km), Plátano (85 km), Sikre (70 km),
Patuca (500 km), Warunta (85 km), Mocorón (92 km), Nacunta (65 km), Kruta (125 km),
Coco or Segovia or Wangki (550 km), Wawa (160 km), Kukalaya (140 km), Prinzapolka
46
(330 km), and Grande de Matagalpa or Awaltara (430 km). Major Pacific versant
watersheds include Estero Real (137 km), Negro (85 km), Choluteca (250 km),
Nacaome (90 km), Goascorán (115 km), Lempa (422 km) and Paz (134 km).
Lakes and coastal lagoons. There are very few large inland water bodies in the
Chortís Block, the most notable of which is Lago de Yojoa (700 m elevation) in central
Honduras. The two other large bodies of freshwater, Embalse El Cajón (285 m) in
Honduras and Lago de Apanás (970 m) in Nicaragua, are both reservoirs created by
hydroelectric dams. There are a number of large coastal lagoons and lagoon complexes
on the Caribbean coast, including Los Micos, Guaymoreto, Ibans, Brus, Tilbalakan,
Laguntara, Warunta, Tansín, Karataska, Kohunta, Bismuna, Pahara, Karatá, Huouhnta,
and Laguna de Las Perlas. I consider Lago de Izabal in Guatemala and Lago Xolotlán
(= Lago de Managua) in Nicaragua extralimital to the Chortís Block and do not include
them.
Islands. The principle islands associated with the Chortís Highlands include the
Honduran Islas de la Bahía (Utila, Roatán, Guanaja, and Cayos Cochinos), the Cayos
Miskitos of Nicaragua, and Isla El Tigre and other small islands of the Gulf of Fonseca.
Characterizing Ecological Associations: Holdridge Forest Formations
Forest formations described below follow the system developed by Holdridge
(1967), as applied to Honduras in previous works (Meyer & Wilson 1971, 1973; Wilson
& Meyer 1985; Wilson & McCranie 1998; Wilson et al. 2001; McCranie & Wilson 2002).
The widely used Holdridge (1967) system uses climatic, edaphic, and atmospheric
conditions to define and determine the distribution of terrestrial ecosystems. The Chortís
Block is typified by a wide range of climatic and elevational regimes, resulting in nine
Holdridge forest formations being recognized within the region. I am using this system,
47
described below, to partially define Chortís Block ecosystems, supplemented with other
published reports, gray literature, and my own observations.
Lowland Moist Forest. Commonly referred to as lowland rainforest, the Lowland
Moist Forest (LMF) formation is defined by a high mean annual temperature (>24°C),
high mean annual precipitation (>2000 mm; with no month of the year having
precipitation <50 mm), and by being found from sea level to about 600 m elevation. In
the Chortís Block, the LMF formation is restricted to the Caribbean versant, the majority
of remaining intact forest being found in the vast region of eastern Honduras and
Nicaragua known as La Mosquitia. In addition to lowland rainforest, the pine savannas
in La Mosquitia, open woodlands intersected by veins of gallery forest, are found within
the Lowland Moist Forest formation. Intact LMF is characterized by having a
heterogeneous canopy dominated by evergreen broadleaf trees regularly reaching 30–
40 m in height (Agüdelo C. 1987).
Lowland Dry Forest. The Lowland Dry Forest (LDF) formation includes habitat
commonly referred to as scrub forest, and is defined by high mean annual temperature
(>24°C), moderate but seasonally variable annual precipitation (1000–2000 mm; with at
least 3–4 months having precipitation <50 mm), and an elevational range of sea level to
about 600 m elevation. In the Chortís Block, the LDF formation is found on the Pacific
versant and in several interior valleys. Intact LDF is characterized by having a
heterogeneous canopy dominated by deciduous trees typically reaching around 25 m in
height (Agüdelo C. 1987).
Lowland Arid Forest. The Lowland Arid Forest (LAF) formation, commonly called
thorn forest, is defined by high mean annual temperature (>24°C), low annual
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precipitation (500–1000 mm; with at least 3–4 months having precipitation <50 mm),
and an elevation range of sea level to approximately 600 m elevation. This formation
has one of the most limited extents in the Chortís Block, known only from the Middle
Aguán Valley and the Upper Motagua Valley. Intact LAF is characterized by having a
low, heterogeneous canopy dominated by deciduous trees typically reaching around 10
m in height, with vegetation dominated by xeric-adapted plants such as cacti (Agüdelo
C. 1987).
Premontane Wet Forest. The Premontane Wet Forest (PWF) formation,
sometimes called highland rainforest (McCranie & Wilson 2002), is defined by a
moderate mean annual temperature (18°–24°C), high annual precipitation (>2000 mm),
and an elevational range of approximately 600 to 1500 m elevation. The PWF formation
bridges the LMF with higher elevation montane forests, and thus contains
characteristics of both. Intact PWF is characterized by having a closed canopy
dominated by evergreen broadleaf trees reaching 25–30 m in height, sometimes
reaching 40 m (Agüdelo C. 1987).
Premontane Moist Forest. The Premontane Moist Forest (PMF) formation,
commonly referred to as upland pine-oak forest, is defined by a moderate mean annual
temperature (18°–24°C), moderate annual precipitation (1000–2000 mm), and an
elevational range of about 600 to 1850 m elevation. The PMF formation is relatively
widespread in the Chortís Highlands, particularly on interior slopes. Various habitat
types are found within the PMF, and are defined below following the classification
system of Carr (1950).
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Premontane Dry Forest. The Premontane Dry Forest (PDF) formation, which can
be termed ―upland scrub forest,‖ is defined by moderate mean annual temperature
(18°–24°C), low annual precipitation (500–1000 mm), and an elevation range of
approximately 600 to 1250 m elevation. This habitat is generally limited to the upper
periphery of some xeric interior valleys that otherwise support LDF or LAF, two
formations with which PDF shares its typical characteristics.
Lower Montane Wet Forest. The Lower Montane Wet Forest (LMWF) formation,
is defined by having a low mean annual temperature (12°–18°C), high annual
precipitation (>2000 mm), and an elevation range of approximately 1500 to 2700 m
elevation (note: habitat typical of this formation can also occur at lower elevations,
particularly in the Cordillera Nombre de Dios). In the Chortís Highlands, LMWF is
primarily distributed on the Caribbean versant, being replaced by Lower Montane Moist
Forest (below) in the somewhat drier Pacific versant highlands. Intact LMWF is
characterized by having a closed canopy dominated by evergreen broadleaf trees
reaching 50 m in height (Agüdelo C. 1987).
Lower Montane Moist Forest. The Lower Montane Moist Forest (LMMF)
formation, also referred to as cloud forest or montane forest, is defined by having a low
mean annual temperature (12°–18°C), moderate annual precipitation (1000–2000 mm),
and an elevation range of approximately 1500 to 2700 m elevation. In the Chortís
Highlands, LMMF is distributed in highland areas, typically on the Pacific versant and on
the leeward slopes of some of the interior-most Caribbean versant peaks. The LMMF
formation contains both pine and broadleaf dominated habitats (better characterized
using the classification system of Carr 1950).
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Montane Rainforest. The Montane Rainforest (MRF) formation is defined by
having a very low mean annual temperature (6°–12°C), high annual precipitation (>2000
mm), and an elevation range of above approximately 2700 m elevation. This formation
is the most geographically limited formation in the Chortís Highlands, being restricted to
the highest slopes of Cerro Celaque (Honduras; maximum elevation 2,849 m), Cerro
Santa Bárbara (Honduras; maximum elevation 2,744 m), and Cerro El Pital (El
Salvador and Honduras; maximum elevation 2,730 m).
Characterizing Ecological Associations: Updating and Operationalizing the Carr (1950) System for Classifying Honduran Ecosystems
Based on four years of first-hand observation made during his time as a professor
at Escuela Agrícola Panamericana (Zamorano), Carr (1950) presented a preliminary
characterization of the ecosystems of Honduras. Carr’s initial interest was in
―determining and attempting to define herpetological habitats,‖ which expanded to
generalize the habitats so as to ―help the visiting naturalist in his preliminary
reconnaissance and shorten his orientation period‖ (Carr, 1950: 569). This work was
the first to classify ecological associations in Honduras, and the accuracy of Carr’s
observations is such as to allow for his ―outline‖ to be developed into an operational
system for classifying animal habitats in Honduras and the greater Chortís Block. As
opposed to the Holdridge (1967) system, the Carr (1950) system is descriptive and is
designed with the intent of being modified and contextualized by specialists to fit their
particular study system or taxonomic group. I developed such an operational system,
which I will refer to as the Carr Classification System for Honduran Ecological
Associations or simply the Carr System, based on a synthesis of the available literature
51
and my own observations from 1999–2011. This system is discussed below, and the
habitat names defined here are used throughout this dissertation.
Lowland-associated Habitats
Selva or Lowland Broadleaf Rainforest. Found primarily within the Lowland
Moist Forest (LMF) formation in the Caribbean Lowlands, selva is characterized by a
tall, multi-layered, closed-canopy that is dominated by evergreen broadleaf trees, with
upper canopy trees normally reaching 30–40 m (Agüdelo C. 1987, Mejía-Ordóñez &
House 2002) and reaching 60 m in some areas (Carr 1950, Wilson & Meyer 1985).
Large expanses of selva are found within Reserva de Hombre y la Biosfera Río Plátano,
PN Patuca, PN Warunta, Reserva Biológica (RB) Rus Rus, Reserva de Biosfera
Tawahka-Asangni, and Reserva de Biosfera Bosawas. Mejía-Ordóñez & House (2002)
listed the following tree species as typical of Honduran selva: Brosimun alicastrum,
Bursera simarouba, Calophyllum brasiliense, Cedrela odorata, Coccoloba anisophylla,
Cordia alliodora, Ficus colubrinae, Ficus insipida, Ficus tonduzii, Guarea grandifolia,
Hernandia stenura, Licania platypus, Luehea candida, Nectandra sp., Ocroma
pyranidale, Pithecoellobium donnel-smithii, Pouteria campechiana, Pouteria sapota,
Rinorea guatemalensis, Symphonia globulifera, Swietenia macrophilla, Tabebuia
chrysantha, Terminalia amazonia, Virola koshnyi and Vochysia hondurensis; the
relatively open understory is made up of palms (Acoelorrhaphe wrightii, Chamaedorea
spp., Bactris spp., and Geonoma spp.), woody plants (Cespedesia macrophylla, Isertia
haenkeana, Piper spp., Cephaelis spp., Psychotria spp.), and herbaceous plants
(Adiantum spp., Polypodium spp., Begonia spp., Selaginella spp., Philodendron spp.,
and Syngonium spp.).
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Figure 2-7. Ecological associations of the Chortís Block I. A) Selva or Lowland
Broadleaf Forest; Río Tapalwás, Reserva Biológica Rus Rus, Depto. Gracias a Dios, 180 m; Lowland Moist Forest formation. B) Mosquitia Pine Savanna; between Rus Rus and Awasbila, with the Montañas de Colón in the background, Depto. Gracias a Dios, 200 m; Lowland Moist Forest formation. C) Coastal Scrub; Caribbean coast near Kaukira, Depto. Gracias a Dios; Lowland Moist Forest formation. D) Mangrove Swamp, near mouth of the Río Kruta, Depto. Gracias a Dios; Lowland Moist Forest formation. E) Seasonal Deciduous Forest; near Teocintecito, Depto. Olancho, 690 m; Premontane Dry Forest formation. F) Freshwater Swamp in Seasonal Deciduous Forest; seepage bog in the upper Valle de Agalta, northeast of Saguay, Depto. Olancho, 570 m; Premontane Dry Forest formation. Photos © J.H. Townsend.
53
Mosquitia Pine Savannas. Although wholly classified as a rainforest area by
Wilson & Townsend (2006) due to being found within the Lowland Moist Forest
formation, the Mosquitia of eastern Honduras and Nicaragua supports large areas of
Pinus caribaea savanna that bear a stronger resemblance to subhumid ecosystems
than to rainforests (Parsons 1955, Zamora Villalobos 2000, Townsend & Wilson 2010b).
The Mosquitia pine savannas resemble an open woodland dominated by P. caribaea,
with a mix of broadleaf trees and shrubs including Agarista mexicana var pinetorum,
Amaioua corymbosa, Arthrostemma ciliatum, Arundinella deppeana, Byrsonima
crassifolia, B. verbasifolia, Calea integrifolia, Cecropia peltata, Cephaelis tomentosa,
Chamaecrista nictitans, Clethra calocephala, Clidemia sericea, Cococypsellum sp.,
Cuphea pinetorum, Davilla kunthii, Guazuma ulmifolia, Gnaphalium semiamplexicaule,
Lasianthaeas fruticosa, Lobelia laxiflora, Miconia albicans, M. glaberrima, Myrica
cerifera, Psychotria suerrensis, Quercus oleoides, Salvia sp., Vernonia agyropappa,
Vigna vexillata, and Xylopia frutescens, with an open understory of fire-tolerant grasses
(Poaceae) and sedges (Cyperaceae), particularly Paspalum pectinatum, Blechnum
serrulatum, Rhynchospora rugosa, Rhynchospora bulbosa, Scleria cyperina, and
Setaria geniculata (Parsons 1955; Zamora Villalobos 2000; Mejía-Ordóñez & House
2002). Herpetofaunal diversity present in the Mosquitia pine savannas is almost
completely congruent with that of the subhumid forests of the intermontane valleys
(Townsend & Wilson 2010b), and phylogenetic analyses of subhumid-specialized taxa
support conspecific relationships among Pacific and pine savanna populations (Incilius
coccifer, Mendelson et al. 2005; Porthidium ophryomegas, Castoe et al. 2005).
Townsend & Wilson (2010b: 702) presented two principal, and as-yet untested,
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hypotheses for explaining the apparent continuing connectivity between the Pacific
lowlands, subhumid intermontane valleys, and Mosquitia pina savannas:
1) The existence subhumid ―corridor‖ located in Nicaragua between the southern
end of the Nuclear Middle American highlands and Lago de Nicaragua, allowing for
dispersal of subhumid species from the Pacific Lowlands of Honduras, El Salvador and
Nicaragua to the pine savannas of the Nicaraguan Mosquitia, which is contiguous with
pine savannas extending to the northern coast of Honduras.
2) Utilization of open areas along large rivers (Patuca, Coco, and Grande de
Matagalpa) that have their upper reaches in subhumid areas as routes for dispersal.
These rivers originate in subhumid intermontane valleys in the Chortís Highlands,
flowing through extensive areas of broadleaf rainforest and on through pine savannas of
La Mosquitia. Secondary connectivity may also occur through coastal strand habitat,
which creates a network among individual river drainages at or near their mouths.
Broadleaf Swamp Forest. These swamp forests are found along poorly-drained
margins and backwater areas of large rivers, with notable expanses of Broadleaf
Swamp Forest found along the Río Patuca in Reserva de Hombre y la Biosfera Río
Plátano, as well as along Río Kruta and in PN Jeannette Kawas. While riverine swamp
forests are restricted to the LMF in the Caribbean Lowlands, there is also broadleaf
swamp forest at the northern and southern ends of Lago de Yojoa (700 m elevation), at
the lower edge of the Premontane Wet Forest (PWF) formation. Mejía-Ordóñez &
House (2002) listed the following species as being found in permanently inundated
broadleaf swamp forest: the trees Crias cauliflora, Pachira aquatica, Pterocarpus
hayesii, and Pterocarpus officinalis, and the palms Roystonea dunlapiana, R. regia var
55
hondurensis, Acoelorrhaphe wrightii, and Desmoncus orthacantus. The following are
found in seasonally inundated broadleaf swamp forest: the trees Castilla elastica,
Coccoloba sp., Combretum cacoucia, Symphonia globulifera, and Vochysia ferruginea;
and in the flooded forests at the northern end of Lago de Yojoa are found the tree
Erythrina fusca and an understory including Calathea spp., Costus spp., Heliconia spp.,
Hymenocallis litoralis, Maranta spp., Thalia geniculata, Smilax spp., Philodendron spp.,
and Syngonium spp.
Palm Swamp. A variety of palm-dominated swamp forests occur in coastal areas.
Tique palm swamps are dominated by the tique (Acoelorrhaphe wrightii), or paurotis
palm, in association with Annona glabra, Chrysobalanus icaco, Coccoloba uvifera,
Conocarpus erectus, Dalbergia ecastaphylla, Dalbergia monetaria, Davilla kunthii,
Morinda citrifolia, Doliocarpus guianensis, Eugenia aeruginea, Henriettea succosa,
Miconia glaberrima, Miconia albicans, Montrichardia arborescens, Myrmecophila
wendlandii, Palicourea tripilla, Symphonia globulifera, Terminalia bucidoides, Thrinax
parviflora, Tococa guianensis, Clidemia sericea, Acrocomia mexicana, Bursera
simaruba, Casearia sylvestris, Chrysophyllum mexicanum, Cordia alliodora, C.
curassavica, Hibiscus tiliaceus, and Ochroma pyramidala (Mejía-Ordóñez & House
2002). Seasonally inundated mixed broadleaf-palm swamps near the Río Kruta and
Cabo Gracias a Dios can have a 40–50 m high canopy dominated by the palm
Roystonea dunlapiana and the understory palm Acoelorrhaphe wrightii, as well as
Mimosa schomburki, Psychotria spp., Alibertia edulis, Spondias mombim, Pachira
aquatica, Desmoncus orthacantus, Bactris sp., Ficus sp., Calophyllum brasiliense,
Coccoloba schiedeana., Hirtella racemosa, Xylopia frutescens, Dialium guianensise,
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Virola koschnyi, Annona glabra, Grias integrifolia, Dalbergia ecastaphyllum, and Trophis
racemosa. In defining the Huiscoyol Swamp as a habitat, Carr (1950: 587) described
thick stands of slender Bactris palms (called huiscoyol in Costa Rica) with ―ghastly,
glass-hard stem spines‖ and recounts one of his most ―harrowing misadventures‖ being
lost in the ―dreary and forbidding environment‖ of a Bactris swamp.
Coastal Scrub. A heterogeneous habitat association found above the beach-line
along the Caribbean coast, Islas de la Bahía, Cayos Cochinos, and Cayos Miskitos,
Coastal Scrub includes low coastal strand forest (typical plants include: Cannavalia
maritima, C. rosea, Euphorbia buxifolia, Ipomoea pescaprae, Sesuvium portulacastrum,
Sporobolus virginicus, Chrysobalanus icaco, Coccoloba uvifera, Citharexylum
caudatum, Hybiscus tiliaceus and Phyllanthus acidus) and its associated grass-covered
dune system (typical ground cover includes Andropogon brevifolius, Aristida sp.,
Eleocharis sp., Eragrostis sp., Fimbristylis spadicea, and Paspalum sp.). This
association is found in relatively long, undisturbed extensions along essentially the
entire Caribbean coast of the Chortís Highlands (Mejía-Ordóñez & House 2002). Carr
(1950) described the somewhat peculiar and specialized coastal scrub habitat found on
Isla El Tigre in the Gulf of Fonseca and a few exposed hillsides facing the gulf as a
distinctive habitat association: Sea-Breeze Scrub Forest. While this forest lies within the
Lowland Dry Forest (LDF) formation, the forest receives most of its moisture in the form
of occult precipitation brought in on Pacific winds. Common plant species include
Bursera simarouba, Cresentia alata, Enterolobium saman, Spondias purpurea, Prosopis
juliflora, Acacia spp., Heamatoxilon brasiletti, and Zizyphum sp.
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Mangrove Swamp. These estuarine swamp forests are found along both the
Caribbean and Pacific coasts. Mangrove swamp communities on both coasts typically
include the mangroves Avicennia germinans and Rhizophora mangle, with Caribbean
swamps including salt-tolerant species such as Laguncularia racemosa, Acrostichum
aureum, Cecropia spp., and Coccoloba uvifera, and Pacific mangroves similarly
accompanied by Sesuvium portulacastrum, Sporobolus virginicus, Acrostichum aureum,
Cecropia spp., Coccoloba uvifera, Conocarpus erectus, and Laguncularia racemosa
(Mejía-Ordóñez & House 2002).
Habitats Shared Between Lowlands and the Chortís Highlands
Vegas and Gallery Forest. This association is found on rich alluvial soils along
stream and river courses, and in areas of low relief around the confluence of two
streams (a vega). I tentatively include Carr’s (1950) habitat classes Dry Gullies and
Fence Rows and Hondonadas in this category, recognizing that all of the constituent
associations are essentially arteries of mesic habitat, often through comparatively xeric
areas. Frequent plants of Caribbean Lowland vegas and gallery forests include Carapa
guianensis, Hirtella racemosa, Xylopia frutescens, Dentropanax arboreus, Dialium
guianense, Ficus sp., Licania platipus, Ochroma lagopus, Pterocarpus rohrii,
Symphonia globulifera, Vochysia hondurensis, Schizolobium parahybum, Cecropia
obtusifolia, Hyeronima alcornoides, Lacmellea panamensis, Prioria copaifera,
Enterolobium schomburki, Apeiba membranaceae, Casearia sylvestris, Cedrela
macrophilla, Dendropanax arboreus, Vismia macrophylla, Xylopia frutescens, and
Zuelania guidonia (Mejía-Ordóñez & House 2002).
Carr (1950: 588) observed that these types of alluvial forest appeared to serve as
―mesic highways for the rainforest biota,‖ that might ―afford often contiguous connection
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Figure 2-8. Ecological associations of the Chortís Block II. A) Thorn Scrub Forest, upper Valle de Aguán, northwest of Coyoles Central, Depto. Yoro, 250 m; Lowland Arid Forest formation. B) Pantano or Freshwater Marsh, northern end of Lago de Yojoa, with the Montañas de Meámbar in the background, Depto. Cortés, 640 m. C) Infrequently burned Ocotal, near Guaymas, Depto. Francisco Morazán, 1,450 m; Premontane Moist Forest formation. D) Frequently burned Ocotal, Cerro de las Cruces, Depto. Olancho, 1,260 m; Premontane Moist Forest formation. E) Broadleaf Transitional Forest, La Liberación, Refugio de Vida Silvestre Texíguat, Depto. Atlántida, 1,030 m; Premontane Wet Forest formation. F) Mixed Transitional Forest, Montaña de Jacaleapa, Depto. Olancho, 1,120 m; Premontane Wet Forest formation. Photos © J.H. Townsend.
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between lower tropical rainforest and upper tropical cloud forest,‖ and therefore ―must
be of prime importance in the ecology of the region.‖ In light of over 60 years of
advancement in our knowledge and understanding, Carr’s insights are still grounds
generating biogeographic hypotheses testable with modern molecular methods.
Seasonal Deciduous Forest. Called Monsoon forest by Carr (1950) and
commonly referred to as tropical dry forest, this habitat has a distribution limited to the
Lowland Dry Forest and Premontane Dry Forest formations in the intermontane valleys
and on the Pacific Lowlands. Mejía-Ordóñez & House (2002) reported the following
species as frequent in Seasonal Deciduous Forest: Enterolobium cyclocarpun, Bursera
simarouba, Ceiba pentandra, Cordia alliodora, Lysiloma auritum, Lysiloma seemanii,
Samanea saman, Swetenia macrophylla, Cochlospermum vitifolium, Gyrocarpus
americana, Apeiba membranacea, Alvaradoa amorphoides, Calycophylum
candidissimum, Tabebuia neochrysanta, Samanea saman, Spondias mombin,
Lonchocarus minimiflorus, and Guazuma ulmifolia.
Thorn Scrub Forest. This low (<4 m in canopy height) habitat is dominated by
spine-bearing shrub-like trees such as Pachycereus sp., Hylocereun spp., Mammillaria
spp., and Opuntia spp., and dry tolerant shrubs and herbaceous plants like Ananas sp.,
Argyreia especiosa, Cnidoscolus tubulosus, Digitaia insularis, Epidendrum xipheses,
Evolvulus sp. Gonolobus sp., Acacia farnesiana, Albizzia neopoides, Combretum
fruticosum, Diphysa ribinoides, Jacquinia macricarpa, Karwinskia calderonii,
Lepidagastris alopecuroidea, Loeselia sp., Melanthera nivea, Thouviinidium decandrum,
and Watheria americana (Mejía-Ordóñez & House 2002). Thorn Scrub Forest is
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restricted to the Lowland Arid Forest and Lowland Dry Forest formations in the
intermontane valleys of the Chortís Highlands.
Pantano or Freshwater Marsh. Freshwater marshes dominated by Typha
domingensis, Phragmites australis, and/or Thalia geniculata form an expansive habitat
association in some areas, especially the wide alluvial plains of La Mosquitia (Carr
1950; Zamora Villalobos 2000; Mejía-Ordóñez & House 2002). Other grasses present
include Andropogon brevifolius, Aristida sp., Eleocharis sp., Eragrostis sp., Fimbristylis
spadicea y Paspalum sp. (Mejía-Ordóñez & House 2002). In La Mosquitia, the vast
pantanos have a similar character to that of the Florida Everglades, including being
dotted with islands of pine (Pinus caribaea) or paurotis palms (Acoelorrhaphe wrightii),
with extensive areas of habitat found around the Laguna de Karataska, the Río Kruta,
and the lower Río Coco.
Habitats of the Chortís Highlands
Ocotal. The ubiquitous Mesoamerican pine-oak forests are found throughout
moderate elevation areas of the serranía and are dominated by ocote pine (Pinus
oocarpa), with representation from P. pseudostrobus and other pines at higher
elevations. Ocotales are extensively distributed in the serranía in the Premontane Moist
Forest formation, and peripherally in the Premontane Dry Forest and Lower Montane
Moist Forest formations, roughly between 800 and 1,600 m elevation. Ocotal is subject
to regular burning by humans, in some areas annually, and, therefore, the biotic
composition is limited to species able to tolerate or escape frequent fires. Besides
pines, the various species of oaks (Quercus spp.) and the hardwood trees and
herbaceous plants Acacia farnesiana, Brahea salvadorensis, Byrsonima crassifolia,
Clethra occidentalis, Myrica cerifera, Enterolobium cyclocarpun, Eritrina berteroana,
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Ficus spp. Lysiloma auritum, Mimosa tenuiflora, Psidum guianense, and Tabebuia
chrysantha are typically found in ocotales (Mejía-Ordóñez & House 2002). Carr (1950)
identified a number of subdivisions of the Ocotal habitat, including shaded ocotal, park
ocotal, ocotal steppe, and ocotal-pedregal, based on edaphic and climatic variation as
well as burn frequency.
Mixed Transitional Cloud Forest. This transitional forest between ocotales and
cloud forest, which Carr (1950) called High Ocotal association, is essentially a humid
ocotal with higher concentrations of bromeliads and other epiphytes, as well as a
denser and more diverse understory. High ocotales are typically found within the
Premontane Moist Forest and Lower Montane Moist Forest formations, between around
1,000–1,500 m elevation on the Caribbean versant and 1,200–1,800 m on the Pacific
versant. Trees of mixed transitional forest include the pines Pinus oocarpa, P.
pseudostrobus, and P. tecunumanii, the hardwoods Arbutus xalapensis, Clethra
macrophylla, Ficus aurea, Heliocarpus apendiculatus, Oreopanax lachnocephalus,
Oreopanax xalapensis, and Quercus cortesii, and an understory that includes Buddleia
americana, Conostegia sp., Miconia sp., Psychotria macrophylla, Vernonia
arborescens, Calyptranthes hondurensis, Lobelia laxiflora, Piper launosum, and
Verbesina sp. (Mejía-Ordóñez & House 2002). In addition to High Ocotales, Carr (1950)
identified two other types of transitional forest, Pinabetales and ―Diquidambales‖ (=
Liquidambales), which I recognize as distinctive localized associations within Pinus and
Liquidambar Transitional Cloud Forest. Pinabetales are ridge-line groves dominated by
the pinabete pine (Pinus pseudostrobus) having epiphyte and understory communities
similar to those of the High Ocotal association, but also incorporating representative
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from higher elevation hardwood forests. Pinabetales are typically found between 1200–
1600 m within the Premontane Moist Forest and Lower Montane Moist Forest
formations. Besides P. pseudostrobus, the pines P. maximinoi and P. tecunumanii can
also be present, as might plants otherwise characteristic of both ocotales and mixed
cloud forest. Liquidambales have a similar composition to Pinabetales, but are
dominated by sweet-gums (Liquidambar styraciflua) and are more typical of leeward
slopes than exposed ridges.
Broadleaf Transitional Cloud Forest. Also referred to as Premontane rainforest,
this high diversity forest blends diversity from both selva below and the cloud forest
above. It is found primarily in the Premontane Wet Forest formation from between 500
m and 1,500 m in elevation, primarily on the windward slopes of mountains along the
Caribbean versant.
Broadleaf Cloud Forest. This is be considered the ―typical‖ cloud forest of the
Lower Montane Wet Forest (LMWF) and Lower Montane Moist Forest (LMMF)
formations, characteristically found between around 1,500–2,300 m elevation on the
Caribbean versant and 1,800–2,600 m elevation on the Pacific versant. This forest
characteristically has a high diversity of large canopy trees, with canopy heights
regularly reaching 40–50 m. Typical vegetation of Broadleaf Cloud Forest in LMWF
includes the trees Alnus arguta, A. jorullensis, Cornus sp. Prunus sp., Olmediella
betschieriana, Abies guatemalensis, Taxus globosa, Podocarpus oleifolius, Acalypha
firmula, Bocona glaucifolia, Cleyera theaeoides, Weinmannia pinnata, W. tuerckheimii,
Daphnopsis strigillosa, Fuchsia paniculata, F. splendens, Hedyosmun mexicanum,
Hoffmannia lineolata, Miconia glaberina, Quercus cortesii, Q. lancifolia, Q. laurina,
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Figure 2-9. Ecological associations of the Chortís Highlands. A) Broadleaf Cloud Forest, above Quebrada Varsovia, Montañas de Meámbar, Depto. Comayagua, 1,620 m; Lower Montane Wet Forest formation. B) Broadleaf Cloud Forest, canyon across top of Montañas de Santa Bárbara, Depto. Santa Bárbara, 2,190 m; Lower Montane Wet Forest formation. C) Broadleaf Cloud Forest, Montaña de Botaderos, Depto. Olancho, 1,715 m; Lower Montane Wet Forest formation. D) Mixed Cloud Forest, Quebrada Cataguana, Montañas de Yoro, Depto. Francisco Morazán, 1,860 m; Lower Montane Wet Forest formation. E) Mixed Cloud Forest, Sierra de Omoa, Depto. Cortés, 1,660 m; Lower Montane Wet Forest formation. F) Mixed Cloud Forest, Sierra de Celaque, Depto. Lempira, 2,130 m; Lower Montane Moist Forest formation. G) Río Arcagual in Mixed Cloud Forest, Sierra de Celaque, Depto. Lempira, 2,580 m; Lower Montane Wet Forest formation. H) Hepatic Forest, Sierra de Celaque, Depto. Lempira, 2,780 m; Montane Rainforest formation. I) Heather Wind Scrub, Montaña Macuzal, Depto. Yoro, 1,730 m; Lower Montane Wet Forest formation. Photos © J.H. Townsend.
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Rondeletia buddleioides, R. laniflora, Rubus eriocarpus, and Saurauia kegeliana, the
herbaceous plants Senecio jurgensenii, Smilax spinosa, Ternstroemia megaloptycha,
Begonia convallariodora, B. fusea, B. oaxacana, Cibotium regale, Deppea grandiflora,
Lobelia nubicola, L. tatea, Parathesis hondurensis, and Peperomia spp., and the ferns
Adiantum piretii, Asplenium harpeodes, A. olivaceum, A. pterocarpus, Blechnum
lehmannii, and Elaphoglossum eximium (Mejía-Ordóñez & House 2002). From
Broadleaf Cloud Forest in LMMF on the Pacific versant, Mejía-Ordóñez & House (2002)
listed the following species as common in PN La Tigra in the Sierra de Lepaterique:
Mauria sessiflora, Ilex chiapensis, Ilex williamsii, Oreopanax xalapensis, Carpinus
caroliniana var tropicalis, Weinmannia balbisina, Hieronyma guatemalensis, Hieronyma
poasana, Quercus cortesii, Q. lanciflia, Q. laurrina, Q. bumelioides, Homalium
racemosum, Olmediella betschieriana, Calatola laevigata, Nectandra heydeana, Ocotea
veraguensis, Phoebe helicterifolia, Magnolia hondurensis, Miconia argentea, Guarea
pittieri, Trophis chorizantha, Ardisia paschalis, Chamaedorea pinnatifrons, Clusia rosea,
Lophosoria quadripionnata, and Cyathea mexicana.
Mixed Cloud Forest. Called Bosque mixto by Mejía-Valdivieso (2001), Mixed
Cloud Forest is typically found within the Lower Montane Wet Forest and Lower
Montane Moist Forest formations, between above about 1,500 m elevation on the
Caribbean versant and 1,800 m on the Pacific versant up to around 2,500 m on both
versants. Trees of Mixed Cloud Forest include the pines Pinus pseudostrobus, P.
tecunumanii, and P. ayacahuite, with a high diversity of oaks (Quercus brumeliodes, Q.
cortesii, Q. rugosa, Q. sapotifolia, and Q. acutifolia) and other hardwoods including
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Arbutus xalapensis, Bernoulia flamea, Brunellia mexicana, Clusia spp., Cornus
discifolia, Cyrilla racemiflora, Dendropanax arboreus, Dendropanax hondurensis,
Hedyosmun mexicanum, Magnolia sp., Liquidambar styraciflua, Myrica cerifera, Ocotea
sp., Oreopanax caspitatus, O. xalapensis, O. lachnocephalus, Picramnia teapensis,
Symplocos vernicosa, Toxicodendron striatum, Viasmia baccifera, and Weinmannia
pinnata (Mejía-Ordóñez & House 2002). At elevations exceeding 2,300 m, particularly
on Cerro Celaque and Montaña de Santa Bárbara, Laurasian trees at the southernmost
extent of their range, such as firs (Abies guatemalensis) and yews (Taxus globosa), are
found syntopically with Gondwanan trees at their northern distributional limit (e.g.
Podocarpus oleifolius).
Coniferous Cloud Forest. This is a rarely encountered association that is
characterized by essentially pure stands of pines (Pinus hartwegii, P. maximinoi, and P.
ayacahuite) as well as other conifers (Cupressus lusitanica and Taxus globosa) and is
recorded from only a few drier, open ridges above 2,400 m on Cerro Celaque and
Montaña de Santa Bárbara (Mejía-Valdivieso 2001). It is called Bosque de coníferas by
Mejía-Valdivieso (2001), who described these stands as appearing to be subject to
natural fires every 3–5 years. I encountered Coniferous Cloud Forest meeting this
description between 1900–2100 m elevation on the southeastern side of Montaña de
Yoro, and within this recently burned high pine forest collected herpetofaunal species
otherwise considered endemic to nearby Broadleaf Cloud Forest.
Montane Mixed Forest. The habitat of the uppermost reaches of LMWF (>2,600
m) and the Montane Rainforest formation, Bosque mixto montano alto Mejía-Valdivieso
(2001) is dominated by the primitive conifers Abies guatemalensis, Taxus globosa, and
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Podocarpus oleifolius, the pines Pinus ayacahuite, P. hartwegii, P. maximinoi, and P.
tecunumanii, and the broadleaf trees Alnus arguta, Cornus sp., Prunus sp., Olmediella
betschieriana, Oreopanax lempirana, Acalypha firmula, Alnus jorullensis, Bocona
glaucifolia, Cleyera theaeoides, Weinmannia pinnata, W. tuerckheimii, Daphnopsis
strigillosa, Fuchsia paniculata, F. splendens, Hedyosmun mexicanum, Hoffmannia
lineolata, Miconia glaberina, Quercus cortesii, Q. lancifolia, Q. laurina, Rondeletia
buddleioides, R. laniflora, Rubus eriocarpus, and Saurauia kegeliana (Mejía-Ordóñez &
House 2002). This habitat is limited to high elevation on Cerro Celaque, Cerro El Pital,
and Montaña de Santa Bárbara.
Hepatic Forest. A type of mountain-top dwarf forest, Hepatic, or Mossy, Forest
(Bosque hepático o musgoso of Mejía-Valdivieso 2001), that appears to be restricted to
the wet upper slopes of the tallest peaks, including at least Cerro La Picucha (2,100–
2,200 m) in the Sierra de Agalta, Cerro Celaque (2,700 m), and Cerro Jilinco (2,200 m)
and Cerro Cusuco (1,990 m) in the Sierra de Omoa (Mejía-Valdivieso 2001, Townsend
& Wilson 2008). The canopy does not exceed 10 m in height and is typically shorter,
with trees taking on a twisted appearance. Nearly all available surface area is covered,
even layered, in epiphytic plants and fungi, up to 50% of which can be liverworts
(Marchantiophyta; Mejía-Valdivieso 2001). In some cases, this luxuriant epiphytic
community creates a living exoskeleton that remains long after the death and decay of
the tree within. Hepatic Forest is often found in association with Heather Wind Scrub,
and appears to be a transitional habitat between the exposed scrub and the cloud forest
below.
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Heather Wind Scrub. Found on exposed portions of the highest peaks, this is a
wind-swept association that Carr (1950) termed Peña Wind Scrub and is variously
referred to as elfin forest or dwarf forest (Townsend & Wilson 2006, 2008), names that
reflect the somehow mystic character of these mountain-top ecosystems. Carr’s (1950:
582) own description of this habitat artfully captures this character:
It is a seemingly incongruous combination of dwarfed and twisted microphyllous and sclerophyllous trees and shrubs, Ericaceae, Myrtiaceae, Myrsinaceae, and the like, implying xeric conditions, but with an astounding array of mosses, filmy ferns, selaginellas, and similar delicate hygrophyllous epiphytes. Although at first glance this is an altogether ill-assorted looking flora, the incongruity is only apparent, since each of the two floristic elements is in its own way adapted to withstand drastic reversals in its water economy. On these peñas the wind blows almost constantly, often violently, and while it usually brings in abundance of moisture, it imposes a heavy penalty when the supply fails for even a short period. The wind-pruned trees meet the situation by conservation of their moisture, while their cryptogamic guests yield freely to desiccation, lapsing into dormancy almost on a moment's notice, and without permanent injury.
As indicated by the name, this habitat is dominated by plants in the family Ericaceae
with a 2–4 m tall ―canopy,‖ with the thick ―understory‖ being comprised of a bewildering
array of bromeliads and other epiphytes. This habitat association is known from Cerro
La Picucha (2,200+ m) in the Sierra de Agalta, Cerro Azul Meámbar (1,950 m+), Cerro
Celaque (various exposed ridges above 2,700 m), and Cerro Jilinco (2,240 m) and
Cerro Cusuco (2,010 m) in the Sierra de Omoa (Hazlett 1980, Mejía-Valdivieso 2001,
Townsend & Wilson 2006). Heather Wind Scrub likely is found in at least small patches
on the tops of most exposed peaks above around 1,900 m elevation.
Elfin Forest. This term is herein reserved for use to describe the unique forest
association found on Cerro La Picucha in the highest portions of the Sierra de Agalta.
Delineated as Bosque enano by Mejía-Valdivieso (2001), this habitat superficially
resembles the Heather Wind Scrub in having a ―canopy‖ not exceeding 3 m in height;
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however, in place of Ericaceae, this true dwarf forest is made up of twisted, epiphyte
covered, bonsai-like versions of the trees Billia hippocastanum, Podocarpus oleifolius,
and Pinus hartwegii, with exposed ground covered in clubmosses (Huperzia and
Lycopodium) and dense patches of ground-dwelling tank bromeliads.
Introduction to Biodiversity of the Chortís Block
Given the wide variation in physiographic and ecological attributes that are evident
in the Chortís Block, it comes as little surprise that the region also supports a rich and
diverse biota. While the Caribbean and Pacific lowlands have biotas that are typically
characterized as being composed of relatively widespread species from both the west
and south, the Chortís Highlands and associated piedmont is an area of considerable
endemic biodiversity.
While investigation of the endemic fauna of the Chortís Highlands has been limited
compared with other areas of the Neotropics, particularly southern Central America, the
dedicated work of a small group of specialists led to the documentation of endemism
across a variety of taxonomic groups. Botanical data may support this better than other
groups, with over 263 described endemic species found in Honduras alone (Nelson-S.
2001, 2008). Areas of elevated plant endemism include mesic highland forests and
xeric intermontane valleys of the Chortís Highlands, and, in particular, the piedmont of
the Cordillera Nombre de Dios (Nelson-S. 2008). Despite the high degree of localized
plant endemism seen across the Chortís Highlands, to date there has been no
published analysis of biogeographic patterns among these taxa. Over 166 native
freshwater fishes have been documented from Honduras, including three described and
at least six undescribed endemic species (Martin 1972, Matamoros et al. 2009,
Matamoros & Schaefer 2010). Among terrestrial vertebrates, birds (one species;
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Monroe 1968) and mammals (three species; Goodwin 1942, Reid 2009) stand out in
having very few described endemic species; however, at least for mammals, this low
level of endemism is almost certainly an artifact of a lack of focused sampling in the
molecular age, particularly for small mammals, by systematic mammalogists in the
Chortís Highlands.
It is the herpetofauna, the amphibians and reptiles, which provides the best
opportunity for elucidating patterns of evolutionary diversification in the Chortís Block.
Systematic herpetologists have been active in the Chortís Block since at least the early
1900’s, and, in Townsend & Wilson (2010a), I detailed the history of herpetological
exploration and research in Honduras. My own work in the Chortís Block began as a
student of Dr. Wilson’s in 1999, and had progressed to the point where, when I began
this dissertation in 2006, I had identified that the Chortís Block, and particularly the
isolated cloud forests of the Chortís Highlands, as being in serious need of intensive
study using molecular-based approaches. However, taking an approach that was both
broad and comprehensive in terms of taxonomic coverage required that virtually all the
areas of the Chortís Block, principally those that were known to support endemic
species, would be sampled or resampled. This sampling was carried out from 2006–
2011, and the results are presented herein.
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CHAPTER 3 TAXONOMIC DIVERSITY, DISTRIBUTIONAL PATTERNS, AND CONSERVATION
STATUS OF THE CHORTÍS BLOCK HERPETOFAUNA
The constituent countries of the Chortís Block (El Salvador, Guatemala, Honduras,
and Nicaragua) each have their own rich histories of herpetological investigation
(Mertens 1952, Stuart 1963, Meyer 1969, Villa 1972, Wilson et al. 2010). Most research
has expectedly taken a geopolitically-delimited approach that is often arbitrary and is
seldom congruent with biogeographic boundaries. While this approach is practical and
largely necessary due to a variety of considerations (e.g., visas, research and export
permits, logistics), it can also come at the expense of a biogeographically-meaningful
approach to research, or of a unified strategy for conservation in transboundary areas.
The Chortís Block is an exemplar of this issue, where national boundaries effectively
divide efforts to document and conserve isolated cloud forest areas in five mountain
ranges that serve to physically delineate national borders.
In some cases, border regions are avoided due to security-related issues.
Honduran frontier zones have become increasingly favored by transnational narcotics
traffickers, particularly over the past decade as the influence of Mexican drug cartels
has expanded into Central America (e.g., Archibold & Cave 2011). In an even more
extreme case, the highest mountain range in Nicaragua (Sierra de Dipilto, maximum
elevation 2,107 m), which also forms the border with Honduras, was considered a
strategic vantage point that was heavily contested, and subsequently landmined, during
the Contra-Sandinista War of the 1980’s (United Nations Mine Action Service 1998).
Despite the apparent biogeographic importance of this mountain range and its potential
for supporting endemic species, little to no biological inventory work has been carried
out in the Sierra de Dipilto. Beyond this mountain range, a large area of the Chortís
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Highlands in northern Nicaragua has also been heavily undersampled as a result of
being the principal zone of conflict in the Contra-Sandinista War, and has only recently
begun to be sampled in a concerted fashion (Sunyer et al. 2009, Travers et al. 2011).
Political boundaries have placed the majority of the endemic-rich Chortís
Highlands within the borders of one country, Honduras, with significant extensions into
three neighboring countries, most notably Nicaragua. Subsequently, no concerted
attempt has been made to date to present a unified understanding of the biogeographic
province’s patterns of biological diversification.
A consequence of research constrained by political boundaries is that systematic
cataloguing of regional diversity has been handicapped. As a result, a number of
endemic species are known from localities in one country but unconfirmed as occurring
across the border in ecophysiographically contiguous areas, as in the cases, for
example, of Cryptotriton monzoni (endemic to the Sierra de Espíritu Santo in
Guatemala) and Anolis johnmeyeri (endemic to the Sierra de Espíritu Santo and Sierra
de Omoa in Honduras). In at least one case, it has been suggested that two species of
Cryptotriton described from opposite sides of the Sierra de Omoa (called the Sierra de
Caral in Guatemala), C. nasalis and C. wakei, actually represent the same species
(McCranie & Wilson 2002).
Minimizing the constraints of these largely political and logistical issues is critical to
accurately analyzing and interpreting regional patterns of biogeography, endemism, and
conservation priority. My goal in this chapter is to synthesize the available data for the
Chortís Block herpetofauna, drawing first from a considerable regional literature base.
This available data are then augmented by the results of sampling efforts from 2006–
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2011 in Honduras and Nicaragua, and presented to provide the basis from which to
further investigate herpetofaunal diversity and assess research and conservation
priorities moving forward.
Methods and Materials
This section serves not only to define the methodologies used in Chapter 2, but
also to provide some of the broader methods and definitions used throughout this
dissertation.
Field Sampling
Between June 2006 and April 2011, I made 17 fieldtrips totaling over 2,577
person-hours of effort (over 12,560 person-hours were logged by expedition
participants) over the course of 275 field-days in Honduras and Nicaragua, sampling
over 60 localities in the Chortís Block (Table 3-1; Figure 3-1). Tissue samples were
taken from freshly euthanized vouchers and stored in SED buffer (250 mM EDTA/20%
DMSO/saturated NaCl; Seutin et al. 1991; Williams 1997). Voucher specimens were
preserved in 10% formalin solution and later transferred to 70% ethanol for permanent
storage. Vouchers were deposited in the Florida Museum of Natural History, University
of Florida (UF), the Museum of Vertebrate Zoology, University of California, Berkeley
(MVZ), and the National Museum of Natural History, Smithsonian Institution (USNM).
Taxonomic Scope and Standards
I recognize a Chortís Block herpetofauna inclusive of species that occur south or
east of the Río Motagua and north of a latitudinal line across the northernmost edge of
Lago Xolotlán (= Lago de Managua). I have included taxa from the Islas de la Bahía and
Cayos Miskitos, as they are continental islands of Chortís Block origin, but not the
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Figure 3-1. Map showing sampling localities in the Chortís Block. Red crosses = localities sampled 2006–2011, blue crosses = localities sampled 1999–2005, green diamonds = localities sampled by collaborators for inclusion here.
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offshore islands of Belize, the smaller cays far offshore from eastern Honduras and
Nicaragua, or the Islas del Cisne, as they neither geological nor biogeographically
related directly to the Chortís Block. I have excluded marine taxa (sea turtle families
Cheloniidae and Dermochelyidae and the sea snake Pelamis platura) and introduced
species, as well as taxa known only from the Salvadoran Cordillera or southwestern
Salvadoran coastal plain, as they are not considered herein to be part of the Chortís
Block.
The taxonomic nomenclature used in this dissertation generally follows that used
by Wilson & Johnson (2010). A number of additions and changes have occurred since
that publication that pertain directly to composition of the Chortís Block herpetofauna,
including description or resurrection of the following taxa: Bolitoglossa nympha
(Campbell et al. 2010), Cerrophidion sp. (Jadin et al., submitted), Ctenosaura
praeocularis (Hasbún & Köhler 2009), Anolis beckeri (Köhler 2010), A. unilobatus
(Köhler & Vesely 2010), Epictia magnamaculata (Adalsteinnsson et al. 2009),
Dendrophidion clarkii (McCranie 2011a), Leptodeira rhombifera (Daza et al. 2009),
Mastigodryas alternatus (McCranie 2011a), Omoadiphas cannula (McCranie & Cruz-
Díaz 2010), Tantilla sp. (Townsend et al., submitted), and Tantilla psittaca (McCranie
2011b). In addition, four new species of salamanders have recently been described, in
part based on results of this dissertation reported in later chapters, and are included in
this chapter for the sake of completeness: Nototriton picucha (Townsend et al. 2011a),
Oedipina koehleri (Sunyer et al. 2011), O. nica (Sunyer et al. 2010), and O. petiola
(McCranie & Townsend 2011). I follow Myers (2011) the species of the Rhadinaea
godmani group as representing a separate genus, Rhadinella.
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Evaluating Conservation Status
I used three different measures to assess the conservation status of the
herpetofauna of the Chortís Block: IUCN Red List categorization, Environmental
Vulnerability Scores (Wilson & McCranie 2003), and Conservation Status Scores
(Wilson & Townsend 2010).
IUCN Red List categorizations were taken from one of three sources: the IUCN
Red List of Threatened Species (v. 2011.1; www.iucnredlist.org) for amphibians, marine
turtles, crocodilians, and Ctenosaura; Townsend & Wilson (2010) for Honduran reptiles,
and Sunyer & Köhler (2010) for Nicaraguan reptiles. Species not previously evaluated
by the IUCN or other authors were assessed using the standard criteria of the IUCN
(2001).
Environmental Vulnerability Scores (EVS) are primarily from Townsend & Wilson
(2010a). Species not assessed in that study were calculated using the methodology
developed and refined by Wilson & McCranie (1992, 2003, 2004a), which is calculated
by taking the total of three rankings: 1) extent of geographic range, 2a) degree of
specialization of reproductive mode for amphibians or 2b) the degree of persecution by
humans for reptiles, and 3) extent of ecological distribution in Honduras; EVS scores
from 10–13 indicate medium vulnerability, and scores from 14–19 are high vulnerability
(Wilson & McCranie 2003).
Conservation Status Scores (CSS) were developed by Wilson & Townsend (2010)
to provide a simple measure for assessing conservation status of amphibians and
reptiles across Mesoamerica. The CSS represents sum of individual scores for 1)
numbers of countries, 2) physiographic regions, and 3) vegetation zones occupied by a
given species of amphibian or reptile. The country score ranges from 1 to 8 (the number
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of countries of Central American plus México), the physiographic region score ranges
from 1 to 21, and the vegetation zone score from 1 to 15 (Wilson & Townsend 2010).
Given this, the CSS can range from 3 (the most restricted endemic species, inhabiting a
single vegetative zone in a single physiographic region in a single country) to the
theoretical maximum of 44 (for a species found literally everywhere in México and
Central America).
Results
Composition of the Herpetofauna
The native, non-marine herpetofauna of the Chortís Block is comprised of 382
species in 134 genera and 41 families, including 145 species of amphibians and 237
reptiles (Tables 3-2, 3-3). The Chortís Block herpetofauna comprises about
approximately 2.3% of global herpetofaunal species diversity (16,301 species as of 6
October 2011; Table 3-3; AmphibiaWeb 2011, Uetz et al. 2011). This includes 2.1% of
global amphibians, with 1% of caecilians, 7% of salamanders, and 1.6% of anurans,
along with 2.5% of global reptiles, with 3.1% of turtles, 8.3% of crocodilians, and 2.5%
of squamates (2.3% of lizards, and 4.2% of snakes). There are 41 families of
amphibians and reptiles in the Chortís Block (Table 3-3), comprising 30.4% of the
families of the world and 65.1% of the families of Mesoamerica (Table 3-3).
Within Mesoamerica (considered in this discussion to include México and Central
America), the Chortís Block herpetofauna contains approximately 20.3% of the regional
herpetofauna (Wilson & Johnson 2010). This includes 19.8% of Mesoamerican
amphibian species, with 12.5% of caecilians, 17.8% of salamanders, and 21.1% of
amphibians, and 20.6% of reptiles, including 18.2% of turtles, two of three crocodilian
species, and 20.6% of squamates (Table 3-3).
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Patterns of Distribution and Endemism within the Chortís Block
Within the Chortís Block, species were considered to occur within one of eight
physiographic regions: the Caribbean Lowlands, Caribbean Versant Intermontane
Valleys, Northern Cordillera of the Chortís Highlands, Central Cordillera of the Chortís
Highlands, Southern Cordillera of the Chortís Highlands, Pacific Lowlands, Pacific
Versant Intermontane Valleys, and Islas de la Bahía (Tables 3-2, 3-4). The Caribbean
Lowlands holds the highest diversity, with 188 species, with the Northern Cordillera
being the most diverse portion of the Chortís Highlands with 163 species (Table 3-4).
The majority of amphibians (51%) that occur in the Chortís Block are endemic, i.e.,
restricted in distribution to within the Chortís Block, with a lesser share of reptiles (24%)
being endemic (Table 3-5). The salamanders have a particularly high degree of
endemism, with 37 of 43 species (86%) being Chortís Block endemics, and 36 of those
37 being endemic to the Chortís Highlands province (Tables 3-2, 3-4). A large share of
named anuran species (37%) is also endemic (Table 3-5).
Distribution of Chortís Highland Endemics
The Northern Cordillera is the most endemic-rich portion of the Chortís Highlands
with 72 species, versus 42 and 35 in the Central and Southern Cordilleras, respectively
(Table 3-6). The Sierra de Omoa is clearly the mountain range supporting the highest
number of Chortís Block endemic species (35), and each of the four mountain ranges of
the Northern Cordillera support more endemic species than any other mountain range in
the Chortís Highlands (Table 3-6). In the Central Cordillera, the Sierra de Sulaco and
Cordillera de La Flor-La Muralla tie for the lead with 13 endemic species, with the Sierra
de Agalta having 11 (Table 3-6). In the Southern Cordillera, the Sierra del Merendón
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supports the most endemic species with 12, followed by the Cordillera Dariense with 9
(Table 3-6).
Conservation Status
A startling portion of the Chortís Block herpetofauna is threatened at the local,
regional, and global levels (Tables 3-2, 3-5). At least 41% of the entire herpetofauna is
at endangered at a globally significant level (listed in one of the top three threat
categories on the IUCN Red List: Critically Endangered, Endangered, or Vulnerable),
including an alarming 74% of salamanders (Table 3-5). Although not surprising given
their typically narrow geographic distributions, 96% of species endemic to the Chortís
Block are also listed in the top three IUCN Red List categories, with 48% of endemic
species listed in the highest risk category: Critically Endangered (Table 3-5). Regionally,
the Conservation Status Score (CSS) was used to gauge the relative degree of threat
facing members of the Chortís Block herpetofauna. Two hundred and ten species (55%
of Chortís Block herpetofauna) have CSS between 3 and 11, placing them in the
category of ―Very High conservation significance,‖ the highest risk category employed at
the Mesoamerican scale by Wilson & Townsend (2010). Within the Chortís Block,
Environmental Vulnerability Score (EVS) was used to provide a local-scale measure of
the relative degree of threat facing herpetofaunal species. Results of the EVS indicated
an elevated degree of susceptibility to degradation for the Chortís Block herpetofauna,
with 146 species (38%) having EVS from 14 and 19, placing them in the ―high
vulnerability‖ category (Townsend & Wilson 2010a).
Sampling Results by Locality
Below is a summary of results, presented by locality, from herpetofaunal sampling
in the Chortís Block from June 2006 to April 2011. For each general locality, typically a
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protected area, the location and geographical extent are provided, along with details of
the legal protection (if any), a list of amphibian and reptile species recorded, the sites
and dates visited, and a summary of findings.
Parque Nacional Celaque
Location and Extent: West-central Departamento de Lempira and eastern
Departamento de Ocotepeque, Honduras; 26,267 ha in extent, highest elevation 2,849
m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Bolitoglossa celaque, Plectrohyla psiloderma.
Site visit summary: Campamento Don Tomás (2,050 m), vicinity of Campamento
Naranjo (2,560-2,850 m), Departamento de Lempira, core zone of PN Celaque. 21–28
June 2008.
Comments: PN Celaque has a large core zone, and the physiographic structure
of the mountain benefits conservation efforts. Steep sides to this mesa-like mountain
protect a large, relatively flat area above 2,500 m elevation that is almost completely
intact. Upon this mesa originates the primary water source for the nearby city of
Gracias, and protection of this and other important watersheds provides added benefit
to the people inhabiting the park’s surroundings. The endemic salamander Bolitoglossa
celaque was found to be locally abundant around the Río Arcagual. Only one of four
species of Plectrohyla reported from Celaque (McCranie & Wilson 2002) was found
during my visit (P. psiloderma), and additional targeted searches for the other three
species (P. guatemalensis, P. hartwegi, and P. matudai) should be carried out
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immediately in an attempt to determine their status. Additional fieldwork in Celaque
would almost certainly produce additional new herpetofaunal species.
Parque Nacional Cerro Azul Copán
Location and Extent: Western Departamento de Copán, Honduras, along the
border with Guatemala; 11,766 ha, highest elevation 2,285 m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Caudata: Bolitoglossa nympha, B. dofleini; Anura:
Dendropsophus microcephalus, Incilius valliceps, Lithobates brownorum, Lithobates
maculatus, Ptychohyla hypomykter, Smilisca baudinii; Squamata: Anolis
ocelloscapularis, Lepidophyma flavimaculatum, Sceloporus schmidti, Adelphicos
quadrivirgatum, Mastigodryas dorsalis, Ninia diademata, N. sebae, Typhlops
stadelmani.
Site visit summary: Quebrada Grande, Departamento de Copán, 1,280–1,400 m
elevation, in the buffer zone of PN Cerro Azul, on the south-southeastern side of Cerro
Azul. 26–30 July 2008.
Summary findings: PN Cerro Azul is both a reserve with high importance with
regard to its amphibian diversity and one at high risk due to a lack of management and
increasing human population and forest clearing. The highest portion of the
southeastern flank of Cerro Azul appears steep enough to deter campesinos from
clearing most of the remaining forest. Unfortunately, there appear to be no streams
flowing through this portion of forest due to the extreme topographical grade. Riparian
areas in the vicinity of Quebrada Grande have been completely cleared and converted
to livestock pastures. Below this area, a larger creek (Quebrada Cañon Oscuro) forms
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from smaller streams running through pastures and rapidly descends into a deep
canyon, inside which remains some riparian forest. The water source for Quebrada
Grande is a spring just above town, with a very small (<1 ha) patch of forest remaining
in the spring’s vicinity. The hillsides above and surrounding the spring have been
converted to agriculture. Additional work is urgently needed to determine the status of
remaining forest both at higher elevations and of the side of Cerro Azul opposite to
Quebrada Grande.
Parque Nacional Cerro Azul Meámbar
Location and Extent: East of Lago de Yojoa in extreme southern Departamento
de Cortés and northern Departamento de Comayagua; 17,872 ha, highest elevation
2,090 m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Caudata: Bolitoglossa mexicana, B. oresbia, Nototriton
limnospectator; Anura: Craugastor laevissimus, C. laticeps, Incilius ibarrai, I. porteri, I.
valliceps, Lithobates maculatus, Ptychohyla hypomykter, Smilisca baudinii, Squamata:
Anolis lemurinus, A. cf. limifrons, Sceloporus variabilis, Sphaerodactylus millepunctatus,
Thecadactylus rapicauda, Atropoides mexicanus, Bothriechis schlegelii, Imantodes
cenchoa,
Site visit summary: Los Pinos Visitor’s Center, Departamento de Cortés, 700–
1,400 m elevation, 3–5 December 2006, 14 July 2007, 4–5 April 2008, 14–17 April
2008, 4–12 June 2008, 25–27 November 2009; Cerro Azul, 800–1,740 m elevation, 18
April 2008, 5–12 July 2008; San José de los Planes, 930-1,290 m elevation, 1–3 June
2008.
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Figure 3-2. Sampling in the Chortís Block I. A) Campamento Don Tomás, 2,080 m, Parque Nacional (PN) Celaque (A–D, June 2008). B) The author in Montane Hepatic Forest, 2,770 m, PN Celaque. C) Campamento Los Naranjos, 2,570 m, PN Celaque. D) I. Luque searches for Bolitoglossa celaque in ground-dwelling bromeliads; Montane Mixed Forest, 2,630 m, PN Celaque. E) Community of Quebrada Grande, 1,320 m, with PN Cerro Azul (July 2008). F) I. Luque preparing to descend over 350 m to Quebrada Grande, 1,690 m (July 2008). G) Hiking along Quebrada Varsovia, 1,670 m, PN Cerro Azul Meámbar (August 2008). Figure 3-2B © I. Luque, all other photos © J.H. Townsend.
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Summary findings: Highland forest areas of this park previously had not been
sampled, and my first two expeditions to cloud forest elevations in July 2008 yielded
significant results, the discovery of Bolitoglossa oresbia, considered the most Critically
Endangered salamander in Honduras whose previous known distribution consisted of a
1 ha patch of forest on top of the otherwise-deforested Cerro El Zarciadero, and
Nototriton limnospectator, previously known only to occur across Lago de Yojoa in
Parque Nacional Montaña de Santa Barbara (Townsend et al. 2011b).
Parque Nacional Cusuco
Location and Extent: Northwestern Depto. Cortés and adjacent northern Depto.
Santa Bárbara, Honduras, near the Guatemalan border; 17,704 ha, highest elevation
2,242 m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Caudata: Bolitoglossa conanti, B. diaphora; Anura:
Duellmanohyla soralia, Plectrohyla dasypus, P. exquisita, Ptychohyla hypomykter;
Squamata: Anolis amplisquamosus, A. cusuco, A. johnmeyeri, Mesaspis moreletii,
Sceloporus schmidti, Cerrophidion sp., Ninia diademata, N. espinali, N. sebae.
Site visit summary: Vicinity of Centro de Visitantes (1,520–1,600 m), buffer zone
of PN Cusuco; Quebrada Cantiles (1,820 m), core zone of PN Cusuco, 11–17 March
2006, 30 August–3 September 2008, 28–30 November 2009.
Summary findings: Details of herpetofaunal work through 2006 are found in
Townsend & Wilson (2008); work in 2008 and 2009 did not appreciably add to this
knowledge base.
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Parque Nacional La Tigra
Location and Extent: South-central Departamento de Francisco Morazán; 24,340
ha, highest elevation 2,290 m.
Status: National Park (legally declared in 1980; Decreto 976-80); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Anura: Incilius porteri, Lithobates maculatus; Squamata:
Anolis laeviventris, A. tropidonotus.
Site visit summary: El Rosario Visitor’s Center (1,500–1,700 m), core zone of PN
La Tigra, 6–8 December 2006.
Comments: The streamside frog Craugastor emleni, has been reported to have
undergone extreme declines, and was feared extinct by McCranie & Wilson (2002). This
species was recently rediscovered from a small stream at 1,600 m elevation in Parque
Nacional La Tigra (McCranie et al. 2010), and additional fieldwork should be undertaken
at this easily accessible cloud forest to determine the extent of the distribution of C.
emleni.
Parque Nacional Montaña de Botaderos
Location and Extent: Northern Departamento de Olancho, and peripherally in
adjacent Departamento de Colón; 64,227 ha, maximum elevation 1,724 m.
Status: National Park (legally declared in 2011; Acuedro 002–2011).
Herpetofaunal results: Caudata: Nototriton sp.; Anura: Craugastor lauraster, C.
noblei, Craugastor pechorum, Lithobates maculatus, Pristimantis ridens, Ptychohyla
hypomykter; Squamata: Anolis capito, A. tropidonotus, Imantodes cenchoa, Ninia
maculata, Stenorrhina degenhardtii.
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Figure 3-3. Sampling in the Chortís Block II. A) Visitor’s Center at Parque Nacional (PN) Cusuco, 1,550 m elevation; the day before the post-coup presidential election, with red-and-white Partido Liberal party members meeting in seclusion (November 2009). B) Looking down from PN La Tigra, with El Rosario in the foreground and the Choluteca Valley beyond (B–C, December 2006). C) S. Townsend at Quebrada de la Cascada, 1,850 m, PN La Tigra. D) R. Ulloa on trail leading to cloud forest, 1,640 m, PN Montaña de Botaderos (D–G, April 2011, Explorer’s Club Flag #93). E) Broadleaf Cloud Forest, 1,720 m, PN Montaña de Botaderos. F) Our supplies and team near Alao, 1,100 m, on expedition into PN Montaña de Botaderos. G) M. Medina (left) recovering from nighttime sampling efforts while O. Reyes (right) prepares botanical samples at our base camp, 1,300 m, PN Montaña de Botaderos. Photos © J.H. Townsend.
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Site visit summary: Cerro de la Cruces and vicinity of Cerro ―Ulloa‖, the highest
ridge in the range, 1,160–1,730 m elevation, 16–19 April 2011.
Summary findings: In April 2011, I participated in an Explorer’s Club expedition
(Flag #93) to the Municipalidad de Gualaco in Departamento de Olancho, which
included the first ever biological expedition to the highest portion of this newly declared
park (approved by the Honduran Congress the same week we were there).
Parque Nacional Montaña de Comayagua
Location and Extent: Southeastern Departamento de Comayagua and adjacent
Departamento de Francisco Morazán; 29,767 ha, maximum elevation 2,410 m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Caudata: Bolitoglossa mexicana; Anura: Craugastor
laevissimus, Ptychohyla hypomykter, Squamata: Anolis sminthus, A. tropidonotus,
Sceloporus malachiticus.
Site visit summary: La Oki, Departamento de Comayagua, 1,680–2,040 m
elevation, edge of core zone for PN Montaña de Comayagua, 21–24 January 2008; Río
Negro, Departamento de Comayagua, 1,100–1,560 m elevation, buffer zone of PN
Montaña de Comayagua, 19–21 April 2008, 15–20 May 2008, 15–22 July 2008.
Comments: Accessing areas of cloud forest above 1,500 m elevation has proven
very challenging; intact cloud forest occurs as low as 1,200 m elevation along large
streams and rivers. The community of Río Negro is a model of community based
conservation and sustainable development, and is a prime candidate to receive funding
to support these areas. Areas of cloud forest above 2,000 m elevation need to be
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sampled for the presence of salamanders, as no salamanders have been found above
1,300 m elevation despite the presence of endemic highland species in surrounding
mountain ranges.
Parque Nacional Montaña de Santa Bárbara
Location and Extent: Southeastern Departamento de Santa Bárbara; 13,202 ha,
maximum elevation 2,744 m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Caudata: Bolitoglossa mexicana, Dendrotriton
sanctibarbarus; Anura: Craugastor laevissimus, C. laticeps, Lithobates maculatus,
Ptychohyla hypomykter, Squamata: Anolis rubribarbaris, Sceloporus malachiticus,
Typhlops tycherus.
Site visit summary: El Cedral, in the buffer zone of Parque Nacional Montaña de
Santa Barbara on the western slope of the mountain, 1,600–1,720 m elevation, 28–29
January 2008; Las Quebradas, in the buffer zone of Parque Nacional Montaña de Santa
Bárbara on the western slope of the mountain, 1,400–1,450 m elevation, 6–7 June
2010; core zone of Parque Nacional Montaña de Santa Barbara, west-to-east canyon
across the crest of the mountain, 1,450–2,180 m elevation, 6–9 November 2010.
Summary findings: The physiography of PN Montaña de Santa Bárbara appears
to be helping ensure the long-term persistence of intact forest inside the park’s core
zone. The steep side and jagged karst composition deter deforestation above 2,000 m,
and both endemic species known from within the park appear to have stable
populations. My work in PN Montaña de Santa Bárbara resulted in two notable
discoveries: a remarkable new large species blindsnake (Typhlops tycherus; Townsend
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Figure 3-4. Sampling in the Chortís Block III. A) I. Luque and M. Medina in Rio Negro, hiking towards Quebrada El Gavilán, 1,200 m, Parque Nacional (PN) Montaña de Comayagua (April 2008). B) Quebrada El Gavilán, 1,260 m, PN Montaña de Comayagua (May 2008). C) J. Austin (foreground) and field team ascending near-vertical trail above El Playón, 1,480 m, en route to PN Montaña de Santa Bárbara (C–E, November 2010). D) J. Austin at basecamp in canyon across top of PN Montaña de Santa Bárbara, 2,200 m. E) L. Herrera setting infrared camera trap for mammal survey in PN Montaña de Santa Bárbara, 2,190 m. F) G) Mesic ravine through Coniferous Cloud Forest, 1,930 m, PN Montaña de Yoro (September 2008). Photos © J.H. Townsend.
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et al. 2008a), and the documentation of variation and distributional records of Anolis
rubribarbaris, a lizard species previously known from only a single poorly preserved
specimen (Townsend et al. 2008b). An expedition into a canyon across the top of Cerro
Santa Bárbara in November 2010 encountered the bromeliad salamander Dendrotriton
sanctibarbarus to be locally abundant, particularly around large, bromeliad-laden
branches that had come to rest on the forest floor.
Parque Nacional Montaña de Yoro
Location and Extent: Northern Departamento de Francisco Morazán and
adjacent southern Departamento de Yoro; 11,766 ha, highest elevation 2,285 m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Caudata: Bolitoglossa cataguana, Nototriton lignicola,
Oedipina kasios, Anura: Incilius porteri, I. valliceps, Lithobates maculatus, Ninia sebae,
Plectrohyla guatemalensis, Squamata: Anolis morazani, A. tropidonotus, A. yoroensis,
Mesaspis moreletii, Sceloporus malachiticus, Cerrophidion sp., Rhadinella godmani.
Site visit summary: Río Maralito, outside Marale (610–630 m), seat of
municipality; Los Planes (1,450–1,500 m), buffer zone community; Cataguana (1,780–
2,020 m), northwestern core zone of PN Montaña de Yoro, 8–14 June 2006, 8–15
March 2007; Montaña de la Sierra (1,920 m), southeastern core zone of PN Montaña
de Yoro, 21–25 September 2008.
Comments: Results from this protected area are discussed in detail below.
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Parque Nacional Pico Bonito
Location and Extent: Eastern Departamento de Atlántida and adjacent
Departamento de Yoro; 107,107 ha, maximum elevation 2,480 m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Anura: Craugastor aurilegulus, C. noblei, Duellmanohyla
salvavida, Pristimantis ridens, Ptychohyla spinipollex; Squamata: Ameiva festiva, Anolis
lemurinus, A. tropidonotus, A. zeus, Basiliscus vittatus, Corytophanes cristatus, Incilius
leucomyos, Mabuya unimarginata, Plestiodon sumichrasti, Sphenomorphus cherriei,
Thecadactylus rapicauda, Leptophis ahaetulla, Oxybelis aeneus.
Site visit summary: Cangrejal, vicinity of the visitor’s center, 200 m elevation, 2
December 2009; Quebrada de Oro, 930–1,380 m elevation, 21–28 May 2010; CURLA
Station, 150 m elevation, 10–12 August 2010; Pico Bonito Lodge, 120 m, 7 April 2011.
Comments: My fieldwork in Parque Nacional Pico Bonito has thus far been limited
to the lowlands, supported by two fieldtrips undertaken by César Cerrato (UNAH) in
2010.
Parque Nacional Pico Pijol
Location and Extent: Southwestern Departamento de Yoro; 11,669 ha, maximum
elevation 2,282 m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetofaunal results: Anura: Craugastor laevissimus, C. rostralis, Lithobates
maculatus, Ptychohyla hypomykter, Smilisca baudinii; Squamata: Anolis yoroensis,
Oxybelis fulgidus.
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Site visit summary: Road above El Porvenir de Morazán, northeastern buffer
zone of PN Pico Pijol in the vicinity of Cerro Las Pajarillos, 1,380–1,520 m elevation,
23–25 July 2008; 17–20 September 2008.
Summary findings: Extensive shade-coffee production dominates the northern
side of the buffer zone of PN Pico Pijol. A single frog, Craugastor laevissimus, was
collected along a path through converted cloud forest; however, a search of a medium
sized upper tributary of Quebrada Las Payas surrounded by moderately disturbed forest
failed to find any of the normally stream-side Craugastor. No individuals of Bolitoglossa
porrasorum were collected, despite targeted searching for this species. A single
Ptychohyla hypomykter and two groups of tadpoles were the only amphibians observed
along the stream.
Parque Nacional Sierra de Agalta
Location and Extent: East-central Departamento de Olancho; 51,793 ha,
maximum elevation 2,354 m.
Status: National Park (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetological results: Caudata: Bolitoglossa mexicana, B. longissima,
Nototriton sp.; Squamata: Anolis cf. sminthus, Atropoides indomitus, Cerrophidion sp.
Site visit summary: Trail to, and vicinity of, Cerro La Picucha, 615–2,230 m
elevation.
Summary findings: Fieldwork led by Melissa Medina-Flores (Universidad
Nacional Autónoma de Honduras) resulting in collection of the first record of Atropoides
indomitus from the Sierra de Agalta and two specimens of an unknown species of
Nototriton (chapters 4 and 5; Townsend et al. 2011a).
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Refugio de Vida Silvestre Texiguat
Location and Extent: Southwestern Departamento de Atlántida and adjacent
northwestern Departamento de Yoro; 15,736 ha, maximum elevation 2,208 m.
Status: Wildlife Refuge (legally declared in 1987; Decreto 87-87); Conservation
International Key Biodiversity Area.
Herpetological results: Caudata: Bolitoglossa nympha, B. cf. porrasorum,
Nototriton cf. barbouri, N. tomamorum, Oedipina gephyra; Anura: Craugastor
aurilegulus, Craugastor cf. rostralis, Duellmanohyla salvavida, Hyalinobatrachium
fleischmanni, Incilius leucomyos, I. valliceps, Leptodactylus fragilis, Plectrohyla
chrysopleura, Ptychohyla spinipollex, Smilisca baudinii, Teratohyla pulverata;
Squamata: Anolis beckeri, A. kreutzi, A. loveridgei, A. yoroensis, A. zeus, Corytophanes
cristatus, Laemanctus longipes, Lepidophyma flavimaculatum, Sceloporus malachiticus,
Sphenomorphus cherriei, Adelphicos quadrivirgatum, Atropoides mexicanus,
Bothriechis marchi, B. schlegelii, Bothrops asper. Dendrophidion percarinatum,
Drymobius chloroticus, Geophis damiani, Hydromorphus concolor, Imantodes cenchoa,
Leptodeira septentrionalis, Micrurus nigrocinctus, Ninia pavimentata, Ninia sebae,
Pliocercus elapoides, Scaphiodontophis annulatus, Sibon dimidiatus, Sibon nebulatus,
Stenorrhina degenhardtii, Tantilla sp., Tropidodipsas sartorii.
Site visit summary: 2.5 km NNE of La Fortuna, buffer zone of RVS Texiguat,
1,500–1,890 m elevation, 8–11 April 2008; 10–21 June 2010, 25 July–1 August 2010.
Comments: RVS Texiguat might be simultaneously the single protected area of
the most biodiversity significance and facing the strongest threat to its long-term survival
in the Honduran protected areas system. The reserve is discussed in detail later in this
chapter.
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Figure 3-5. Sampling in the Chortís Block IV. A) Cerro de Pajarillos, 1,460 m, Parque Nacional (PN) Pico Pijol (July 2008). B) J. Slapcinsky (left) and J. Butler (right) at basecamp, La Fortuna, 1,650 m, Refugio de Vida Silvestre Texíguat (B–C, April 2008). C) Type locality of Isthmohyla insolita and Nototriton tomamorum, La Fortuna, 1,550 m, Refugio de Vida Silvestre Texíguat. D) Cattle pond with explosive breeding aggregation of Exerodonta catracha and Hypopachus barberi, dark masses in water are H. barberi eggs; 2,210 m, Reserva Biológica (RB) Guajiquiro (D–E, May 2008). E) Male Exerodonta catracha guarding egg clutches in pond from Figure 3-5D. F) Degraded Mixed Cloud Forest, 2,100 m, RB Güisayote; Anolis heteropholidotus and Mesaspis moreletii were abundant in the pasture in the foreground (F–G, June 2008). G) Camping under the communications tower at the top RB Güisayote, 2,270 m. Photos © J.H. Townsend.
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Reserva Biológica Cerro Uyuca
Location and Extent: Southeastern Departamento de Francisco Morazán, 772
ha, maximum elevation 2,006 m.
Status: Biological Reserve (legally declared in 1987; Decreto 87-87);
Conservation International Key Biodiversity Area.
Herpetological results: Anura: Incilius porteri, Lithobates brownorum X forreri
(this population is considered to be interspecific hybrids by McCranie & Wilson 2002), L.
maculatus, Ptychohyla salvadorensis, Rhinella marina, Tlalocohyla loquax; Squamata:
Anolis laeviventris, A. tropidonotus, Sceloporus malachiticus.
Site visit summary: Vicinity of Cabot Biological Station, 1,620 –1,700 m
elevation, 17–18 March 2007, 17–19 July 2007.
Summary findings: Sampling in Reserva Biológica Cerro Uyuca took place in
the vicinity of the biological station managed by the Centro Zamorano de Biodiversidad,
which includes access to a small reservoir supporting a dense population of Lithobates
brownorum/forreri.
Reserva Biológica Guajiquiro
Location and Extent: Departamento de La Paz; 17,165 ha, maximum elevation
2,330 m.
Status: Biological Reserve (legally declared in 1987; Decreto 87-87);
Conservation International Key Biodiversity Area.
Herpetofaunal results: Caudata: Bolitoglossa celaque; Anura: Exerodonta
catracha, Hypopachus barberi, Incilius ibarrai, Lithobates maculatus; Squamata: Anolis
crassulus, Drymobius chloroticus, Ninia espinali, Thamnophis fulvus.
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Site visit summary: Guajiquiro and surrounding countryside, 1,900–2,240 m
elevation, 23–25 May 2008, 14–15 August 2008.
Summary findings: Highland areas above about 2000 m elevation in the vicinity
of the town of Guajiquiro are a matrix of both traditional and modern agriculture and
maintained patches of old growth cloud forest. In some places, proximity of existing
patches and make-up of the intervening agricultural areas is such as to allow species
such as Bolitoglossa cf. celaque and Exerodonta catracha to persist and, in some
cases, apparently thrive. Cattle ponds in small pastures were readily being used for
breeding by the anurans E. catracha and Hypopachus barberi (Ketzler et al. 2011,
Luque-Montes et al. 2011), and B. cf. celaque was found in a forest patch surrounding a
communications tower. Additional highland areas with forest patches in the area need to
be visited to fully and accurately assess the conservation needs of the relatively large
but biogeographically connected highland area.
Reserva Biológica Güisayote
Location and Extent: Departamento de Ocotepeque; 12,677 ha, maximum
elevation 2,330 m.
Status: Biological Reserve (legally declared in 1987; Decreto 87-87);
Conservation International Key Biodiversity Area.
Herpetofaunal results: Caudata: Bolitoglossa conanti; Anura: Hypopachus
barberi; Squamata: Anolis heteropholidotus, Mesaspis moreletii, Sceloporus
malachiticus.
Site visit summary: Communication towers southeast of El Portillo de
Ocotepeque, core zone of RB Güisayote, 2,080-2,230 m elevation, 18-21 June 2008.
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Summary findings: The core zone of RB Güisayote has an access road running
along the top of the reserve through high pastures and remnant cloud forest to a set of
communications towers. This reserve appears to support a surprising amount of forest
given that it lies in a region that is otherwise heavily impacted by human activity. The
status of Leptodactylus silvanimbus is unclear, it has been documented previously
inhabiting open fields and pastures with flooded areas in the vicinity.
Reserva Biológica Yerbabuena
Location and Extent: Southwestern Departamento de Francisco Morazán 3,522
ha, maximum elevation 2,243 m.
Status: Biological Reserve (legally declared in 1987; Decreto 87-87);
Conservation International Key Biodiversity Area
Herpetological results: Caudata: Bolitoglossa carri; Anura: Incilius ibarrai;
Squamata: Anolis sminthus, A. tropidonotus, Sceloporus malachiticus.
Site visit summary: Finca La Alondra, cafetal in region of Cerro Cantagallo, and
other fincas in the area, 1,750–2,020 m elevation, 16–17 July 2007.
Summary findings: Despite the fact that most of the forest around Cerro
Cantagallo is disturbed and much of that is fully converted to agriculture, Bolitoglossa
carri can still be found relatively easily inside bromeliads in remaining forest patches.
Additional work should be done to determine the extent of remaining forest on the
highest portions of Cerro Cantagallo.
Reserva de la Biosfera Bosawas
Location and Extent: Departamento de Jinotega and Región Autónoma Atlántico
Norte; 1,992,000 ha.
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Status: UNESCO Man and the Biosphere Reserve (legally declared in 1991 and
revised and expanded in 1997 and 2001; Decreto 44–91, Decreto 32–96, and Ley 407).
Herpetological results: Gymnophiona: Gymnopis multiplicata; Caudata:
Bolitoglossa striatula; Anura: Agalychnis callidryas, Cochranella granulosa, Craugastor
fitzingeri, C. lauraster, C. megacephalus, C. mimus, C. noblei, Dendropsophus
microcephalus, Diasporus diastema, Incilius valliceps, Leptodactylus melanonotus,
savagei, Lithobates vallanti, Pristimantis cerasinus, P. ridens, Rhaebo haematiticus,
Rhinella marina, Smilisca baudinii, S. phaeota, S. sordida, Teratohyla pulverata;
Squamata: Ameiva festiva, Anolis capito, A. limifrons, A. lionotus, A. quaggulus,
Basiliscus plumifrons, B. vittatus, Corytophanes cristatus, Iguana iguana,
Sphaerodactylus millepunctatus, Sphenomorphus cherriei, Thecadactylus rapicauda,
Adelphicos quadrivirgatum, Boa constrictor, Bothrops asper, Drymarchon melanurus,
Imantodes cenchoa, Leptodeira septentrionalis, Mastigodryas melanolomus, Micrurus
nigrocinctus, Ninia sebae, Oxybelis aeneus, O. brevirostris, Porthidium nasutum,
Pseustes poecilonotus, Sibon longifrenis, S. nebulatus, Tretanorhinus nigroluteus;
Testudines: Kinosternon leucostomum, Rhinoclemmys annulata, R. funerea, Trachemys
venusta.
Site visit summary: Muru Ta, 12–13 June 2007, 180 m elevation; Muru Lak, 13–
18 June 2007, 190 m elevation; Kalum Kitang, 18–21 June 2007, 180 m elevation; Aran
Dak, 11 and 22 June 2007, 150 m elevation; Raiti, 23 June 2007, 140 m elevation.
Summary findings: Results from this expedition, the first in a series, to the core
zone of Bosawas were reported in Sunyer et al. (2009) and Travers et al. (2011).
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Figure 3-6. Sampling in the Chortís Block V. A) Cerro Yaluk, Departamento de Olancho, Honduras, seen from the Río Coco (A–D, June 2007). B) Aran Dak, most remote Mayangna community on Río Lakus, 150 m, Reserva de la Biósfera Bosawas, Nicaragua. C) L. Wilson (seated) being poled down the upper Río Lakus by Miskitu parataxonomist S. Charley (standing); core zone of Reserva de la Biósfera Bosawas, 170 m. D) Preparing samples; (left to right) L. Wilson, S.Travers (seated), Miskitu parataxonomists R. Picado and S. Charley, J. Sunyer (seated), and Mayangna parataxonomist J. Lopez; Muru Lak, 180 m, core zone of Reserva de la Biósfera Bosawas. E) I. Luque ascending the volcanic peak of Isla El Tigre, with a view of the Golfo de Fonseca and the volcanoes of eastern El Salvador; 550 m (August 2010). F) Campsite at the summit of Cerro Zarciadero, 1,890 m, Honduras (July 2007). Photos © J.H. Townsend.
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Jardín Botánico Lancetilla
Location and extent: Western Departamento de Atlántida; 2,255 ha, maximum
elevation 710 m.
Status: National Park (legally declared in 1990; Decreto 48-90); Conservation
International Key Biodiversity Area.
Herpetological results: Anura: Craugastor aurilegulus, Leptodactylus
melanonotus, Lithobates brownorum, L. vallanti, Smilisca baudinii; Squamata: Ameiva
festiva, Anolis lemurinus, A. cf. zeus, Lepidophyma flavimaculatum, Sphaerodactylus
millepunctatus, Sphenomorphus cherriei, Clelia clelia, Coniophanes imperialis.
Site visit summary: 7–9 June 2010, 22–24 July 2010.
Summary findings: Besides the extensive grounds of the botanical gardens,
Lancetilla also protects the entire watershed of the Río Lancetilla. This includes 1,281
ha of virgin lowland rainforest, one of the best preserved fragments of lowland rainforest
along the northern coast of Honduras.
Área de Uso Multíple Isla del Tigre
Location and Extent: Island in the Golfo de Fonseca on the Pacific Coast,
Departamento de Valle; 601 ha, maximum elevation 783 m.
Status: Multiple-Use Area (legally declared in 1999; Decreto 5–99–E).
Herpetological results: Anura: Incilius coccifer; I. porteri; Squamata: Sceloporus
squamosus.
Site visit summary: Amapala and trail to summit, 5–783 m elevation, 16–17
August 2010.
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Non-Protected Areas
Cerro El Zarciadero
Location: Northern Departamento de Comayagua.
Herpetological results: Caudata: Bolitoglossa oresbia; Anura: Exerodonta
catracha, Incilius porteri; Squamata: Drymobius margaritiferus.
Site visit summary: Cerro El Zarciadero, 1,845–1,890 m elevation, 14-15 July
2007.
Comments: The small patch of forest on top of Cerro El Zarciadero remains
intact, and is essentially protected as private property around a set of communications
towers. A family lives at the entrance to the tower complex and the husband is paid to
guard and maintain the grounds. The residents were already familiar with Bolitoglossa
oresbia and the idea that they are protecting the only known habitat of this animal,
which was found active on vegetation on the only night we spent on top of the mountain.
Exerodonta catracha was also found actively calling and breeding in and around a very
small water basin and stream just below the road and towers. The situation with the
remaining forest patch, tiny as it is, appears stable for the time, since it provides a buffer
area around the communications towers at the top of the mountain. The discovery of
Bolitoglossa oresbia in PN Cerro Azul Meámbar also lessens the urgency with which
earlier conservation efforts surrounding El Zarciadero were being pursued.
Highlands surround the Meseta de La Esperanza
Location: Central Departamento de Intibucá, mountainous areas surrounding the
Meseta de La Esperanza; 1,700–2,100 m elevation.
Herpetological results: Caudata: Bolitoglossa celaque; Anura: Exerodonta
catracha, Incilius ibarrai, Lithobates brownorum X forreri (this population is considered
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to be made up of interspecific hybrids [McCranie & Wilson 2002]); Squamata: Anolis
crassulus, A. sminthus, Sceloporus malachiticus, S. variabilis.
Site visit summary: San Pedro La Loma, 1,960–2,020 m elevation, 21–24
January 2008, 16–17 August 2008; Cerro El Pelón, 2,065 m elevation, 30 June 2008;
Zacate Blanco, 1,950–2,100 m elevation, 29–30 June 2008, 18–19 August 2008.
Summary findings: As is the case in RB Guajiquiro, highland areas above
around 2,000 m elevation in the vicinity of La Esperanza are a matrix of both traditional
and modern agriculture and patches of remnant cloud forest. In some places, proximity
of existing patches and make-up of the intervening agricultural areas are such as to
allow species such as Bolitoglossa cf. celaque and Exerodonta catracha to persist and,
in some cases, apparently thrive. Additional highland areas with forest patches in the
area need to be visited to fully and accurately assess the conservation needs of the
relatively large but biogeographically connected highland area.
Los Naranjos
Location: Near the border of Departamento de Cortés and Departamento de
Santa Bárbara, between Lago de Yojoa to the east and Parque Nacional Montaña de
Santa Bárbara to the west; 700–730 m elevation.
Herpetological results: Caudata: Bolitoglossa mexicana; Anura: Craugastor
laevissimus, Dendropsophus microcephalus, Engystomops pustulosus,
Hyalinobatrachium fleischmanni, Hypopachus variolosus, Incilius valliceps, Lithobates
brownorum, L. maculata, Rhinella marina, Smilisca baudinii; Squamata: Ameiva
undulata, Anolis laeviventris, A. lemurinus, A. tropidonotus, A. unilobatus, A. cf. zeus,
Sphaerodactylus millepunctatus, Sphenomorphus cherriei, Ninia diademata, N. sebae,
Tantilla taeniata.
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Site visit summary: 13–15 August 2007, 30–31 January 2008, 5 April 2008, 11–
12 April 2008, 20–22 May 2008, 7 June 2010.
Summary findings: Collections in this area were primarily made on the Plowden
family farm, now called Compañia Agrícola El Paraíso. This large property includes
numerous springs, shade coffee plots, and shaded horticultural plots.
Montaña de Jacaleapa
Location: Central Departamento de Olancho, vicinity of Nahoan community of El
Norte, 980–1,180 m elevation.
Herpetological results: Anura: Craugastor laevissimus, C. lauraster, C. noblei,
Lithobates maculatus, Pristimantis ridens, Ptychohyla hypomykter; Squamata: Anolis
sp., A. tropidonotus, Sceloporus malachiticus, Sphenomorphus cherriei.
Site visit summary: 11–12 April 2011.
Summary findings: This isolated patch of mesic highland forest had not
previously been surveyed by biologists, and supports over 500 ha of intact premontane
rainforest.
Montaña Macuzal
Location: Southern Departamento de Yoro, west of Yorito.
Herpetological results: Caudata: Bolitoglossa porrasorum, Nototriton barbouri;
Anura: Craugastor rostralis; Squamata: Anolis laeviventris, A. pijolensis, A. yoroensis,
Sceloporus malachiticus.
Site visit summary: El Panal, southwest side of Montaña de Macuzal, 1500–1800
m elevation, Departamento de Yoro, 31 January–3 February 2008, 6–7 April 2008.
Comments: While the flanks of Montaña de Macuzal are converted to shade
coffee cultivation or completely cleared of all natural vegetation, the area above 1780 m
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Figure 3-7. Sampling in the Chortís Block VI. A) ―Island‖ fragment of Broadleaf Cloud Forest surrounded by converted corn fields, 2,230 m, Sierra de Opalaca west of La Esperanza (July 2008). B) Small reservoir supporting population of Lithobates brownorum X forreri, 2,010 m, Cerro San Pedro, east of La Esperanza (January 2008). C) Converted cloud forest, Zacate Blanco, highest point 2,250 m (July 2008). D) L. Wilson and I. Luque searching for Bolitoglossa cf. celaque in bromeliads that had been cut and left for cattle feed, 2,010 m, Cerro San Pedro. E) Intact bromeliad cover, 2,020 m, Cerro San Pedro. F) L. Wilson at Pozo Azul, a karstic spring near Los Naranjos, 680 m. G) Montaña Macuzal, viewed from the northeast, showing strip of remnant Broadleaf Cloud Forest at highest elevations (maximum 1,905 m). H) Montaña Macuzal, viewed from the southwest near El Panal, 1,480 m, with yellow wildflowers covered the completely deforested slopes; access to the cloud forest visible in the saddle (January 2008). I) N. Stewart (front) and J. Butler (back) crossing upper deforested slope of Montaña Macuzal (April 2008). Photos © J.H. Townsend.
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elevation still supports an approximately 5–10 ha patch of moderately disturbed cloud
forest on karstic soils, and Bolitoglossa porrasorum and Nototriton barbouri are
persisting, and in the case of the former species, abundantly so. A stream flowing out of
the northern corner of Montaña de Macuzal near the community of El Portillo should be
checked for signs of Duellmanohyla salvavida and/or Plectrohyla guatemalensis
(McCranie & Wilson 2002), as well as other priority species.
Saguay
Location: Upper Valle de Agalta, Departamento de Olancho.
Herpetological results: Anura: Hypopachus variolosus, Incilius valliceps,
Leptodactylus fragilis, Lithobates maculatus, Ptychohyla hypomykter, Smilisca baudinii,
Tlalocohyla loquax; Squamata: Anolis capito, A. quaggulus, A. wermuthi, Sceloporus
malachiticus; Testudines: Kinosternon scorpioides.
Site visit summary: Teocintecito ravine, 720 m elevation, and a seepage bog
outside Saguay, 580 m elevation, 10 April 2011.
Summary findings: Survey sites in remnant dry forest patches in the foothills
around the upper Río Grande (also called the Sico, Tinto, and Negro at different
portions downstream) watershed. One locality was a relatively large seepage bog,
covered with a think mat of floating vegetation that arises from the middle of the dry
valley floor.
San José de Texíguat
Location: Southern side of the upper Río Leán valley in the foothills of Texíguat,
150–200 m elevation.
Herpetological results: Caudata: Bolitoglossa nympha; Anura: Craugastor
aurilegulus, Duellmanohyla salvavida, Hyalinobatrachium fleischmanni, Leptodactylus
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fragilis; Squamata: Anolis cf. zeus, Iguana iguana, Lepidophyma flavimaculatum,
Atropoides mexicanus, Hydromorphus concolor.
Site visit summary: 10–11 November 2010.
Summary findings: Sampling was carried out in a deep, protected ravine just
south of the town. Craugastor aurilegulus and Duellmanohyla salvavida were found in
abundance around the small, spring-fed creek. A juvenile Hydromorphus concolor was
found in a rocky fissure at the spring’s source.
Selva Negra
Location: Between cities of Jinotega and Matagalpa, Departamento de
Matagalpa, 1,200–1,300 m elevation.
Herpetological results: Anura: Agalychnis callidryas, Craugastor lauraster,
Incilius valliceps, Lithobates cf. taylori, Ptychohyla hypomykter, Smilisca baudinii,
Tlalocohyla loquax; Squamata: Anolis capito, A. quaggulus, A. wermuthi, Sceloporus
malachiticus.
Site visit summary: 13–15 August 2007.
Summary findings: Collections were made in the premontane rainforest above
the Selva Negra coffee farm and lodge.
Yeguare Valley
Location: Valley associated with an upper tributary of the Río Choluteca, 810 m
elevation.
Herpetological results: Anura: Engystomops pustulosus; Squamata: Basiliscus
vittatus, Gonatodes albogularis, Porthidium ophryomegas; Testudines: Kinosternon
scorpioides, Trachemys venusta.
Site visit summary: 16–17 March 2007; 3–4 June 2010.
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Figure 3-8. Sampling in the Chortís Block VII. A) O. Reyes (left) and M. Bonta (right) hiking through the Nahoan community of El Norte en route to Montaña de Jacaleapa, 1,100 m (A–E, April 2011). B) Premontane rainforest stream, 1,120 m, Montaña de Jacaleapa. C) The author with a giant (10+ m) teocinte cycad (Dioon mejiae) near Saguay, 630 m, Valle de Agalta. D) La Puzunca, upper reach of the Río Grande, 560 m, Valle de Agalta; distinctive green plants on far hillsides are teocinte cycads. E) Giant paddle cactus (Nopalea cf. hondurensis), 580 m, Valle de Agalta. F) Artificial lagoon, 1,220 m, Selva Negra, Nicaragua (F–H, August 2007). K. Townsend (front) and S. Travers (back) climb a trail through premontane rainforest, 1,460 m, Selva Negra. H) Premontane rainforest creek, 1,420 m, Selva Negra. Photos © J.H. Townsend.
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Summary findings: Collections made in agricultural areas and remnant
premontane dry forest in and around the campus of Escuela Agrícola Panamericana
Zamorano.
Discussion
Baseline Herpetological Inventory of Parque Nacional Montaña de Yoro
In June 2006, March 2007, and September 2008, I led the initial herpetological
survey work carried out in Parque Nacional Montaña de Yoro, a relatively large yet
herpetologically-unknown protected area in central Honduras. Parque Nacional
Montaña de Yoro was established in 1987 and sits along the boundary between the
Honduran departments of Francisco Morazán and Yoro, with about two-thirds of its area
in the municipality of Marale in northernmost Francisco Morazán (COHECO 2003). With
a total area of over 154 km2, more than 47 km2 of cloud forest supporting area above
1,800 m, Parque Nacional Montaña de Yoro potentially contains one of the largest
areas of cloud forest remaining in Honduras (COHECO 2003). Next to nothing has been
documented with regard to the park’s biodiversity, and only 14 herpetofaunal species
are mentioned in the park management plan, with most of those being relatively
widespread species that commonly are found around human habitation or in habitats
below cloud forest (Townsend & Wilson 2009). Additionally, Parque Nacional Montaña
de Yoro protects some of the highest portions of the Montañas de la Flor, which is home
to the last traditional communities of indigenous Tolupanes that maintain the Tol
language and culture (Chapman 1992). Within the park’s borders are over 4,700 people
spread across 55 communities, with the population consisting of Tolupan, mestizos, and
mixed Tolupan-mestizo farmers (COHECO 2003). Most of these people inhabit the
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Figure 3-9. Exemplar paratypes and habitats from Parque Nacional Montaña de Yoro.
A) Adult male paratype (UF 150000) of Anolis morazani sp. nov. B) Adult female paratype (MCZ 185612) of A. morazani sp. nov. C) Dewlap of UF 150000. D) Adult female paratype (MVZ 258030) of Bolitoglossa cataguana (―B. sp. inquirenda 1‖ in Chapter 4). E) Arboreal tank bromeliads in disturbed mixed cloud forest, Cataguana, 1,880 m. F) Quebrada Cataguana, 1,820 m. G) Remote homestead at Cataguana, 1,910 m. Photos © J.H. Townsend.
nearly completely deforested buffer zone of Parque Nacional Montaña de Yoro, and as
the buffer zone population grows, increasing pressure is being placed on the remaining
cloud forest in the nuclear zone. Parque Nacional Montaña de Yoro has become so
heavily impacted by the encroaching agricultural frontier that at one point it was
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recommended that the park be re-designated as a biological reserve and that its
borders be reduced to the remaining extent of intact cloud forest (Vreugdenhil et al.
2002).
My work in Parque Nacional Montaña de Yoro was limited to the vicinity of two
sites, Cataguana on the northwestern side of the core zone, and the highlands above
Guaymas (sometimes referred to as Montaña de la Sierra; however, this is not to be
confused with the Montañas de la Sierra of Departamento de La Paz). Despite the
relatively limited amount of fieldwork carried out, the expeditions were nonetheless
fruitful and resulted in the discovery of a new species of anole (Anolis morazani;
Townsend & Wilson 2009), and salamanders from three genera that could not be
unambiguously assigned to a named species.
A New Species of Anole
Fieldwork in Parque Nacional Montaña de Yoro uncovered a relatively common
anole lizard assignable to the Anolis crassulus group, characterized by having
moderately to strongly enlarged medial dorsal scales, no more than two scales
separating the supraorbital semicircles, four to seven rows of loreals, suboculars, and
supralabials in contact under the central portion of the orbit, enlarged postanals in
males, and heterogeneous flank squamation (McCranie et al. 1992; Köhler et al. 1999).
The majority of the species in the A. crassulus group are endemic to the Chortís
Highlands, including A. amplisquamosus, A. heteropholidotus, A. muralla, A.
rubribarbaris, A. sminthus, and A. wermuthi (Köhler 2008). In addition, one widespread
species, A. crassulus, is found across the highlands of Nuclear Central America from
Chiapas, México, to El Salvador and southwestern Honduras. The population from
Parque Nacional Montaña de Yoro was demonstrated to be morphologically distinctive
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from all other species in the A. crassulus group based on hemipenial structure and
scalation, and I subsequently described it as the new species Anolis morazani
(Townsend & Wilson 2009).
Salamanders of Uncertain Taxonomic Assignment
Populations of at least three different salamanders were discovered in Parque
Nacional Montaña de Yoro. A series of Bolitoglossa, assignable to the B. dunni species
group based on having well-developed subdigital pads and bluntly rounded, free toe tips
but with coloration differing from other described species, was collected at Cataguana in
2006 and 2007 and above Guaymas in 2008. Three specimens of Nototriton were also
collected at Cataguana from within ground cover, and a small Oedipina was collected in
a deep mesic ravine through coniferous cloud forest. Taxonomic assignment of these
three populations, referred to as Bolitoglossa sp. inquirenda 1, Nototriton sp. inquirenda
5, and Oedipina sp. inquirenda 1, are addressed in Chapter 4.
Parque Nacional Montaña de Yoro appears to be both overlooked and
undervalued by national and international conservation planners, due to perceived lack
of documented ―conservation-priority‖ species; however, this apparent lack of diversity
is a result of undersampling and is not reflective of the true significance of the park’s
biodiversity. Prior to initiation of survey work in Parque Nacional Montaña de Yoro,
Parque Nacional Montaña de Yoro was a virtual ―black hole‖ of biodiversity data,
surrounded by literally dozens of cloud forest areas, many of which have well-
documented and diverse endemic biotas (Wilson & McCranie 2004b). Given the
biodiversity present in other cloud forest areas in Honduras, it is highly probable that
additional undescribed species await discovery in Parque Nacional Montaña de Yoro.
Future work in Parque Nacional Montaña de Yoro should continue to shed light on
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these relationships and provide a clearer picture of highland biogeography in eastern
Nuclear Central America.
Hotspot within a Hotspot: the Special Case of Refugio de Vida Silvestre Texíguat
The Refugio de Vida Silvestre (RVS) Texíguat was established in 1987 and
consists of approximately 33,267 ha of premontane and lower montane rainforest
straddling the border of the Honduran departments of Atlántida and Yoro (CIPF 2009).
RVS Texíguat is administered by the Instituto Nacional de Conservación y Desarrollo
Forestal, Áreas Protegidas y Vida Silvestre (ICF) as part of the Sistema Nacional de
Áreas Protegidas de Honduras (SINAPH), with management authority for the reserve in
the hands of the non-governmental organization Fundación para la Protección de
Lancetilla, Punta Sal y Texíguat (PROLANSATE). Most herpetological surveys in RVS
Texíguat have been conducted since 1991 on the leeward side of the park in
Departamento de Yoro, at elevations above 1,500 m in the vicinity of a coffee farm
known locally as La Fortuna (Holm & Cruz 1994; McCranie et al. 1993; McCranie &
Castañeda 2004a, b; Townsend et al. 2010a; Wilson et al. 1994, 1998).
Situated at the western end of the Cordillera Nombre de Dios, the leeward side of
RVS Texíguat and its counterpart at the eastern end of the Cordillera, Parque Nacional
(PN) Pico Bonito, are the most significant areas of herpetofaunal diversity in a country
whose national level of endemism has already been demonstrated to be the highest in
Central America (Wilson & Johnson 2010). Our preliminary results from the windward
side of RVS Texíguat indicate that this area represents a unique opportunity for
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Figure 3-10. La Liberación de Texíguat. A) Valley of the Río Jilamito, with the remote
encampment known as La Liberación de Texíguat partially visible as the lower clearing in the center of the picture beyond the emergent palm; the entire expanse from La Liberación to the farthest peak (Cerro Texíguat, 2,208 m) is undisturbed premontane and lower montane rainforest. B) The initial leg of the expedition to La Liberación requires a 2 hour mule ride through the lowlands (L.D. Wilson on mount). C) The mule ride is followed by a 6–8 hour hike into the mountain, with around two-thirds the trail within this deep, high-grade trench (M. Medina-Flores following our guides and pack animals). Photos © J.H. Townsend.
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conserving the remarkable diversity that has already been documented on the leeward
side of RVS Texíguat, and for expanding the known herpetofaunal diversity of the
reserve.
Discovery of Plectrohyla chrysospleura
Plectrohyla chrysopleura (Anura: Hylidae) is a large, critically endangered
spikethumb frog only known from the vicinity of its type locality in Parque Nacional Pico
Bonito (Cruz et al. 2004). The type locality, Quebrada de Oro, is a premontane
rainforest locality that has been under relatively intensive study since 1980 and is
among the most remarkable sites of amphibian endemism in Central America
(McCranie & Wilson 2002). Unfortunately, this locality also has the distinction of being
one of the best-documented cases of catastrophic amphibian decline in Central America
(McCranie & Wilson 2002; McCranie & Castañeda 2005, 2007; Townsend & Wilson
2010). It is the type locality for six species of amphibians (Craugastor aurilegulus, C.
chrysozetetes, C. fecundus, Duellmanohyla salvavida, Plectrohyla chrysopleura, and
Rhinella chrysophora), and is just below the type locality (Cerro Búfalo) of two other
species (Craugastor cruzi and C. saltuarius). Almost all of these species are considered
to be in decline, with even some considered to be extinct or close to extinction
(McCranie & Castañeda 2007).
Like other species from Quebrada de Oro that have declined or disappeared, P.
chrysopleura is apparently extirpated from that locality, and given that Quebrada de Oro
is the only locality where this species has been found despite consistent focused work
in the area (McCranie and Castañeda 2005, 2007), it raises the concern that the
species might be near extinction, if not already extinct. The last time P. chrysopleura
was documented as extant was in May 1996, when two metamorphs and two tadpoles
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Figure 3-11. Plectrohyla chrysopleura (Hylidae) from La Liberación. A) Adult female
Plectrohyla chrysopleura (USNM 573993) from La Liberación, 1,030 m elevation, Refugio de Vida Silvestre Texiguat, Honduras. B) Adult male P. chrysopleura (USNM 573995) from Cerro El Chino, 1,420 m elevation, Refugio de Vida Silvestre Texiguat, Honduras. C) Juvenile P. chrysopleura (USNM 573994) from La Liberación. D) Recently metamorphosed P. chrysopleura (not collected) from La Liberación. E) Río Jilamito at La Liberación, 1,020 m. E) Tributary of Río Jilamito, La Liberación, 1,030 m. Photos © J.H. Townsend.
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were collected along Quebrada de Oro (McCranie and Wilson 2002, McCranie and
Castañeda 2005). At that time, one of two tadpoles collected had deformed mouthparts
(McCranie and Wilson, 2002). Based on these data and additional considerations, Cruz
et al. (2004), IUCN (2011), and Townsend and Wilson (2010) all judged P. chrysopleura
to be Critically Endangered, based on IUCN criteria (IUCN, 2001). For P. chrysopleura,
the particular red list status was Critically Endangered (A2ace, B1ab[iii,v]+2ab[iii,v]),
meaning that a reduction in population size of ≥ 80% was observed, estimated, inferred,
or suspected over the last 10 years based on direct observation, a decline in area of
occupancy, extent of occurrence and quality of habitat, and the suspected impact and
susceptibility to decline from chytridiomycosis.
In June and July 2010, a series of Plectrohyla chrysopleura was collected around
La Liberación and Cerro El Chino on the windward side of RVS Texíguat, providing the
first evidence of this species’ survival in 14 years and the second known locality for this
species, approximately 55 km west-southwest of the type locality (Townsend et al.
2011c). Of the six endemic species of premontane forest amphibians described from
the Quebrada de Oro area, we now know that two of them (Duellmanohyla salvavida
and Plectrohyla chrysopleura) occur at La Liberación. Given the robust nature of the
populations of these two treefrogs and the intactness of the premontane rainforest in
this area, I remain hopeful that perhaps others of the endemic anurans that have
undergone decline at Quebrada de Oro will be discovered still resident at La Liberación.
Underestimated Salamander Diversity?
Three species of salamanders were previously known from RVS Texíguat,
Bolitoglossa porrasorum sensu lato, Nototriton barbouri s.l., and Oedipina gephyra s.l.,
each of which is considered endemic to two or more isolated localities in northern
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Honduras (McCranie & Wilson 2002). Bolitoglossa porrasorum is known from the type
locality at Pico Pijol, Montaña Macuzal, Texíguat, and Pico Bonito; however, only the
Pico Bonito population has been included previously in phylogenetic studies (Parra-
Olea et al. 2004). Nototriton barbouri is considered to have the same distribution as B.
porrasorum, whereas O. gephyra is known from its type locality at La Fortuna and from
a single specimen from Pico Bonito (McCranie & Wilson 2002). Both N. barbouri and O.
gephrya have been shown to demonstrate species-level divergence between the
Texíguat and Pico Bonito populations (García-París & Wake 2000), and I supplement
this existing data with newly collected samples representing both putative taxa in
Chapter 4. In April 2008, a single specimen of Nototriton possessing the distinctive
morphological traits of enlarged nostrils, syndactylous feet, and a contrasting pale
venter was collected within leaf litter packed into a crevice in the side of a small mesic
canyon near La Fortuna (1,550 m elevation). This species, described as N. tomamorum
by Townsend et al. (2010a), is analyzed genetically in Chapter 4 and reviewed
morphologically in Chapter 5.
Highly Endemic and Highly Endangered
The leeward side of RVS Texíguat (herein referred to as Yoro Texíguat) is highly
imperiled due to continued illegal logging of valuable hardwoods and forest clearing for
subsistence agriculture, which I witnessed firsthand in April 2008 (Townsend et al.
2010a). Despite the rapid advancement of deforestation in Yoro, little exploration of the
virtually unknown Atlántida side of the refuge has been conducted to date. I led three
expeditions to the windward side of RVS Texíguat (Atlántida Texíguat) during 2010;
these visits were limited to 12 days (10–21 June 2010) and seven days (26 July–2
August 2010) in the vicinity of La Liberación (15.53°N/87.29°W; camp was established
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at 1,030 m elevation), and three days (10–12 November 2010) in the vicinity of San
José de Texíguat (15.52°N/87.45°W), yet we recorded 46 species (Townsend et al.,
submitted A), compared to 40 species amassed during the approximately two-decade
span of limited study of Yoro Texíguat (Wilson & McCranie 2004b; Townsend et al.
2010a). This pattern suggests that herpetofaunal diversity and endemism demonstrated
on the Yoro side will likely be exceeded on the windward side.
The 2010 work in this area, along with past work on the leeward slope of RVS
Texíguat (summarized in Townsend et al. 2010a) and in Parque Nacional Pico Bonito
(summarized in McCranie & Castañeda 2005), demonstrates that 29 of the 93 endemic
species (close to one-third) of amphibians and reptiles reported from Honduras by
Townsend & Wilson (2010) occur within these three areas of the same cordillera
(Townsend et al., In press A). At least 10 species of amphibians and reptiles are
Texíguat-restricted endemics, and RVS Texíguat is home to 14 more species endemic
to the Chortís Block (Townsend et al., In press A).
Given the preliminary successes of efforts towards documenting and promoting
the conservation of herpetofaunal diversity in RVS Texíguat, I believe that the serious
problems facing the reserve can be addressed through continued efforts in the coming
years to provide enduring protection for this vitally important component of the
Honduran patrimony.
Cryptozoic Snake Diversity
Cryptozoic snake taxa include some of the most species-rich groups of snakes,
and their remarkable diversity is exceeded by their ability to remain concealed and
evade detection, even in relatively well studied field sites (Myers 2003; Stafford 2004;
Townsend 2009). Genera such as Geophis, Ninia, and Tantilla are all cryptozoic in
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nature, typically small in size and often inhabit the interface between leaf litter and soil.
Many of these secretive species are known only from one or a handful of specimens,
yet are distinctive enough in terms of external morphology to be promptly recognized as
distinct species (e.g., Campbell 1998; Stafford 2004; Townsend 2009).
A New Species of Centipede Snake (genus Tantilla) from La Liberación
The genus Tantilla currently consists of 63 described species (Townsend et al. In
press B), broadly distributed in all three of the major geographic sections of the Western
Hemisphere (North America, Mesoamerica, and South America; Wilson 1999), including
at least seven species in the Chortís Block (McCranie 2011b). During survey work in
July 2010 around La Liberación on the windward side of RVS Texíguat, we collected a
single specimen of Tantilla possessing a set of distinctive morphological characteristics
that stand out as unique within the genus. Based on having pale middorsal and/or
lateral stripes and pale markings on the nape, we posit that this snake is assignable to
the T. taeniata species group (sensu Wilson & Meyer 1971, Campbell 1998, Wilson &
McCranie 1999), but represents a previously unknown taxon, which is described in a
manuscript submitted for publication in August 2011. The new species differs
significantly from all congeners on the basis of its dorsal body pattern, consisting of a
pale middorsal stripe composed of narrow spots and confined to the middorsal row and
a lateral coloration of pale spots on each of rows 1, 2, and 4. In addition, it possesses a
middorsally interrupted pale nuchal band and dark brown pigment on the lateral edges
of the ventrals. The new species appears to have no close affinities within the T.
taeniata group, and elucidation of its phylogenetic relationships will have to await a
group or genus-wide assessment, which, given the difficulties in securing fresh material
of these taxa, might not occur in the near future.
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A Large New Species of Blindsnake (Typhlops tycherus)
Blindsnakes of the genus Typhlops (Squamata: Typhlopidae) have a cosmopolitan
and primarily tropical distribution (McDiarmid et al. 1999), with the majority of diversity in
the Western Hemisphere confined to the islands of the West Indies (Dixon & Hendricks
1979; Thomas & Hedges 2007). Four native species of Typhlops previously were known
to occur in Mesoamerica (Dixon & Hendricks 1979; Köhler 2008): T. costaricensis
(Honduras to Costa Rica), T. microstomus (Yucatan Peninsula), T. stadelmani (western
and northern Honduras), and T. tenuis (Veracruz, México, to Guatemala). A fifth
typhlopid, the parthenogenetic Ramphotyphlops braminus, has been introduced to
scattered localities throughout Mesoamerica, primarily around urban areas (Köhler,
2008).
Two species of blindsnakes (T. costaricensis and T. stadelmani) are known to
occur in the Chortís Highlands. Both of these species occur in Honduras; Typhlops
costaricensis is known from localities in the mesic lowlands of Departamento de Gracias
a Dios and from mid-elevation pine-oak forest localities between Tegucigalpa and
Parque Nacional La Tigra in Departamento de Francisco Morazán (McCranie et al.
2006; Wilson et al. 1988), and T. stadelmani, which is reported from mid-elevation
localities in the departments of Atlantída, Copán, and Yoro (McCranie & Castañeda
2005; McCranie & Wilson 2001). Typhlops stadelmani was, until recently, considered a
junior synonym of T. tenuis (Dixon & Hendricks 1979), and was resurrected by
McCranie & Wilson (2001) after collection of a large series that verified the
distinctiveness of T. stadelmani from T. tenuis, based primarily on differences in the
number of scales between rostral and tail tip and in color.
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Figure 3-12. New species of Tantilla (Colubridae) and Typhlops (Typhlopidae). A)
Dorsal, lateral, and central views of the head of adult male holotype (USNM 574000) of Tantilla sp. nov., 1,150 m elevation, La Liberación de Texiguat. B) sulcate and asulcate views of the hemipenis of USNM 574000. C) dorsal and lateral coloration of USNM 574000. D) subadult Typhlops tycherus sp. nov. from El Cedral, Montaña de Santa Bárbara, 1,550 m. Photos © J.H. Townsend.
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In January 2008, a single specimen of Typhlops was found freshly killed on an
unpaved road between two small communities near the lower edge of intact cloud forest
in Parque Nacional Montaña de Santa Bárbara, Honduras. This specimen differed from
all other Middle American blindsnakes in its large size, in having 22–22–22 scales
around the body, and by having a dark brownish gray dorsum with a well-defined pale
yellowish gray to immaculate white ventral coloration. This specimen formed the basis
for describing the species Typhlops tycherus, which was confirmed in April 2011 by
collection of a second specimen from the vicinity of the type locality by M. Medina-
Flores (UNAH).
Geophis damiani at La Liberación
The genus Geophis (Squamata: Colubridae: Dipsadinae) is currently comprised of
47 species of secretive semifossorial snakes distributed across nearly every terrestrial
habitat from México to northern South America (Downs 1967, Wilson & Townsend
2007, Townsend 2009). Six members of the genus are known to occur in the Chortís
Block: Geophis damiani, G. dunni, G. fulvoguttatus, G. hoffmanni, G. nephodrymus, and
G. rhodogaster, four of which (G. damiani, G. dunni, G. fulvoguttatus and G.
nephodrymus) are endemic (Townsend 2009). Geophis damiani is one of the least
known snakes in the Chortís Block, and was only known from two adult specimens
(Wilson et al. 1998, McCranie & Castañeda 2004). On 29 July 2010, an adult male
Geophis damiani (USNM 573999) was collected during survey work around La
Liberación, representing the third adult specimen and second adult male specimen
known for this taxon. The snake was found at 22h30 while active in the bottom of a
deep, trench-like trail at 1,075 m elevation in moderately disturbed Premontane Wet
Forest. The snake had apparently fallen into and become trapped inside the trench,
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which was about 2 m deep at the collection site and over 3.5 m deep in some places.
This locality lies around 10 km NNW of the previously reported localities, and the
elevation of the new record is 475 m below the previously-known lowest elevational
distribution attributed to this species, 1,550 m (based on UF 142543, an egg and
embryo), and 605 m below the lowest verified elevation for the species (1,680 m; USNM
573999). All previously reported localities for G. damiani are in the Lower Montane Wet
Forest formation. In Townsend et al. (2010d), we provided morphological data and color
notes for USNM 573999, and compared it to the two previously known specimens of G.
damiani.
Noteworthy Ninia
Ninia pavimentata. Ninia pavimentata is a small semifossorial snake reported
from pine-oak and cloud forest areas in central Guatemala, as well as from a single
locality in northwestern Honduras (Smith & Campbell 1996, Townsend et al. 2005). This
taxon was previously considered a synonym of N. maculata (Peters 1861), until Smith &
Campbell (1996) resurrected N. pavimentata (Bocourt 1883) to species level on the
basis of non-overlapping segmental count ranges and other morphological
characteristics. The distributions of N. maculata and N. pavimentata are presently
known to be separated by a roughly 315 airline km gap in Honduras, with N.
pavimentata reaching its easternmost known distribution in the Sierra de Omoa, outside
of Parque Nacional Cusuco, Departamento de Cortés (15.51ºN, 88.18ºW), 1,250 m
elevation, and N. maculata its northernmost known locality at Quebrada Machín,
Reserva de la Biósfera Río Plátano, Departamento de Colón (15.32ºN, 85.28ºW), 540
m elevation (McCranie et al. 2001; Townsend et al. 2005). On 10 April 2008, J. Butler
and I collected a female Ninia pavimentata (UF 152810) from under a rock at the edge
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Figure 3-13. Noteworthy cryptozoic snakes. A) Third adult specimen, and second male,
Geophis damiani (USNM 573999), 1,075 m elevation, La Liberación de Texiguat. B) Ninia espinali, a Chortís Highlands endemic recorded for the first time in Cerro Azul Meámbar. C) Ninia pavimentata, recorded for the first time in Refugio de Vida Silvestre Texíguat. Photos © J.H. Townsend.
of a fragment of cleared cloud forest in Refugio de Vida Silvestre Texiguat (15.44°N,
87.30°W), 1,715 m elevation, Departamento de Yoro, Honduras (Townsend et al.
2009b). This habitat is similar to that of most N. pavimentata specimens, which are
known from 1,120–1,825 m elevation in pine-oak or cloud forest (Smith & Campbell
1996), as well as to the disturbed habitat (a shade cafetal) where the other Honduran
specimen originated. Examination of the specimen showed it to fall with the known
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range of variation in N. pavimentata (Smith & Campbell 1996; Townsend et al. 2005;
Townsend et al. 2009b), providing further evidence for the specific status of this taxon.
This record extends the known range of Ninia pavimentata approximately 65 airline km
east from its known distribution. The new locality also narrows the geographic gap
between N. pavimentata and its most similar congener and presumed sister taxon, N.
maculata, to approximately 250 airline km.
Ninia espinali. Ninia espinali is known to occur in western Honduras and northern
El Salvador, where it inhabits highland rainforests from 1,580–2,270 m elevation (Köhler
2008). On 9 July 2008, I. Luque and I collected an adult female N. espinali on a steep
slope approximately 200 m above the Río de Varsovia (14°47.95’N, 87°53.47’W; 1,660
m elevation) in Parque Nacional Cerro Azul Meámbar, extending the known range of
this species approximately 85 km SSE of localities in Parque Nacional Cusuco,
Deptartamento de Cortés, and approximately 75 km N of localities in the vicinity of
Guajiquiro, Departamento de La Paz (Luque-Montes & Townsend 2009). The snake
was active at night in an exposed root mass on a steep slope near the top of a ridge.
Unidentified Salamander Populations
As indicated above, fieldwork in Parque Nacional Montaña de Yoro and Refugio
de Vida Silvestre Texíguat resulted in collection of samples representing five
populations of salamanders that could not be assigned unambiguously to a known
species. Besides these five entities, at least five other populations of salamanders were
sampled that cannot be unequivocally assigned to a known taxon. From Parque
Nacional Cerro Azul Meámbar, a series of Nototriton and a single distinctively colored
Bolitoglossa require additional attention, as do samples representing at least two forms
of Oedipina from northern Nicaragua. In 2010 and 2011, fieldwork in Departamento de
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Olancho resulted in discovery of two previously unknown allopatric populations of
Nototriton, one from the Sierra de Agalta and a second from the Sierra de Botaderos.
These 10 populations of salamanders, as well as other allopatric populations of
questionable taxonomic assignment (e.g., Bolitoglossa porrasorum and Nototriton
barbouri from Refugio de Vida Silvestre Texíguat), are the subject of molecular
investigation and taxonomic evaluation in Chapter 4.
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Table 3-1. Summary of fieldwork undertaken in the Chortís Block, 2006–2011. DATES LOCALITIES PARTICIPANTS
3 Jun – 18 Jun 2006 PN Montaña de Yoro: Cataguana JHT, Larry David Wilson 2 – 10 Dec 2006 PN Cerro Azul Meámbar: Los Pinos Brian Campesano, Lorraine Ketzler, Scott
Travers, JHT, Steve Townsend PN La Tigra " " 8 – 20 Mar 2007 PN Montaña de Yoro: Cataguana Jason Butler, Lorraine Ketzler, Scott Travers,
JHT, Larry David Wilson, et al. RB Cerro Uyuca Jason Butler, Lorraine Ketzler, Scott Travers, JHT 7 – 29 Jun 2007 Biosfera Bosawas (7 localities) Lenin Obando, Javier Sunyer, Scott Travers, JHT,
Larry David Wilson, et al. 13 – 21 Jul 2007 PN Cerro Azul Meámbar: Los Pinos Lorraine Ketzler, JHT, Larry David Wilson RB Cerro Uyuca " " RB Yerbabuena " " Cerro Zarciadero " " 11 – 23 Aug 2007 Leon Scott Travers, JHT, Katielynn Townsend Selva Negra Scott Travers, JHT, Katielynn Townsend 20 Jan–5 Feb 2008 PN Montaña de Comayagua: La Okí Lorraine Ketzler, Ileana Luque-Montes, JHT, Larry
David Wilson PN Montaña de Santa Bárbara: El
Cedral " "
Marcala " " San Pedro La Loma " " Los Naranjos Ileana Luque-Montes, JHT, Larry David Wilson Montaña Macuzal Ileana Luque-Montes, JHT, Larry David Wilson Yeguare Valley Ileana Luque-Montes, JHT, Larry David Wilson 4 – 20 Apr 2008 PN Cerro Azul Meámbar: Los Pinos Carlos Andino, César Cerrato, Gabriela Diaz,
Lorraine Ketzler, Ileana Luque-Montes, Melissa Medina-Flores, Aaron Mendoza, Wendy Naira, JHT, Larry David Wilson
PN Cerro Azul Meámbar: Aldea Cerro Azul
César Cerrato, Ileana Luque-Montes, Melissa Medina-Flores, JHT, Larry David Wilson
PN Montaña de Comayagua: Río Negro Ileana Luque-Montes, Melissa Medina-Flores, JHT, Larry David Wilson
RVS Texíguat: La Fortuna Jason Butler, Lorraine Ketzler, Nathaniel Stewart, JHT, Larry David Wilson
Montaña Macuzal " " 14 – 28 May 2008 PN Montaña de Comayagua: Río Negro James Austin, Lorraine Ketzler, JHT, Larry David
Wilson RB Guajiquiro César Cerrato, Lorraine Ketzler, Ileana Luque-
Montes, JHT, Larry David Wilson Los Naranjos James Austin, Lorraine Ketzler, JHT, Larry David
Wilson 12 Jun–29 Jul 2008 PN Celaque Lorraine Ketzler, Ileana Luque-Montes, JHT, Larry
David Wilson PN Cerro Azul Copán: Quebrada Grande Ileana Luque-Montes, JHT, Larry David Wilson PN Pico Pijol: Quebrada Las Payas " " PN Montaña de Comayagua: Río Negro " " PN Cerro Azul Meámbar: Aldea Cerro
Azul/Varsovia Ileana Luque-Montes, JHT
RB Güisayote Lorraine Ketzler, Ileana Luque-Montes, Melissa Medina-Flores, JHT, Larry David Wilson
Copán Ruinas Lorraine Ketzler, Ileana Luque-Montes, Melissa Medina-Flores, JHT, Larry David Wilson
La Esperanza area (3 localities) Lorraine Ketzler, Ileana Luque-Montes, JHT, Larry David Wilson
14 Aug–1 Oct 2008 PN Cerro Azul Meámbar: Aldea Cerro Azul/Varsovia
Ileana Luque-Montes, JHT
PN Cusuco César Cerrato, Ileana Luque-Montes, Melissa Medina-Flores, JHT, Larry David Wilson
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Table 3-1. Continued. TRIP DATES LOCALITIES PARTICIPANTS
PN Montaña de Yoro: above Guaymas
Ileana Luque-Montes, JHT, Larry David Wilson
PN Pico Pijol: Pino Alto César Cerrato, Ileana Luque-Montes, JHT, Larry David Wilson
RB El Pital César Cerrato, Melissa Medina-Flores, Larry David Wilson
RB Güisayote " " RB Mixicuri " " Erandique " " La Esperanza area " " 10 – 20 April 2009 PN Montaña de Comayagua: Río
Negro Sergio Gonzalez, Christina Martin, Mario Solis, JHT, Rony Valle, Christopher Wolf
25 Nov – 6 Dec 2009 PN Cerro Azul Meámbar: Los Pinos César Cerrato, Vladlen Henriquez, JHT PN Cusuco " " PN Pico Bonito " " 1 – 26 Jun 2010 RVS Texíguat: La Liberación Benjamin Atkinson, César Cerrato, Luis Herrera,
Mayron McKewy-Mejía, JHT, Larry David Wilson, et al.
JB Lancetilla Benjamin Atkinson, César Cerrato, Luis Herrera, Mayron McKewy-Mejía, Ciro Navarro, JHT
20 Jul – 21 Aug 2010 PN Cerro Azul Meámbar: Los Pinos Anne Donnelly, Matthew Donnelly, Ileana Luque-Montes, JHT
RVS Texíguat: La Liberación Levi Gray, Luis Herrera, Melissa Medina-Flores, Alexander Stubbs, JHT, etc.
JB Lancetilla " " Roatán Anne Donnelly, Matthew Donnelly, Yensi Flores,
Ileana Luque-Montes, Melissa Medina-Flores, Sandy Pereira, JHT
Utila Anne Donnelly, Matthew Donnelly, Ileana Luque-Montes, Melissa Medina-Flores, Sandy Pereira, JHT
5 – 16 Nov 2010 PN Cerro Azul Meámbar: Los Pinos James Austin, Luis Herrera, Melissa Medina-Flores, JHT
PN Montaña de Santa Bárbara James Austin, Luis Herrera, JHT, Alicia Ward, et al. San José de Texíguat James Austin, Luis Herrera, JHT 7 – 22 April 2011 PN Montaña de Botaderos Christopher Begley, Mark Bonta, Robert Hyman,
David Medina, Melissa Medina-Flores, Onán Reyes, Fito Steiner, JHT
PN Pico Bonito Robert Hyman, David Medina, Melissa Medina-Flores, Fito Steiner, JHT
RB Colibrí Esmeralda Robert Hyman, Fito Steiner, JHT Montaña deJacaleapa Mark Bonta, Onán Reyes, JHT Rio Grande, Valle de Agalta Christopher Begley, Mark Bonta, Robert Hyman,
David Medina, Melissa Medina-Flores, Onán Reyes, Fito Steiner, JHT
137
Table 3-2. Conservation status and physiographic distribution of the native non-marine herpetofauna of the Chortís Highlands. Data primarily sourced from Wilson & Johnson (2010) and supplemented by Acevedo et al. (2010), McCranie (2011a), Sunyer & Köhler (2010), Townsend & Wilson (2010a), and my own observations. Taxa followed by an asterisk (*) indicated new taxa described or being described through the course of this dissertation; details of taxonomic assignment of these species are provided in Chapter 3. IUCN Red List status follows is from the IUCN (2011; www.iucnredlist.org) when available, with other sources indicated by footnotes. Elevational Distributions are range–wide and not confined to the Chortís Highlands. Conservation Status Scores (CSS) are from Wilson & Townsend (2010a), and Environmental Vulnerability Scores (EVS) are sources cited above. Species are allocated to one of two General Distribution categories: CB = endemic to the Chortís Block, WS = widespread outside Chortís Block. Physiographic distribution is related to the Chortís Highlands (Chapter 1 provides details of each province), and includes: CL = Caribbean Lowlands physiographic province, CV = Caribbean versant intermontane valleys, NC = Northern Cordillera of the Serranía, CC = Central Cordillera of the Serranía, SC = Southern Cordillera of the Serranía, PL = Pacific Lowlands physiographic province, PV = Pacific versant intermontane valleys, IB = Islas de la Bahía; a plus (+) indicates the taxon is found within the province.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
GYMNOPHIONA
Caeciliaidae (2)
Dermophis mexicanus Vulnerable A2ac1 20 12 0–1500 WS + + +
Gymnopis multiplicata Least Concern1 14 12 0–1400 WS + +
CAUDATA
Plethodontidae (43)
Bolitoglossa carri Critically
Endangered
B1ab(iii)+2ab(iii) 1
3 17 1840–2070 CB +
Bolitoglossa cataguana* Critically
Endangered
B1ab(iii)+2ab(iii)2
3 16 1800–2080 CB +
Bolitoglossa celaque Endangered
B1ab(iii) 1
3 16 1900–2820 CB +
Bolitoglossa conanti Endangered
B1ab(iii) 1
5 14 950–2010 CB + +
138
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Bolitoglossa decora Critically
Endangered
B1ab(iii)+2ab(iii) 1
3 17 1430–1550 CB +
Bolitoglossa diaphora Critically
Endangered
B2ab(iii) 1
3 16 1470–2200 CB +
Bolitoglossa dofleini Near Threatened1 10 14 100–1550 WS + + +
Bolitoglossa dunni Endangered
B1ab(iii) 1
5 14 1020–1600 CB +
Bolitoglossa heiroreias Endangered
B1ab(iii) 1
5 15 1840–2300 CB +
Bolitoglossa longissima Critically
Endangered
B1ab(iii) 1
3 17 1840–2240 CB +
Bolitoglossa mexicana Least Concern1 14 9 0–1900 WS + + + +
Bolitoglossa nympha Near Threatened3 6
3 12
3 30–1400 CB + + +
Bolitoglossa oresbia Critically
Endangered
B1ab(iii)+2ab(iii) 1
3 17 1560–1880 CB +
Bolitoglossa porrasorum Endangered
B1ab(iii) 1
4 15 980–1920 CB + +
Bolitoglossa striatula Least Concern1 10 14 2–1055 WS +
Bolitoglossa synoria Critically
Endangered
B1ab(iii) 1
4 15 2150–2715 CB +
Cryptotriton monzoni Critically
Endangered
B1ab(iii) 1
3 174 1570 CB +
Cryptotriton nasalis Endangered
B1ab(iii) 1
5 15 1220–2200 CB +
139
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Cryptotriton wakei Critically
Endangered
B1ab(iii) 1
3 174 1150 CB +
Dendrotriton sanctibarbarus Endangered
B1ab(iii) 2
[Vulnerable D21]
3 16 1830–2744 CB +
Nototriton barbouri Endangered
B1ab(iii)1
3 15 1530–1920 CB +
Nototriton brodiei Critically
Endangered
B1ab(iii) 1
3 17 875–1140 CB +
Nototriton lignicola Critically
Endangered
B1ab(iii) 1
3 17 1760–2020 CB +
Nototriton limnospectator Endangered
B1ab(iii) 1
3 16 1640–1980 CB +
Nototriton picucha* Critically
Endangered
B1ab(iii)3
33 17
3 1890–1920 CB +
Nototriton saslaya Vulnerable D21 3 17
5 1280–1500 CB +
Nototriton stuarti Data Deficient1 3 17
4 744 CB +
Nototriton tomamorum* Critically
Endangered
B1ab(iii)+2ab(iii)2
33 17
3 1550 CB +
Nototriton sp A (Pico Bonito)* Critically
Endangered
B1ab(iii)3
33 17
3 1210–1540 CB +
Nototriton sp B (Texiguat)* Critically
Endangered
B1ab(iii)+2ab(iii)3
33 17
3 1420–1800 CB +
140
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Nototriton sp. C (Botaderos)* Critically
Endangered
B1ab(iii)3
33 17
3 1700–1735 CB +
Oedipina elongata Least Concern1 9 15 10–770 WS + +
Oedipina gephyra Critically
Endangered
B1ab(iii)+2ab(iii)3
[Endangered
B1ab(iii) 1]
3 16 1580–1810 CB +
Oedipina ignea Data Deficient1 7 14 1000–2000 WS +
Oedipina kasios Endangered
B1ab(iii) 2
4 15 950–1920 CB +
Oedipina koehleri* Endangered
B1ab(iii)3
33 15
3 628–945 CB +
Oedipina leptopoda Endangered
B1ab(iii) 2
3 15 700–1300 CB +
Oedipina nica* Endangered
B1ab(iii)3
33 15
3 1360–1660 CB +
Oedipina quadra Vulnerable B1ab(iii) 2 3 15 70–540 CB + + +
Oedipina petiola* Critically
Endangered
B1ab(iii)3
33 17
3 1580 CB +
Oedipina stuarti Data Deficient1 6 15 0–1000 CB + +
Oedipina taylori Least Concern1 8 15 140–1140 WS +
Oedipina tomasi Critically
Endangered
B2ab(iii) 1
3 16 1800 CB +
ANURA
Bufonidae (10)
Incilius campbelli Near Threatened1 11 10 70–1200 WS + +
141
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Incilius coccifer Least Concern1 15 6 0–1350 WS + + + + +
Incilius ibarrai Endangered
B1ab(iii) 1
7 11 1500–1730 WS + + +
Incilius leucomyos Endangered
B1ab(iii) 1
6 11 0–1600 CB + + +
Incilius luetkenii Least Concern1 16 7 0–1300 WS + + + + +
Incilius porteri Endangered
B1ab(iii)3 [Data
Deficient1]
3 13 1524–1890 CB + +
Incilius valliceps Least Concern1 26 5 0–2000 WS + + + + + +
Rhaebo haematiticus Least Concern1 12 11 0–1300 WS +
Rhinella chrysophora Endangered A2ac &
B1ab(iii,v) 1
4 12 750–1760 CB +
Rhinella marina Least Concern1 35 5 0–2000 WS + + + + + + + +
Centrolenidae (8)
Cochranella granulosa Least Concern1 11 12 0–1500 WS +
Espadarana prosoblepon Least Concern1 14 12 0–1900 WS +
Hyalinobatrachium chirripoi Near Threatened1 9 12 0–700 WS +
Hyalinobatrachium
colymbiphyllum
Least Concern1 10 12 0–1710 WS +
Hyalinobatrachium fleischmanni Least Concern1 27 9 0–1730 WS + + + + +
Sachatamia albomaculata Least Concern1 12 12 0–1500 WS + + +
Teratohyla pulverata Least Concern1 11 12 0–950 WS + + +
Teratohyla spinosa Least Concern1 9 13 0–560 WS +
Craugastoridae (29)
Craugastor anciano Critically
Endangered
B1ab(iii,v)+2ab(iii,v)1
4 15 1400–1840 CB +
Craugastor aurilegulus Endangered
B1ab(iii,v)+2ab(iii,v)1
6 14 50–1550 CB + +
Craugastor bransfordii Least Concern1 10 11
5 20–1535 WS +
142
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Craugastor chac Near Threatened1 8 14 0–1000 WS +
Craugastor charadra Endangered
B1ab(iii, v) 1
7 13 30–1370 CB + +
Craugastor chrysozetetes EXTINCT1 3 17 880–1130 CB +
Craugastor coffeus Critically
Endangered
B1ab(iii) + 2ab(iii) 1
3 17 1000 CB +
Craugastor cruzi Critically
Endangered A2ace,
B1ab(iii,v)
+2ab(iii,v)1
3 17 1520 CB +
Craugastor cyanochthebius Critically
Endangered
B1ab(iii)+2ab(iii)2
[Near Threatened1]
3 17 900–1200 CB +
Craugastor emleni Critically
Endangered A2ace,
B2ab(v) 1
3 14 800–2000 CB +
Craugastor epochthidius Critically
Endangered A3ce1
5 15 150–1450 CB +
Craugastor fecundus Critically
Endangered A2ace1
5 15 200–1260 CB +
Craugastor fitzingeri Least Concern1 14 13 1–1520 WS + +
Craugastor laevissimus Endangered A2ace1 11 8 0–2000 CB + + + + +
Craugastor laticeps Near Threatened1 13 14 10–1600 WS + +
Craugastor lauraster Endangered
B1ab(iii) 1
6 14 40–1200 CB + + +
Craugastor megacephalus Least Concern1 10 14 1–1200 WS +
Craugastor merendonensis Critically
Endangered A2ace,
B1ab(v)+ 2ab(v) 1
3 17 150–200 CB +
143
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Craugastor milesi Critically
Endangered A2ae1
4 15 1050–1720 CB +
Craugastor mimus Least Concern1 9 13 15–700 WS +
Craugastor nefrens Data Deficient1 3 17
4 800–1000 CB +
Craugastor noblei Least Concern1 11 13 4–1200 WS + + +
Craugastor olanchano Critically
Endangered A2ace1
3 16 1180–1350 CB
Craugastor omoaensis Critically
Endangered A2ace,
B1ab(iii) 1
3 16 760–1150 CB +
Craugastor pechorum Endangered
B1ab(iii) 1
5 15 150–680 CB +
Craugastor rhodopis Least Concern1 16 14 0–1370 WS +
Craugastor rostralis Near Threatened1 6 14 850–1800 WS + +
Craugastor saltuarius Critically
Endangered A2ace1
3 16 1550–1800 CB +
Craugastor stadelmani Critically
Endangered A2ace1
4 15 1125–1900 CB + +
Eleutherodactylidae (1)
Diasporus diastema Least Concern1 11 14 0–1620 WS +
Hylidae (35)
Agalychnis callidryas Least Concern1 17 10 0–1200 WS + + + + +
Agalychnis moreletii Critically
Endangered A3e1
19 13 200–2130 WS + + +
Agalychnis saltator Least Concern1 9 13 0–819 WS +
Anotheca spinosa Least Concern1 11 15 95–2068 WS +
Bromeliohyla bromeliacia Endangered A2ace1 8 15 900–1790 WS +
Cruziohyla calcarifer Least Concern1 9 12 30–820 WS +
Dendropsophus ebraccatus Least Concern1 16 11 0–1320 WS +
Dendropsophus microcephalus Least Concern1 19 5 0–1200 WS + + + + + + +
144
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Duellmanohyla salvavida Critically
Endangered
B2ab(iii,v) 1
5 12 90–1400 CB +
Duellmanohyla soralia Critically
Endangered
B2ab(iii,v) 1
7 10 40–1570 CB +
Ecnomiohyla miliaria Vulnerable;
B1ab(iii)1
9 15 0–1330 WS +
Ecnomiohyla salvaje Critically
Endangered
B1ab(iii) 1
5 16 1370–1520 CB +
Exerodonta catracha Endangered
B1ab(iii)+2ab(iii) 1
3 13 1800–2160 CB + +
Isthmohyla insolita Critically
Endangered
B1ab(iii)+2ab(iii) 1
3 16 1550 CB +
Isthmohyla melacaena Critically
Endangered
B2ab(iv) 2
[Near Threatened1]
3 16 1550 CB +
Plectrohyla chrysopleura Critically
Endangered A2ace,
B1ab(iii,v)+
2ab(iii,v)1
4 13 930–1550 CB +
Plectrohyla dasypus Critically
Endangered A2ace,
B1ab(iii,v)
+2ab(iii,v)1
3 13 1410–1990 CB +
Plectrohyla exquisita Critically
Endangered A3e1
3 13 1490–1680 CB +
145
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Plectrohyla guatemalensis Critically
Endangered A3e1
11 9 900–2800 WS + + +
Plectrohyla hartwegi Critically
Endangered A3e1
9 12 925–2700 WS +
Plectrohyla matudai Vulnerable B1ab(iii) 1 8 10 700–2300 WS + +
Plectrohyla psiloderma Endangered
B1ab(iii)1
4 12 2400–2530 CB +
Ptychohyla euthysanota Near Threatened1 10 11
4 200–2200 WS +
Ptychohyla hypomykter Critically
Endangered A3e1
11 9 340–2070 CB + + +
Ptychohyla salvadorensis Endangered
B1ab(iii) 1
8 11 700–2050 CB +
Ptychohyla spinipollex Endangered
B1ab(iii)+2ab(iii) 1
6 11 160–1580 CB +
Scinax boulengeri Least Concern1 11 11 0–700 WS +
Scinax staufferi Least Concern1 25 5 0–1530 WS + + + + + + + +
Smilisca baudinii Least Concern1 30 4 0–1925 WS + + + + + + + +
Smilisca phaeota Least Concern1 11 10 0–1116 WS + +
Smilisca sordida Least Concern1 13 11 0–1525 WS +
Tlalocohyla loquax Least Concern1 18 6 0–1585 WS + + + + +
Tlalocohyla picta Least Concern1 15 9 0–1300 WS + +
Trachycephalus venulosus Least Concern1 25 5 0–1610 WS + + +
Triprion petasatus Least Concern1 12 12 0–740 WS +
Leiuperidae (1) Least Concern1
Engytomops pustulosus Least Concern1 24 6 0–1540 WS + + + + +
Leptodactylidae (4) Least Concern1
Leptodactylus fragilis Least Concern1 25 6 0–1700 WS + + + + + + +
Leptodactylus melanonotus Least Concern1 25 6 0–1440 WS + + + + + +
Leptodactylus savagei Least Concern1 15 11 0–1200 WS +
146
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Leptodactylus silvanimbus Critically
Endangered
B2ab(iii,v) 1
4 13 1470–2000 CB +
Microhylidae (3)
Gastrophryne elegans Least Concern1 13 11 0–1500 WS +
Hypopachus barberi Vulnerable B1ab(iii) 1 10 11 1300–2500 WS +
Hypopachus variolosus Least Concern1 31 6 0–2200 WS + + + + +
Ranidae (6)
Lithobates brownorum Least Concern1 18 3 0–1200 WS + + + +
Lithobates forreri Least Concern1 20 8 0–1960 WS + +
Lithobates maculatus Least Concern1 16 6 40–3000 WS + + + +
Lithobates vaillanti Least Concern1 21 7 0–990 WS + + + +
Lithobates warszewitschii Near Threatened1 13 11 0–2500 WS +
Lithobates sp. nov. Endangered
B1ab(iii)+2ab(iii)3
CB +
Rhinophrynidae (1)
Rhinophrynus dorsalis Least Concern1 18 9 0–700 WS + +
Strabomantidae (2) Least Concern1
Pristimantis cerasinus Least Concern1 9 14 19–680 WS + +
Pristimantis ridens Least Concern1 12 12 0–1600 WS + + +
REPTILIA
TESTUDINES
Chelydridae (2)
Chelydra acutirostris Data Deficient3 12 13 0–1164 WS + +
Chelydra rossignonii Vulnerable A2d1 11 14 0–660 WS + +
Emydidae (1)
Trachemys venusta Near Threatened2 26 12 0–650 WS + +
Geoemydidae (4)
Rhinoclemmys annulata Near Threatened2
[Lower risk/least
concern1]
11 13 2–920 WS
147
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Rhinoclemmys areolata Near Threatened1 12 12 0–600 WS +
Rhinoclemmys funerea Near Threatened2
[Lower risk/least
concern1]
7 16 2–600 WS
Rhinoclemmys pulcherrima Near Threatened2 19 9 0–1480 WS + + +
Kinosternidae (3)
Kinosternon leucostomum Least Concern2 21 9 0–1500 WS + +
Kinosternon scorpioides Least Concern2 24 9 0–1500 WS + +
Staurotypus triporcatus Near Threatened2
[Lower risk/least
concern1]
10 15 0–300 WS +
CROCODILIA
Alligatoridae (1)
Caiman crocodilus Least Concern2
[Lower risk/least
concern1]
15 16 0–300 WS + +
Crocodylidae (1)
Crocodylus acutus Vulnerable A1ac1 22 13 0–650 WS + + + +
SQUAMATA: LIZARDS
Anguidae (6)
Abronia montecristoi Endangered
B2ab(iii) 2
[Endangered
B1+2c1]
4 15 1370 CB + +
Abronia salvadorensis Endangered
B2ab(iii) 2
3 16 2020–2125 CB +
Celestus bivittatus Near Threatened2 7 13 1510–1980 CB +
Celestus montanus Endangered
B1ab(iii)2
5 14 915–1372 CB +
148
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Celestus scansorius Endangered
B2ab(iii)2 [Near
Threatened1]
3 14 1550–1590 CB + +
Mesaspis moreletii Least Concern2 13 13 1450–3060 WS + + +
Corytophanidae (7)
Basiliscus plumifrons Least Concern2 11 13 0–780 WS +
Basiliscus vittatus Least Concern2 25 7 0–1500 WS + + + + + + + +
Corytophanes cristatus Least Concern2 20 11 0–1640 WS + +
Corytophanes hernandesii Least Concern2 14 12 0–1400 WS +
Corytophanes percarinatus Vulnerable B1ab(iii)2 11 14 200–2200 CB +
Laemanctus longipes Least Concern2 17 9 0–1200 WS + +
Laemanctus serratus Least Concern1 17 12 0–1600 WS +
Eublepharidae (1)
Coleonyx mitratus Least Concern2 16 10 0–1435 WS + + + + +
Gymnophthalmidae (1)
Gymnophthalmus speciosus Least Concern2 24 8 0–1320 WS + + + +
Helodermatidae (1)
Heloderma horridum Near Threatened4
[Least Concern1]
11 144 100–1530 WS +
Iguanidae (8)
Ctenosaura bakeri Critically
Endangered
B1ab(i,ii,iii,v)+
2ab(i,ii,iii,v) 1
3 19 0–5 CB +
Ctenosaura flavidorsalis Endangered
B1ab(iii,v)+2ab(iii,v)1
8 13 370–750 CB + +
Ctenosaura melanosterna Critically
Endangered
B1ab(iii,v) 1
5 17 0–300 CB + +
149
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Ctenosaura oedirhina Critically
Endangered
B1ab(iii) 1
3 18 0–20 CB +
Ctenosaura palearis Endangered
B1ab(i,ii,iii,iv,v)+
2ab(i,ii,iii,iv,v) 1
3 174 150–700 CB +
Ctenosaura praeocularis Endangered
B1ab(iii,v)3 [Data
Deficient1]
33 17
3 800–1000 CB +
Ctenosaura quinquecarinata Endangered
B1ab(iii,v)+2ab(iii,v)1
5 165 0–250 WS + +
Ctenosaura similis Least Concern1 22 11 0–1320 WS + + + + + + + +
Iguana iguana Least Concern2 26 12 0–1000 WS + + + + + + + +
Phrynosomatidae (3)
Sceloporus malachiticus Least Concern2 16 8 540–3800 WS + + +
Sceloporus variabilis Least Concern2 25 7 0–1500 WS + + + +
Sceloporus squamosus Least Concern2 14 10 0–2500 WS + + +
Phyllodactylidae (3)
Phyllodactylus palmeus Endangered
B2ab(iii)2
3 15 0–30 CB +
Phyllodactylus tuberculosus Least Concern2 23 10 0–1230 WS + + +
Thecadactylus rapicauda Least Concern2 21 10 0–1052 WS + + + +
Polychrotidae: (38)
Anolis allisoni Least Concern2 7 13 0–30 WS +
Anolis amplisquamosus Endangered
B2ab(iii, v)1
3 16 1530–2200 CB +
Anolis beckeri Least Concern2 22 11 0–1780 WS + +
Anolis bicaorum Endangered
B2ab(iii)2
3 16 0–20 CB +
Anolis biporcatus Least Concern2 23 10 0–2000 WS + + + +
Anolis capito Least Concern2 19 11 0–1250 WS + + + +
150
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Anolis carpenteri Least Concern1 6 13
5 4–682 WS +
Anolis crassulus Least Concern2 11 13 1200–3200 WS +
Anolis cupreus Least Concern2 13 9 0–1435 WS +
Anolis cusuco Endangered
B1ab(iii) 1
3 16 1550–1935 CB +
Anolis heteropholidotus Endangered
B2ab(iii)2
4 14 1860–2200 CB +
Anolis johnmeyeri Endangered
B1ab(iii)2
3 15 1340–1825 CB +
Anolis kreutzi Critically
Endangered
B1ab(iii)+2ab(iii)2
3 16 1670–1690 CB +
Anolis laeviventris Least Concern2 17 9 500–2000 WS + + +
Anolis lemurinus Least Concern2 26 9 0–2000 WS + + + +
Anolis limifrons Least Concern2 13 12 0–1340 WS +
Anolis lionotus Least Concern1 5 13 20–1200 WS +
Anolis loveridgei Endangered
B1ab(iii)1
6 14 550–1600 CB +
Anolis morazani* Critically
Endangered
B1ab(iii)2
3 16 1780–2150 CB +
Anolis muralla Vulnerable D21;
Critically
Endangered
B1ab(iii)+2ab(iii)2
3 15 1440–1740 CB +
Anolis ocelloscapularis Endangered
B1ab(iii)2
4 15 1150–1450 CB +
Anolis petersii Vulnerable B1ab(iii)2 14 13 200–2130 WS +
Anolis pijolensis Critically
Endangered
B1ab(iii)2
4 14 1180–2050 CB +
151
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Anolis purpurgularis Endangered
B1ab(iii)+2ab(iii)2
3 15 1550–2040 CB +
Anolis quaggulus Least Concern2 8 12 0–1350 WS +
Anolis roatanensis Endangered
B1ab(iii)+2ab(iii)2
3 15 0–30 CB +
Anolis rodriguezii Least Concern2 16 10 0–2000 WS + +
Anolis rubribarbaris Critically
Endangered
B1ab(iii)2
3 16 1700 CB +
Anolis sminthus Endangered
B1ab(iii)+2ab(iii)2
[Data Deficient1]
4 15 1450–2200 CB +
Anolis tropidonotus Least Concern2 20 5 0–1900 WS + + + + + +
Anolis uniformis Least Concern2 13 11 0–1370 WS +
Anolis unilobatus Least Concern2 26 7 0–1200 WS + + + +
Anolis utilensis Critically
Endangered
B1ab(iii) 2
3 16 0–5 CB +
Anolis wampuensis Endangered
B2ab(iii) 2
3 16 95–110 CB +
Anolis wermuthi Vulnerable B1ab(iii)5 3 15
5 1230–1660 CB +
Anolis yoroensis Endangered
B1ab(iii)+2ab(iii) 2
4 14 1180–1600 CB +
Anolis zeus Endangered
B1ab(iii) 2
5 14 90–900 CB + +
Polychrus gutturosus Least Concern2 12 12 6–700 WS +
Scincidae (6)
Mabuya unimarginata Least Concern2 27 7 0–1800 WS + + + + + + +
Mesoscincus managuae Least Concern2 10 12 0–920 WS +
Plestiodon sumichrasti Least Concern2 16 11 0–1000 WS + +
Sphenomorphus assatus Least Concern2 16 13 0–2500 WS +
152
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Sphenomorphus cherriei Least Concern2 23 7 0–1860 WS + + + + + +
Sphenomorphus incertus Vulnerable B1ab(iii)2 6 12 1350–1670 WS +
Sphaerodactylidae (5)
Gonatodes albogularis Least Concern2 20 10 0–1000 WS + + + +
Sphaerodactylus dunni Vulnerable B1ab(iii)2
[Least Concern1]
4 14 60–230 CB + +
Sphaerodactylus glaucus Least Concern2 14 13 0–1000 WS +
Sphaerodactylus millepunctatus Least Concern2 19 7 0–1000 WS + + + + + +
Sphaerodactylus rosaurae Endangered
B2ab(iii) 2
3 15 0–20 CB +
Teiidae (5)
Ameiva festiva Least Concern2 20 10 0–1400 WS + + + +
Ameiva undulata Least Concern2 27 7 0–1800 WS + + +
Aspidoscelis deppii Least Concern1 22 8 0–1200 WS + + + +
Aspidoscelis motaguae Least Concern1 12 9 175–1200 WS + +
Cnemidophorus lemniscatus Least Concern2 9 12 0–1000 WS +
Xantusiidae (2)
Lepidophyma flavimaculatum Least Concern2 19 11 0–1400 WS + + +
Lepidophyma mayae Vulnerable
B1ab(iii)2
7 13 100–800 +
SQUAMATA: SNAKES
Anomalepididae (1)
Anomalepis mexicanus Data Deficient2 8 11 5–500 WS +
Boidae (2)
Boa constrictor Least Concern2 32 8 0–1500 WS + + + + + + + +
Corallus annulatus Least Concern2 9 11 0–400 WS +
Colubridae (110)
Adelphicos quadrivirgatum Least Concern2
[Data Deficient1]
19 8 0–1740 WS + + + + + +
Amastridium sapperi Least Concern2 18 12 100–1600 WS +
Chironius grandisquamis Least Concern2 12 12 0–1600 WS + + +
153
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Clelia clelia Least Concern2 18 11 0–1000 WS + + + +
Coniophanes bipunctatus Least Concern2 18 11 0–1000 WS + +
Coniophanes fissidens Least Concern2 28 9 0–2200 WS + + + + +
Coniophanes imperialis Least Concern1 19 11 0–2000 WS + + + + +
Coniophanes piceivittis Least Concern1 23 11 0–1305 WS + + +
Conophis lineatus Least Concern1 22 9 0–1500 WS + + + +
Crisantophis nevermanni Least Concern2 11 14 0–1385 WS +
Dendrophidion clarkii Least Concern2 17 12 30–1500 WS + + +
Dendrophidion percarinatum Least Concern2 13 12 4–1200 WS + + +
Dendrophidion vinitor Least Concern1 18 13 15–1500 WS + +
Dipsas bicolor Least Concern2 8 11 4–1100 WS + +
Drymarchon melanurus Least Concern1 35 9 0–2500 WS + + + + + + + +
Drymobius chloroticus Vulnerable;
B1ab(iii)2
[Least Concern1]
18 11 500–2500 WS + + +
Drymobius margaritiferus Least Concern2 33 7 0–2000 WS + + + + + + +
Drymobius melanotropis Least Concern1 8 14 0–1400 WS + +
Enuliophis sclateri Least Concern2 10 11 0–1235 WS +
Enulius bifoveatus Critically
Endangered
B1ab(iii) 2
3 15 0–10 CB +
Enulius flavitorques Least Concern2 26 6 0–3000 WS + + + + +
Enulius roatanensis Endangered
B1ab(iii)+2ab(iii) 2
3 15 0–10 CB +
Erythrolamprus mimus Least Concern2 12 12 70–1400 WS + +
Ficimia publia Least Concern2 18 11 0–1000 WS +
Geophis damiani Critically
Endangered
B1ab(iii)+2ab(iii) 2
3 15 1075–1750 CB +
Geophis dunni Data Deficient1 3 16
5 900 CB +
154
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Geophis fulvoguttatus Endangered
B2ab(iii) 2
6 12 1680–2200 CB + +
Geophis hoffmanni Least Concern2 14 12 18–670 WS + + + +
Geophis nephodrymus Endangered
B2ab(iii) 2
3 14 1560–1580 C +
Geophis rhodogaster Endangered
B1ab(iii) 2 [Least
Concern1]
8 12 1480–2600 WS +
Hydromorphus concolor Least Concern2 16 9 1–1500 WS + + +
Imantodes cenchoa Least Concern2 30 6 0–2063 WS + + + +
Imantodes gemmistratus Least Concern2 26 10 2–1435 WS + + +
Imantodes inornatus Least Concern1 12 10 5–1450 WS + + +
Lampropeltis triangulum Least Concern2 36 9 0–2500 WS + + + + + + +
Leptodeira nigrofasciata Least Concern2 18 10 0–1300 WS + + +
Leptodeira rhombifera Least Concern3 28 8 0–2000 WS + + + + + +
Leptodeira septentrionalis Least Concern2 33 9 0–2000 WS + + + + +
Leptodrymus pulcherrimus Least Concern2 14 10 10–1300 WS + + + + +
Leptophis ahaetulla Least Concern2 24 8 0–1680 WS + + + +
Leptophis depressirostris Least Concern5 9 13
5 4–1120 WS +
Leptophis mexicanus Least Concern2 28 8 0–1700 WS + + + + + + +
Leptophis modestus Endangered
B1ab(iii)2
8 15 1500–2500 WS + + +
Leptophis nebulosus Least Concern2 12 14 0–1600 WS +
Masticophis mentovarius Least Concern2 32 11 0–2500 WS + + + + + +
Mastigodryas alternatus Least Concern3 N/E 14
6 20–3006 WS +
Mastigodryas dorsalis Vulnerable B1ab(iii)2 10 12 635–1900 WS + + +
Mastigodryas melanolomus Least Concern1 N/E 9
6 0–10406 WS + + + +
Ninia diademata Least Concern1 19 8 0–2200 WS + + + +
Ninia espinali Endangered
B1ab(iii) 2 [Near
Threatened1]
5 12 1590–2242 CB + + +
155
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Ninia maculata Least Concern2 13 12 36–1800 WS +
Ninia pavimentata Endangered
B1ab(iii)2
5 12 1300–1500 WS +
Ninia sebae Least Concern2 28 4 0–2200 WS + + + + + + +
Nothopsis rugosus Least Concern1 11 12 2–830 WS +
Omoadiphas aurula Endangered
B2ab(iii) 2
3 15 1250–1900 CB +
Omoadiphas cannula Critically
Endangered
B1ab(iii)+2ab(iii)3
33 14
3 1250 CB +
Omoadiphas texiguatensis Critically
Endangered
B1ab(iii)+2ab(iii) 2
[Data Deficient1]
3 14 1690 CB +
Oxybelis aeneus Least Concern2 35 9 0–2500 WS + + + + + + +
Oxybelis brevirostris Least Concern2 12 13 4–800 WS +
Oxybelis fulgidus Least Concern2 27 10 0–1600 WS + + + + +
Oxybelis wilsoni Endangered
B1ab(iii)+2ab(iii)2
3 15 0–95 CB +
Oxyrhopus petola Least Concern2 18 13 0–800 WS + + +
Pliocercus elapoides Least Concern1 25 10 0–2000 WS + + + + +
Pliocercus euryzonus Least Concern1 13 14 0–1250 WS +
Pseudelaphe flavirufa Least Concern1 21 12 0–1200 WS + + +
Pseustes poecilonotus Least Concern1 22 12 0–1330 WS + + + +
Rhadinella anachoreta Endangered
B1ab(iii) 2
9 12 500–1180 CB + +
Rhadinella decorata Least Concern2 20 11 0–1400 WS + +
Rhadinella godmani Vulnerable B1ab(iii) 2 13 9 1200–2200 WS + + +
Rhadinella kinkelini Least Concern1;
Vulnerable B1ab(iii) 2
10 12 1370–2085 CB + + +
156
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Rhadinella lachrymans Least Concern1;
Vulnerable B1ab(iii) 2
12 13 500–3000 WS +
Rhadinella montecristi Endangered
B1ab(iii)2
7 12 1370–2620 CB + +
Rhadinella pegosalyta Critically
Endangered
B1ab(iii)+2ab(iii) 2
3 14 CB +
Rhadinella rogerromani Vulnerable B1ab(iii)5 3 16
5 1450 CB +
Rhadinella tolpanorum Endangered
B1ab(iii)+2ab(iii) 2
3 15 1690–1900 CB +
Rhinobothryum bovallii Least Concern1 9 15 4–550 WS +
Scaphiodontophis annulatus Least Concern2 19 12 0–1400 WS + + + +
Scaphiodontophis venustissimus Least Concern2 11 11 2–830 WS +
Scolecophis atrocinctus Least Concern2 14 14 100–1530 WS + +
Senticolis triaspis Least Concern2 30 10 10–2500 WS + + +
Sibon annulatus Least Concern2 10 12 2–1300 WS +
Sibon anthracops Least Concern2 12 14 4–915 WS + +
Sibon carri Endangered
B1ab(iii)2
8 12 30–800 CB + +
Sibon dimidiatus Least Concern1 18 11 0–1600 WS + + + +
Sibon longifrenis Least Concern2 9 11 60–750 WS +
Sibon manzanaresi Critically
Endangered
B1ab(iii)+2ab(iii) 2
3 15 250–300 CB +
Sibon miskitus Critically
Endangered
B1ab(iii)+2ab(iii) 2
3 15 150 CB +
Sibon nebulatus Least Concern2 27 8 0–1690 WS + + + +
Spilotes pullatus Least Concern2 30 9 0–1500 WS + + + + + +
Stenorrhina degenhardtii Least Concern2 23 10 0–1900 WS + + + + + +
Stenorrhina freminvillei Least Concern1 22 11 0–2000 WS + + + +
157
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Storeria dekayi Least Concern1 13 9 0–1900 WS + + +
Tantilla armillata Least Concern2 14 9 0–1435 WS + + + +
Tantilla impensa Least Concern1 10 12 300–1600 CB +
Tantilla lempira Endangered
B1ab(iii)+2ab(iii) 2
4 13 1450–1730 CB +
Tantilla sp. nov. * Critically
Endangered
B1ab(iii)+2ab(iii)3
33 16
3 1150 CB +
Tantilla psittaca Vulnerable B1ab(iii) 53 12
3 5–420 CB +
Tantilla schistosa Least Concern2 24 10 40–1680 WS + + +
Tantilla taeniata Least Concern2 13 10 0–1280 WS + + + +
Tantilla tritaeniata Critically
Endangered
B1ab(iii)+2ab(iii)2
3 15 0 CB +
Tantillita lintoni Least Concern1 15 13 0–550 WS +
Thamnophis fulvus Least Concern1 10 14 1680–3500 WS +
Thamnophis marcianus Least Concern2 22 13 0–1400 WS +
Thamnophis proximus Least Concern1 27 9 0–2500 WS + + + + +
Tretanorhinus nigroluteus Least Concern2 18 8 0–1200 WS + + +
Trimorphodon quadruplex Least Concern2 14 10 0–2000 WS + +
Tropidodipsas fischeri Least Concern1 12 12 1000–3000 WS +
Tropidodipsas sartorii Least Concern2 26 12 0–2000 WS + + + +
Urotheca decipiens Least Concern2 10 11 15–1500 WS +
Urotheca guentheri Least Concern1 13 12 25–1600 WS +
Xenodon rabdocephalus Least Concern2 24 12 0–1300 WS + + + + +
Elapidae (6)
Micrurus alleni Least Concern2 11 15 1–1620 WS +
Micrurus browni Least Concern3 15 13 0–2200 WS +
Micrurus diastema Least Concern2 19 12 50–600 WS + + +
Micrurus mipartitus Least Concern5 6 15
5 2–1160 WS +
Micrurus nigrocinctus Least Concern2 21 9 0–1600 WS + + + +
158
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Micrurus ruatanus Critically
Endangered
B1ab(iii)1
3 17 0–20 CB +
Leptotyphlopidae (2)
Epictia ater Least Concern6 33 6 0–1600 WS + + + +
Epictia magnamaculata Endangered
B1ab(iii)+2ab(iii)
5 9 0–25 CB +
Loxocemidae (1)
Loxocemus bicolor Least Concern2 16 11 0–750 WS + + +
Typhlopidae (3)
Typhlops costaricensis Least Concern2 11 11 540–1500 WS + +
Typhlops stadelmani Endangered
B1ab(iii) 2
6 12 320–1370 CB + + +
Typhlops tycherus* Data Deficient2 3 14 1550 CB +
Ungaliophiidae (1)
Ungaliophis continentalis Vulnerable B1ab(iii)2 11 12 990–2300 WS + +
Viperidae (12)
Agkistrodon bilineatus Near Threatened1 17 15 0–1500 WS +
Atropoides indomitus Endangered
B1ab(iii)2
33 17 670–1200 CB +
Atropoides mexicanus Least Concern2 17 12 0–1600 WS + + + +
Atropoides occiduus Vulnerable4 7 15
4 100–1600 WS +
Bothriechis marchi Endangered
B1ab(iii, iv)2
5 16 500–1840 CB + +
Bothriechis schlegelii Least Concern2 21 12 0–1530 WS + + + +
Bothriechis thalassinus Vulnerable
B1ab(iii)+2ab(iii)2
5 15 1370–1750 CB + +
Bothrops asper Least Concern2 25 12 0–1300 WS + + + + +
Cerrophidion sp. Vulnerable B1ab(iii)2 15 12 1300–2875 WS + + +
159
Table 3-2. Continued.
Taxon
IUCN Red List
Status CSS EVS
Elevational
Distribution
(m)
General
Distribution CL CV NC CC SC PL PV IB
Crotalus simus Least Concern2 21 12 500–2600 WS + + + + +
Porthidium nasutum Least Concern1 18 12 0–1100 WS + + + +
Porthidium ophryomegas Least Concern2 15 9 0–1400 WS + + + +
Sources for Red List Status: 1IUCN Red List (2011) 2Townsend & Wilson (2010) 3Evaluated for this study 4Acevedo et al. (2010) 5Sunyer & Köhler (2010) 6McCranie (2011a) Table 3-3. Composition of the Chortís Block herpetofauna, compared with regional (Mesoamerica = MA; Wilson &
Johnson 2010) and global (worldwide = WW; AmphibiaWeb 2011, Uetz et al. 2011). FAMILIES GENERA SPECIES CB MA WW CB MA CB MA WW
Gymnophiona 1 1 9 2 4 2 16 188 Caudata 1 4 10 5 17 43 241 614
Anura 11 16 38 33 68 100 474 6,086 AMPHIBIA 13 21 57 40 89 145 731 6,888 Crocodylia 2 2 3 2 2 2 3 24 Testudines 4 9 14 5 19 10 55 323 Squamata 22 31 61 87 179 225 1,090 8,883 REPTILIA 28 42 78 94 200 237 1,148 9,413
TOTALS 41 63 135 134 289 382 1,879 16,301
160
Table 3-4. Broad distributional patterns of herpetofaunal diversity in the Chortís Block. CB = Chortís Block restricted, WS = widespread, CL = Caribbean Lowlands, CV = Caribbean Intermontane Valleys, NC = Northern Cordillera, CC = Central Cordillera, SC = Southern Cordillera, PL = Pacific Lowlands, PV = Pacific Intermontane Valleys, IB = Islas de la Bahia.
Distribution Physiographic Regions CB WS CL CV NC CC SC PL PV IB
Gymnophiona 0 2 2 2 0 0 0 1 0 0 Caudata 37 6 6 1 19 17 9 2 2 0
Anura 37 63 51 18 50 37 30 12 16 6 AMPHIBIA 74 71 59 21 69 54 39 15 18 6 Crocodylia 0 2 2 2 0 0 0 2 0 1 Testudines 0 10 6 6 0 0 0 2 1 0
Squamata: Sauria 26 61 36 31 32 21 20 18 20 13 Squamata: Serpentes 32 107 85 64 62 60 41 27 36 14
REPTILIA 57 180 129 103 94 81 61 49 57 28 TOTALS 131 251 188 124 163 135 100 64 75 34
Table 3-5. Endemic and conservation priority herpetofaunal diversity from the Chortís Block.
Families Genera Species
Endemic Species (% of endemic
species)
Critically Endangered
Species Endangered
Species Vulnerable
Species
Total % of Species that
are CR/EN/VU
Total % of Endemic
Species that are
CR/EN/VU
Gymnophiona 1 2 2 0 0 0 1 50% – Caudata 1 5 43 36 (84%) 19 12 2 74% 87%
Anura 11 33 100 37 (37%) 26 15 3 44% 100% AMPHIBIA 13 40 145 73 (51%) 45 27 6 54% 94% Crocodylia 2 2 2 0 0 0 1 50% – Testudines 4 5 10 0 0 0 1 10% – Squamata:
Sauria 13 26 87 32 (37%) 9 23 6 44% 97%
Squamata: Serpentes
9 61 139 32 (23%) 10 18 9 27% 90%
REPTILIA 28 94 237 64 (27%) 19 41 17 33% 96% TOTALS 41 134 382 134 (35%) 64 68 23 41% 96%
161
Table 3-6. Distribution by mountain ranges of the endemic amphibians and reptiles of the Chortís Highlands (exclusive of Caribbean and Pacific Lowlands and islands); mountain ranges are defined in Chapter 2.
Northern Cordillera Central Cordillera Southern Cordillera
Taxon Nom
bre
de D
ios:
Texíg
uat
Nom
bre
de D
ios:
Pic
o B
onito
Om
oa
Espír
itu S
anto
Jocon
al
Santa
Bárb
ara
Meám
bar
Monte
cill
os
Com
ayagu
a
Sula
co
La F
lor-
La M
ura
lla
Agalta
Bota
dero
s
Punta
Pie
dra
Patu
ca
Monte
cristo
Mere
ndón
Cela
qu
e
Era
nd
iqu
e
Puca-O
pa
laca
De la S
ierr
a
Lep
ate
rique
Dip
ilto
Coló
n
Dariense
CAUDATA Plethodontidae (36) Bolitoglossa carri + Bolitoglossa cataguana* + Bolitoglossa celaque + + + + Bolitoglossa conanti + + + Bolitoglossa decora + Bolitoglossa diaphora + Bolitoglossa dunni + + Bolitoglossa heiroreias + Bolitoglossa longissima + Bolitoglossa nympha + + + + + Bolitoglossa oresbia + Bolitoglossa porrasorum + + + Bolitoglossa synoria + Cryptotriton monzoni + Cryptotriton nasalis + Cryptotriton wakei + Dendrotriton sanctibarbarus + Nototriton barbouri + Nototriton brodiei + Nototriton lignicola + Nototriton limnospectator + + Nototriton picucha* + Nototriton saslaya + Nototriton stuarti + Nototriton tomamorum* +
162
Table 3-6. Continued.
Northern Cordillera Central Cordillera Southern Cordillera
Taxon Nom
bre
de D
ios:
Texíg
uat
Nom
bre
de D
ios:
Pic
o B
onito
Om
oa
Espír
itu S
anto
Jocon
al
Santa
Bárb
ara
Meám
bar
Monte
cill
os
Com
ayagu
a
Sula
co
La F
lor-
La M
ura
lla
Agalta
Bota
dero
s
Punta
Pie
dra
Patu
ca
Monte
cristo
Mere
ndón
Cela
qu
e
Era
nd
iqu
e
Puca-O
pa
laca
De la S
ierr
a
Lep
ate
rique
Dip
ilto
Coló
n
Dariense
Nototriton sp A (Pico Bonito)*
+
Nototriton sp B (Texiguat)* + Nototriton sp. C (Botaderos)*
+
Oedipina gephyra + Oedipina kasios + Oedipina koehleri* + Oedipina leptopoda + + Oedipina nica* + Oedipina quadra + + Oedipina petiola* + Oedipina tomasi + ANURA (37) Bufonidae (3) Incilius leucomyos + + + Incilius porteri + + Rhinella chrysophora + + Craugastoridae (20) Craugastor anciano + Craugastor aurilegulus + + Craugastor charadra + + Craugastor chrysozetetes + Craugastor coffeus + + Craugastor cruzi + Craugastor cyanochthebius + Craugastor emleni + Craugastor epochthidius + + Craugastor fecundus + Craugastor laevissimus + + + + + + +
163
Table 3-6. Continued.
Northern Cordillera Central Cordillera Southern Cordillera
Taxon Nom
bre
de D
ios:
Texíg
uat
Nom
bre
de D
ios:
Pic
o B
onito
Om
oa
Espír
itu S
anto
Jocon
al
Santa
Bárb
ara
Meám
bar
Monte
cill
os
Com
ayagu
a
Sula
co
La F
lor-
La M
ura
lla
Agalta
Bota
dero
s
Punta
Pie
dra
Patu
ca
Monte
cristo
Mere
ndón
Cela
qu
e
Era
nd
iqu
e
Puca-O
pa
laca
De la S
ierr
a
Lep
ate
rique
Dip
ilto
Coló
n
Dariense
Craugastor lauraster + + + + + + + + Craugastor merendonensis + Craugastor milesi + + Craugastor nefrens + Craugastor olanchano + + Craugastor omoaensis + Craugastor pechorum + + Craugastor saltuarius + + Craugastor stadelmani + + + + HYLIDAE (13) Duellmanohyla salvavida + + Duellmanohyla soralia + + Ecnomiohyla salvaje + + Exerodonta catracha + + + + Isthmohyla insolita + Isthmohyla melacaena + Plectrohyla chrysopleura + + Plectrohyla dasypus + Plectrohyla exquisita + Plectrohyla psiloderma + + Ptychohyla hypomykter + + + + + + + + + + + + Ptychohyla salvadorensis + + + + + Ptychohyla spinipollex + + Leptodactylidae (1) Leptodactylus silvanimbus + + Ranidae (1) Lithobates sp. nov. + + + + SQUAMATA: LIZARDS (32)
Anguidae (5)
164
Table 3-6. Continued.
Northern Cordillera Central Cordillera Southern Cordillera
Taxon Nom
bre
de D
ios:
Texíg
uat
Nom
bre
de D
ios:
Pic
o B
onito
Om
oa
Espír
itu S
anto
Jocon
al
Santa
Bárb
ara
Meám
bar
Monte
cill
os
Com
ayagu
a
Sula
co
La F
lor-
La M
ura
lla
Agalta
Bota
dero
s
Punta
Pie
dra
Patu
ca
Monte
cristo
Mere
ndón
Cela
qu
e
Era
nd
iqu
e
Puca-O
pa
laca
De la S
ierr
a
Lep
ate
rique
Dip
ilto
Coló
n
Dariense
Abronia montecristoi + + + Abronia salvadorensis + Celestus bivittatus + + + Celestus montanus + + Celestus scansorius + + Corytophanidae (1) Corytophanes percarinatus + + Polychrotidae: (17) Anolis amplisquamosus + Anolis cusuco + Anolis heteropholidotus + + Anolis johnmeyeri + + Anolis kreutzi + Anolis loveridgei + + + Anolis morazani* + Anolis muralla + Anolis ocelloscapularis + + Anolis pijolensis + Anolis purpurgularis + + Anolis rubribarbaris + Anolis sminthus + + + + Anolis wampuensis + Anolis wermuthi + + Anolis yoroensis + + + Anolis zeus + + + Sphaerodactylidae (1) Sphaerodactylus dunni + SQUAMATA: SNAKES (27) Colubridae (21) Geophis damiani +
165
Table 3-6. Continued.
Northern Cordillera Central Cordillera Southern Cordillera
Taxon Nom
bre
de D
ios:
Texíg
uat
Nom
bre
de D
ios:
Pic
o B
onito
Om
oa
Espír
itu S
anto
Jocon
al
Santa
Bárb
ara
Meám
bar
Monte
cill
os
Com
ayagu
a
Sula
co
La F
lor-
La M
ura
lla
Agalta
Bota
dero
s
Punta
Pie
dra
Patu
ca
Monte
cristo
Mere
ndón
Cela
qu
e
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Geophis dunni + Geophis fulvoguttatus + + Geophis nephodrymus * + Ninia espinali + + + + Omoadiphas aurula + Omoadiphas cannula + Omoadiphas texiguatensis + Rhadinella anachoreta + + Rhadinella montecristi + + + + + Rhadinella pegosalyta + Rhadinella rogerromani + Rhadinella tolpanorum + Sibon manzanaresi + Sibon miskitus + Tantilla impensa + + Tantilla lempira + Tantilla psittaca + Tantilla sp. nov. * + Typhlopidae (2) Typhlops stadelmani Typhlops tycherus* Viperidae (4) Atropoides indomitus + Bothriechis marchi + + + + + + + + Bothriechis thalassinus + + + + Cerrophidion sp. + + + + + + + + + +
RANGE TOTALS 26 22 35 22 1 8 9 2 3 13 13 11 5 4 3 7 12 7 3 5 6 9 3 3 10
CORDILLERA TOTALS 72 42 37
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CHAPTER 4 THE CHORTIS BLOCK IS AN UNDERESTIMATED HOTSPOT OF AMPHIBIAN
DIVERSITY AND ENDEMISM
Over the past 20 years, amphibians have become emblematic of the myriad of
environmental issues that have led to the recognized global loss of biodiversity (Wake &
Vredenburg 2008). The global phenomenon of amphibian declines and disappearances,
termed the Global Amphibian Crisis, began coming to light at the First World
Herpetology Congress in 1989 as amphibian researchers met and related similar stories
of unexplained declines from opposite sides of the globe, often from seemingly pristine
habitats (Stuart et al. 2004; Mendelson 2011). Since that time, amphibian declines have
been traced to a variety of factors, including habitat loss and fragmentation (Cushman
2006), emerging diseases such as chytridiomycosis (Berger et al. 1998; Skerratt et al.
2007) and Ranavirus (Gray et al. 2009), and environmental contamination (Reylea &
Diecks 2008). Current rates of extinction in amphibians may approach 45,000 times the
background rate (Wake & Vredenburg 2008; Honeycutt et al. 2010), indicating that
amphibians as a group may be facing the worst threat to their survival as a group in
their 365 million-year existence. Furthermore, extinction risk is not evenly distributed
globally, with species found in tropical areas, and particular tropical streams, facing the
highest degree of threat (Dudgeon et al. 2006).
Paradoxically, the past 20 years has also seen the discovery and taxonomic
description of amphibian species increase at a remarkable pace (Köhler et al. 2005),
with number of recognized species rising 52% from 1992 (4,533; Duellman 1993) to
October 2011 (6,885; AmphibiaWeb 2011), meaning about one-quarter of all known
amphibians have been described in the past two decades. A principal reason for this
increase is the advent and widespread implementation of molecular approaches in
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systematic biology, allowing for rapid evaluation of large numbers of samples and
identification of candidate species (e.g. Vieites et al. 2009; Crawford et al. 2010). This
rapid increase in amphibian discovery and description was documented in Köhler et al.
(2005), whose meta-analysis demonstrated that most recently described species were
not simply subdivisions of described species and were as or more distinctive (as
measured by DNA sequence divergence) as species described in previous eras of
taxonomic activity, therefore refuting the notion that the recent rise in new amphibian
discoveries is an artifact of taxonomic inflation. Rather, the increase is being fuelled by
wider implementation of molecular methods in biodiversity inventory, intensified efforts
to sample poorly-known areas, particularly in tropical regions, and a rise in the number
of working taxonomists from developing countries, i.e. those countries that contain the
majority of undescribed diversity (Joppa et al. 2011).
The juxtaposition of increasing loss of diversity and habitats with the accelerated
documentation of new diversity has a number of important implications. First, this
suggests that amphibians in some of the world’s most diverse regions may be going
extinct without ever becoming known to the scientific community (Köhler et al. 2005;
Crawford et al. 2010). As pointed out in a number of recent works (e.g., Janzen et al.
2009; Monaghan et al. 2009; Honeycutt et al. 2010), this potential loss underscores the
need for rapid taxonomic assessments across a wide taxonomic breadth. The use of a
single or multiple DNA fragments (i.e. DNA barcoding) has been proposed, and widely
implemented, as a standardized method for rapidly assessing taxonomic diversity
(Hebert et al. 2003).
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DNA barcoding initially received a mixed reception among specialists and potential
practitioners (Moritz & Cicero 2004), largely fuelled by a backlash to the effort of a
limited number of advocates (Tautz et al. 2002, 2003) for the development of a single-
marker based ―DNA taxonomy‖ for broad-scale use in the assignment of unknown
samples to named taxa and the enhancement of taxonomic discovery (Lipscomb et al.
2003; Seberg et al. 2003). Even promotion of the term ―DNA barcode‖ is a point of
contention and misunderstanding, given its inherent implication that each species
possesses a fixed identification marker analogous to the Universal Product Code (UPC)
on the side of a cereal box rather than a perpetually evolving sequence of biological
molecules (Moritz & Cicero 2004).
A single fragment of the mitochondrial gene cytochrome oxidase subunit I (COI),
~650 base-pair (bp) in length, has been intended for use as a universal metazoan DNA
marker, with the goal of generating a comprehensive reference dataset for use in DNA
barcode-based biodiversity inventory projects (Hebert et al. 2003; Smith et al. 2008).
While COI has been demonstrated as effective for species-delimitation in mammals
(Clare et al. 2007), birds (Kerr et al. 2007), fishes (Ward et al. 2009), and a variety of
invertebrates (Virgilio et al. 2010), its use as a ―universal‖ marker for amphibians has
been somewhat controversial. In some groups of amphibians, COI shows a
misleadingly high degree of intraspecific variation that can overlap with interspecific
divergence and mask species boundaries (Vences et al. 2005a, 2005b), while in other
groups is has been used effectively (Smith et al. 2008; Xia et al. 2011), demonstrating a
clear gap between intraspecific and interspecific sequence divergence, i.e. the
―barcoding gap‖. A principal problem limiting the universal implementation of COI in
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amphibians is in fact its high degree of variation, with variability in the priming regions
across multiple groups leading to high rates of failure in PCR amplification (Vences et
al. 2005b), which can be addressed by the use of degenerate primers (Meyer 2003) or
by designing group-specific primer sets (Smith et al. 2008), however taking these steps
also diminishes the ―universality‖ that is promoted as an advantage of DNA barcoding.
The proposed alternative to COI is use of a ~530 bp fragment of the large subunit
rRNA gene (16S) as a ―universal amphibian barcoding gene,‖ which has a number of
benefits compared with COI, including 1) conserved priming regions that amplify
successfully across amphibian groups using a single set of primers (Mueller 2006), 2)
reduced frequency of overlap between intraspecific and interspecific divergence
(Vences et al. 2005a, 2005b), and 3) widespread use of 16S in amphibian studies prior
to widespread implementation of DNA barcoding methods, providing a relatively large
and well-explored reference dataset for comparison of newly acquired sequence data
(e.g. García-París & Wake 2000).
An alternative to selecting a single marker for use in amphibian barcoding studies
is to take a two-gene barcoding approach, for which I see the following advantages:
1. Distance-based analyses of COI and 16S data can be directly compared for congruence in species delimitation, reducing concerns over erroneous species identification based on use of a single marker.
2. Expansion of available reference data by allowing comparisons to sequences only available for one marker or the other.
3. Taken together, COI and 16S represent fragments of two classes (protein-coding and rRNA) of mitochondrial genes with differential rates of evolution, a preferable combination of characteristics for use in phylogenetic analysis.
As the benefits and limitations of DNA barcoding have become more clearly
defined (Hebert & Gregory 2005; Hajibabaei et al. 2007), the approach has gained
acceptance among systematic biologists as a useful, even powerful, addition to the
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methods used for the exploration and description of biological diversity (e.g. Vieites et
al. 2009). Rather than consider DNA barcoding as an alternative to traditional taxonomic
methods, I view it as a means of providing verifiable taxonomic assignment of samples
and for identifying samples in need of more rigorous evaluation; the molecular analog to
the process of providing preliminary taxonomic assignments to samples morphologically
using a dichotomous key. In this capacity, sequence data is evaluated using distance-
based methods with the sole intention of providing a means of DNA-based taxonomic
assignment and identification of potential candidate species, rather than generating
hypotheses of evolutionary relationships, which is the goal of phylogenetics.
Consequently, distance-based neighbor-joining (NJ) trees used in DNA barcoding are
simply graphical representations of genetic distances used to quickly assess the
presence of reciporically-monophyletic sequence clusters. In cases where further
analysis appears warranted, the sequence data used in the barcoding study should be
supplemented with data from additional loci and subject to more rigorous phylogenetic
analysis.
Scientists engaged in rapid biodiversity inventories using DNA barcoding should
also be committed to following up that work, or at least tangibly supporting the follow-up
to the work, with focused work in descriptive systematics. The taxonomic description of
new species is considered a top priority as systematic biology moves through the era of
elevation biodiversity loss, and is given the same level of importance as the biodiversity
inventory work itself by Systematics Agenda 2000 (1994) and the IUCN Global
Amphibian Assessment (Parra-Olea et al. 2007). An accurate and functioning taxonomy
provides the critical basis for not only conservation and management planning, but also
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communicating about biodiversity conservation with the general public (Parra-Olea et al.
2007; Honeycutt et al. 2010). While the relative ease with which new species can be
identified using molecular methods has led to the dramatic rise in known amphibian
diversity, the proverbially painstaking and specialized work required to address alpha
taxonomy leads to a lag between the molecular identification of potential candidate
species and the formal description of newly identified taxa (Wheeler 2004).
The amphibian fauna of the Chortís Block has largely mirrored the global patterns
of both decline and discovery (Townsend & Wilson 2010a). More than half (54%) of
Chortís Block amphibians are in one of the three highest IUCN threat categories
(Critically Endangered, Endangered, and Vulnerable), and include an alarming 74% of
salamanders (Chapter 3, Table 3-5). Honduras, the country making up the majority of
the geographic territory of the Chortís Block, has 49 endemic amphibians, 46 of which
were discovered and described since 1976 (Townsend & Wilson 2010a). While the
Chortís Block has been demonstrated to have a regionally distinctive component of
endemic biodiversity, particularly in amphibians (Campbell 1999; Wilson & Johnson
2010), molecular characterization of Chortís Block amphibian diversity has been
restricted to a few studies of wider geographic focus and limited within-region sampling
(García-París & Wake 2000; Parra-Olea et al. 2004; Hillis & Wilcox 2005; Frost et al.
2006).
Given these considerations, I followed an iterative process to inventory and
characterize phylogenetic diversity in Chortís Block amphibians. I present p-distance-
based results from COI and 16S sequencing of 456 samples representing 52 named
species in nine amphibian families, and use these results to identify samples using the
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existing taxonomy and to delimit potential candidate species for future study. Among
Chortís Block amphibians, salamanders exhibit both the highest degree of endemism
and extinction risk, and, based on the current taxonomy, are the most comprehensively
sampled group among my data. I provide tentative taxonomic assignments for ten
unidentified populations of salamanders (discussed in Chapter 3), identifying both new
candidate species and new populations and morphotypes of known species. I then
employ maximum likelihood-based phylogenetic analysis to evaluate evolutionary
relationships among Chortís Block salamanders. Implications for taxonomy,
biogeography, and conservation are discussed.
Methods and Materials
Sampling and Sample Identification
Specimens were collected in the field between 2006 and 2011 (Chapter 3 for
details), with fresh tissue samples typically being preserved in SED buffer (20% DMSO,
0.25 M EDTA, pH 7.5, NaCl2 saturated; Seutin et al. 1991; Williams 2007), or 95%
ETOH. Vouchers were deposited in the Florida Museum of Natural History (FLMNH) at
the University of Florida (UF), Museum of Vertebrate Zoology, University of California,
Berkeley (MVZ), Senckenberg Museum, Frankfurt am Main, Germany (SMF), and
National Museum of Natural History, Smithsonian Institution (USNM). In addition, tissue
samples were deposited at the FLMNH Genetics Resources Repository in May 2009.
Species assignments for samples are based on morphological identification, and, in the
case of endemic species with limited distributions, collecting locality was also used to
help inform taxonomic assignments. The label ―sp. inquirenda‖ or ―sp. inq.‖ is applied to
samples of uncertain taxonomic assignment, determined a priori.
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Extraction, Amplification, and Sequencing
For salamanders, Template DNA was extracted from muscle tissue using the
Gentra PureGene Tissue Kit (QIAGEN, Valencia, CA) following manufacturer’s
instructions. Concentration and purity of DNA extract was estimated using a NanoDrop
1000 spectrophotometer (Thermo Fisher Scientific, Waltham, MA).
Regions of two mitochondrial genes were selected for amplification and
sequencing: 16S large subunit RNA (16S) and cytochrome oxidase subunit I (COI). The
locus 16S is widely used in studies of amphibian phylogeny, and is considered the
―amphibian barcoding gene‖ (Vences et al. 2005a, Vieites et al. 2009); COI is widely
promoted as the ―universal metazoan barcoding gene‖ (Hebert et al. 2003), but has not
been widely used in amphibians (Smith et al. 2008, Xia et al. 2011). Fragments of the
mitochondrial genes 16S and COI were amplified using the primers 16Sar-L and 16Sbr-
H for 16S (Palumbi et al. 1991) and dgLCO-1490 and dgHCO-2198 for COI (Meyer
2003). PCR reactions were typically 20L in total volume, containing ~25ng of DNA
template, 4 L 5X PCR buffer (final concentration 1X), 1.2 L of 25 mM MgCl2 (final
concentration 1.5 mM), 0.09 L of 10 mM dNTPs (0.045 mM), 0.8 L of each 10 M
primer (0.04 M), 0.01U of GoTaq Flexi polymerase (1U/L; Promega, Madison, WI,
USA), and 11.91 L H2O. Amplification profile for 16S consisted of an initial
denaturation for 3 minutes at 94°C, 35 cycles of denaturation at 94°C for 45 seconds,
annealing at 50°C for 45 seconds, and extension at 72°C for 45 seconds, with a final
elongation at 72°C for 5 minutes. COI used an initial denaturation for 1.5 minutes, 37
cycles of 94°C for 40 seconds, 45°C for 40 seconds and 72°C for 40 seconds, and a
final elongation at 72°C for 5 minutes. PCR products were verified using electrophoresis
174
on a 1.5% agarose gel stained with ethidium bromide. Unincorporated nucleotides were
removed from PCR product using 1 uL of ExoSAP-IT (USB, Santa Clara, CA, USA) per
10L of PCR product. Product was cycle sequenced forward and reverse stands using
the BigDye Terminator v3.1 Cycle Sequencing kit (Applied Biosystems, Inc., Carlsbad,
CA [ABI]); sequencing reactions typically included 0.8–1.2 L of PCR product, 1.1 L
5X ABI sequencing buffer, 0.22 L primer, and the balance in ddH2O for a total volume
of 5 L. The sequenced product was cleaned using spin column filtration through
Sephadex (G-50; GE Healthcare, London, UK). Cleaned product was electrophoresed
on an ABI 3130xl Genetic Analyzer.
Anuran samples were amplified and sequenced at the Smithsonian Institution
Laboratory of Analytical Biology (Suitland, Maryland) following standardized DNA
Barcode of Life (BOLD) protocols (Hebert et al. 2003, Borisenko et al. 2009). For these
samples, Template DNA was obtained using phenol-chloroform extraction implemented
by an AutoGen Geneprep 965 (AutoGen, Holiston, MA) automated DNA isolation robot.
Template DNA was then amplified for COI using the primers LCO-1490 and HCO-2198
(Folmer et al. 1994) and for 16S using the primers 16Sar-L and 16Sbr-H (Palumbi et al.
1991). Unincorporated nucleotides were removed from PCR product using 2 uL of
ExoSAP-IT per sample. Product was cycle sequenced using BigDye Terminator v3.1
Cycle Sequencing kit (ABI), cleaned using spin column filtration through Sephadex, and
electrophoresed on an ABI 3730xl DNA Analyzer.
Sequence Evaluation and Alignment
Sequences were manually assembled and trimmed using CLC Combined
Workbench 3 (CLCbio, Denmark). DNA barcode identification was carried out by
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comparing generated sequences to those in the National Center for Biological
Information (NCBI) database (http://www.ncbi.nlm.nih.gov/). Representatives from all
sampled species and unassigned samples were searched against the NCBI database
using BLASTN (Zhang et al. 2000) in order to identify reference sequences for inclusion
in this analysis; a complete list of samples used in this analysis is presented in Table 4-
1. A large number of reference sequences were included from a recent study of
Panamanian amphibians (Crawford et al. 2010), and referenced sequences for Ranidae
were from Hillis & Wilcox (2005). Samples representing ten populations of salamanders
of uncertain taxonomic assignment were searched using BLASTN against the NCBI
database. For use in BLASTN searching, consensus sequences were generated in CLC
Combined Workbench 3 for each set of non-divergent 16S samples representing a
single species. Finally, my newly generated sequences and reference sequences
identified in BLASTN searches were aligned under the default parameters using
ClustalW (Thompson et al. 1994) as implemented by the program MEGA5 (Tamura et
al. 2011). Alignments were then visually inspected and adjusted. No stop codons were
present in the COI sequences, indicating that these all were amplified from
mitochondrial COI and not nuclear pseudogenes (Song et al. 2008, Buhay 2009).
Distance-Based Barcode Metrics
Data analysis was undertaken at various scales. First, to provide a graphical view
of the family and generic level taxonomic discrimination of Chortís Block amphibians, all
newly generated sequences (Caudata + Anura) were used to construct neighbor-joining
(NJ) trees in MEGA5 under the uncorrected (p-distance) model using default settings
and with nodal support calculated with 1,000 nonparametric bootstrap replicates. Then,
newly generated data were combined with BLASTN reference sequences and
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separated into six datasets representing distantly-related monophyletic clades (Frost et
al. 2006, Pyron & Wiens 2011): Bolitoglossa, other Plethodontidae, Bufonidae, Hylidae,
Ranidae, and a ―Terrarana+‖ dataset containing Craugastoridae, Eleutherodactylidae,
Leptodactylidae, and Strabomantidae (these four groups do not form a monophyletic
group in combination). For each dataset, NJ trees were generated for both 16S and COI
under the uncorrected (p-distance) method described above, with 5,000 nonparametric
bootstrap replicates. Sequence divergences were estimated using uncorrected p-
distances, using the default parameters in MEGA5.
Phylogenetic Analysis
Evolutionary model-based hypotheses of phylogenetic relationships were
estimated for the salamander data, to provide a more rigorous evaluation of candidate
species identified in p-distance-based results. The 16S and COI alignments were
concatenated into a single dataset, and redundant haplotypes were removed to
streamline analysis. The combined dataset then was subjected to maximum likelihood
(ML) phylogenetic analysis using the program RAxML v7.2.8 (Stamatakis 2006),
performed with 1,000 bootstrap replicates under the GTR-GAMMA substitution model
(RAxML has a limited number of substitution models that can be implemented), with
data partitioned by 16S, COI codon position 1, COI codon position 2, and COI codon
position 3.
Species Delimitation and Candidate Species
Degrees of divergence between two sequences or groups of sequences (based on
uncorrected p-distance) are herein characterized as ―shallow‖ (16S: <0.5%; COI:
<1.0%), ―moderate‖ (16S: 0.5–2.0%; COI: 1.0–6.0%), or ―deep‖ (16S: >2.0%; COI:
>6.0%). To label samples of uncertain taxonomic assignment identified a posteriori, I
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use the terminology Confirmed Candidate Species, Unconfirmed Candidate Species,
and Deep Conspecific Lineage, as proposed by Vieites et al. (2009). Unconfirmed
Candidate Species (UCS) are lineages identified as being deeply divergent
genealogical lineages that have not yet been studied for differences in morphology or
other characters, but may represent distinct, unnamed species. Confirmed Candidate
Species (CCS) are unnamed but moderately to deeply divergent genealogical lineages
that are supported by morphological characters or other evidence of distinctiveness.
Deep Conspecific Lineages (DCL) are shallow to deeply divergent genealogical
lineages that lack clear morphological or other differences with described sister species,
yet represent putative evolutionary species that warrant further investigation. In general
discussion, I refer to all three categories as Potential Candidate Species.
Results
Broad Results for Distance-based Analyses
Newly-generated sequence fragments of the mitochondrial genes COI and 16S
were analyzed for a total of 437 individual samples representing 52 nominal species, 17
genera, and nine families of amphibians, as well as ten populations of salamanders with
undetermined taxonomic assignments (Figure 4-1, Table 4-1; previously-discussed in
Chapter 3). For my 437 samples, 391 COI sequences (10.5% failure rate) and 434 16S
sequences (0.7% failure rate) were successfully obtained. Average sequence lengths
and nucleotide compositions are summarized in Table 4-2. In each of the six
taxonomically-delimited datasets, 16S datasets included a greater number of reference
sequences than COI datasets, due to widespread use of 16S as the ―universal
amphibian barcode gene‖ (e.g., Zimkus & Schick 2010, Vieites et al. 2009).
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Figure 4-1. Radial phylogram showing coverage of higher-level taxonomic groups.
Family-level for anurans, genus/subgenus-level for salamanders. Phylogram generated using neighbor-joining method with uncorrected p-distances and1,000 bootstrap pseudoreplicates. Stars indicate potential candidate species identified in this study.
Analysis of both 16S and COI datasets revealed at least 36 new Potential
Candidate Species in eight of nine sampled amphibian families (Table 4-3), including 13
Confirmed Candidate Species (CCS), 17 Unconfirmed Candidate Species (UCS), and
six Deep Conspecific Lineages (DCL). If both CCS and UCS are assumed to represent
distinct undescribed species, then a 24.4% increase in diversity among the nine
targeted families is projected. However, this study focused on just 52 named species of
the 123 represented in those families, and these results represent a 57.7% increase
among ingroup taxa.
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Mean uncorrected p-distance between Anura and Caudata was 0.244 for 16S and
0.238 for COI, and mean genetic distance within Anura was 0.206 for COI and 0.146 for
16S, and within Caudata was 0.155 for COI and 0.084 for 16S. For Anuran families with
more than one species-level lineage sampled, intra-family mean genetic distance for
COI was 0.122 for Bufonidae, 0.113 for Craugastoridae, 0.154 for Hylidae, and 0.130
for Ranidae, and for 16S was 0.051 for Bufonidae, 0.104 for Craugastoridae, 0.068 for
Hylidae, and 0.064 for Ranidae. Between anuran families, mean genetic distance for
COI ranged from 0.199 (Bufonidae /Leptodactylidae) to 0.269
(Eleutherodactylidae/Ranidae), and for 16S from 0.128 (Hylidae/Leptodactylidae) to
0.278 (Craugastoridae/Ranidae). All samples of Caudata represent a single family,
Plethodontidae, which accounted for 36% of all COI and 38% of all 16S sequences
analyzed (Table 4-1), far more representation than any other family. Analysis of the
Caudata dataset recovered the same deeply-diverged higher-order clades (family,
genus, subgenus) as published phylogenetic hypotheses (García-París & Wake 2000,
Parra-Olea et al. 2004, Wiens et al. 2007, McCranie et al. 2008), however relationships
within these clades are poorly resolved (Figure 4-2).
Identification of Potential Candidate Species of Anura
Twenty new Potential Candidate Species of anurans were identified through
uncorrected p-distance analysis of the COI and 16S data (Table 4-3). A comprehensive
comparative dataset for 16S is available for Central American Bufonidae, based largely
on the work of Mendelson et al. (2005), Mendelson & Mulcahy (2010), Mulcahy &
Mendelson (2000), and Mulcahy et al. (2006). Reference sequences for COI were
limited to Panamanian samples assigned to Incilius coniferus and Rhaebo haematiticus
(Crawford et al. 2010), and two samples of I. nebulifer, the sister species to I. valliceps.
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Figure 4-2. Maximum likelihood phylogram of COI data showing generic and
subgeneric relationships of salamander samples.
181
Samples from this study were shown to be conspecific with the nominal species I.
coccifer (16S=0.2%), I. ibarrai (16S=0.3%; COI=0.5%), I. leucomyos (16S=0.2%;
COI=0.7%), I. luetkenii (16S=0.4%), I. porteri (16S=0.5%; COI=0.8%), and I. valliceps
(16S=0.8%; COI=0.7%). Two Unconfirmed Candidate Species were identified among
the Bufonidae data: I. cf. coniferus and R. cf. haematiticus (Figure 4-3).
The majority of Craugastoridae samples represented taxa that lacked comparative
reference sequences; only one sample of Craugastor fitzingeri (N060) was confirmed by
COI and 16S data (Figure 4-4). Most clades correspond with a priori taxonomic
assignments. Three Unconfirmed Candidate Species were identified: a divergent
population of C. cf. aurilegulus; and two from northern Nicaragua, C. sp. inquirenda 1
and C. sp. inquirenda 2 (Figure 4-4).
Reference sequences for the genus Diasporus (Eleutherodactylidae) were
available for four putative species (Crawford et al. 2010). Four samples of Diasporus cf.
diastema from northern Nicaragua form a well-supported clade based on 16S and the
single COI sequence is also deeply divergent (16S=7.1%; COI=15.7%) from the closest
available reference sequences (Fig . 4-4), representing an Unconfirmed Candidate
Species awaiting comparative morphological evaluation.
While a large number of congeneric reference sequences are available for 16S,
and to a lesser extend COI, all newly generated samples of Hylidae represented either
the first sequence data available for a putative species for both COI and 16S (the case
for at least 10 taxa), or a Potential Candidate Species assigned to another taxon.
Purported congeners tended to cluster together, except in the cases of Ptychohyla
salvadorensis, two species of Duellmanohyla, and two species of Exerodonta in the 16S
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Figure 4-3. COI (left) and 16S (right) neighbor-joining trees for Bufonidae. ** = boostrap
support ≥ 99, * = boostrap support ≥ 90; candidate species indicated with red stars.
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Figure 4-4. COI (left) and 16S (right) neighbor-joining trees for Craugastoridae,
Eleutherodactylidae, Leptodactylidae, and Strabomantidae. ** = boostrap support ≥ 99, * = boostrap support ≥ 90; candidate species indicated with red stars.
184
NJ tree (Figure 4-5). At least five Unconfirmed Candidate Species were identified in the
16S NJ tree and supported by the COI NJ tree (Figure 4-5, Table 4-3): a Plectrohyla,
two Ptychohyla, and two Smilisca.
Samples representing a single putative species, Leptodactylus fragilis
(Leptodactylidae), were the only members of this family included in this study. Four
samples from Honduras and Nicaragua are deeply divergent (16S=3.6%; COI=15.7%)
from that of Panamanian samples assigned to L. fragilis (Figure 4-4).
Only two 16S reference sequences provided taxonomic matches: Lithobates
macroglossa and L. taylori (Figure 4-6). Two GenBank samples are referred to L.
macroglossa; one sample clusters with samples from Caribbean versant localities in
Honduras that were identified as L. brownorum; the second L. macroglossa sample
forms a weakly supported sister lineage to the L. taylori clade (Figure 4-6). I tentatively
consider the latter sequence to represent L. macroglossa, while the widespread clade
represents L. brownorum. Two series of samples, one from Cerro Uyuca and one from
San Pedro La Loma, that were considered hybrids between L. brownorum and L. forreri
by McCranie & Wilson (2002) form well-supported clades for both COI and 16S (Figure
4-6). The 16S data places these as sister to a sample representing an undescribed
highland leopard frog from Costa Rica (Lithobates sp. 5 sensu Hillis & Wilcox 2005).
Among samples thought to represent the highland and piedmont stream-inhabiting L.
maculatus, considerable genetic diversity is seen in both COI and 16S data, and this
taxon apparently masks at least four Unconfirmed Candidate Species in the Chortís
Highlands (Figure 4-6). Samples assigned to L. warszewitschii from northern Nicaragua
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Figure 4-5. COI (left) and 16S (right) neighbor-joining trees for Hylidae. ** = bootstrap
support ≥ 99, * = boostrap support ≥ 90; candidate species indicated with red stars.
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Figure 4-6. COI (left) and 16S (right) neighbor-joining trees for Ranidae. ** = boostrap
support ≥ 99, * = boostrap support ≥ 90; candidate species indicated with red stars.
187
also a deeply divergent clade from L. warszewitschii samples from Panamá (Figure 4-
6).
Within the family Strabomantidae, samples from northern Nicaragua assigned to
Pristimantis ridens are shown to represent an Unconfirmed Candidate Species, deeply
divergent (16S=4.8%; COI=9.1%) from Panamanian samples referred to P. ridens, but
in themselves represent three candidate species (Figure 4-4).
BLASTN Results for Unassigned Salamander Sequences
Two of ten unassigned salamander populations matched available 16S references
sequences from NCBI: Nototriton sp. inquirenda 4 with N. lignicola, and Oedipina sp.
inquirenda 1 with O. kasios (Table 4-4). Both unidentified samples were from mixed
cloud forest in Parque Nacional (PN) Montaña de Yoro and matched with species
previously considered endemic to nearby PN La Muralla. A third population from the
same localities in PN Montaña de Yoro, Bolitoglossa sp. inquirenda 1, also matches its
counterpart from PN La Muralla, B. decora (Table 4-4), however these species exhibit
markedly different external morphology, discussed in further detail below. The
remaining seven salamander populations do not closely match with any sequences in
NCBI database (≤97% max ident by BLASTN).
Distance-Based Analyses of Caudata
A relatively comprehensive 16S reference dataset is available for Mexican and
Central American salamanders (García-París & Wake 2000, Parra-Olea et al. 2004,
Wiens et al. 2007, Adams et al. 2009); however, only five COI sequences (two
Bolitoglossa, two Oedipina, and one Nototriton) were available through NCBI. Intra-
generic divergence was lowest for Nototriton (16S=3.5%, n=25; COI=9.7%, n=16),
compared with Bolitoglossa (16S=5.5%, n=192; COI=12.7%, n=114), Cryptotriton
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Figure 4-7. COI (left) and 16S (right) neighbor-joining trees for Bolitoglossa. ** =
boostrap support ≥ 99, * = boostrap support ≥ 90; candidate species indicated with red stars.
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(16S=5.1%, n=5) and Oedipina (16S=7.5%, n=50; COI=13.5%, n=10). Between
salamander genera, mean genetic divergence for COI ranged from 20.5%
(Nototriton/Oedipina and Cryptotriton/Nototriton) to 21.9% (Cryptotriton/Oedipina), and
for 16S ranged from 11.3% (Nototriton /Oedipina) to 20.2% (Bolitoglossa/Cryptotriton).
New samples were recovered as conspecific with the following nominal species
(intraspecific divergence indicated parenthetically): Cryptotriton veraepacis (16S =0.0%;
COI=0.0%), Nototriton limnospectator (16S=0.3%; COI=0.2%), N. lignicola (16S=0.2%),
Oedipina gephyra (16S=0.1%; COI=0.0%), O. kasios (16S=0.1%), Bolitoglossa celaque
(16S=1.5%; COI=1.9%), B. conanti (16S=1.6%; COI=1.9%), B. diaphora (16S=0.0%;
COI=0.1%), B. dofleini (16S=0.3%; COI=0.1%), B. dunni (16S=0.3%), B. heiroreias
(16S=0.0%), B. longissima (16S=0.3%; COI=1.2%), B. mexicana (16S=2.1%;
COI=1.2%), B. nympha (16S=3.0%; COI=1.4%), and B. synoria (16S=0.1%;
COI=0.0%).
Sixteen Potential Candidate Species of salamanders were identified in the 16S
and COI data (Table 4-2). Populations assigned to B. porrasorum and N. barbouri from
Texíguat and Pico Bonito are divergent from each other at an interspecific level, and are
deeply divergent from samples representing the terra tipica of each nominal taxa
(Figures 4-7, 4-8). Samples from the Cordillera de Agalta (Nototriton sp. inq. 2) and
Sierra de Botaderos (Nototriton sp. inq. 3), representing the first known samples of
Nototriton from either mountain range, are sister clades (intraclade divergence 0.0% for
16S and 0.2–0.6% for COI; interclade divergence 1.7% for 16S and 0.29% for COI) and
are both Confirmed Candidate Species (CCS). Other CCS include a divergent sample
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Figure 4-8. COI (left) and 16S (right) neighbor-joining trees for Cryptotriton,
Dendrotriton, Nototriton, and Oedipina. ** = boostrap support ≥ 99, * = boostrap support ≥ 90; candidate species indicated with red stars.
from Texíguat (Nototriton sp. inq. 1), Oedipina cf. gephyra from Pico Bonito, Oedipina
sp. inq. 2 from the Cordillera de Dariense in Nicaragua, Oedipina sp. inq. 3 from the
southeastern piedmont of the Chortís Highlands in Nicaragua, and Bolitoglossa cf.
rufescens from the northern foothills of the Sierra de Omoa. Clusters of geographically-
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discrete, moderately divergent subclades (within subclade divergence 16S=0.0–0.8%;
COI=0.0–0.3%; between subclade divergence 16S=0.6–1.6%; COI=1.7–3.6%) were
also present in samples assigned to B. celaque and B. conanti (Figure 4-7), which have
not previously been differentiated morphologically (McCranie & Wilson 2002) and
therefore are considered Deeply Conspecific Lineages pending further evaluation of
morphological variation.
Phylogenetic Analysis of Caudata
After removing identical redundant haplotypes, data from 16S and COI were
concatenated into a single dataset consisting of 276 individual samples, with a total
aligned sequence length of 1,178 bp. Maximum likelihood (ML) analysis recovered a
topology largely congruent with previous analyses of available reference data (Figure 4-
9; García-París and Wake 2000, Parra-Olea et al. 2004, Wiens et al. 2007, McCranie et
al. 2008).
For Bolitoglossa, clades representing the subgenera Bolitoglossa, Eladinea,
Magnadigita, Nanotriton, and Pachymandra were recovered as monophyletic (Figure 4-
9). A clade corresponding to the Bolitoglossa dunni species group was also recovered,
containing the nominal taxa B. carri, B. cataguana, B. celaque, B. conanti, B. decora, B.
diaphora, B. dunni, B. flavimembris, B. heiroreias, B. longissima, B. morio, B. oresbia,
B. porrasorum, B. cf. porrasorum (Pico Bonito), B. cf. porrasorum (Texíguat), and B.
synoria (Figure 4.9). Within the B. dunni group, four phylogenetic divisions are
apparent, each corresponding to a discretely distributed group of species: Clade A (B.
celaque, B. heiroreias, B. synoria; across the ignimbrite highlands of the Southern
Cordillera), Clade B (B. carri, B. conanti, B. diaphora, B. dunni, B. oresbia; from the
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Figure 4-9. Maximum likelihood phylogram for the genus Bolitoglossa. Combined
16S/COI dataset, partitioned by gene with 1,000 bootstrap replicates.
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Sierra de Omoa southward to the Sierra del Merendón, then eastward to the Sierra de
Lepaterique and north again to the Montañas de Meámbar), Clade C (B. cataguana, B.
decora, B. longissima, B. porrasorum, B. cf. porrasorum [Pico Bonito], B. cf. porrasorum
[Texíguat]; the highlands of northern and north-central Honduras east to the Sierra de
Agalta), and Clade D (B. flavimembris, B. morio; Guatemala).
Taxonomic discrepencies in distance-based analyses (Figure 4-7) were confirmed
by ML analysis (Figure 4-9). Samples assigned to B. celaque from three mountain
ranges in the Southern Cordillera are recovered as an eastern clade (La Paz + Intibuca)
and a western clade (Celaque), with the La Paz samples forming a shallow sub-clade
within the eastern clade (Figure 4-9). Samples assigned to B. conanti also form a clade
of geographically-discrete, shallowly-divergent, monophyletic groups corresponding to
the Sierra de Espíritu Santo, Sierra del Merendón, Sierra de Omoa, and Cerro del
Mono, with the B. conanti complex clade recovered as sister to B. carri, itself endemic to
the Sierra de Lepaterique (Figure 4-9). Samples from the B. rufescens complex (sensu
McCranie & Wilson 2002) are assignable to either B. nympha or to an unnamed lineage
(Figure 4-9).
Clades corresponding to the putative genera Nototriton, Oedipina, and Cryptotriton
were supported in the ML analysis (Figure 4-10). For Nototriton, clades representing the
N. barbouri group, N. picadoi group, and N. richardi group were recovered as
monophyletic (Figure 4-10). As with Bolitoglossa, phylogenetic results were congruent
with distance-based results in terms of delimiting species-level lineages (Figures 4-8, 4-
10). Nototriton sp. inq. 1 was shown to be a phylogenetically distinctive and deeply
divergent lineage, sister to the entire N. barbouri group. Together, the Nototriton sp. inq.
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Figure 4-10. Maximum likelihood phylogram for the genera Nototriton, Oedipina, Dendrotriton, and Cryptotriton.
Combined 16S/COI dataset, partitioned by gene with 1,000 bootstrap replicates.
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1 and N. barbouri group clades represent an radiation endemic to the Chortís
Highlands. Inclusion of material from the type locality of N. barbouri in phylogenetic
analysis revealed the taxon to be widely paraphyletic with respect to populations from
Pico Bonito and Texíguat (Figure 4-10). Nototriton barbouri sensu stricto from the
vicinity of the type locality is the sister species to N. limnospectator, while the Pico
Bonito and Texiguat populations (themselves forming two distinct monophyletic
lineages) form a clade with N. brodiei from the highlands along the
Guatemala/Honduras border. Nototriton sp. inquirenda 4 and N. sp. inquirenda 5 from
central Honduras are shown to be conspecific with N. limnospectator and N. lignicola,
respectively. In reference to the N. picadoi group, N. saslaya was recovered as the
sister lineage to the remaining species of the group, and represents the only
representative of the N. picadoi group found in the Chortís Block.
For Oedipina, clades corresponding to the subgenera Oedipina, Oedipinola, and
Oeditriton were recovered as monophyletic (Figure 4-10). Samples of Oedipina from
five localities in northern Nicaragua were included, and represent two unnamed
lineages, O. sp. inquirenda 2 and O. sp. inquirenda 3; one in the Oeditriton clade and
one in the Oedipina clade. Oedipina sp. inquirenda 2, found at three isolated mountain
localities in northern Nicaragua, is a well-supported sister lineage to the other highland
dwelling species of Oeditriton, O. kasios, with the lowland form O. quadra remaining as
sister to the two highland lineages. The second Nicaraguan candidate species, O. sp.
inquirenda 3, is sister to a clade containing O. cyclocauda and O. pseudouniformis
(Figure 4-10). The nominal species O. gephyra, from Parque Nacional Pico Bonito and
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Reserva de la Vida Silvestre Texiguat, contains two monophyletic lineages (one at each
locality), and is itself a monophyletic group. Oedipina tomasi is the sister taxon to the
Oedipina gephyra complex, forming a monophyletic clade that is sister to the remaining
Oedipinola. A sample from a previously unknown allopatric population of Oedipina from
central Honduras, O. sp. inquirenda 1, is shown to be conspecific with O. kasios (Figure
4-10).
Discussion
Candidates for Further Taxonomic Study Among Anurans
Undescribed diversity in the Chortís Highlands is both geographically and
phylogenetically widespread. While a disproportionately large share of potential
candidate species are salamanders (n=16; 44%), unexpected diversity is present in all
families included in this study, with the exception of Microhylidae (containing three
widespread species that occur in the Chortís Block). Not surprisingly, the majority of
Potential Candidate Species have distributions limited to one or a few localities in the
Chortís Highlands, however even lowland anuran taxa heretofore considered to be
widespread throughout Central America (Köhler 2011), such as Diasporus diastema,
Leptodactylus fragilis, Pristimantis ridens, Lithobates warszewitschii, Rhaebo
haematiticus, and Smilisca baudinii, demonstrate deep divergence indicative of species-
level diversification (Table 4-3).
Below I present a brief account of each Potential Candidate Species, as well as
unassigned species identified through this study, providing details of distribution and
taxonomy relative to nominal taxa.
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Incilius coccifer/ibarrai/porteri
The toads of the Incilius coccifer species complex include three apparently
parapatric species in Honduras, although the distribution and taxonomic status of these
species are disputed by authorities (Mendelson et al. 2005; McCranie 2009). The
taxonomy of these populations has long been recognized as inadequate in terms of
characterizing the existing diversity (McCranie & Wilson 2002), and Mendelson et al.
(2005) revised the Incilius coccifer complex, including resurrection of the taxon I. ibarrai
(Figure 4-11A) and description of a new taxon, I. porteri (Figure 4-11B), to
accommodate premontane and highland populations of I. coccifer complex toads in the
Chortís Highlands. A leading authority on Honduran amphibians, James McCranie,
steadfastly has refused to recognize these taxa as valid (McCranie & Castañeda 2007;
McCranie 2006, 2009), stating that ―despite the recent review of the I. coccifer complex
by Mendelson et al. (2005), a thorough review of this complex is needed that includes
all known populations,‖ citing ―the reasons discussed by McCranie & Castañeda
(2007)‖, a Spanish-language field guide the Honduran amphibian fauna. McCranie
provided the following principal reasons for not recognizing the validity of I. ibarrai and I.
porteri:
1. ―Numerous problems‖ with the dissertation work of Mendelson (in which Mendelson presented morphological analyses of the I. coccifer complex) detailed by ―McCranie (in McCranie & Wilson 2002)‖(as stated in McCranie & Castañeda 2007:125), and the lack of address given to those concerns in Mendelson et al.’s (2005) monograph.
2. The single sample of Honduran I. coccifer sensu stricto included by Mendelson et al. (2005) is from the mesic portion of eastern Honduras, which McCranie (by inference) considers distinctive from populations of the Pacific lowlands and therefore not representative of typical I. coccifer.
3. The lack of inclusion of ―large specimens‖ from southern Honduras in the work of Mendelson et al. (McCranie 2009:4).
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Results from my 16S and COI data support recognition of both I. ibarrai and I.
porteri as valid species (Figure 4-3), and also demonstrate that populations of I. coccifer
from eastern Honduras are indeed conspecific with those from the Pacific lowlands and
apparently have a continuous distribution through subhumid areas around the southern
terminus of the Nuclear Central American highlands in northern Nicaragua.
The distribution of these taxa is more complicated and intertwined than was
initially recognized by Mendelson et al. (2005), and includes at least one area of
sympatry or near-sympatry between I. ibarrai and I. porteri on the southern side of
Parque Nacional Cerro Azul Meámbar in Departamento de Comayagua (CAC044, I.
porteri from Río Bonito, 1,570 m elevation; and IRL002 and IRL 004-05, I. ibarrai from
San Jose de Los Planes, 1,290 m elevation, approximately 6 airline km east-northeast
of Río Bonito, and JHT 2205 (Figure 4-11A) from Cerro Zarciadero, 1,835 m,
approximately 6 km south of Río Bonito). Even more curious, samples representing
both I. coccifer and I. porteri were collected on Isla del Tigre in the Golfo de Fonseca,
with I. coccifer (JHT3301) know from 190 m elevation and I. porteri (JHT 3302) known
from 520 m elevation. Clearly, further sampling and investigation is needed to determine
the extent of each species’ distribution, identify areas of sympatry, and explore
ecological or behavioral mechanisms isolating these closely related species.
Incilius coniferus
The toads referred to the taxon Incilius coniferus are distributed from northern
Nicaragua (Travers et al. 2011) south to the Pacific versant of Colombia and northern
Ecuador (Savage 2002). A single sample from Bosawas (Figure 4-11C) is included in a
clade with the holotype of I. karenlipsae (Mendelson & Mulcahy 2010) and eight
samples referred to as I. coniferus (Figure 4-3). In comparisons with the available COI
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Figure 4-11. Candidate Species I: Bufonidae and Craugastoridae. A) Incilius ibarrai,
Cerro Zarciadero, 1,800 m (Photo © J.H. Townsend [JHT]). B) I. porteri, Cerro Uyuca 1,640 m. C) I. cf. coniferus, Biosfera Bosawas, 180 m (Photo © Scott Travers). D) Rhaebo cf. haematiticus, Biosfera Bosawas, 180 m (Photo © Javier Sunyer). E) Craugastor cf. aurilegulus, adult female, San José de Texíguat, 200 m (Photo © JHT). F) C. cf. aurilegulus, adult male, same data as E (© JHT); G) C. laevissimus, Río Negro de Comayagua, 1,220 m (Photo © JHT). H) C. laevissimus, Cerro Azul Meámbar, 800 m (Photo © JHT).
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data, the Bosawas sample (N416) is a strongly supported, distant sister to eight other
samples from Panamá (Figure 4-3).
Rhaebo haematiticus
This species is considered a relatively common and widespread inhabitant of
lowland and premontane rainforest from eastern Honduras to northern South America
(McCranie et al. 2006, Savage 2002). The Nicaraguan samples of Rhaebo haematiticus
(Figure 4-11D) forms a well-supported (bootstrap ≥99) reciprocally monophyletic sister
clade to Panamanian reference samples for both COI and 16S (Figure 4-3).
Craugastor aurilegulus
This species is currently recognized as endemic to the Cordillera Nombre de Dios.
Samples of C. aurilegulus from the vicinity of the type locality (Pico Bonito) and the
vicinity of Texíguat (Figures 4-11E, 4-11F) form well supported (bootstrap ≥99) clades
for both COI and 16S (Figure 4-4), and accordingly the Texíguat population is assigned
Deep Conspecific Lineage status and warrants further investigation to clarify its
taxonomic status.
Craugastor laevissimus
These data confirm the species C. laevissimus as a widespread member of the C.
rugulosus group with a distribution congruent with that defined by Campbell & Savage
(2000). Samples from the vicinity of the type locality in the Sierra de Omoa (JHT1824)
and from throughout the serranía in Honduras (Figures 4-11G, 4-11H; JHT series
samples) and into northern Nicaragua (N series samples) demonstrate relatively low
divergence between samples and no outwardly clean pattern of haplotype distribution
(Figure 4-4).
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Craugastor sp. inquirenda 1 & 2
Two Unconfirmed Candidate Species (Figure 4-12A) from northern Nicaragua
form a well-supported (bootstrap ≥99) but deeply-divergent clade with C. bransfordii
samples from Panamá (Figure 4-4). It may be that one of these populations will be
assigned to C. lauraster, a small species known from eastern Honduras and northern
Nicaragua (Köhler 2011), following investigation of morphological affinities of these
samples.
Diasporus diastema
Only a single putative species of Eleuthodactylidae, D. diastema, is considered to
naturally occur in northern Central America (Köhler 2011, McCranie et al. 2006). The
type locality of D. diastema is at the extreme eastern edge of its distribution in the
Panama Canal Zone, and samples from northern Nicaragua (Figure 4-12B) clearly
represent a monophyletic lineage divergent from Panamanian samples (Figure 4-4).
Further investigation is needed, preferably with inclusion of samples in the dataset from
eastern Honduras, southern Nicaragua, and Costa Rica.
Plectrohyla cf. guatemalensis
The taxon P. guatemalensis has long been recognized as a potential composite
taxon masking undescribed diversity (Duellman & Campbell 1992: 8, McCranie &
Wilson 2002: 301), and the ability to study the phylogenetic relationships of populations
assigned to this taxon has suffered from declines and disappearances of this cloud
forest treefrog from many localities where it previously was abundant. I have only
encountered one population of treefrogs assigned to P. guatemalensis (type locality:
Patzicia, Departamento de Chimaltenango, Guatemala; Stuart 1963): cloud forest
above 1,750 m in Parque Nacional Montaña de Yoro (Figures 4-12C, 4-12D). In both
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the 16S and COI NJ trees, this population is recovered as a divergent clade, and below
the intra-generic level does not demostrate any particular relationship to the single
reference available sequence (Figure 4-4). Populations assigned to this species are
known from across the Chortís Highlands (Duellman 2001), and a lack of representative
sampling will likely continue to hinder phylogeny-based taxonomic evaluation.
Ptychohyla hypomykter
Samples from across the serranía in Honduras and Nicaragua, including the type
locality at Quebrada Grande, appear to represent a single widespread species.
However single reference sequence assigned to this taxon (ENS8486 from Izabal,
Guatemala; Faivovich et al. 2005) is not recovered as part of the P. hypomykter clade,
nor does it cluster closely with any other species of Ptychohyla, representing an
Unconfirmed Candidate Species (Figure 4-5).
Ptychohyla spinipollex
This species is presently considered endemic to the vicinities of Texíguat and Pico
Bonito in the Cordillera Nombre de Dios. A single 16S reference sequence from
Quebrada de Oro in Parque Nacional Pico Bonito was surprising divergent from a series
of samples from La Liberación in Refugio de Vida Silvestre Texíguat, well into the range
normally applied to intraspecific relationships (Figure 4-5). Given the large genetic
distance between the Pico Bonito sample and the 18 samples from Texíguat, it is
somewhat surprising to see that the extreme variability in color pattern variation
exhibited by P. cf. spinipollex from Texíguat (Figure 4-12E–H) was not reflected by
genetic variation in 16S and COI.
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Figure 4-12. Candidate Species II: Eleutherodactylidae and Hylidae. A) Craugastor sp.
inquirenda 1, Cerro Saslaya, 1,000–1,600 m (Photo © Javier Sunyer). B) Diasporus cf. diastema, Biosfera Bosawas, 180 m (Photo © Javier Sunyer). C) Plectrohyla cf. guatemalensis, adult female, Montaña de Yoro, 1,820 m (Photo © J.H. Townsend [JHT]). D) P. cf. guatemalensis, adult male, Montaña de Yoro, 1820 m (Photo © JHT). E–G) Ptychohyla cf. spinipollex, La Liberación de Texíguat, 1,080–1,120 m. (Photo © JHT).
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Smilisca baudinii
This large treefrog is considered something of a ―trash‖ species that occurs from
México to Panamá, and is often abundant around areas of human disturbance. It is
likely that the disregard shown this taxon in the past, despite indications that there is
somewhat considerable geographically-linked morphological variation across its
distribution (Duellman 2001), has led to an underestimation of species-level diversity.
Both 16S and COI data support this notion, with two potential candidate species (one in
Honduras, one in northern Nicaragua) that are relatively deeply divergent from available
reference sequences assignable to S. baudinii (Figure 4-5).
Leptodactylus fragilis
This species is currently considered to have a range extending from Texas to
Venezuela (Heyer 2002), with a type locality of ―Tehuantepec, Mexique‖ (Brocchi 1877).
Samples assigned to L. fragilis from Honduras and Nicaragua form a clade that is
deeply divergent with respect to Panamanian samples referred to L. fragilis (Figure 4-4).
Given that the type locality is in México but remains unsampled, I will continue to refer
to Honduran and Nicaraguan samples as L. fragilis, and consider Panamanian samples
to be an Unconfirmed Candidate Species pending further investigation.
Lithobates brownorum X forreri
An unresolved taxonomic problem in the Chortís Highlands relates to the status of
populations of Lithobates that occur at high elevation ponds and wetlands in the
Southern Cordillera of the Chortís Highlands. McCranie and Wilson (2002: 478–479)
considered these frogs to represent morphological intermediates that possess a blend
of diagnostic features from both L. brownorum on the Caribbean versant and L. forreri
on the Pacific versant, and judged these intermediate populations to represent hybrids
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between the lowland forms L. brownorum and L. forreri (Figures 4-13A, 4-13B). These
high-elevation pond-breeding frogs apparently have an extended larval period, with
tadpoles regularly reaching or exceeding the size of adult males (Figure 4-13B). A total
of 15 samples were analyzed , eight from Cerro Uyuca in Departamento de Francisco
Morazán and seven from San Pedro La Loma in Departamento de Intibucá (Table 4-1).
All samples are supported as a single clade representing a Potential Candidate Species
(Figure 4-6). Analysis of 16S places this candidate species as sister to an undescribed
species from the central highlands of Costa Rica (Rana sp. 5 sensu Hillis & Wilcox
2005). The addition of data from the mitochondrial gene 12S would allow for these
Lithobates sp. inquirenda samples to be directly compared to a geographically
comprehensive dataset of Mexican Lithobates (Zaldívar-Riverón et al. 2004) in addition
to that of Hillis & Wilcox (2005), and should further elucidate the relationships of these
Honduran highland populations.
Lithobates brownorum
Examination of the Honduran ―hybrid‖ problem calls into focus a series of
unresolved taxonomic problems related to Central American frogs of the L. berlandieri
group. The identity of lowland forms from the Caribbean versant of Honduras and
northern Nicaragua, variously referred to as L. berlandieri (McCranie & Wilson 2002)
and L. brownorum (after Zaldívar-Riverón et al. 2004), is unconfirmed due to a lack of
comparative sequence data overlapping this dataset and both those of Zaldívar-Riverón
et al. (2004) and Hillis & Wilcox (2005).
Lithobates forreri
The status of the lowland frogs from the Pacific versant is even less clearly
defined, and they have been assigned to L. forreri from México to Costa Rica (McCranie
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Figure 4-13. Candidate Species III: Ranidae and Strabomantidae. A) Lithobates sp. 1 (―brownorum X forreri‖) Cerro Uyuca, 1,640 m (Photo © Jason Butler). B) Lithobates sp. 1 (―brownorum X forreri‖), comparing tadpole and adult male, Cerro Uyuca, 1,640 m (Photo © Jason Butler). C) Lithobates cf. maculatus, adult male, Cerro Saslaya, 1,000–1,600 m (Photo © Javier Sunyer). D) L. cf. maculatus, adult male, Cerro Saslaya, 1,000–1,600 m (Photo © Javier Sunyer). E) L. cf. maculatus, adult female, Montaña de Yoro, 1,820 m (Photo © J.H. Townsend). F) Lithobates cf. warszewitschii, Biosfera Bosawas, 180 m (Photo © Scott Travers). G) Pristimantis cf. ridens, Biosfera Bosawas, 180 m (Photo © Javier Sunyer). H) P.cf. ridens, Cerro Saslaya, 180 m (Photo © Javier Sunyer).
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& Wilson 2002; Savage 2002). Based on phylogenetic analysis of 12S mtDNA data,
Zaldívar-Riverón et al. (2004:47) demonstrated that the taxon L. forreri is referable only
to frogs from southern Sonora, México, south along the Pacific coastal plain not farther
than northern Jalisco, and in México alone there are no fewer than four well-supported
species masked under the name L. forreri. The relationship between Pacific lowland
populations assigned to L. forreri from Guatemala, El Salvador, Honduras, Nicaragua,
and Costa Rica, as well as the taxonomic assignment of various populations, remains
unresolved.
Lithobates maculatus
The putative species Lithobates maculatus currently is considered to be found at
premontane and lower montane elevations (and peripherally in the lowlands) throughout
Nuclear Central America (IUCN 2011; Köhler 2011). Both 16S and COI data indicate
the existence of at least four discretely-distributed Potential Candidate Species among
the Chortís Highland samples (Figure 4-6): one from northeastern Nicaragua, including
Cerro Saslaya and adjacent lowland rainforest areas (Figure 4-13C, 4-13D); one from
highland areas in north-central Nicaragua, including Cerro Kilambé and Peñas Blancas;
one from the southern side of the Texíguat cloud forest and the northern side of Pico
Pijol in north-central Honduras; and one from the rest of the Honduran serranía (Figure
4-13E). The ―serranía‖ clade itself is composed of four geographically discrete,
reciprocally monophyletic subclades (Figure 4-6). Two 16S sequence fragments
assigned to L. maculatus were available for comparison: KU 195258, from 19 km NW
Rizo de Oro, Oaxaca, México, and USNM 559483, from Quebrada de Oro in Parque
Nacional Pico Bonito, Honduras (Table 4-1). The Quebrada de Oro sample appears to
represent a fifth Potential Candidate Species (Figure 4-6). The Oaxaca sample may or
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may not be typical L. maculatus, whose type locality is Totonicapán, Guatemala, some
350 km southwest of the Oaxacan locality.
Lithobates taylori
The boundaries between the aforementioned L. brownorum and another
Caribbean lowland leopard frog, L. taylori, lack clear definition (McCranie & Wilson
2002, Savage 2002, Hillis & Wilcox 2005). While L. taylori is generally considered to
occur from somewhere in the central portion of Nicaragua and extend southward into
Costa Rica and presumably Panamá (Köhler 2011), the boundary between it and L.
brownorum to the north (if a boundary exists) is undefined, and the status of populations
of Lithobates from Panamá also is unclear (Hillis & Wilcox 2005). Interestingly, all
Lithobates berlandieri group samples from highland areas in northern Nicaragua cluster
with a single sample from a lowland site in eastern Nicaragua (Figure 4-6) that is
assigned to L. taylori by Hillis & Wilcox (2005), and I tentatively refer those samples to
L. taylori pending additional sampling throughout eastern Nicaragua.
Lithobates warszewitschii
This species is considered a relatively common and widespread inhabitant of
lowland and premontane rainforest from eastern Honduras south to central Panamá
(McCranie et al. 2006, Savage 2002). Previously published barcoding data (Crawford et
al. 2010) indicates that there are potentially two cryptic species concealed under L.
warszewitschii in Panamá, and samples from northeastern Nicaragua (Figure 4-13F)
form a third clade for both 16S and COI (Figure 4-6).
Pristimantis ridens
This species is considered a relatively common and widespread inhabitant of
lowland and premontane rainforests from northern Honduras to northern South America
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(Wang et al. 2008). Samples from low and moderate elevation in northern Nicaragua
(Figures 4-13G, 4-13H) form a clade in both 16S and COI analyses, deeply divergent
from samples from Panama (Figure 4-2). The Panamanian samples themselves appear
to represent three candidate species (Crawford et al. 2010).
Candidate Species and Allopatric Populations of Salamanders
I began this study with samples representing ten populations of salamanders that
could not be assigned unequivocally to a known species, due either to morphological
distinctiveness or from being found in a new locality that was geographically and
ecologically isolated from congeners. Four of these populations (Bolitoglossa sp.
inquirenda 1, Nototriton sp. inquirenda 1, Oedipina sp. inquirenda 1, and Oedipina sp.
inquirenda 2), do not correspond to any known species-level taxa, and have
subsequently been described as distinct taxa (Sunyer et al. 2010, 2011; Townsend et
al. 2009a, 2010a). One population, Nototriton sp. inquirenda 2, represents an
undescribed species from the Sierra de Agalta in eastern Honduras, and is further
evaluated in Chapter 5. Another population, Nototriton sp. inquirenda 3 from Montaña
de Botaderos, also represents an undescribed species. In the cases of Bolitoglossa sp.
inquirenda 2, Nototriton sp. inquirenda 4, N. sp. inquirenda 5, and Oedipina sp.
inquirenda 1, these samples were found to represent new allopatric populations of
species previously thought to be endemic to a single highland area (Townsend et al.
2011b). These cases, as well as a summary of information related to potential candidate
species and other resulting taxonomic considerations are detailed below.
Bolitoglossa (Magnadigita) sp. inquirenda 1
In June 2006, during the first herpetological expedition into the core zone of PN
Montaña de Yoro, two specimens of an unknown salamander diagnosable to the
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Bolitoglossa (Magnadigita) dunni species group were collected in the vicinity of
Cataguana (1,780–2,020 m elevation) in northern Departamento de Francisco Morazán.
On a return trip in March 2007, five additional samples were collected at the same
locality. BLASTN searches of 16S returned a high degree of similarity to B. decora from
PN La Muralla (Table 4-4). No 16S sequence divergence was observed between
samples series from two localities in Montaña de Yoro and the single available
sequence for B. decora, typically an indication that samples are conspecific. However,
the Montaña de Yoro series differs from B. decora in coloration, head width, and digit
length, as well as being allopatric and found within a different elevational band. This
evidence, supported by subsequent sequencing and comparative analysis of a widely
used fragment of the mitochondrial gene cytochrome b (cyt b), led Townsend et al.
(2009a) to recognize the PN Montaña de Yoro population as a young but distinct
species, Bolitoglossa cataguana (Figures 4-14A, 4-14B).
Bolitoglossa (Magnadigita) oresbia / sp. inquirenda 2
On 17–18 July 2007, I visited Cerro El Zarciadero in central Honduras, the type
locality of Bolitoglossa oresbia, finding a single subadult B. oresbia (UF 156333) active
on vegetation at night. This species was described recently on the basis of three
specimens collected from an irregular patch of remnant cloud forest (Lower Montane
Wet Forest formation) less than 1 hectare in total extent on the peak of Cerro El
Zarciadero (McCranie et al. 2005). This patch is the only remaining forest near the peak
of this mountain, and is adjacent to a set of communications towers and surrounded by
agricultural clearings given over primarily to corn and other staple crops. In the original
description, the authors indicated that B. oresbia was ―the most critically endangered
salamander in Honduras‖ (McCranie et al. 2005:111), and, given its extremely limited
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and vulnerable distribution, this species is classified as Critically Endangered on the
IUCN Red List and could be considered one of the most threatened amphibians on
earth. From 6–13 July 2008, we surveyed a ridge above Quebrada Varsovia
(14.79913°N, 87.89128°W), on the southwestern side of Parque Nacional Cerro Azul
Meámbar in Departamento de Comayagua. Seven specimens of Bolitoglossa were
collected, One adult salamander (Bolitoglossa sp. inquirenda 2; UF 156532) with a
distinctive golden yellow coloration covering most of its body (Figure 4-14C) was
collected in moist leaf litter during the morning of 12 July 2008 along the trail leading to
the aforementioned campsite (14.79618°N, 87.89527°W), 1,560 m elevation. This
golden individual was so distinctive in terms of color pattern that it was assumed to
represent a distinct taxon from B. oresbia; however both distance-based (sequence
divergence between Zarciadero and Meámbar samples 0.0–0.2% for 16S and 0.1% for
COI) and phylogenetic analyses confirm that this individual is conspecific with typical B.
oresbia (Figures 4-7). One adult male (UF 156529) and four small juveniles (UF
156526–27, 156530–31) were found while active on vegetation at night along a trail that
follows a steep hillside through undisturbed Lower Montane Wet Forest, 1,640–1,680 m
elevation. An adult female (UF 156528; Figure 4-14D) was collected along the same
trail during the daytime, when it was dislodged from a standing, rotten tree trunk
approximately 1 m above the ground. Two of the juveniles were red-orange in color and
resembled the golden morph of B. oresbia (Figure 4-14E), while the adults (Figure 4-
14D) and other two juveniles (Figure 4-14F) demonstrate coloration more typical of B.
oresbia. These new localities are only around 8 airline km north of Cerro Zarciadero,
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Figure 4-14. Candidate Species IV: Bolitoglossa. A) Bolitoglossa sp. inquirenda 1 (= B.
cataguana), adult female holotype, Montaña de Yoro, 1,820 m; B) B. sp. inquirenda 2 (= B. oresbia), subadult male, Cerro Azul Meámbar, 1,560 m; C) B. sp. inquirenda 2 (= B. oresbia), subadult male, Cerro Azul Meámbar, 1,640 m; D) B. sp. inquirenda 2 (= B. oresbia), adult female, Cerro Azul Meámbar, 1,640 m; E) B. sp. inquirenda 2 (= B. oresbia), juvenile, Cerro Azul Meámbar, 1,640 m; F) B. sp. inquirenda 2 (= B. oresbia), juvenile, Cerro Azul Meámbar, 1,640 m; G) B. celaque, adult female, Cerro Celaque, 2,560 m. Photos © J.H. Townsend.
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and the intervening area, while wholly converted to agriculture, is no lower than 1,300 m
elevation at any given point.
Bolitoglossa (Magnadigita) celaque
As currently recognized, Bolitoglossa celaque is a highland salamander found
across three mountainous areas of the Southern Cordillera of the Chortís Highlands,
including the Sierra de Celaque (Figure 4-14G; the type locality), the Sierra de Puca-
Opalaca, and the Montaña de la Sierra. Both 16S and COI data indicate that samples
from these three ranges each form clades (Figure 4-7). Although divergence among
these three clades is moderate (1.7–3.6%), the clear phylogeographic structure (within-
mountain range divergence ≤0.8% for 16S and ≤0.3% for COI) associated with these
samples indicates they may represent a complex of relatively young species, and
should be the focus of further study using finer-scale population-level approaches,
environmental niche modeling, and comparative morphology to clarify the systematic
status of populations assigned to B. celaque.
Bolitoglossa (Magnadigita) conanti
This highland salamander is presently considered to occur in the Sierra de Omoa,
Sierra de Espíritu Santo, and Sierra del Merendón, and is characterized by a high
degree of variability in coloration within populations (McCranie & Wilson 1993, 2002).
Both 16S and COI data revealed clades corresponding to geographically isolated
mountains ranges (Figure 4-7). As with B. celaque, divergence among these clades is
moderate (2.5–3.0% for COI) and within-mountain range is very low (0.0–0.2% for 16S
and 0.0% for COI), indicating relatively recent diversification, and should be the focus of
further study using multiple avenues of finer-scale investigation.
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Bolitoglossa (Magnadigita) porrasorum
As with the two other species of Chortís Highland Magnadigita currently thought to
occur at more than one isolated cloud forest locality, B. porrasorum populations are not
recovered as conspecific in distance-based analyses of 16S or COI data (Figure 4-7) or
ML analysis of the combined dataset (Figure 4-9). Populations of B. porrasorum from
the Sierra de Sulaco (where the type locality is found) and Texíguat and Pico Bonito in
the Cordillera Nombre de Dios each form geographically-discrete clades, although the
lineages assigned to B. porrasorum demonstrate greater genetic distances than those
of the B. celaque and B. conanti complexes and are potentially paraphyletic or
polyphyletic with respect to B. cataguana, B. decora, and B. longissima (Figure 4-7).
Samples from Texíguat demonstrate a remarkable degree of color polymorphism
(Figure 4-15), however all samples from this locality appear to represent a single taxon
(Figure 4-7).
Bolitoglossa (Nanotriton) rufescens/nympha
Salamanders of the Bolitoglossa rufescens complex in the Chortís Highlands
have a confusing taxonomic history (McCranie & Wilson 2002). Recently, Campbell et
al. (2010) described a new species from this complex, B. nympha, from a locality on the
western side of the Sierra de Caral in eastern Guatemala. Unfortunately, this description
did little to resolve the systematic relationships of the B. rufescens complex in the
Chortís Highlands, as it was based on 12S and cyt b sequence data from a single
sample. The use of only a single sample precludes characterization of diversity and
distribution of B. nympha, and the choice of 12S in favor of the previously ubiquitous (at
least for neotropical salamanders) 16S minimizes the ability of other researchers to
directly compare Campbell et al.’s (2010) results with the comprehensive existing
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Figure 4-15. Candidate Species V: Bolitoglossa cf. porrasorum. A–F) variation in color
pattern in conspecific samples of Bolitoglossa cf. porrasorum, La Liberación de Texíguat, 1,080–1,420 m. Photos © J.H. Townsend.
dataset available at NCBI. Comparative morphological analyses of other species and
populations in the B. rufescens complex, particularly the multiple known populations
from across the border (albeit in some cases in the same mountains) in Honduras are
also not available. Based on the type locality and description of B. nympha, I am
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inferring that four samples from two localities, one in the Sierra de Omoa and one in the
Sierra de Espíritu Santo, are conspecific with B. nympha (Figure 4-7). Surprisingly, of
five samples collected syntopically in El Paraiso Valley on the northern slope of the
Sierra de Omoa, three appear to be conspecific with B. nympha while two others
represent a deeply divergent (divergence between syntopic samples 5.5% for 16S and
17.6% for COI) cryptic species that is recovered in the 16S NJ tree as the sister to a
sample assigned to B. rufescens (MVZ 194254) from Chiapas, México.
Nototriton barbouri
All analyses support that two populations currently assigned to N. barbouri from
the Cordillera Nombre de Dios are paraphyletic with respect to a sample from the
vicinity of the type locality of N. barbouri (Figures 4-8, 4-10). Furthermore, those two
populations, one from Texíguat and one from Pico Bonito (McCranie 1996a), represent
two Potential Candidate Species, forming a clade with N. brodiei from the Sierra de
Omoa and Sierra de Caral (Figure 4-8). A systematic revision of this taxon is presented
in Chapter 5.
Nototriton sp. inquirenda 1
During a trip in April 2008 to the leeward side of RVS Texiguat in the vicinity of La
Fortuna, a single specimen of Nototriton was collected that possesses a series of
morphological characteristics unique among Honduran congeners. This single
salamander had greatly large nares, syndactylous hands and feet with pointed toe tips,
and a pale ventral surface with light mottling, characteristics typical of species in the N.
richardi group (Costa Rica) or the genus Cryptotriton. Data from 16S and COI indicate
that this species forms a sister clade to the remaining species of Chortís Highlands
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Nototriton (Figure 4-8), and this species was described as N. tomamorum by Townsend
et al. (2010a).
Nototriton sp. inquirenda 2
Two specimens of Nototriton were collected in July 2010 from cloud forest in PN
Sierra de Agalta, the first record of this genus from eastern Honduras. Both distance
and model-based analyses of COI and 16S data supports these samples as conspecific
and representative an unnamed species (Figure 4-8), which is further analyzed and
formally described in Chapter 5 (Townsend et al. 2011a).
Nototriton sp. inquirenda 3
Four specimens of Nototriton were collected in April 2011 along the highest ridge
(1,700+ m elevation) in the Sierra de Botaderos in northeastern Olancho. Both distance
and model-based analyses of COI and 16S data indicate that these samples are
conspecific and represent a new candidate species that is sister to Nototriton sp. inq. 2
(Figure 4-8). This candidate species is being described outside of this dissertation.
Nototriton lignicola / sp. inquirenda 4
On 10 June 2006, we collected a juvenile Nototriton (UF 156544) from inside a
fractured rock alongside Quebrada Cataguana (15.01°N, 87.10°W), 1,820 m elevation,
Parque Nacional Montaña de Yoro, in northern Departamento de Francisco Morazán.
On 14 March 2007, we collected two adult Nototriton (UF 156542–43) from inside rotten
logs on Cerro El Filón above Quebrada Cataguana, 2,020 m elevation. These samples
are shown to be conspecific with N. lignicola (Figure 4-8), a Critically Endangered
species previously known only from 13 specimens collected inside two rotten logs at
Cerro de Enmedio, Parque Nacional La Muralla, 1,760–1,780 m elevation (McCranie &
Wilson 2002).
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Nototriton limnospectator / sp. inquirenda 5
Nototriton limnospectator is an Endangered moss salamander previously known
only from forest above 1,600 m elevation in Parque Nacional Montaña de Santa
Bárbara, an isolated karstic mountain to the west of Lago de Yojoa. During 2008, four
specimens of Nototriton were collected from three sites in Parque Nacional Cerro Azul
Meámbar, including two individuals (UF 156539–40) found on 7 and 9 July 2008
alongside juvenile Bolitoglossa oresbia (UF 156526–27, 156530–31) while active on low
vegetation at night. Another individual (UF 156541) was collected on 27 August 2008
from near a campsite farther up the Quebrada Varsovia (14.80°N, 87.89°W), 1,710 m
elevation, while it was active at night on a root buttress. All three of these localities are
in the Lower Montane Wet Forest formation. In addition, a juvenile N. limnospectator
(UF collection) was collected from underneath a moss mat at night on 7 June 2008
along Sendero Bosque Nublado, 1,105 m elevation, above Centro de Visitantes de
Parque Nacional Cerro Azul Meámbar ―Los Pinos‖ (14.87°N, 87.91°W), Departamento
de Cortés, a locality that lies in the Premontane Wet Forest formation. These samples
were shown to be conspecific with reference samples of N. limnospectator from Parque
Nacional Montaña de Santa Bárbara (Figure 4-8). The new localities are approximately
20–25 km east of the nearest locality in Parque Nacional Montaña de Santa Bárbara
(McCranie & Wilson 2002), from which they are isolated by Lago de Yojoa, the largest
freshwater lake in Honduras.
Oedipina kasios / sp. inquirenda 1
On 25 September 2008, a single specimen of Oedipina (Figure 4-16A; UF 156500)
was collected in a small mesic ravine on Montaña de la Sierra (14.95°N, 87.061°W),
1,920 m elevation, in coniferous cloud forest on the southeastern side of Parque
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Nacional Montaña de Yoro. This specimen was shown to be conspecific with Oedipina
kasios Figure 4-8), a species recently described from Parque Nacional La Muralla as a
member of a divergent, Chortís Highlands endemic clade (subgenus Oeditriton;
McCranie et al. 2008). This species occurs from 950–1,780 m elevation, and has been
found in the same logs as Nototriton lignicola (McCranie et al. 2008). The Critically
Endangered amphibians Bolitoglossa cataguana and Plectrohyla guatemalensis were
also collected within and along the outer margins of this and similar ravines. The forest
in this part of PN Montaña de Yoro is typified by regularly burned pine-oak forest with an
open grassy understory interrupted by deep, narrow seepage ravines that support
dense mesic vegetation, providing refuge for species like O. kasios during fire events.
Oedipina nica / sp. inquirenda 2
Nicaraguan worm salamanders (Oedipina) have long been a source of taxonomic
uncertainty, the byproduct of conserved morphology and sparse sampling. During
2008–2009, a series of 18 Oedipina were collected from three highland localities in
northern Nicaragua (Figure 4-16B). These samples could not be assigned to a taxon
based on comparisons from BLASTN searches, NJ tree clustering, or sequence
divergence, and appeared to represent an undescribed species of the subgenus
Oeditriton (Figure 4-8). Sequencing and subsequent analysis of cyt b data, as well as
comparative morphology, confirmed that these samples represent a new species, which
we recently described as Oedipina nica (Sunyer et al. 2010).
Oedipina koehleri / sp. inquirenda 3
In his pioneering monograph of Oedipina, Brame (1968) described the taxon O.
pseudouniformis from central Costa Rica, and included eight paratypes collected in July
1957 from ―Hacienda La Cumplida, 1.5 km north of Matagalpa, 731 m elevation,‖
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Figure 4-16. Candidate Species VI: Oedipina. A) Oedipina sp. inquirenda 1 (= O.
kasios), Montaña de Yoro, 1,920 m (Photo © J.H. Townsend). B) O. sp. inquirenda 2 (= O. nica), Macizos de Peñas Blancas, 1,515 m (Photo © Scott Travers). C) O. sp. inquirenda 3 (= O. koehleri), Cerro Musún, 724 m (Photo © Javier Sunyer).
Figure 4-17. Candidate Species VII: Oedipina cf. gephyra (= O. petiola). A) dorsal view
of right hind foot of O. cf. gephyra (= O. petiola), Cerro Búfalo, 1,580 m; B) dorsal view of right hind foot of O. gephyra, Texíguat, 1,820 m; C) ventral view of right hind foot of O.cf. gephyra (= O. petiola); D) ventral view of right hind foot of O. gephyra, Texíguat, 1,820 m. Photos © J.H. Townsend.
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Departamento de Matagalpa, Nicaragua. Premontane forests in this area have been
severely degraded since 1957, and remaining patches of mesic forest are restricted to
the most marginal upper portions of the surrounding peaks. Köhler et al. (2004) later
assigned two specimens from pristine forest between approximately 600 and 945 m
elevation in Parque Nacional Cerro Saslaya, Región Autónoma Atlántico Norte,
Nicaragua, to O. pseudouniformis, recognizing that these samples appeared conspecific
with those from Hacienda La Cumplida. Analysis of recently collected samples from PN
Cerro Saslaya and an isolated mountain to the south, Cerro Musún (Figure 4-16C),
revealed them to represent a single undescribed species (Figure 4-8). We described
this species as O. koehleri based on evidence from phylogenetic analyses,
macroecological models, and morphology (Sunyer et al. 2011).
Oedipina gephyra
The endemic species Oedipina gephyra was described from the leeward side of
Reserva de Vida Silvestre Texíguat in the western portion of the Cordillera Nombre de
Dios, Honduras (McCranie et al. 1993), and soon after was reported from Parque
Nacional Pico Bonito in the central portion of the Cordillera Nombre de Dios (McCranie
1996b). A single representative from each of the two populations assigned to O.
gephyra was included in the phylogenetic analyses of García-París & Wake (2000), who
reported interspecific-level sequence divergence between the two samples (García-
París & Wake 2000: 70), suggesting that more than one species may be concealed
under O. gephyra. Multiple attempts to secure additional material from PN Pico Bonito
were unsuccessful, however the addition of two new samples of O. gephyra from the
vicinity of the type locality demonstrates that the two populations are reciprocally
monophyletic (Figure 4-8), supporting recognition of two species. Following the
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phylogenetic results, McCranie & Townsend (2011) also found diagnostic differences in
foot morphology (Figure 4-17), and subsequently described the Pico Bonito population
as O. petiola.
Amphibian Endemism and Conservation Priorities in the Chortís Block
The Chortís Block is already known to possess a diverse endemic amphibian
fauna, with 74 regionally endemic species with distributions restricted to within the
region (Chapter 3, Table 3-5). The identification of as many as 36 new species from a
subset of about 36% of named Chortís Block amphibians indicates that the ―true‖
diversity is largely underestimated. One-third of the Potential Candidate Species (12/36)
appear to be restricted to localities in the Northern Cordillera of the Chortís Highlands, a
region already known to support the highest level of amphibian endemism in the Chortís
Block (Chapter 3, Table 3-6). It comes as little surprise to me that six Potential
Candidate Species are from the vicinity of Texíguat at the western end of the Cordillera
Nombre de Dios (Table 4-3), a mountain range identified as one of most significant
endemism hotspots in Mesoamerica (Chapter 3; Townsend et al. 2010a, 2011c,
Submitted A). Four more species are from the vicinity of Pico Bonito, and another two
from the Sierra de Omoa (Table 4-3). Given that established protected areas
encompass most of the remaining highland forest in each of these three mountains
ranges, tangible opportunities for conserving extant populations of both named and un-
named endemic species already exist and could be strengthened by the description of
additional endemic diversity from within each park’s boundaries.
If it is assumed that at least the CCS and UCS represent distinct species, then,
including the six candidate species that have already been formally described, a total of
30 new endemic amphibian species are identified in the Chortís Block. Of these 30, at
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least 12 would immediately qualify as Critically Endangered based on IUCN Red List
criteria (IUCN 2001), and at least an additional nine species would be classified as
Endangered (Table 4-3).
A somewhat surprising finding was the identification of Potential Candidate
Species from sampled populations assumed a priori to represent widespread lowland
taxa such as Diasporus diastema, Lithobates warszewitschii, Pristimantis ridens,
Rhaebo haematiticus, and Smilisca baudinii. Should these populations be confirmed as
distinct species, the implication that there exists a previously unknown endemic
amphibian fauna inhabiting the Caribbean lowlands of northeastern Nicaragua (and
presumably eastern Honduras) would rather dramatically alter the understanding of
patterns influencing Chortís Block biogeography and diversification. Given the large
number of species that are presently considered to meet the northern limit of their
distribution in this area (as was the case with the aforementioned candidate species),
this revelation would warrant a comprehensive re-evaluation of conservation and
management objectives in the transboundary Mosquitia region, which is currently aimed
at the maintenance of ecological corridors principally to support populations of large
mammals such as jaguar, tapir, and white-lipped peccaries (CIPF 2009).
Accomplishment of a rapid amphibian inventory, emphasizing the collection of
molecular data, is urgently needed to assess the extent of endemic cryptic diversity
currently overlooked in the Caribbean lowlands of the Chortís Block.
Iterative Taxonomic Approaches to Biodiversity Inventory
In this chapter, I have provided the first comprehensive assessment of amphibian
evolutionary diversity for the Chortís Block of Central America, a region already
recognized for its elevated endemism. I have deliberately employed an iterative,
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heuristic approach to the systematic evaluation of regional diversity, with two principal
aims in mind. First, to initiate development of a comprehensive molecular reference
dataset upon which future work in the region can be directed and compared. Doing so
contributes to the goals set out by both the Systematics Agenda 2000 (1994) and the
IUCN Global Amphibian Assessment (2007) chief of which are the execution of rapid
inventories to catalog global biodiversity and the generation of a ―Tree of Life‖
phylogeny of all species to serve as the basis for classification and as a framework for
use by researchers in the life sciences. Second, the use of this approach is
advantageous in that it allows for, what I consider to be, the appropriate application of
DNA barcoding data and methods in taxonomy.
After establishing the ecophysiographic setting in Chapter 2 and providing a
comprehensive faunal treatment of the region’s amphibians and reptiles, I presented
and analyzed a comprehensive two-gene DNA barcoding dataset for Chortís Block
amphibians. As part of an iterative process, the distance-based analyses used in
association with DNA barcoding provide a vital step that can be used to guide how and
where to focus analytical resources moving forward. In this study, the Class Caudata
(the salamanders) represents both the most taxonomically comprehensive dataset
among groups of amphibians analyzed, and presents both the most Potential Candidate
Species (Table 4-3) and the highest degree of extinction risk (Chapter 3, Table 3-5). As
the next step, I used the two-gene barcoding dataset as the basis for model-based
maximum likelihood (ML) phylogenetic analysis in order to generate a phylogenetic
hypothesis that can be used to more rigorously establish species limits than can be
done using distance-based methods alone, and, to address a principal deficiency of
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distance-based analysis, estimate evolutionary relationships at a deeper level than that
of species and species-delimitation. Utilization of the two-gene approach to DNA
barcoding in this case allows for the initial dataset to be more informative
phylogenetically and therefore of more utility at later stages in the process of taxonomic
evaluation.
In the case of Chortís Block salamanders, DNA barcoding analyses indicated that
there are at least 12 CCS and USC and another four DCL that are in need of further
systematic study (Table 4-3). Phylogenetic analysis supports each of these Potential
Candidate Species as a monophyletic group (Figures 4-9, 4-10), and revealed further
details of evolutionary relationships within and among amphibian clades. One group in
particular, the moss salamanders (Nototriton), exhibited a relatively high degree of
cryptic diversification, and will serve as the model group for use in my subsequent
systematic evaluation. Phylogenetic analyses recovered three geographically-
circumscribed clades (Figure 4-10): a Northern Cordillera clade consisting of N. brodiei
from the Sierra de Omoa and Sierra de Caral, N. sp. 2 CCS from Pico Bonito, and N.
sp. 3 CCS from Texíguat; a central clade, consisting of N. barbouri sensu stricto from
the Sierra de Sulaco and N. limnospectator from Montaña de Santa Bárbara and the
Montañas de Meámbar; and an eastern clade, consisting of N. sp. inquirenda 2 (=N.
picucha; Townsend et al. 2011a) and N. sp. inquirenda 3 from the Sierra de Botaderos.
Nototriton sp. inquirenda 1 (=N. tomamorum; Townsend et al. 2010a), which possesses
distinctive morphological traits, was recovered as the sister lineage to the rest of the
Chortís Block endemic clade corresponding to the N. barbouri species group (sensu
García-París & Wake 2000). The Cordillera de La Flor-La Muralla endemic N. lignicola
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is recovered as sister to the rest of the in-group. Chapter 5 deals with the molecular and
morphological systematics and taxonomic revision associated with this group, providing
what is, in my estimation, the most critically overlooked yet definitively fundamental
activity for contemporary systematic biologists to engage in: the formal taxonomic
treatment of candidate taxon identified in molecular studies.
Conservation planners, ecologists, legislators, and the general public have little
use for metrics based on un-named, un-described diversity, and I do not foresee an
entity such as ―Nototriton sp. inq. 1 CCS‖ being promoted as part of a regional
conservation strategy or public outreach campaign. Despite the best intentions and
most diligent labor of biologists, in the end it is the greater share of society, made up of
non-scientists, which will determine the success or failure of this generation’s challenge
to preserve our shared biodiversity resources. Taxonomy provides the most basic
means for which the specialist can identify and communicate information about
biological diversity, and to carry out molecular inventories of biodiversity without
promoting the direct taxonomic evaluation of the results is, in my view, a disservice to
the study organisms themselves, our field of study, and to society as a whole.
228
Table 4-1. Voucher information for samples used in this study. Voucher abbreviations are as follows: JHT = author’s field series; IRL = Ileana R. Luque-Montes field series; AJC = Andrew J. Crawford field series; AMNH = American Museum of Natural History; JSF = John Frost tissue collection; KRL = Karen R. Lips field series; KU = University of Kansas Natural History Museum; MVUP = Museo de Vertebratos de la Universidad de Panamá, SIUC = Herpetology Collection, Southern Illinois University at Carbondale; USNM = National Museum of Natural History, Smithsonian Institution.
Taxon Voucher Locality 16S COI Data source
CAUDATA Plethodontidae (29) Bolitoglossa sp. inq. 1 JHT2087 Honduras: Cataguana + — This study (= B. cataguana) JHT2113 Honduras: Cataguana + — This study JHT2114 Honduras: Cataguana + — This study JHT2115 Honduras: Cataguana + + This study JHT2125 Honduras: Cataguana + — This study JHT2964 Honduras: above Guaymas + — This study JHT2965 Honduras: above Guaymas + + This study Bolitoglossa celaque JHT2743 Honduras: Cerro Celaque + + This study JHT2744 Honduras: Cerro Celaque + + This study JHT2745 Honduras: Cerro Celaque + + This study JHT2747 Honduras: Cerro Celaque + + This study JHT2748 Honduras: Cerro Celaque + + This study JHT2749 Honduras: Cerro Celaque + — This study JHT2750 Honduras: Cerro Celaque + + This study JHT2751 Honduras: Cerro Celaque + + This study JHT2752 Honduras: Cerro Celaque + + This study JHT2753 Honduras: Cerro Celaque + + This study JHT2754 Honduras: Cerro Celaque + + This study JHT2755 Honduras: Cerro Celaque + + This study JHT2756 Honduras: Cerro Celaque + + This study JHT2757 Honduras: Cerro Celaque + + This study JHT2903 Honduras: Intibucá + + This study JHT2904 Honduras: Intibucá + + This study JHT2910 Honduras: Intibucá + + This study JHT2911 Honduras: Intibucá + + This study JHT2912 Honduras: Intibucá + + This study JHT2618 Honduras: Guajiquiro + + This study JHT2867 Honduras: Guajiquiro + + This study JHT2868 Honduras: Guajiquiro + + This study JHT2869 Honduras: Guajiquiro + + This study JHT2306 Honduras: Intibucá + — This study JHT2307 Honduras: Intibucá + + This study JHT2877 Honduras: Intibucá + + This study
229
Table 4-1. Continued. JHT2878 Honduras: Intibucá + + This study JHT2879 Honduras: Intibucá + + This study JHT2880 Honduras: Intibucá + + This study JHT2887 Honduras: Intibucá + + This study JHT2888 Honduras: Intibucá + + This study JHT2889 Honduras: Intibucá + + This study JHT2890 Honduras: Intibucá + + This study Bolitoglossa colonnea CH 6526 Panamá: El Copé FJ784318 FJ766578 Crawford et al. (2010) Bolitoglossa conanti JHT2922 Honduras: Cusuco + + This study JHT2923 Honduras: Cusuco + + This study JHT2924 Honduras: Cusuco + + This study JHT2925 Honduras: Cusuco + + This study JHT2725 Honduras: Ocotepeque + + This study JHT2741 Honduras: Ocotepeque + + This study JHT2742 Honduras: Ocotepeque + + This study UTA A58141 Guatemala: Cerro El Mono + + This study Bolitoglossa diaphora JHT2917 Honduras: Cusuco + + This study JHT2918 Honduras: Cusuco + — This study JHT2919 Honduras: Cusuco + + This study JHT2920 Honduras: Cusuco + + This study JHT2921 Honduras: Cusuco + + This study JHT2989 Honduras: Cusuco + + This study JHT2990 Honduras: Cusuco + + This study JHT2991 Honduras: Cusuco + + This study Bolitoglossa dofleini JHT2430 Honduras: Texíguat (Yoro) + + This study JHT2854 Honduras: Quebrada Grande + + This study UTA A56787 Guatemala + + This study Bolitoglossa dunni UTA A51488 Guatemala: Sierra de Caral + + This study Bolitoglossa heiroreias UTA A54712 Guatemala: Chiquimula + + This study Bolitoglossa longissima JHT3194 Honduras: Cerro La Picucha + — This study JHT3195 Honduras: Cerro La Picucha + + This study JHT3196 Honduras: Cerro La Picucha + + This study JHT3197 Honduras: Cerro La Picucha + + This study JHT3198 Honduras: Cerro La Picucha + — This study JHT3199 Honduras: Cerro La Picucha + — This study JHT3200 Honduras: Cerro La Picucha — + This study JHT3201 Honduras: Cerro La Picucha + — This study Bolitoglossa mexicana JHT2390 Honduras: Los Naranjos + — This study JHT2572 Honduras: Comayagua + + This study JHT2573 Honduras: Comayagua + — This study JHT2960 Honduras: above Guaymas + + This study JHT2512 Honduras: Azul Meámbar + — This study JHT3182 Sierra de Agalta + — This study
230
Table 4-1. Continued. Bolitoglossa nympha
1 JHT1766 Honduras: El Paraiso Valley + — This study
JHT1793 Honduras: El Paraiso Valley + + This study JHT1823 Honduras: El Paraiso Valley + + This study JHT2803 Honduras: Quebrada Grande + + This study Bolitoglossa oresbia JHT2225 Honduras: Cerro Zarciadero + + This study (includes Bolitoglossa sp. inq. 2) IRL071 Honduras: Azul Meámbar + + This study IRL072 Honduras: Azul Meámbar + + This study IRL074 Honduras: Azul Meámbar + + This study IRL075 Honduras: Azul Meámbar + + This study IRL079 Honduras: Azul Meámbar + + This study IRL080 Honduras: Azul Meámbar + — This study IRL081 Honduras: Azul Meámbar + + This study Bolitoglossa porrasorum JHT2359 Honduras: Macuzal + + This study JHT2360 Honduras: Macuzal + + This study JHT2371 Honduras: Macuzal + + This study JHT2372 Honduras: Macuzal + + This study JHT2373 Honduras: Macuzal + + This study JHT2374 Honduras: Macuzal + — This study JHT2419 Honduras: Macuzal + — This study Bolitoglossa cf. porrasorum JHT2431 Honduras: Texíguat (Yoro) + + This study JHT2432 Honduras: Texíguat (Yoro) + — This study JHT2449 Honduras: Texíguat (Yoro) + + This study JHT2450 Honduras: Texíguat (Yoro) + + This study JHT2453 Honduras: Texíguat (Yoro) + + This study JHT2454 Honduras: Texíguat (Yoro) + — This study JHT2455 Honduras: Texíguat (Yoro) + + This study JHT3104 Honduras: Texíguat (Atlántida) + + This study JHT3105 Honduras: Texíguat (Atlántida) + + This study JHT3106 Honduras: Texíguat (Atlántida) + + This study JHT3143 Honduras: Texíguat (Atlántida) + + This study JHT3144 Honduras: Texíguat (Atlántida) + + This study JHT3145 Honduras: Texíguat (Atlántida) + + This study JHT3146 Honduras: Texíguat (Atlántida) + — This study JHT3147 Honduras: Texíguat (Atlántida) + + This study JHT3148 Honduras: Texíguat (Atlántida) + + This study JHT3149 Honduras: Texíguat (Atlántida) + + This study JHT3150 Honduras: Texíguat (Atlántida) + — This study JHT3151 Honduras: Texíguat (Atlántida) + + This study JHT3152 Honduras: Texíguat (Atlántida) + + This study JHT3153 Honduras: Texíguat (Atlántida) + + This study JHT3171 Honduras: Texíguat (Atlántida) + + This study JHT3172 Honduras: Texíguat (Atlántida) + + This study JHT3229 Honduras: Texíguat (Atlántida) + + This study
231
Table 4-1. Continued. JHT3230 Honduras: Texíguat (Atlántida) + — This study JHT3231 Honduras: Texíguat (Atlántida) + + This study JHT3250 Honduras: Texíguat (Atlántida) + + This study JHT3251 Honduras: Texíguat (Atlántida) + + This study JHT3252 Honduras: Texíguat (Atlántida) + + This study JHT3253 Honduras: Texíguat (Atlántida) + + This study JHT3254 Honduras: Texíguat (Atlántida) + + This study JHT3255 Honduras: Texíguat (Atlántida) + + This study JHT3256 Honduras: Texíguat (Atlántida) + + This study JHT3257 Honduras: Texíguat (Atlántida) + + This study JHT3264 Honduras: Texíguat (Atlántida) + + This study JHT3265 Honduras: Texíguat (Atlántida) + + This study JHT3266 Honduras: Texíguat (Atlántida) + + This study Bolitoglossa cf. rufescens JHT1767 Honduras: El Paraiso Valley + + This study JHT1797 Honduras: El Paraiso Valley + + This study Bolitoglossa schizodactyla USNM 572791 Panamá: El Copé FJ784482 FJ766579 Crawford et al. (2010) Bolitoglossa striatula N145 Nicaragua: Bosawas + + This study Bolitoglossa synoria JHT2900 Honduras: Cerro El Pital + + This study JHT2901 Honduras: Cerro El Pital + + This study Cryptotriton alvarezdeltoroi MVZ 158942 México: Chiapas AF199196 — García-París & Wake (2000) Cryptotriton sierraminensis MVZ 160907 Guatemala: Sierra Las Minas AF199198 — García-París & Wake (2000) Cryptotriton veraepacis GAR059 Guatemala: Baja Verapaz + + This study (E.N. Smith, UTA) UTA A51396 Guatemala: Baja Verapaz + + This study (E.N. Smith, UTA) MVZ 215913 Guatemala: Baja Verapaz AF199197 — García-París & Wake (2000) Dendrotriton rabbi UTA A51086 Guatemala: Uspantán AF199232 — García-París & Wake (2000) Nototriton abscondens UCR 12071 Costa Rica: Cascada La Paz AF199199 — García-París & Wake (2000) Nototriton barbouri JHT2420 Honduras: Macuzal + + This study Nototriton ―barbouri‖ (N. sp. A) USNM 339712 Honduras: Pico Bonito AF199201 — García-París & Wake (2000) Nototriton ―barbouri‖ (N. sp. B) JHT3159 Honduras: Texíguat (Atlántida) + + This study Nototriton brodiei UTA A51490 Guatemala: Sierra de Caral AF199202 + 16S: García-París & Wake
(2000); COI: This study (E.N. Smith, UTA)
MVZ(FN252407) Honduras: Sierra de Omoa + — This study (S.M. Rovito, MVZ) Nototriton gamezi MVZ 207122 Costa Rica: Monteverde AF199200 — García-París & Wake (2000) Nototriton guanacaste MVZ 207106 Costa Rica: Volcán Cacao AF199203 — García-París & Wake (2000) Nototriton lignicola (=N. sp. inq. 4)
USNM 497540 Honduras: La Muralla AF199204 — García-París & Wake (2000)
JHT2122 Honduras: Cataguana + + This study Nototriton limnospectator None Honduras: Santa Bárbara + — S.M. Rovito (MVZ) (=N. sp. inq. 5) IRL035 Honduras: Azul Meámbar + — This study IRL070 Honduras: Azul Meámbar + + This study IRL076 Honduras: Azul Meámbar + + This study IRL088 Honduras: Azul Meámbar + + This study
232
Table 4-1. Continued. Nototriton picadoi MVZ 225899 Costa Rica: Tapantí AF199205 — García-París & Wake (2000) Nototriton richardi UCR 12057 Costa Rica: Cascajal de Las
Nubes AF199206 — García-París & Wake (2000)
Nototriton saslaya N650 Nicaragua: Cerro Saslaya + — This study SMF collection Nicaragua: Cerro Saslaya + — This study Nototriton sp. inq. 1 (= N. tomamorum)
JHT2437 Honduras: Texíguat (Yoro) + + This study
Nototriton sp. inq. 2 JHT3192 Honduras: Cerro La Picucha + + This study (= N. picucha) JHT3193 Honduras: Cerro La Picucha + + This study Nototriton sp. inq. 3 JHT3398 Honduras: Sierra de Botaderos + + This study JHT3399 Honduras: Sierra de Botaderos + + This study JHT3400 Honduras: Sierra de Botaderos + + This study JHT3401 Honduras: Sierra de Botaderos + + This study Oedipina alleni MVZ 190857 Costa Rica: Sirena AF199207 — García-París & Wake (2000) MVZ 225903 Costa Rica: Damas AF199208 — García-París & Wake (2000) Oedipina carablanca None Costa Rica: Limón FJ196862 — McCranie et al. (2008) Oedipina collaris SIUC H-08896 Panamá: El Copé FJ196863 — Crawford et al. (2010) Oedipina complex DBW5105 Panamá: Barro Colorado AF199213 — García-París & Wake (2000) DBW5787 Panamá: Cerro Campana AF199212 — García-París & Wake (2000) Oedipina cyclocauda MVZ 138916 Costa Rica: La Selva AF199214 — García-París & Wake (2000) MVZ 293747 Costa Rica: La Selva AF199215 — García-París & Wake (2000) Oedipina elongata UTA A56809 Guatemala + + This study (E.N. Smith, UTA) UTA A56810 Guatemala + — This study (E.N. Smith, UTA) Oedipina gephyra JHT2443 Honduras: Texíguat (Yoro) + + This study JHT2451 Honduras: Texíguat (Yoro) + + This study USNM 530582 Honduras: Texíguat (Yoro) AF199218 — García-París & Wake (2000) Oedipina cf. gephyra (= O. petiola)
USNM 343462 Honduras: Pico Bonito AF199217 — García-París & Wake (2000)
Oedipina gracilis MVZ 210398 Costa Rica: La Selva AF199219 — García-París & Wake (2000) Oedipina grandis MVZ 225904 Costa Rica: Cerro Pando AF199220 — García-París & Wake (2000) Oedipina cf. ignea USNM 530586 Honduras: Cerro El Pital AF199231 — García-París & Wake (2000) Oedipina kasios MVZ 232825 Honduras: La Muralla FJ196866 — McCranie et al. (2008) (=Oedipina sp. inq. 1) JHT2974 Honduras: above Guaymas + + This study Oedipina parvipes AJC1786 Panamá: El Copé FJ784316 FJ766760 Crawford et al. (2010) MVZ 210404 Panamá: Nusagandi AF199210 — García-París & Wake (2000) MVZ 210405 Panamá: Río Frijoles AF199211 — García-París & Wake (2000) Oedipina poelzi MVZ 163703 Costa Rica: Vara Blanca AF199224 — García-París & Wake (2000) MVZ 207128 Costa Rica: Monteverde AF199225 — García-París & Wake (2000) MVZ 206398 Costa Rica: Braulio Carrillo AF199223 — García-París & Wake (2000) Oedipina quadra MVZ 232824 Honduras: Warunta FJ196865 — McCranie et al. (2008) Oedipina savagei UCR LG961327 Costa Rica: Cerro Zapote AF199209 — García-París & Wake (2000) Oedipina sp. SMF 78738 Nicaragua + — García-París & Wake (2000) JHT2974 Honduras: above Guaymas + + This study
233
Table 4-1. Continued. Oedipina sp. inq. 2 (= O. nica) N567 Nicaragua: Cerro Kilambé + + This study N569 Nicaragua: Cerro Kilambé + — This study N570 Nicaragua: Cerro Kilambé + — This study N964 Nicaragua: Cerro Kilambé + + This study N965 Nicaragua: Cerro Kilambé + + This study N1029 Nicaragua: Peñas Blancas + — This study N1030 Nicaragua: Peñas Blancas + — This study Oedipina sp. inq. 3 (= O. koehleri) N614 Nicaragua: Cerro Saslaya + + This study JS782 Nicaragua: Cerro Musún + — This study Oedipina stenopodia MVZ 163649 Guatemala: San Rafael AF199228 — García-París & Wake (2000) Oedipina taylori UGSC 1134 Guatemala: Zacapa HM068304 — Sunyer et al. (2010) Oedipina tomasi JHT1553 Honduras: Sierra de Omoa + — This study MVZ 258037 Honduras: Sierra de Omoa + — Oedipina uniformis MVZ 190853 Costa Rica: Ciénega Colorado AF199229 — García-París & Wake (2000) MVZ 203751 Costa Rica: Tapantí AF199230 — García-París & Wake (2000) ANURA Bufonidae (14) Crepidophryne chompipe UCR 16075 Costa Rica HM563859 — Mendelson et al. (In press) Incilius coccifer
JHT3301 Honduras: Isla El Tigre + + This study
JS1016 Nicaragua: Ometepe + — This study JS1058 Nicaragua: Ometepe + — This study JS1150 Nicaragua: Atlántico Norte + — This study SDSNH AEH-013 Nicaragua: Ometepe AY927857 — Mendelson et al. (2005) KU 290030 El Salvador: Morazán AY927856 — Mendelson et al. (2005) USNM 547980 Honduras: Rus Rus AY929301 — Mendelson et al. (2005) Incilius coniferus MVUP 1820 Panamá: El Copé FJ784379 FJ766768 Crawford et al. (2010) USNM 572086 Panamá: El Copé FJ784382 FJ766767 Crawford et al. (2010) USNM 572087 Panamá: El Copé FJ784444 FJ766766 Crawford et al. (2010) USNM 572092 Panamá: El Copé FJ784586 FJ766765 Crawford et al. (2010) toe 140 Panamá: El Copé FJ784595 FJ766764 Crawford et al. (2010) toe 141 Ocon Panamá: El Copé FJ784597 FJ766732 Crawford et al. (2010) toe 144 Ocon Panamá: El Copé FJ784599 FJ766762 Crawford et al. (2010) toe 151 Ocon Panamá: El Copé FJ784601 FJ766761 Crawford et al. (2010) Incilius cf. coniferus N416 Nicaragua: Bosawas + + This study Incilius cycladen UTA-JRM 4607 Mexico: Guerrero AY927858 — Mendelson et al. (2005) Incilius ibarrai JHT2205 Honduras: Cerro Zarciadero + + This study JHT2604 Honduras: Guajiquiro + + This study JHT2605 Honduras: Guajiquiro + + This study JHT2763 Honduras: Intibucá + + This study JHT2765 Honduras: Intibucá + + This study JHT2874 Honduras: Intibucá + — This study JHT2906 Honduras: Intibucá + + This study IRL002 Honduras: Comayagua + + This study
234
Table 4-1. Continued. IRL004 Honduras: Comayagua + + This study IRL005 Honduras: Comayagua + + This study Incilius karenlipsae UTA A-59522 Panamá: El Copé GU552454 — Mendelson & Mulcahy (2010) Incilius leucomyos JHT3034 Honduras: Texíguat (Atlántida) + + This study JHT3242 Honduras: Texíguat (Atlántida) — + This study CAC013 Honduras: Pico Bonito + + This study CAC059 Honduras: Pico Bonito + + This study Incilius luetkenii JS853 Nicaragua: Las Nubes + + This study Incilius porteri JHT2228 Honduras: Cerro Uyuca + + This study JHT3302 Honduras: Isla El Tigre + + This study CAC044 Honduras: Comayagua + + This study JHT2249 Honduras: Francisco Morazán HM563882 — Mendelson et al. (In press) Incilius valliceps JHT2013 Honduras: Marale + + This study JHT2271 Nicaragua: Selva Negra + + This study JHT2428 Honduras: Texíguat (Yoro) + + This study JHT2519 Honduras: Azul Meámbar + + This study JHT2807 Honduras: Quebrada Grande + + This study JHT3175 Honduras: Texiguat (Atlántida) + — This study IRL047 Honduras: Azul Meámbar + + This study LK005 Honduras: Cerro Santa Bárbara + + This study N089 Nicaragua: Bosawas + + This study USNM 509524 Honduras: Pico Bonito AY008231 — Mulcahy & Mendelson (2000) Rhaebo haematiticus MVUP 1842 Panamá: El Copé FJ784439 FJ766816 Crawford et al. (2010) USNM 572094 Panamá: El Copé FJ784404 FJ766818 Crawford et al. (2010) USNM 572095 Panamá: El Copé FJ784426 FJ766817 Crawford et al. (2010) USNM 572096 Panamá: El Copé FJ784452 FJ766815 Crawford et al. (2010) USNM 572097 Panamá: El Copé FJ784546 FJ766814 Crawford et al. (2010) USNM 572098 Panamá: El Copé FJ784560 FJ766813 Crawford et al. (2010) Toe 120 Panamá: El Copé FJ784593 FJ766812 Crawford et al. (2010) Rhaebo cf. haematiticus N063 Nicaragua: Bosawas + + This study N137 Nicaragua: Bosawas + + This study N594 Nicaragua: Bosawas + + This study Rhinella marina MVUP 1802 Panamá: El Copé FJ784357 FJ766819 Crawford et al. (2010) Craugastoridae (11) Craugastor angelicus MVZ 149762 Costa Rica: Volcán Barba EU186681 — Hedges et al. (2008) Craugastor aurilegulus JHT2993 Honduras: Pico Bonito + + This study JHT3015 Honduras: Lancetilla + + This study JHT3016 Honduras: Lancetilla + + This study JHT3017 Honduras: Lancetilla + + This study JHT3018 Honduras: Lancetilla + + This study JHT3241 Honduras: Texíguat (Atlántida) + + This study C007 Honduras: Pico Bonito + + This study C024 Honduras: Pico Bonito + + This study
235
Table 4-1. Continued. Craugastor cf. azueroensis KRL0680 Panamá: El Copé FJ784332 FJ766637 Crawford et al. (2010 USNM 572219 Panamá: El Copé FJ784393 FJ766636 Crawford et al. (2010 USNM 572278 Panamá: El Copé FJ784324 FJ766675 Crawford et al. (2010 USNM 572279 Panamá: El Copé FJ784325 FJ766674 Crawford et al. (2010 Craugastor bransfordii USNM 572220 Panamá: El Copé FJ784339 FJ766631 Crawford et al. (2010) MVUP 1803 Panamá: El Copé FJ784358 FJ766630 Crawford et al. (2010) USNM 572221 Panamá: El Copé FJ784376 FJ766629 Crawford et al. (2010) MVUP 1841 Panamá: El Copé FJ784427 FJ766628 Crawford et al. (2010) USNM 572222 Panamá: El Copé FJ784481 FJ766627 Crawford et al. (2010) USNM 572223 Panamá: El Copé FJ784496 FJ766626 Crawford et al. (2010) Craugastor charadra JHT1820 Honduras: El Paraiso Valley + + This study JHT1826 Honduras: El Paraiso Valley + + This study Craugastor fitzingeri N060 Nicaragua: Bosawas + + This study KRL 0693 Panamá: El Copé FJ784337 — Crawford et al. (2010) USNM 572256 Panamá: El Copé FJ784344 — Crawford et al. (2010) MVUP 1798 Panamá: El Copé FJ784356 — Crawford et al. (2010) Craugastor laevissimus JHT1824 Honduras: El Paraiso Valley — + This study JHT2489 Honduras: Azul Meámbar + + This study JHT2501 Honduras: Azul Meámbar + + This study JHT2510 Honduras: Azul Meámbar + + This study JHT2517 Honduras: Azul Meámbar + + This study JHT2529 Honduras: Comayagua — + This study JHT2539 Honduras: Comayagua — + This study JHT2552 Honduras: Comayagua — + This study JHT2559 Honduras: Comayagua — + This study JHT2779 Honduras: Pico Pijol — + This study JHT2978 Honduras: Azul Meámbar + + This study JHT2979 Honduras: Azul Meámbar + + This study JHT3000 Honduras: Cerro Santa Bárbara + + This study JHT3004 Honduras: Los Naranjos + + This study IRL023 Honduras: Azul Meámbar + + This study N556 Nicaragua: Cerro Kilambé — + This study N557 Nicaragua: Cerro Kilambé — + This study N639 Nicaragua: Cerro Saslaya — + This study N950 Nicaragua: Cerro Kilambé — + This study N961 Nicaragua: Cerro Kilambé — + This study Craugastor punctariolus MVUP 1784 Panamá: El Copé FJ784333 FJ766673 Crawford et al. (2010) USNM 572281 Panamá: El Copé FJ784411 FJ766672 Crawford et al. (2010) USNM 572282 Panamá: El Copé FJ784417 FJ766671 Crawford et al. (2010) USNM 572283 Panamá: El Copé FJ784418 FJ766670 Crawford et al. (2010) Craugastor sandersoni UTA-A49803 Guatemala: Sierra de Santa Cruz EF493712 — Heinicke et al. (2007) Craugastor tabasarae KRL0706 Panamá: El Copé FJ784342 — Crawford et al. (2010) KRL1373 Panamá: El Copé FJ784512 — Crawford et al. (2010)
236
Table 4-1. Continued. KRL1387 Panamá: El Copé FJ784515 — Crawford et al. (2010) Craugastor underwoodi UCR 16315 EF562362 — Streicher et al. (2009) USNM 561403 EF562361 — Streicher et al. (2009) Eleutherodactylidae (3) Diasporus aff. diastema MVUP 1783 Panamá: El Copé FJ784338 — Crawford et al. (2010) USNM 572442 Panamá: El Copé FJ784425 — Crawford et al. (2010) MVUP 1830 Panamá: El Copé FJ784395 — Crawford et al. (2010) Diasporus cf. diastema N546 Nicaragua: Cerro Kilambé + + This study N928 Nicaragua: Cerro Kilambé + + This study N934 Nicaragua: Cerro Kilambé + + This study Hylidae (15) Duellmanohyla soralia JHT1585 Honduras: Sierra de Omoa + + This study UTA A50812 Guatemala: Sierra de Caral AY843584 — Faivovich et al. (2005) Exerodonta catracha JHT2209 Honduras: Cerro Zarciadero + + This study JHT2211 Honduras: Cerro Zarciadero + + This study JHT2315 Honduras: Intibucá + — This study JHT2316 Honduras: Intibucá + + This study JHT2647 Honduras: Guajiquiro + + This study JHT2648 Honduras: Guajiquiro + + This study JHT2649 Honduras: Guajiquiro + + This study JHT2650 Honduras: Guajiquiro + + This study JHT2651 Honduras: Guajiquiro + + This study JHT2652 Honduras: Guajiquiro + — This study JHT2653 Honduras: Guajiquiro + + This study JHT2654 Honduras: Guajiquiro — — This study JHT2655 Honduras: Guajiquiro + + This study JHT2656 Honduras: Guajiquiro + + This study JHT2657 Honduras: Guajiquiro + — This study JHT2658 Honduras: Guajiquiro + + This study JHT2659 Honduras: Guajiquiro + + This study JHT2660 Honduras: Guajiquiro + + This study JHT2661 Honduras: Guajiquiro + + This study JHT2861 Honduras: Guajiquiro + + This study JHT2862 Honduras: Guajiquiro + + This study JHT2863 Honduras: Guajiquiro — — This study JHT2864 Honduras: Guajiquiro + + This study JHT2870 Honduras: Guajiquiro + + This study JHT2871 Honduras: Guajiquiro + + This study JHT2872 Honduras: Guajiquiro + — This study JHT2896 Honduras: Intibucá + + This study JHT2897 Honduras: Intibucá + + This study JHT2898 Honduras: Intibucá + + This study JHT2899 Honduras: Intibucá + + This study
237
Table 4-1. Continued. JHT2907 Honduras: Intibucá + — This study Plectrohyla chrysopleura JHT3077 Honduras: Texíguat (Atlántida) + + This study JHT3081 Honduras: Texíguat (Atlántida) + + This study JHT3142 Honduras: Texíguat (Atlántida) + + This study JHT3166 Honduras: Texíguat (Atlántida) + + This study JHT3167 Honduras: Texíguat (Atlántida) + + This study JHT3169 Honduras: Texíguat (Atlántida) + + This study Plectrohyla dasypus JHT1624 Honduras: Cusuco + + This study JHT2988 Honduras: Cusuco + + This study Plectrohyla exquisita JHT1600 Honduras: Cusuco + + This study JHT1601 Honduras: Cusuco + + This study JHT1623 Honduras: Cusuco + + This study Plectrohyla guatemalensis JHT2058 Honduras: Cataguana + + This study JHT2059 Honduras: Cataguana + + This study JHT2060 Honduras: Cataguana + + This study Plectrohyla psiloderma JHT2746 Honduras: Cerro Celaque + + This study Ptychohyla euthysanota JS1244 Guatemala: Los Tarrales — + This study UTA A-54786 México: Chiapas AY843744 — Faivovich et al. (2005) Ptychohyla hypomykter JHT1622 Honduras: Cusuco + + This study JHT2272 Nicaragua: Selva Negra + — This study JHT2273 Nicaragua: Selva Negra + + This study JHT2274 Nicaragua: Selva Negra + + This study JHT2276 Nicaragua: Selva Negra + + This study JHT2300 Honduras: Comayagua + + This study JHT2494 Honduras: Azul Meámbar + + This study JHT2530 Honduras: Comayagua — + This study JHT2540 Honduras: Comayagua + + This study JHT2541 Honduras: Comayagua + + This study JHT2548 Honduras: Comayagua + + This study JHT2855 Honduras: Quebrada Grande + + This study JHT2916 Honduras: Cusuco + + This study JHT2930 Honduras: Pico Pijol — + This study JHT2931 Honduras: Pico Pijol + + This study JHT2933 Honduras: Pico Pijol + + This study JHT2934 Honduras: Pico Pijol + + This study JHT2935 Honduras: Pico Pijol + + This study JHT2936 Honduras: Pico Pijol + + This study JHT2945 Honduras: Pico Pijol + + This study JHT2946 Honduras: Pico Pijol + + This study JHT2949 Honduras: Pico Pijol + + This study JHT2950 Honduras: Pico Pijol + + This study JHT2951 Honduras: Pico Pijol + + This study JHT2954 Honduras: Pico Pijol + — This study
238
Table 4-1. Continued. JHT2998 Honduras: Cerro Santa Bárbara + + This study JHT2999 Honduras: Cerro Santa Bárbara + + This study IRL067 Honduras: Azul Meámbar + + This study IRL091 Honduras: Azul Meámbar + + This study IRL092 Honduras: Azul Meámbar + + This study IRL093 Honduras: Azul Meámbar + + This study IRL094 Honduras: Azul Meámbar + + This study IRL095 Honduras: Azul Meámbar + + This study N293 Nicaragua: Cerro Saslaya + + This study N528 Nicaragua: Cerro Kilambé + + This study N547 Nicaragua: Cerro Kilambé + + This study N993 Nicaragua: Cerro Peñas Blancas + + This study N1000 Nicaragua: Cerro Peñas Blancas + + This study N1004 Nicaragua: Cerro Peñas Blancas + + This study N1028 Nicaragua: Cerro Peñas Blancas + + This study Ptychohyla cf. hypomykter ENS8486 Guatemala: Izabal AY843745 Faivovich et al. (2005) Ptychohyla salvadorensis JHT2262 Honduras: Cerro Uyuca + + This study Ptychohyla spinipollex USNM 514381 Honduras: Pico Bonito AY843748 — Faivovich et al. (2005) Ptychohyla cf. spinipollex JHT3041 Honduras: Texíguat (Atlántida) + + This study JHT3042 Honduras: Texíguat (Atlántida) + + This study JHT3055 Honduras: Texíguat (Atlántida) + + This study JHT3056 Honduras: Texíguat (Atlántida) — + This study JHT3057 Honduras: Texíguat (Atlántida) + + This study JHT3058 Honduras: Texíguat (Atlántida) + + This study JHT3059 Honduras: Texíguat (Atlántida) + + This study JHT3070 Honduras: Texíguat (Atlántida) + + This study JHT3071 Honduras: Texíguat (Atlántida) + + This study JHT3072 Honduras: Texíguat (Atlántida) + + This study JHT3073 Honduras: Texíguat (Atlántida) + + This study JHT3114 Honduras: Texíguat (Atlántida) — + This study JHT3115 Honduras: Texíguat (Atlántida) + + This study JHT3116 Honduras: Texíguat (Atlántida) + + This study JHT3154 Honduras: Texíguat (Atlántida) + + This study JHT3170 Honduras: Texíguat (Atlántida) + + This study JHT3233 Honduras: Texíguat (Atlántida) + + This study JHT3234 Honduras: Texíguat (Atlántida) + + This study JHT3235 Honduras: Texíguat (Atlántida) + + This study JHT3236 Honduras: Texíguat (Atlántida) + + This study Smilisca cf. baudinii JHT2277 Nicaragua: Selva Negra + + This study JHT2592 Honduras: Los Naranjos + + This study JHT2593 Honduras: Los Naranjos + — This study JHT2938 Honduras: Pico Pijol + + This study N781 Nicaragua: Bosawas + + This study
239
Table 4-1. Continued. N1019 Nicaragua: Peñas Blancas + + This study Smilisca phaeota USNM 572702 Panamá: El Copé FJ784413 FJ766835 Crawford et al. (2010) USNM 572703 Panamá: El Copé FJ784433 FJ766834 Crawford et al. (2010) Smilisca sila USNM 572707 Panamá: El Copé FJ784578 FJ766837 Crawford et al. (2010) USNM 572708 Panamá: El Copé FJ784579 FJ766836 Crawford et al. (2010) Smilisca sordida N030 Nicaragua: Bosawas + + This study N031 Nicaragua: Bosawas + + This study N114 Nicaragua: Bosawas + + This study N115 Nicaragua: Bosawas — + This study N819 Nicaragua: Bosawas + + This study Tlalocohyla loquax JHT2247 Honduras: Cerro Uyuca + + This study JHT2268 Nicaragua: Selva Negra + + This study JHT2269 Nicaragua: Selva Negra — + This study Leptodactylidae (1) Leptodactylus fragilis JHT3238 Honduras: Texíguat (Atlántida) + + This study N462 Nicaragua: Bosawas + + This study N653 Nicaragua: Bosawas + + This study N841 Nicaragua: Bosawas + + This study Leptodactylus cf. fragilis USNM 572722 Panamá: El Copé FJ784331 FJ766745 Crawford et al. (2010) USNM 572725 Panamá: El Copé FJ784416 FJ766744 Crawford et al. (2010) MVUP 1836 Panamá: El Copé FJ784437 FJ766743 Crawford et al. (2010) USNM 572727 Panamá: El Copé FJ784453 FJ766742 Crawford et al. (2010) Leptodactylus savagei MVUP 1828 Panamá: El Copé FJ784394 FJ766748 Crawford et al. (2010) Leptodactylus poecilochilus KRL 0118 Panamá: El Copé FJ784321 — Crawford et al. (2010) Microhylidae (1) Hypopachus barberi JHT2630 Honduras: Guajiquiro + + This study JHT2634 Honduras: Guajiquiro + + This study Ranidae (4) Lithobates areolata KU 204370 USA: Kansas AY779229 — Hillis & Wilcox (2005) Lithobates berlandieri JSF1136 USA: Texas AY779235 — Hillis & Wilcox (2005) Lithobates brownorum JHT2329 Honduras: Los Naranjos + — This study JHT2349 Honduras: Los Naranjos + — This study JHT2350 Honduras: Los Naranjos + — This study JHT2351 Honduras: Los Naranjos + — This study JHT2466 Honduras: Los Naranjos + — This study JHT2525 Honduras: Comayagua + — This study JHT2560 Honduras: Comayagua + — This study JHT2561 Honduras: Comayagua + — This study JHT2562 Honduras: Comayagua + — This study JHT2563 Honduras: Comayagua + — This study JHT2564 Honduras: Comayagua + — This study JHT2565 Honduras: Comayagua + — This study JHT2566 Honduras: Comayagua + — This study
240
Table 4-1. Continued. JHT2567 Honduras: Comayagua + — This study JHT2569 Honduras: Comayagua + — This study JHT2760 Honduras: Intibucá + — This study JHT2761 Honduras: Intibucá + — This study JHT2814 Honduras: Quebrada Grande + — This study JHT2815 Honduras: Quebrada Grande + — This study JHT2818 Honduras: Quebrada Grande + — This study JHT2955 Honduras: above Guaymas + — This study JHT2956 Honduras: above Guaymas + — This study JHT2957 Honduras: above Guaymas + — This study JHT2958 Honduras: above Guaymas + — This study IRL051 Honduras: Azul Meámbar + — This study LK002 Honduras: Cerro Santa Bárbara + — This study Lithobates brownorum X forreri JHT2138 Honduras: Cerro Uyuca + + This study JHT2139 Honduras: Cerro Uyuca + + This study JHT2140 Honduras: Cerro Uyuca — + This study JHT2141 Honduras: Cerro Uyuca + + This study JHT2142 Honduras: Cerro Uyuca + + This study JHT2143 Honduras: Cerro Uyuca + + This study JHT2144 Honduras: Cerro Uyuca + + This study JHT2145 Honduras: Cerro Uyuca + + This study JHT2153 Honduras: Cerro Uyuca + + This study JHT2308 Honduras: Intibucá + + This study JHT2310 Honduras: Intibucá + + This study JHT2314 Honduras: Intibucá + + This study JHT2327 Honduras: Intibucá + + This study JHT2328 Honduras: Intibucá + + This study JHT2772 Honduras: Intibucá + + This study JHT2883 Honduras: Intibucá + + This study Lithobates capito TNHC 60195 USA: Florida AY779231 — Hillis & Wilcox (2005) Lithobates catesbeiana DMH 84-R2 USA: Kansas AY779206 — Hillis & Wilcox (2005) None No data GBX12841 — Hillis & Wilcox (2005) Lithobates chiricahuensis KU 194442 México: Durango AY779225 — Hillis & Wilcox (2005) KU 194419 USA: Arizona AY779226 — Hillis & Wilcox (2005) Lithobates clamitans JSF1118 USA Missouri AY779204 — Hillis & Wilcox (2005) Lithobates forreri KU 194581 México: Sinaloa AY779233 — Hillis & Wilcox (2005) Lithobates grylio MVZ 175945 USA: Florida AY779201 — Hillis & Wilcox (2005) Lithobates heckscheri MVZ 164908 USA: Florida AY779205 — Hillis & Wilcox (2005) Lithobates ―macroglossa‖ KU 195138 México: Chiapas AY779242 — Hillis & Wilcox (2005) UTA A-17185 Guatemala: Sololá AY779243 — Hillis & Wilcox (2005) Lithobates maculatus KU 195258 México: Oaxaca AY779207 — Hillis & Wilcox (2005) USNM 559483 Honduras: Pico Bonito DQ283303 — Frost et al. (2006) Lithobates maculatus (―Anura sp.‖) None México — B:AAE6665 BOLD Database
241
Table 4-1. Continued. Lithobates maculatus complex JHT2007 Honduras: Marale + + This study JHT2028 Honduras: Los Planes + + This study JHT2029 Honduras: Los Planes + + This study JHT2117 Honduras: Cataguana + + This study JHT2136 Honduras: Cerro Uyuca + + This study JHT2137 Honduras: Cerro Uyuca + + This study JHT2204 Honduras: Cerro Zarciadero + + This study JHT2244 Honduras: Cerro Uyuca + + This study JHT2439 Honduras: Texíguat (Yoro) + + This study JHT2492 Honduras: Azul Meámbar + + This study JHT2528 Honduras: Comayagua + + This study JHT2571 Honduras: Comayagua + + This study JHT2594 Honduras: Los Naranjos + + This study JHT2617 Honduras: Guajiquiro + + This study JHT2851 Honduras: Quebrada Grande + + This study JHT2852 Honduras: Quebrada Grande + + This study JHT2853 Honduras: Quebrada Grande + + This study JHT2939 Honduras: Pico Pijol + + This study JHT2940 Honduras: Pico Pijol + + This study IRL015 Honduras: Azul Meámbar + + This study IRL016 Honduras: Azul Meámbar + + This study IRL017 Honduras: Azul Meámbar + + This study IRL018 Honduras: Azul Meámbar + + This study IRL019 Honduras: Azul Meámbar + + This study IRL020 Honduras: Azul Meámbar + — This study IRL052 Honduras: Azul Meámbar + + This study IRL053 Honduras: Azul Meámbar + + This study IRL057 Honduras: Azul Meámbar + + This study IRL058 Honduras: Azul Meámbar + + This study IRL087 Honduras: Azul Meámbar + — This study N285 Nicaragua: Cerro Saslaya + + This study N371 Nicaragua: Bosawas + + This study N610 Nicaragua: Cerro Saslaya + + This study N638 Nicaragua: Cerro Saslaya + — This study N649 Nicaragua: Cerro Saslaya + + This study N920 Nicaragua: Cerro Kilambé + + This study N1009 Nicaragua: Peñas Blancas + + This study N1021 Nicaragua: Peñas Blancas + + This study Lithobates magnaocularis KU 194592 México: Sonora AY779239 — Hillis & Wilcox (2005) Lithobates montezumae KU 195251 México: Morelos AY779223 — Hillis & Wilcox (2005) Lithobates neovolcanica KU 194536 México: Michoacan AY779236 — Hillis & Wilcox (2005) Lithobates okaloosae None (toe clip) USA: Florida AY779203 — Hillis & Wilcox (2005) Lithobates omiltemana KU 195179 México: Guerrero AY779238 — Hillis & Wilcox (2005)
242
Table 4-1. Continued. Lithobates palmipes KU 202896 Ecuador: Napo AY779211 — Hillis & Wilcox (2005) Lithobates palustris KU 204425 USA: Indiana AY779228 — Hillis & Wilcox (2005) Lithobates pipiens JSF1119 USA: Ohio AY779221 — Hillis & Wilcox (2005) None No data GBX12841 — Hillis & Wilcox (2005) Lithobates septentrionalis TNHC (no #) Canada: Ontario AY779200 — Hillis & Wilcox (2005) Lithobates sevosa TNHC 60194 USA: Mississippi AY779230 — Hillis & Wilcox (2005) Lithobates spectabilis KU 195186 México: Hidalgo AY779232 — Hillis & Wilcox (2005) Lithobates sphenocephalus JSF845 USA: Kansas AY779251 — Hillis & Wilcox (2005) USC7448 USA: Florida AY779252 — Hillis & Wilcox (2005) Lithobates subaquavocalis TNHC (no #) USA: Arizona AY779227 — Hillis & Wilcox (2005) Lithobates sylvatica MVZ 137426 USA: New York AY779198 — Hillis & Wilcox (2005) Lithobates taylori JHT2263 Nicaragua: Selva Negra + + This study JHT2264 Nicaragua: Selva Negra + + This study JHT2265 Nicaragua: Selva Negra — + This study N918 Nicaragua: Cerro Kilambé + + This study N919 Nicaragua: Cerro Kilambé + + This study N997 Nicaragua: Peñas Blancas + + This study N1020 Nicaragua: Peñas Blancas + + This study TCWC 55963 Nicaragua: 2.5 mi NW Rama AY779244 — Hillis & Wilcox (2005) Lithobates tlaloci KU 194436 México: Districto Federal AY779234 — Hillis & Wilcox (2005) Lithobates vibicarius MVZ 149033 Costa Rica: San José AY779208 — Hillis & Wilcox (2005) Lithobates warszewitschii USNM 572770 Panamá: El Copé FJ784454 FJ766752 Crawford et al. (2010) USNM 572779 Panamá: El Copé FJ784552 FJ766751 Crawford et al. (2010) USNM 572780 Panamá: El Copé FJ784558 FJ766750 Crawford et al. (2010) Lithobates ―warszewitschii‖ JSF1127 Panamá: Coclé AY779209 — Hillis & Wilcox (2005) Lithobates aff. warszewitschii USNM 572787 Panamá: El Copé FJ784384 FJ766749 Crawford et al. (2010) Lithobates cf. warszewitschii N334 Nicaragua: Bosawas — + This study N599 Nicaragua: Bosawas + + This study Lithobates spp. (―Anura sp.‖) None México — B:AAB6680 BOLD Database None México — B:AAB6680 BOLD Database None México — B:AAB6680 BOLD Database None México — B:AAB6680 BOLD Database None México — B:AAB6680 BOLD Database None México — B:AAB6680 BOLD Database None México — B:AAB6680 BOLD Database None México — B:AAB6680 BOLD Database None México — B:AAB6679 BOLD Database None México — B:AAB6679 BOLD Database None México — B:AAB6678 BOLD Database None México — B:AAB6681 BOLD Database None México — B:AAB6682 BOLD Database None México — B:AAB6682 BOLD Database None México — B:AAB6682 BOLD Database
243
Table 4-1. Continued. None México — B:AAE6666 BOLD Database None México — B:AAK8798 BOLD Database None México — B:AAC6120 BOLD Database None México — B:AAC6120 BOLD Database Lithobates sp. 1 QCAZ 13219 Ecuador: Esmeraldas AY779213 — Hillis & Wilcox (2005) Lithobates sp. 2 KU 2044420 México: San Luis Potosí AY779224 — Hillis & Wilcox (2005) Lithobates sp. 3 KU 194559 México: Michoacan AY779250 — Hillis & Wilcox (2005) Lithobates sp. 4 AMNH 124167 Panama: Chiriquí AY779245 — Hillis & Wilcox (2005) Lithobates sp. 5 LACM 146764 Costa Rica: Heredia AY779246 — Hillis & Wilcox (2005) Lithobates sp. 6 LACM 146810 Costa Rica: Puntarenas AY779247 — Hillis & Wilcox (2005) Lithobates sp. 7 KU 194492 México: Jalisco AY779241 — Hillis & Wilcox (2005) Lithobates sp. 8 KU 195346 México: Puebla AY779248 — Hillis & Wilcox (2005) Strabomantidae (2) Pristimantis caryophyllaceus MVUP 1925 Panamá: El Copé FJ784473 FJ766776 Crawford et al. (2010) USNM 572343 Panamá: El Copé FJ784375 FJ766772 Crawford et al. (2010) Pristimantis cerasinus N121 Nicaragua: Bosawas + — This study Pristimantis ridens A USNM 572416 Panamá: El Copé FJ784388 FJ766808 Crawford et al. (2010) USNM 572417 Panamá: El Copé FJ784389 FJ766807 Crawford et al. (2010) Pristimantis ridens B MVUP 1829 Panamá: El Copé FJ784398 FJ766806 Crawford et al. (2010) USNM 572415 Panamá: El Copé FJ784399 FJ766805 Crawford et al. (2010) Pristimantis cf. ridens N090 Nicaragua: Bosawas + + This study N143 Nicaragua: Bosawas + + This study N144 Nicaragua: Bosawas + + This study N201 Nicaragua: Bosawas + + This study N263 Nicaragua: Cerro Saslaya + + This study N541 Nicaragua: Cerro Kilambé — + This study N998 Nicaragua: Cerro Peñas Blancas + + This study N1008 Nicaragua: Cerro Peñas Blancas + + This study
244
Table 4-2. Average nucleotide compositions of various taxonomic groups Taxon # of sequences Avg. Length A G C T
COI Amphibia 390 636.3 23.9% 18.0% 27.6% 30.5% Anura 256 629.3 23.3% 18.1% 28.0% 30.6% Caudata 144 649.5 25.1% 17.9% 26.7% 30.2% 16S
Amphibia 436 537.0 31.0% 20.1% 23.2% 25.7% Anura 277 553.6 30.0% 20.2% 23.8% 26.1% Caudata 269 512.5 33.2% 19.9% 22.3% 24.7%
245
Table 4-3. Potential candidate species identified through this study; UCS = Unconfirmed Candidate Species, CCS = Confirmed Candidate Species; DCL = Deep Conspecific Lineage; for IUCN Red List categories, CR = Critically Endangered, EN = Endangered, and VU = Vulnerable. Interspecific divergences are measured at the genus-level.
A priori
taxonomic assignment Current status
Potential
IUCN
Red List
Intraspecific
Divergence Interspecific Divergence Notes
Plethodontidae (16)
Bolitoglossa sp. inq. 1 Bolitoglossa cataguana CR 16S =0.0%
COI =0.7%
16S =2.3–8.7%,
COI =11.6–20.9%
(0.0% from B. decora for 16S)
Described by Townsend et al. (2009a)
Bolitoglossa sp. inq. 2 Bolitoglossa oresbia CR 16S =0.2%
COI =0.1%
16S =3.0–9.7%
COI =10.0–22.1%
Conspecific with B. oresbia and to
represent a range extension
(Townsend et al. 2011b)
Bolitoglossa celaque Bolitoglossa sp. 1 DCL EN 16S =0.8%
COI =0.3%
16S =1.8–10.0%
COI =4.5–21.7%
(within B. celaque complex:
16S =1.0–1.5%, COI =1.7–
3.0%)
Population from Sierra de Puca-
Opalaca; under study by author
Bolitoglossa celaque Bolitoglossa sp. 2 DCL EN 16S =0.3%
COI =0.2%
16S =2.0–10.3%
COI =5.2–21.5%
(within B. celaque complex:
16S =1.3–1.5%, COI =1.7–
3.6%)
Population from Montañas de la
Sierra; under study by author
Bolitoglossa conanti Bolitoglossa sp. 3 DCL EN 16S =0.0%
COI =0.0%
16S =3.1–9.3% COI =9.6–21.4% (within B. conanti complex: 16S =0.6–1.6%, COI =2.7–3.1%)
Population from Sierra de Omoa;
under study by author
Bolitoglossa conanti Bolitoglossa sp. 4 DCL EN 16S =0.0%
COI =0.0%
16S =3.5–9.4% COI =9.6–20.4% (within B. conanti complex: 16S =0.8–1.6%, COI =2.5–3.7%)
Population from Sierra del Merendón;
under study by author
Bolitoglossa
porrasorum
Bolitoglossa sp. 5 CCS CR 16S =0.2%
COI =0.7%
16S =2.0–8.6%
COI =9.2–23.3%
Population from Texíguat; under study
by author
Bolitoglossa
porrasorum
Bolitoglossa sp. 6 CCS CR 16S =N/A
COI = N/A
16S =2.0–8.1%
COI = N/A
Population from Pico Bonito; under
study by author
Bolitoglossa rufescens Bolitoglossa sp. 7 CCS 16S =0.2% 16S =5.5–10.3% Syntopic in Sierra de Omoa with B.
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COI =0.2%
COI =17.6–22.7% nympha; under study by author
Nototriton sp. inq. 1 Nototriton tomamorum CR 16S = N/A
COI = N/A
16S =3.3–5.4%
COI =11.3–14.1%
Described by Townsend et al. (2010a)
Nototriton sp. inq. 2 Nototriton picucha CR 16S =0.0%
COI =0.2%
16S =1.2–5.2%
COI = 2.9–12.3%
Described in Chapter 5 and by
Townsend et al. (2011a)
Nototriton sp. inq. 3 Nototriton sp. 1 CCS CR 16S =0.0%
COI =0.6%
16S =1.7–5.8%
COI =2.9–12.5%
Population from Sierra de Botaderos
Nototriton sp. inq. 4 Nototriton limnospectator N/A 16S =0.3%
COI =0.2%
16S =1.2–5.2%
COI =7.8–12.6%
Conspecific with N. limnospectator and
to represent a range extension
(Townsend et al. 2011b)
Nototriton sp. inq. 5 Nototriton lignicola N/A 16S =0.2%
COI = N/A
16S =2.4–5.9%
COI =10.0–13.9%
Conspecific with N. lignicola and to
represent a range extension
(Townsend et al. 2011b)
Nototriton barbouri Nototriton sp. 2 CCS CR 16S =N/A
COI = N/A
16S =1.2–6.0%
COI = N/A
Population from Pico Bonito; described
in Chapter 5 (as N. sp. A)
Nototriton barbouri Nototriton sp. 3 CCS CR 16S =N/A
COI = N/A
16S =1.7–5.8%
COI =5.9%–13.6%
Population from Texíguat; described in
Chapter 5 (as N. sp. B)
Oedipina sp. inq. 1 Oedipina kasios N/A 16S =0.1%
COI = N/A
16S =2.6–11.3%
COI =6.6–15.7%
Conspecific with O. kasios and to
represent a range extension
(Townsend et al. 2011b)
Oedipina sp. inq. 2 Oedipina nica EN 16S =0.1%
COI =0.0%
16S =2.6–10.2%
COI =6.6–16.4%
Described by Sunyer et al. (2010)
Oedipina sp. inq. 3 Oedipina koehleri EN 16S =0.0%
COI = N/A%
16S =3.1–8.4%
COI =14.4–16.2%
Described by Sunyer et al. (2011)
Oedipina gephyra Oedipina petiola CR 16S = N/A
COI = N/A
16S =3.7–10.5%
COI = N/A
Described by McCranie & Townsend
(2011)
Bufonidae (2)
Incilius coniferus Incilius sp. DCL DD 16S = N/A
COI = N/A
16S =3.6–9.3% COI =11.2–17.5% (from Panamanian I. coniferus: 16S =0.7%, COI =3.5%)
Population from northern Nicaragua;
under study by Sunyer, Townsend, and
Travers
Rhaebo haematiticus Rhaebo sp. UCS DD 16S =0.0%
COI = 0.2%
16S =10.3–12.4% COI =16.1–19.5% (from Panamanian R. haematiticus: 16S =2.2%, COI =5.4%)
Population from northern Nicaragua;
under study by Sunyer, Townsend, and
Travers
Craugastoridae (3)
Craugastor aurilegulus Craugastor sp. 1 DCL EN 16S =0.1% 16S =4.9–21.0% Population from vicinity of Texíguat;
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COI =0.6% COI =11.2–25.6%
(from Pico Bonito C.
aurilegulus: 16S =1.1%, COI
=3.9%)
may represent DCL
Craugastor sp. inq. 1 Craugastor sp. 2 UCS DD 16S = N/A
COI = N/A
16S =7.5–21.1%
COI =16.8–26.6%
Population from northern Nicaragua;
field identification Diasporus diastema
Craugastor sp. inq. 2 Craugastor sp. 3 UCS DD 16S =0.0%
COI =0.0%
16S =7.5–21.3%
COI =11.4–26.7%
Population from northern Nicaragua
Eleutherodactylidae
(1)
Diasporus diastema Diasporus sp. UCS DD 16S = N/A
COI = N/A
16S =7.1–21.6%
COI =15.7–27.2%
Population from northern Nicaragua
Hylidae (5)
Plectrohyla
guatemalensis
Plectrohyla sp. UCS CR 16S =0.0%
COI =0.1%
16S =2.6–13.8%
COI =8.8–23.8%
Population from Cordillera de La Flor-
La Muralla
Ptychohyla
hypomykter
Ptychohyla sp. 1 UCS DD 16S =N/A
COI = N/A
16S =5.5– 14.7%
COI = N/A
Population from eastern Guatemala
Ptychohyla spinipollex Ptychohyla sp. 2 UCS CR 16S =0.2%
COI =0.5%
16S =4.8–13.4%
COI =15.1–22.6%
Population from vicinity of Texíguat;
may represent DCL
Smilisca baudinii Smilisca sp. 1 UCS LC 16S =0.0%
COI =0.0%
16S =1.6–15.0 %
COI =6.6–22.7%
Populations from northern Nicaragua
Smilisca baudinii Smilisca sp. 2 UCS LC 16S =0.0%
COI =0.1%
16S =1.6–14.4%
COI =6.6–22.7%
Populations from Honduras
Leptodactylidae (1)
Leptodactylus fragilis Leptodactylus sp. UCS LC 16S =0.0%
COI =0.3%
16S =3.6–21.4%
COI =15.7–26.2%
Populations from Panama (Crawford et
al. 2010); Chortís Block samples
considered conspecific with nominal
form
Ranidae (7)
Lithobates brownorum
X forreri
Lithobates sp. 1 CCS EN 16S =0.8%
COI =0.5%
16S =2.2–16.5%
COI =9.7–22.4%
Populations from Southern Cordillera
of Serranía; being described by author
Lithobates maculatus Lithobates sp. 2 UCS EN 16S =0.0%
COI =0.1%
16S =1.6–12.2%
COI =2.4–20.5%
Populations from highlands in north-
central Nicaragua; under study by
author
Lithobates maculatus Lithobates sp. 3 UCS EN 16S =0.4%
COI =0.5%
16S =1.6–12.8%
COI =2.4–21.1%
Populations from low to moderate
elevations in northeastern Nicaragua;
under study by author
Lithobates maculatus Lithobates sp. 4 UCS EN 16S =0.0%
COI =0.0%
16S =1.8–12.8%
COI =5.7–20.7%
Populations from Texíguat and Sierra
de Sulaco; under study by author
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Lithobates maculatus Lithobates sp. 5 UCS EN 16S =0.6%
COI =1.2%
16S =2.9–12.3%
COI =7.2–21.5%
Populations from throughout Honduran
Serranía; under study by author
Lithobates maculatus Lithobates sp. 6 UCS EN 16S =N/A
COI =N/A
16S =2.6–12.6%
COI = N/A
Population from vicinity of Pico Bonito;
under study by author
Lithobates
warszewitschii
Lithobates sp. 7 UCS DD 16S =0.6%
COI = N/A
16S =8.2–17.2
COI =10.1–22.8%
Populations from northern Nicaragua
Strabomantidae (1)
Pristimantis ridens Pristimantis sp. UCS DD 16S =0.3%
COI =0.1%
16S =4.8–22.2%
COI =9.1–27.0%
Populations from northern Nicaragua
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Table 4-4. Results of BLASTN searches of the NCBI database for 16S consensus sequences representing 10 populations of taxonomically-unassigned salamanders.
Sample Matching sequence (GenBank accession #) Max ident
Max score
Query coverage
Bolitoglossa sp. inq. 1 1. Bolitoglossa decora (GU725449) 99% 904 100% Cataguana 2. Bolitoglossa morio (GU725452) 97% 830 100% 3. Bolitoglossa porrasorum (AF526151) 96% 824 100% 4. Bolitoglossa morio (AF218495) 96% 819 100% 5. Bolitoglossa flavimembris (GU725449) 96% 808 100% Bolitoglossa sp. inq. 2 1. Bolitoglossa flavimembris (GU725449) 96% 843 100% IRL 081 2. Bolitoglossa diaphora (GU725447) 95% 833 100% 3. Bolitoglossa morio (AF526144) 95% 821 100% 4. Bolitoglossa morio (GU725452) 95% 815 100% 5. Bolitoglossa dunni (GU725446) 95% 811 100% Nototriton sp. inq. 1 1. Nototriton lignicola (AF199204) 95% 780 100% Texiguat 2. Nototriton barbouri (AF199201) 94% 760 100% 3. Nototriton richardi (AF199206) 94% 758 100% 4. Nototriton abscondens (AF199199) 94% 758 100% 5. Nototriton brodiei (AF199202) 94% 754 100% Nototriton sp. inq. 2 1. Nototriton lignicola (AF199204) 97% 837 100% Agalta 2. Nototriton brodiei (AF199202) 96% 804 100% 3. Nototriton barbouri (AF199201) 96% 804 100% 4. Nototriton richardi (AF199206) 95% 785 100% 5. Nototriton saslaya (GU981761) 95% 776 100% Nototriton sp. inq. 3 1. Nototriton lignicola (AF199204) 96% 813 99% Botaderos 2. Nototriton barbouri (AF199201) 96% 802 99% 3. Nototriton richardi (AF199206) 95% 784 99% 4. Nototriton brodiei (AF199202) 95% 780 99% 5. Nototriton saslaya (GU981761) 94% 758 99% Nototriton sp. inq. 4* 1. Nototriton lignicola (AF199204) 99% 898 100% Cataguana 2. Nototriton brodiei (AF199202) 96% 798 100% 3. Nototriton barbouri (AF199201) 96% 798 100% 4. Nototriton richardi (AF199206) 95% 780 100% 5. Nototriton saslaya (GU981761) 94% 743 100% Nototriton sp. inq. 5 1. Nototriton lignicola (AF199204) 96% 821 100% Meámbar 2. Nototriton brodiei (AF199202) 96% 804 100% 3. Nototriton barbouri (AF199201) 96% 804 100% 4. Nototriton richardi (AF199206) 96% 797 100% 5. Nototriton saslaya (GU981761) 94% 765 100% Oedipina sp. inq. 1* 1. Oedipina kasios (FJ196866) 99% 893 100% Mta de Yoro 2. Oedipina kasios (FJ196867) 99% 893 100% 3. Oedipina quadra (FJ196865) 95% 769 99% 4. Oedipina uniformis (AF199230) 91% 682 100% 5. Oedipina grandis (FJ196864) 91% 676 100% Oedipina sp. inq. 2 1. Oedipina kasios (FJ196866) 97% 837 99% nica 2. Oedipina kasios (FJ196867) 97% 835 99% 3. Oedipina quadra (FJ196865) 94% 765 100% 4. Oedipina poelzi (AF199223) 92% 691 99% 5. Oedipina grandis (FJ196864) 91% 680 99% Oedipina sp. inq. 3 1. Oedipina cyclocauda (AF199214) 96% 811 100% 2. Oedipina pseudouniformis (AF199227) 96% 808 100% 3. Oedipina cyclocauda (AF199215) 96% 806 100% 4. Oedipina uniformis (AF199230) 95% 782 100% 5. Oedipina uniformis (AF199229) 95% 776 100%
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CHAPTER 5 CRYPTIC DIVERSITY AND REVISIONARY SYSTEMATICS OF CHORTÍS HIGHLAND
MOSS SALAMANDERS (CAUDATA: PLETHODONTIDAE)
Inconspicuous form, obscure or secretive behavior, and challenging habitat
associations are principal reasons why cryptozoic1 diversity historically has been
overlooked and understudied (Pfenninger & Schwenk 2007). Molecular phylogenetic
analyses, facilitated through techological advances like PCR (Mullis 1990), Sanger
sequencing (Sanger et al. 1977), and next generation DNA sequencing (Schuster
2008), have led to the discovery of numerous genetically divergent but morphologically
cryptic lineages (Bickford et al. 2007). Many tropical lungless salamanders (Amphibia:
Caudata: Plethodontidae) are characterized by their small size, conserved morphology,
and secretive habits, and present some of the most challenging subjects for systematic
study (e.g. Wake & Elias 1983; Highton 1995; Jockusch et al. 2001).
As revealed in the preceding chapters, lungless salamanders (Caudata:
Plethodontidae) represent the most diverse (in both named and candidate species) and
the most endangered group of vertebrates in the Chortís Block. In this chapter, I
evaluate cryptic diversity and provide a taxonomic revision of an endemic clade of
cryptozoic salamanders: the genus Nototriton, or moss salamanders.
Salamanders as Models for Evolutionary Study
Wake (2009) provided an excellent review of the advances in the biological
sciences that have resulted in taxon-based research focusing on salamanders. In brief
(Wake 2009:333):
The clade [Caudata] is widespread and diverse, yet sufficiently small that one can keep all of the species in mind. This facilitates research from
1 Cryptozoic – Refers to organisms of small size, cryptic coloration, and that exhibit secretive behavior
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diverse perspectives: systematics and phylogenetics, morphology, development, ecology, neurobiology, behavior, and physiology. Different avenues of research offer unique perspectives on how a relatively old vertebrate clade has diversified. An integrated, hierarchically organized, multidimensional program of research on a taxon illuminates many general principles and processes. Among these are the nature of species and homology, adaptation and adaptive radiations, size and shape in relation to issues in organismal integration, ontogeny and development in relation to phylogeny, the ubiquity of homoplasy, ecological niche conservation, species formation, biodiversity, and conservation.
Specific to the use of salamanders as a study group in the Chortís Block, I
recognize a number of advantages. The majority of living salamanders (613 species;
AmphibiaWeb, 2 September 2011) are members of the family Plethodontidae (417
species, 68% of all living Caudata), and the majority of plethodontids are members of
Neotropical-restricted genera (265 Neotropical species, 63.6% of all Plethodontidae,
43% of all living Caudata), indicating that an ancient order underwent extraordinary
Cenozoic diversification in tropical America. The Chortís Block is demonstrated to have
a diverse endemic salamander fauna, with the majority of endemism found in the
highlands (McCranie & Wilson 2002; Wilson & McCranie 2004b). In another highland
area of high ecophysiographic heterogeneity, the comparatively well-studied
Appalachian Mountains of eastern North America, plethodontids are highly diverse and
demonstrate a wide variety of evolutionary patterns and processes, including both
adaptive and non-adaptive radiations, parallel evolution, and ecological niche
conservatism accompanied with morphological conservatism (e.g. Tilley & Mahoney
1996; Kozak & Wiens 2006, 2010; Kozak et al. 2006; Crespi et al. 2010).
Among the taxa known from the Chortís Highlands, a number of taxonomic
problems exist, and numerous areas of presumably suitable habitat remain unsampled.
The Chortís Highlands salamander fauna is highly threatened by loss of habitat,
252
potentially due to climate change (as demonstrated in the Appalachian Mountains by
Milanovich et al. 2010), and by both direct and indirect effects from wider declines in
highland amphibian communities (Rovito et al. 2009). Of the 36 species of salamanders
recorded from the Chortís Highlands (reviewed in Appendix 1), 11 are Critically
Endangered, 12 are Endangered, 2 are Vulnerable, 1 is Near Threatened, 6 are Least
Concern, and 4 are Data Deficient (AmphibiaWeb 2011, IUCN 2011), meaning that
close to 70% of all known salamander species in the Chortís Highlands are in the
IUCN’s three highest threat categories (over 80% when poorly-known, Data Deficient
species are included).
Salamander Diversity in the Chortís Block
Salamanders originated and initially diversified in Laurasia (Zhang and Wake
2009), with a single family, Plethodontidae, dispersing into the Neotropics beginning in
the late Cretaceous Period (Hanken and Wake 1982; Vieites et al. 2007). Plethodontid
salamanders are hypothesized to have dispersed from north-to-south as the Central
American land bridge formed, possibly colonizing the Chortís Block prior to the
divergence of Cryptotriton from remaining neotropical plethodontids (Appendix 3 of
Wiens et al. 2007).
Neotropical salamanders can be characterized by their high degree of
diversification and widespread morphological conservatism and homoplasy (Wake
1991; Parra-Olea & Wake 2001). Diverse radiations of plethodontids are well
documented in western Nuclear Central America (southern México and Guatemala;
Wake 1987) and southern Central America (Costa Rica and western Panama; Wake
2005); however, much of this cryptic diversity has been revealed only recently by
molecular studies (e.g., Garcia-París et al. 2000; Hanken et al. 2005). Perhaps the best
253
example of this taxonomic uncertainty is seen in the suite of small salamanders
currently divided into the genera Chiropterotriton, Cryptotriton, Dendrotriton, and
Nototriton (García-París & Wake 2000). As recently as 1983, these morphologically
conserved genera were considered part of a single wide-ranging genus, Chiropterotriton
(Wake & Elias 1983). The application of molecular techniques coupled with increased
sampling and rigorous studies of external and internal morphology have led to the
current taxonomy, which continues to be refined as new populations and taxa are
discovered and described (e.g., McCranie et al. 2008; Townsend et al 2010a). Even
among well-studied taxa and regions, such as Bolitoglossa in Costa Rica,
morphologically conserved taxa have presented long-standing problems that can best
be resolved using an integrative approach that maximizes use of both molecular and
morphological evidence (e.g., Hanken et al. 2005).
Like western Nuclear and southern Central America, the Chortís Highlands are a
site of remarkable plethodontid diversity (McCranie and Wilson 2002). The Bolitoglossa
(Magnadigita) dunni species group, a Chortís Highlands endemic radiation of 12
nominal species (McCranie et al. 2005), has the highest estimated rate of diversification
of any major clade of Mesoamerican salamanders (Wiens et al. 2007).
Prior to initiation of this study, there were 13 recognized species of moss
salamanders, genus Nototriton, distributed across Central American highland forests
(García-París & Wake 2000). These salamanders are difficult to differentiate, given their
small adult size (all species < 40 mm standard length) and highly conserved
morphology (Good & Wake 1993; García-París & Wake 2000). Their utilization of moss
mats, deep leaf litter, and rotten logs as habitat makes them particularly difficult to
254
detect (Good & Wake 1993). The genus is subdivided into three well-supported species
groups: the N. barbouri group, the N. picadoi group, and the N. richardi group
(Papenfuss & Wake 1987, Savage 2002). Each morphologically-defined species group
corresponds to a clade supported by data from the mitochondrial genes 16S and
cytochrome b (García-París & Wake 2000, Wiens et al. 2007).
The Nototriton barbouri group is the only clade of Nototriton restricted to the
Chortís Highlands (García-París & Wake 2000). This group contains five nominal
species inhabiting highland forests in eastern Guatemala and northern and central
Honduras. The five putative species of the N. barbouri group are each endemic to
isolated cloud forest localities in the Chortís Highlands (Figure 5-1): N. barbouri
(Schmidt 1936), N. brodiei Campbell & Smith 1998, N. lignicola McCranie & Wilson
1996 [1997], N. limnospectator McCranie, Wilson & Polisar 1998 and N. stuarti Wake &
Campbell 2000. Another species of Nototriton found in the Chortís Highlands, Nototriton
saslaya, is extralimital to the Nototriton barbouri group, representing the northernmost
representative of the N. picadoi group, endemic to a single highland forest area at the
southern edge of the Nuclear Central American piedmont in north-central Nicaragua.
Nototriton saslaya aside, the remaining five species of Chortís Highland Nototriton all
occur in small areas of highland forest in a belt from easternmost Guatemala to north-
central Honduras, corresponding to the Northern and Central Cordilleras of the Chortís
Highlands (Figure 5-1).
While the salamander fauna of Nuclear Central America has been the focus of
considerable study (Dunn 1924; Schmidt 1933, 1936; Wake 1987; McCranie & Wilson
1993, 1997; Campbell & Smith 1998), new species continue to be discovered and
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Figure 5-1. Distribution of Nototriton in the Chortís Highlands. Shaded areas >1000 m
elevation; open circle = N. picucha; open triangles = N. brodiei; closed triangles = N. limnospectator; open square = N. sp. A; solid square = N. barbouri; open star = N. tomamorum, N. sp. B; solid star = N. stuarti; open diamonds = N. lignicola; solid diamond = N. saslaya; N. sp A. and N. sp. B refer to populations currently assigned to N. barbouri.
described, often from areas that are considered relatively well known in terms of their
amphibian diversity (Campbell et al. 2010; McCranie et al. 2005, 2008; Rovito et al.
2010; Townsend et al. 2009a, 2010a; Vásquez-Almazán et al. 2009). This can be
attributed in part to the small size and cryptic nature of many tropical salamanders,
which, in the case of Nototriton, results in the majority of species being known from 10
or fewer specimens (Good & Wake 1993; McCranie & Wilson 2002). Indeed, the five
species of the N. barbouri group have been represented previously in published
phylogenetic studies by only seven samples from four putative taxa (García-París &
Wake 2000; Wiens et al. 2007; Adams et al. 2009).
256
Intensive sampling in the Chortís Highlands over the past six years has led to the
collection of additional samples of nominal taxa and the discovery of new populations of
Nototriton from isolated localities (Chapters 3 and 4). In order to evaluate the
evolutionary relationships among Chortís Highland Nototriton in light of their currently
accepted taxonomy, I employed two strategies for analysis of a three gene mtDNA
dataset, which supplements the 16S/COI dataset used in Chapter 4 with the a fragment
of the gene cytochrome b (cyt b). First, I used a DNA barcoding approach to identify
potential species boundaries and candidate species by evaluating intra- and
interspecific sequence divergence and the effectiveness of each gene for species
delimitation using uncorrected distance-based methods. Second, I inferred phylogenetic
relationships using Bayesian and maximum likelihood (ML) analysis with evolutionary
models partitioned by gene and codon. Finally, I applied the distance-based and
phylogenetic results, supplemented by comparative data from external morphology and
osteology, to redefine N. barbouri and describe three new species of Nototriton endemic
to the Chortís Highlands of Honduras.
Methods and Materials
Sampling
Taxa and samples used in this study, along with their associated locality data and
museum and GenBank accession numbers, are presented in Table 5-1. All nominal
taxa in the N. barbouri group were included, with the exception of N. stuarti, which is
only known from a single specimen collected in 1991 (Wake & Campbell 2000).
Nototriton saslaya, the only representative of the N. picadoi group found in the Chortís
Highlands, was used as an outgroup. Institutional abbreviations follow those
standardized by the American Society of Ichthyologists and Herpetologists
257
(http://www.asih.org/codons.pdf), except for IRL (field series of Ileana R. Luque-Montes)
used for a sample donated to the Florida Museum of Natural History in May 2009 that
remains uncataloged. Forest formations follow Holdridge (1967) as applied by McCranie
& Wilson (2002).
In this chapter, I present genetic evidence for two undescribed species heretofore
considered synonymous with N. barbouri. However, I do not include the morphological
diagnoses and descriptions associated with those species, as they have not yet been
published at the time of completing this dissertation.
DNA Extraction, PCR Amplification, and Sequencing
Template DNA was extracted from muscle tissue using the Qiagen PureGene
DNA Isolation Kit following manufacturer’s instructions. Fragments of the mitochondrial
genes 16S large subunit RNA (16S), cytochrome b (cyt b), and cytochrome oxidase
subunit I (COI) were amplified using the primers 16Sar-L and 16Sbr-H for 16S (Palumbi
et al. 1991), MVZ15L and MVZ16H for cyt b (Moritz et al. 1992), and dgLCO-1490 and
dgHCO-2198 for COI (Meyer 2003). PCR reactions were typically 20L in total volume,
containing ~25ng of DNA template, 4 L 5X PCR buffer, 1.2 L MgCl2 (25mM), 0.09 L
dNTPs (10 mM), 0.8 L of each primer (10M), 0.2 L GoTaq Flexi polymerase
(Promega, Madison, WI, USA), and 11.91 L H2O. Amplification profiles were as
follows: for 16S, an initial denaturation for 3 minutes at 94°C, 35 cycles of denaturation
at 94°C for 45 seconds, annealing at 50°C for 45 seconds, and extension at 72°C for 45
seconds, with a final elongation at 72°C for 5 minutes; for cyt b, an initial denaturation
for 3 minutes at 94°C, followed by 38 cycles of 94°C for 30 seconds, 48°C for 1 minute,
and 1 minute for 45 seconds, final elongation at 72°C for 5 minutes; and for COI,
258
denaturation for 1.5 minutes, 37 cycles of 94°C for 40 seconds, 45°C for 40 seconds
and 72°C for 40 seconds, with a final elongation at 72°C for 5 minutes. All PCR
products were verified using electrophoresis on a 1.5% agarose gel stained with
ethidium bromide. Unincorporated nucleotides were removed from PCR products using
1 uL of ExoSAP-IT (USB, Santa Clara, CA, USA) per 10uL of PCR product. I cycle
sequenced both forward and reverse stands using the BigDye Terminator 3.1 Cycle
Sequencing kit, followed by spin column filtration through Sephadex before
electrophoresing the products on an ABI 3130xl (Applied Biosystems, Inc).
Sequence Alignment and Model Selection
A dataset containing all available sequences of Nototriton was generated from a
combination of our newly generated sequence data (Table 5-1) and published data
available from NCBI (http://www.ncbi.nlm.nih.gov/). Sequences were aligned using
ClustalW (Thompson et al. 1994) within the program package MEGA5 (Tamura et al.
2011) using the default parameters. The dataset was partitioned by gene (16S, which
codes for RNA) and by codon position (1st, 2nd, 3rd) for cyt b and COI (both protein-
coding genes), and selected the best fit model of nucleotide evolution for each gene and
each partition with the program jModeltest v0.1 (Posada 2008), which uses PhyML 3.0
(Guindon & Gascuel 2003) to estimate models under a likelihood framework. The
number of substitution schemes was set to three to limit the number of models tested to
24, corresponding to the number of different models that can be implemented in
MrBayes 3.1.2 (Huelsenbeck & Ronquist 2001). Models selected for each partition are
summarized in Table 5-2.
259
Sequence Analyses
A DNA barcoding approach was utilized in order to determine whether
monophyletic clusters of samples corresponding to named taxa, as well as to identify
candidate species for further taxonomic evaluation (Vences et al. 2005; Smith et al.
2008). Uncorrected (p-distance) pairwise sequence divergence was calculated for all
samples and for each gene, and uncorrected neighbor-joining (NJ) distance trees
(10,000 bootstrap pseudoreplicates) were estimated to provide graphical representation
of intra- and interspecific variation. Sequence divergence estimation and NJ analyses
were performed in MEGA5 (Tamura et al. 2011).
Two of the three target genes are protein-coding, making them potentially
susceptible to substitution saturation at the third codon position that, when excessive,
can render the locus phylogenetically uninformative (Halanych & Robinson 1999; Farias
et al. 2004; Parra-Olea et al. 2004). Substitution saturation was evaluated using an
entropy-based index calculated in the program package DAMBE 5.2.34 (Xia & Xie
2001), which uses two simulated topologies (one perfectly symmetrical and one
extremely asymmetrical) based on the supplied sequence data to calculate an Index of
Substitution Saturation (ISS). High substitution saturation is indicated by an ISS
significantly greater than or not significantly different than the Critical ISS (ISS.C) for both
the perfectly symmetrical topology and an extremely asymmetrical topology (Xia et al.
2003; Xia & Lemey 2009) determined with two-tailed t-test. Prior to measuring
substitution saturation, the proportion of invariant sites was estimated for each gene in
DAMBE 5.2.34 (Xia & Xie 2001) using a goodness-of-fit test with a Poisson+Invariant
distribution, and the proportion of invariant sites was used as a parameter to optimize
estimation of substitution saturation.
260
Bayesian Inference and Maximum Likelihood Phylogenetic Analyses
Bayesian inference (BI) was performed using MrBayes 3.1.2 (Huelsenbeck &
Ronquist 2001), and consisted of two parallel runs of four Markov chains (three heated,
one cold) run for 10 x 106 generations and sampled every 1,000 generations, with a
random starting tree and the first 2 x 106 generations discarded as burnin. Maximum
likelihood analysis was carried out in RAxML v7.2.8 (Stamatakis 2006), with 1000
bootstrap pseudoreplicates under the default GTR-GAMMA substitution model (the
simplest model implemented in RAxML); the dataset was partitioned by gene for 16S
and by codon position for cyt b and COI.
Comparative Morphology
Morphological measurements were taken with precision digital calipers and a
stereo microscope with an optical micrometer, with measurements rounded to the
nearest 0.1 mm. Abbreviations used for morphological measurements are as follows:
snout to posterior edge of vent, SL; axilla–groin length, AG; trunk width at midbody, TW;
head length from tip of snout to gular fold, HL; head width taken at maximum, HW; tail
length, TL; hind limb length, HLL; forelimb length, FLL; combined forelimb and hind limb
lengths, CLL; hind foot length, HFL; hind foot width, HFW; and nares length, NL. To
allow for comparative studies across taxa, most measurements are standardized by SL;
morphological comparisons of the aforementioned characters are presented in Table 5-
4. Comparative data for other taxa not examined by the authors is taken from Good &
Wake (1993), Campbell & Smith (1998), Lynch & Wake (1978), McCranie et al. (1998),
Ehmcke & Clemen (2000), Köhler (2002), McCranie & Wilson (2002), Savage (2002),
and Wake & Campbell (2000).
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Results
Best fit nucleotide substitution models varied by gene and codon position,
supporting use of a gene and codon based partitioning strategy (Table 5-2). For the 489
bp of 16S, 10.8% of nucleotides were variable. Variability increased to 27.4% and
27.8% for COI (658 total bp) and cyt b (702 total bp) respectively. Distance-based
analyses of each gene yielded unambiguous results in terms of delimiting species-level
lineages and clusters, displaying a bimodal pattern of pairwise sequence divergence
(i.e., a ―barcoding gap‖) for each locus that can be represented graphically and easily
interpreted using distance-scaled NJ trees (Figure 5-2). The smallest range of
intraspecific sequence divergence in our data was for COI (0.002–0.003%), followed by
16S (0.0–0.6%) and cyt b (0.0–1.9%). Interspecific divergence ranged from 1.2–6.4%
for 16S, the most conservative gene, to 6.1–13.9% for COI and 5.2–14.7% for cyt b
(Table 5-3). For all three genes, the bimodal distribution of sequence divergence allows
for simple identification between the ranges of intra- and interspecific divergence
(Figure 5-2), with 16S having the narrowest gap (0.6%), followed by cyt b (3.3%) and
COI (5.8%).
Substitution saturation was not a factor for 16S, with the ISS value (0.2197) being
highly significantly less than the critical ISS+C value for both the symmetrical
(ISS+C(SYM)=0.7112, P=0.0000) and asymmetrical (ISS+C(ASYM)=0.4960, P=0.0000)
topologies. Likewise, COI did not exhibit evidence of substitution saturation, with an ISS
value (0.3667) significantly less than the critical ISS+C value for both the symmetrical and
asymmetrical topologies (ISS+C (SYM)=0.7320, P=0.0000; ISS+C (ASYM)=0.5482, P=0.0000).
For cyt b, however, ISS (0.7722) was significantly larger than ISS+C for both the
symmetrical (ISS+C(SYM)=0.7337, P=0.0005) and asymmetrical (ISS+C(ASYM)=0.5254,
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Figure 5-2. Comparison of ―barcoding gaps‖ for three mitochondrial genes used to delimit species boundaries in Nototriton. Unrooted neighbor-joining trees (10,000 bootstrap replicates) scaled by uncorrected p-distance, with shaded area representing gap between upper limit of intraspecific variation and lower limit of interspecific variation. Note that the trees for COI and cyt b are scaled to 0.01, while the 16S tree is scaled to 0.005 due to lower overall divergence. Numbers following taxon labels refer to those in Table 5-1.
263
264
P=0.0000) topologies, indicating that excessive substitution saturation was present and
the data, therefore, were poorly suited for use phylogenetic study (Xia et al. 2003; Xia &
Lemey 2009). To further investigate, I tested for substitution saturation at each codon
position on cyt b, and found the third position to have a higher but not significantly
different ISS value (0.6981) on the perfectly symmetrical topology (ISS+C(SYM)=0.6797,
P=0.4553) and to be significantly higher than the asymmetrical topology
(ISS+C(ASYM)=0.4554, P=0.0000), while the 1st and 2nd codon positions did not show
evidence of saturation (1st codon position: ISS=0.3721; ISS+C (SYM)=0.6797, P=0.0000;
ISS+C (ASYM)=0.5482, P=0.0509; 2nd codon position: ISS=0.3438; ISS+C (SYM)=0.6797,
P=0.0000; ISS+C (ASYM)=0.5482, P=0.0094).
Phylogenetic analyses were performed both on the complete combined
mitochondrial dataset, as well the combined dataset with the 3rd codon position of cyt b
excluded, in order to account for saturation (Figure 5-3). Both analyses recovered a
strongly supported ―northern‖ clade (bs=100/100; pp=1.0/1.0) consisting of N. brodiei
and two unnamed candidate species (N. sp. A and B) currently referred to as N.
barbouri sensu lato. Also strongly supported by both analyses is the sister relationship
between N. barbouri sensu stricto and N. limnospectator (bs=82/87; pp=1.0/1.0), a
―central‖ clade of the N. barbouri group.
The two datasets yielded different topologies in terms of the placement of N.
tomamorum and the N. sp. inquirenda 2 with respect to the remaining members of the
N. barbouri group. The phylogeny excluding 3rd position recovers a topology congruent
with recently published phylogenies of Nototriton (Townsend et al. 2010a)
supplemented by additional sampling, including two samples from a newly discovered
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Figure 5-3. Bayesian phylograms showing discordance between combined mtDNA phylogenies due to saturation at the third codon position for cytochrome b. Note the alternative placement of Nototriton tomamorum and N. picucha sp. nov. as sister to the remaining N. barbouri group. Bootstrap scores from maximum likelihood analyses shown above branches; posterior probability values from Bayesian inference shown below branches.
population in eastern Honduras. The new species is recovered as sister to the
remaining N. barbouri group (bs=82; pp=1.0), with N. tomamorum as sister to the entire
clade (bs=100; pp=1.0), including the new species (Figure 5-3). The phylogeny
including 3rd position recovers N. tomamorum as sister to N. lignicola (bs=72; pp=0.84),
and, instead, places the new species as sister to a N. barbouri group (bs=100; pp=1.0).
266
Discussion
DNA Barcode Identification of Chortís Highland Moss Salamanders
Sequence divergence data from 16S, cyt b, and COI all exhibit a bimodal
distribution of uncorrected pairwise comparisons, each demonstrating a ―barcoding gap‖
indicative of clear differentiation between intra- and interspecific variation (Figure 5-2).
Results for all three loci were congruent, identifying the same sample groupings and
unambiguously separating putative species-level lineages and revealing three potential
candidate species: a newly discovered population from the Sierra de Agalta, N. barbouri
sensu lato from Parque Nacional Pico Bonito (N. sp. A), and N. barbouri sensu lato
Reserva de Vida Silvestre Texíguat (N. sp. B). Samples representing two recently
discovered allopatric populations of Nototriton were also included in this study: one from
the vicinity of Cataguana in Parque Nacional Montaña de Yoro and the other from
Parque Nacional Cerro Azul Meámbar on the eastern side of Lago de Yojoa. All three
gene loci clearly indicated that these samples were conspecific with N. lignicola and N.
limnospectator, respectively, and, therefore, confirm that these samples represent new
populations of two species previously considered to be highly threatened single-site
endemics (Townsend et al. 2011b).
In the case of Chortís Highland Nototriton, analysis of mtDNA sequence data
using a barcoding approach is shown here to be an effective means of identifying
potential candidate species and newly discovered populations of known taxa, but in and
of itself is not grounds for proposing new taxa or making other taxonomic changes.
Rather, I view the barcoding approach as an effective and increasingly necessary first
step in an integrative process that leads to correct taxonomic allocation of newly
collected samples, particularly in difficult and cryptic groups like Nototriton.
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Influence of Substitution Saturation in Cytochrome B Dataset
Our analyses of sequence data from cyt b revealed excessive substitution
saturation at the third codon position, a phenomenon that has been shown to lead to
bias in phylogenetic inference in studies of deep relationships among salamanders
(Zhang & Wake 2009), including plethodontids (Mueller et al. 2004; Macey 2005; Vieites
et al. 2011). This study provides an example of excessive saturation biasing
phylogenetic results at the interspecific level in salamanders, and its influence appears
to be limited, at least in this case, to two species-level lineages. That the saturation
problem has not been previously identified in Nototriton can be attributed to use of a
longer fragment of cyt b (702 bp) than had been used in previous phylogenetic analyses
of the genus (385 bp; García-París & Wake 2000; Townsend et al. 2010a). When our
dataset is trimmed to 385 bp to match the length of most cyt b sequences available from
NCBI (http://www.ncbi.nlm.nih.gov/) for Nototriton, substitution saturation is not a factor
at any codon position, with all ISS values being significantly less than the critical ISS+C
value for both the symmetrical topologies (1st codon position: ISS=0.2396,
ISS+C(SYM)=0.6639, P=0.0000; 2nd codon position: ISS=0.0.989, ISS+C(SYM)=0.6630,
P=0.0000; 3rd codon position: ISS=0.3061, ISS+C(SYM)=0.6690, P=0.0000) and
asymmetrical topologies (1st codon position: ISS = ISS+C(ASYM)=0.4113, P=0.0037; 2nd
codon position: ISS+C(ASYM)=0.4101, P=0.0004; 3rd codon position: ISS+C(ASYM)=0.4575,
P=0.0000). Phylogenetic analysis using the 385 bp cyt b fragment (not shown)
produced a topology completely congruent with that of the dataset that excluded the 3rd
codon position of cyt b (468 bp), suggesting that the 385 bp fragment is short enough to
mitigate bias from 3rd position saturation.
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Phylogenetic Systematics and Candidate Species
As indicated here, paraphyly exists among populations currently referred to as
Nototriton barbouri (Schmidt 1936). Populations from Reserva de Vida Silvestre
Texíguat and Parque Nacional Pico Bonito in northern Honduras referred to N. barbouri
(McCranie & Wilson 1995; McCranie 1996a; McCranie & Wilson 2002; McCranie &
Castañeda 2007) are paraphyletic with respect to a sample from Montaña de Macuzal,
the presumed type locality of N. barbouri (McCranie and Wilson 2002: 145). Based on
our phylogenetic results (Figure 5-3), N. barbouri sensu stricto is the sister species to N.
limnospectator, which together form a ―central‖ clade distributed in highland forests from
Montaña de Santa Bárbara eastward through the Sierra de Sulaco to Montaña de
Macuzal.
García-París & Wake (2000:49) suggested that samples of N. barbouri sensu lato
from Parque Nacional Pico Bonito (USNM 339712, 497552) and Reserva de Vida
Silvestre Texíguat (USNM 509333) might represent distinct taxa, an assertion well
supported by our results. Populations of N. barbouri sensu lato from Parque Nacional
Pico Bonito (N. sp. A) and Reserva de Vida Silvestre Texíguat (N. sp. B) form a well-
supported clade with N. brodiei of eastern Guatemala and northwestern Honduras,
together forming the ―northern‖ clade of the N. barbouri group (Figure 5-3). Somewhat
surprisingly, given their geographic distributions, and contrary to the previous cyt b-
based phylogenetic hypothesis (García-París & Wake 2000), both combined
phylogenies strongly support N. sp. B, from north-central Honduras, as sister to a N.
brodiei/N. sp. A clade (bs=100; pp=1.0). These results provide phylogenetic support for
recognition of both N. sp. A and N. sp. B as species-level taxa; however one known
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population of N. barbouri sensu lato remains to be evaluated phylogenetically (Pico Pijol
in Departamento de Yoro).
Two samples from a newly discovered population of Nototriton in Parque Nacional
Sierra de Agalta in eastern Honduras are shown to be conspecific with each other and a
relatively divergent lineage within the group (Figure 5-3). This undescribed species
appears to be a typical member of the N. barbouri group in terms of external
morphology, with relatively small nostrils and free, well-differentiated toes, which leads
us to conclude that the phylogeny excluding 3rd codon position on cyt b, which includes
the new species as part of an ingroup that is sister to N. tomamorum, most accurately
represents the evolutionary history of these salamanders. The alternative phylogenetic
hypothesis, obtained using the concatenated mtDNA dataset with cyt b fragment
including the saturated 3rd codon position, implies that the distinctive morphology of N.
tomamorum, such as enlarged nostrils and syndactylous feet, are derived characters
that evolved as the result of the divergence of N. tomamorum and N. lignicola from a
common ancestor. Future analyses that include additional samples and nuclear gene
loci should provide some measure of resolution of the phylogenetic position of N.
tomamorum.
Systematics
A Divergent New Lineage from Refugio de Vida Silvestre Texíguat
During my first visit to Refugio de Vida Silvestre Texíguat in April 2008,
malacologist John Slapcinsky collected a small salamander in leaf litter packed into a
crevice along the stream below the La Fortuna campsite. This single specimen
possesses a series of morphological characteristics unique among Honduran
salamanders. Comparison of morphological and mitochondrial DNA sequence data
270
confirms that this specimen represents a distinctive and undescribed species, and a
relict lineage sister to the clade corresponding to the Nototriton barbouri group (Figure
5-4).
Nototriton tomamorum Townsend, Butler, Wilson, & Austin 2010a
Figure 5-4
Nototriton sp. inq. 1: Chapter 3.
Holotype. UF 155477, a female from 2.5 km north-northeast of La Fortuna, 1,550
m elevation, Refugio de Vida Silvestre Texíguat, Departamento de Yoro, Honduras.
GenBank accession numbers GU971731 (16S), GU971732 (cyt b), JN377407 (COI).
Diagnosis. A small member of the genus Nototriton (SVL=26.9 mm; Table 5-4)
based on having 13 costal grooves (>16 costal grooves in Oedipina), hands and feet
longer than broad (hands and feet broader than long in Bolitoglossa), and nares that are
smaller than most Cryptotriton and Dendrotriton (Figure 5-4A, B; 0.018 NL/SVL; 0.020–
0.029 NL/SVL in Cryptotriton [except some individuals of C. veraepacis] and
Dendrotriton). Cryptotriton veraepacis has nares ranging from 0.017–0.027 NL/SVL
(mean 0.022), and can be differentiated from N. tomamorum by having a uniformly dark
gray ventral surface (ventral surface pale with gray flecks in N. tomamorum; Figure 5-
4B). Generic placement in Nototriton is also strongly supported by sequence data from
the mitochondrial genes 16S, COI, and cyt b (Table 5-3; Figures 5-2, 5-3). This new
species is distinguished from all other Nototriton, except N. richardi and N. tapanti, by
having syndactylous hands and feet (Figure 5-4D, E; hands and feet with free,
differentiated toes in all other species) and relatively large nares (Figure 5-3C, B; 0.018
NL/SVL versus 0.010–0.016 in N. picadoi, 0.003–0.014 in N. abscondens, 0.012 in N.
stuarti, 0.005–
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Figure 5-4. Nototriton tomamorum. A) Dorsal and ventral views of the holotype of N.
tomamorum (UF 155377), standard length 26.9 mm. B) Dorsal view of the head of the holotype of N. tomamorum. C) Lateral view of the head of the holotype of N. tomamorum. D) Dorsal view and E) ventral view of right hind foot of the holotype of N. tomamorum, showing the lack of separation or differentiation in the toes, and absence of subdigital pads. Photos © J.H. Townsend.
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0.011 in N. barbouri, 0.006–0.009 in N. lignicola, 0.004–0.009 in N. guanacaste, 0.004–
0.005 in N. brodiei, 0.003 in N. limnospectator, 0.003 in N. major, and 0.002–0.003 in N.
saslaya). Nototriton tomamorum can be further differentiated from members of the N.
barbouri group by having a broader head (0.145 HW/SVL versus 0.138 in N. stuarti,
0.104–0.132 in N. barbouri, 0.120 in N. brodiei, 0.103–0.118 in N. lignicola, and 0.095–
0.118 in N. limnospectator) and fewer maxillary teeth (26, versus 36 in N. stuarti, 41–54
in N. barbouri, 42–55 in N. limnospectator, 46–54 in N. lignicola, and 60–62 in N.
brodiei), from members of the N. picadoi group by having a relatively shorter tail (0.911
TL/SVL, versus 1.441 in N. major, 1.123–1.344 in N. picadoi, 1.013–1.365 in N.
abscondens, 1.210–1.337 in N. guanacaste, and 1.10–1.30 in N. gamezi) and narrower
feet (0.037 HFW/SVL, versus 0.058–0.071 in N. abscondens, 0.059 in N. major, 0.060–
0.070 in N. picadoi, and 0.066–0.072 in N. guanacaste), and from N. saslaya by having
shorter forelimbs (0.160 FLL/SVL, versus 0.194–0.210 in N. saslaya) and hind limbs
(0.197 HLL/SVL, versus 0.217–0.244 in N. saslaya) and narrower feet (0.037
HFW/SVL, versus 0.075–0.091 in N. saslaya). The new species also differs from N.
richardi and N. tapanti in having a pale ventral surface mottled with gray
chromatophores (ventral surface brown with dark flecks in N. richardi and dark brown in
N. tapanti), by having a tail that is shorter than the snout-vent length (0.91 TL/SVL,
versus 1.072–1.482 in N. richardi and 1.205 in N. tapanti), longer forelimbs (0.160
FLL/SVL, versus 0.140–0.146 in N. richardi and 0.147 in N. tapanti), longer hind limbs
(0.197 HLL/SVL, versus 0.174–0.187 in N. richardi and 0.174 in N. tapanti), and
narrower feet (0.037 HFW/SVL, versus 0.044–0.050 in N. richardi and 0.041 in N.
tapanti). This new species is also well differentiated from all other species of Nototriton
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based on mitochondrial sequence data, and is 3.5–5.7% divergent on 16S, 11.5–13.9%
divergent on COI, and 9.5–13.1% divergent on cyt b from other Chortís Highland
Nototriton (Table 5-3).
Description of holotype. Nototriton tomamorum is known only from a single,
presumably female (mental gland and cloacal papillae absent) specimen, preserved
with its mouth open and tongue extended, and is a relatively small member of the genus
(SVL=26.9 mm, total length=51.4 mm) with a slender body and reduced limbs. Its head
is rounded and slightly broader than the body, and the nostrils are relatively large
(NL/SVL=0.018), and the snout is rounded and of moderate length (Figure 5-4B, C).
The nasolabial protuberances are apparent but not well developed, and barely extend
below the upper lip line. The eyes are relatively large and protuberant, and the parotoid
glands appear large but not well defined. The teeth are exceedingly small; there are
approximately 26 maxillaries, 4 premaxillaries set slightly forward from the maxillary
teeth, and 11 vomerines; vomerine teeth are arranged in two short medially-positioned
arches. The limbs are short (CLL/SVL=0.36), with the adpressed limbs being separated
by approximately 5.5 costal grooves. The hands and feet are narrow and have poorly-
developed, poorly-differentiated digits that are fused and lack subdigital pads (Figure 5-
4D, E). The free tips of digits III on the hands and III and IV on the feet are pointed, and
digits I, II and IV on the hands and I, II, and V on the feet are very short and essentially
completely fused, being demarcated by shallow grooves on the dorsal side of the feet.
The relative length of the digits is I<IV<II<III on the hands and V<I<II<IV<III on the feet.
The tail is slightly shorter than the body (TL/SVL=0.91), with a slight basal constriction
274
most apparent on the ventral side, and is slightly compressed laterally (tail depth 1.17
times tail width at level of basal constriction).
Measurements of holotype (in mm). SVL 26.9; AG 15.2; TW 3.6; HL 4.8; HW
3.9; TL 24.5; HLL 5.3; FLL 4.3; CLL 9.6; HFL 1.7; HFW 1.2; NL 0.5; eye length 1.6; eye
width 1.2; interorbital distance 1.4; anterior rim of orbit to snout 1.1; distance separating
internal nares 0.8; distance separating external nares 1.8; snout projection beyond
mandible 0.6; tip of snout to axilla 7.7; distance from axilla to groin 15.2; snout to
anterior edge of vent 24.9; tail depth at basal constriction 2.8; tail width at basal
constriction 2.4.
Coloration of holotype. Dorsal surfaces of head, body, and tail medium grayish
brown, with profuse pale chromatophores laterally, becoming less abundant
dorsolaterally. The head has some pale mottling on the top of the snout, and two
irregular lines of pale chromatophores extending from the lateral region above the
forelimbs onto the posterior portion of the head and parotoid glands. There is a very
thin, pale middorsal stripe, with a herringbone pattern with lines extending from the
middorsal stripe posteriorly. There is an indistinct dark dorsolateral stripe starting about
one-third the way down the trunk and extending onto the proximal one-third of the tail.
Ventral surface of head, body, and tail cream, mottled with dark gray chromatophores,
becoming somewhat more profuse toward the distal end of the tail.
Etymology. The specific name ―tomamorum‖ means ―belonging to the Tomams.‖
Tomams are the highest level of deities recognized in the belief system of the
indigenous Tolupan of Honduras, of which there are four: Tomam Pones Popawai
(Grandfather Tomam), his wife Tomam Pones Namawai (mother of all that exists), and
275
their children Tomam the Elder and Tomam the Younger (Chapman 1992). This name
is given in recognition that the Tolupan are the traditional inhabitants of this area and
that this new species is known only from the Cordillera Nombre de Dios, or ―Name of
God Mountains,‖ a name which, ironically, was given by 15th century Spanish explorers.
Distribution and Natural History. The single known specimen was collected
during the daytime from leaf litter packed onto a rock ledge alongside a small creek at
about 1,550 m elevation in the Lower Montane Wet Forest formation (Townsend et al.
2010a). This species is presumably endemic to the vicinity of the type locality, and is
sympatric with a congener, N. sp. A, and three other plethodontids: Bolitoglossa dofleini,
Bolitoglossa cf. porrasorum, and Oedipina gephyra.
Conservation Status. Critically Endangered B1ab(iii)+2ab(iii).
A New Species from the Sierra de Agalta
Nototriton picucha Townsend, Medina-Flores, Murillo, and Austin 2011a
Figure 5-5
Nototriton sp. inq. 2: Chapter 3.
Holotype: USNM 578299 (Figures 5-5A, 5-5B), a female, from the northwestern
slope of Cerro La Picucha (14.9733°N, 85.9279°W), 1,890 m, Parque Nacional Sierra
de Agalta, Departamento de Olancho, Honduras, collected 17 July 2010 by M. Medina
F., J. L. Murillo, I. Zúniga, and J. M. Soto. Original field number JHT 3192; Genbank
accession numbers: JN377388 (16S), JN377392 (cyt b), JN377404 (COI).
Paratype: USNM 578298 (Figure 5-5C), same collection data as holotype, except
from 1,920 m elevation. Genbank accession numbers: JN377389 (16S), JN377393 (cyt
b), JN377405 (COI).
276
Diagnosis. A member of the genus Nototriton (SL=27.9 mm) possessing 13 costal
grooves (>16 costal grooves in Oedipina), hands and feet longer than broad (hands and
feet broader than long in Bolitoglossa), and small nares (0.007 NL/SL; 0.017–0.029
NL/SL in Cryptotriton and Dendrotriton). Placement of the new species in the Nototriton
barbouri species group is supported by phylogenetic analysis of the mitochondrial
genes 16S and cyt b (Figure 5-2). In addition to molecular characteristics, the new
species is distinguished from other members of the N. barbouri group by having a
broader head (HW/SL≥0.140), and is further differentiated from N. barbouri, N. brodiei,
N. lignicola, and N. stuarti by having relatively longer front limbs (FLL/SL≥0.179, versus
0.142–0.174 in N. barbouri, 0.148–0.151 in N. brodiei, 0.137–0.160 in N. lignicola, and
0.172 in N. stuarti) and relatively longer hind limbs (HLL/SL≥0.204–0.218, versus
0.153–0.200 in N. barbouri, 0.166–0.180 in N. brodiei, 0.158–0.181 in N. lignicola, and
0.178 in N. stuarti), and from N. limnospectator by having narrower hind feet
(HFW/SL≤0.043, versus 0.048–0.061) and larger nares (NL/SL≥0.007, versus 0.003).
Nototriton tomamorum can be distinguished from N. picucha by having enlarged nares
(NL/SL=0.018, versus 0.007–0.008 in N. picucha), syndactylous feet lacking subdigital
pads (toes well differentiated with subdigital pads in N. picucha), and fewer maxillary
and vomerine teeth (MT=26 and VT=11, versus 41 and 16–19 and N. picucha).
Nototriton saslaya, a member of the N. picadoi group, is known from a single highland
forest site in northern Nicaragua, and differs from the new species in having fewer
maxillary teeth (17–23, versus 41 in N. picucha) and vomerines (3–11, versus 16–19 in
N. picucha), relatively longer front limbs (FLL/SL 0.194–0.210, versus 0.179–0.191 in N.
picucha) and relatively wider hind feet (HFW/SL 0.075–0.091, versus 0.042–0.043 in N.
277
Figure 5-5. Nototriton picucha. A) Dorsolateral and ventrolateral views of the holotype of
N. picucha (USNM 578299), standard length 27.9 mm (photo © J.H. Townsend). B) X-ray radiograph of the holotype of N. picucha (photo © J.H. Townsend). C) Paratype of N. picucha (USNM 578298) in life, standard length 25.7 mm (photo © Melissa Medina-Flores).
picucha). Comparative morphological data for Chortís Highland Nototriton are
summarized in Table 5-4.
Description of holotype. A relatively small female (SL=27.9 mm, total
length=59.8 mm) with a slender body and reduced limbs. The head is rounded, slightly
broader than the body; nostrils are relatively small (NL/SL=0.007), and the snout is
acutely rounded and of moderate length. The nasolabial groove is apparent, but
nasolabial protuberances are not well developed and barely visible. The eyes are
relatively large and protuberant, and the parotoid glands are apparent, but relatively flat
and not well defined. There are 41 maxillary teeth, 2 slightly enlarged premaxillary teeth
278
in line with the maxillaries, and 19 vomerine teeth. The limbs are short (CLL/SL=0.38),
with the adpressed limbs being separated by approximately 3.5 costal grooves. The
hands and feet are narrow with well-developed digits that bear subdigital pads. The
relative length of the digits is I<IV<II<III on the hands and I<V<II<IV<III on the feet. The
tail is slightly longer than the body (TL/SL=1.14), with a slight basal constriction that is
only apparent on the ventral side, and is slightly compressed laterally (tail depth 1.08
times tail width at level of basal constriction).
Measurements of holotype (in mm). SL 27.9; AG 16.8; TW 3.9; HL 5.5; HW 3.4;
TL 31.9; HLL 5.7; FLL 5.0; CLL 10.7; FFL 1.4; FFW 0.8; HFL 1.7; HFW 1.2; NL 0.2; eye
length 1.7; eye width 0.8; interorbital distance 1.2; anterior rim of orbit to snout 1.1;
distance separating internal nares 1.1; distance separating external nares 1.5; snout
projection beyond mandible 0.4; tip of snout to axilla 7.3; snout to anterior edge of vent
25.3; tail depth at basal constriction 2.6; tail width at basal constriction 2.4.
Coloration of holotype. Dorsal surfaces of head, body, and tail with medium to
dark reddish brown ground color; abundant pale yellowish-brown blotching , present on
dorsal surface of snout and eyes, between eyes, and on paratoid glands, becoming
more profuse posteriorly until becoming solid and fully encircling the distal one-third of
tail. Pale yellowish-brown herringbone pattern on dorsal surface of body, with pale
yellowish brown dorsolateral stripes arising anterior to insertion of hind limbs and
continuing onto tail, where pattern grades into solid yellowish brown towards tip of tail;
lower edge of dorsolateral stripes bordered by solid dark brown coloration. Irregular pale
chromatophores scattered on anterior dorsal surface of head and lateral surfaces of
body. Dorsal and ventral coloration sharply demarcated laterally by an irregular line of
279
pale chromatophores separating dark reddish-brown dorsal and dorsolateral ground
color from dark blackish gray ventral ground color; venter with some sparse whitish gray
spotting primarily on the chin and around ventral midline; yellowish brown coloration
extends down from the dorsolateral surfaces around the basal portion of the tail to
surround the vent with yellowish brown mottling. Proximal one-half to two-thirds of
forelimbs and two-thirds to three-quarters of hind limbs mottled yellowish brown dorsally
and ventrally. Ventral surface of head, body, and tail cream, mottled with dark gray
chromatophores, becoming somewhat more profuse toward the distal end of the tail.
See Figure 5-4b for color photographs of the dorsal and ventral surfaces of the
holotype.
Variation in paratype. The female paratype (Figure 5-5c; USNM 578298,
SL=25.7, tail missing) agrees almost completely with the holotype in most
characteristics and standardized ratios, with the only notable differences being more
premaxillaries (6, same size as and in line with the maxillaries), fewer vomerines (16),
and in having a limb interval of approximately 4.5. Coloration is also similar to that seen
in the holotype.
Osteology. Based on examination of digital radiographs for both the holotype
(Figure 5-5b) and paratype, Nototriton picucha is a typical member of the genus (Wake
& Elias 1983) possessing a single cervical vertebra, 14 trunk vertebrae (the anterior 13
of which bear ribs), 2 caudosacral vertebrae; a complete skull roof formed through
contact of the parietal bones; frontal processes of premaxilla fused at point of origin and
separate immediately dorsoposterior to origin; septomaxillary bones absent; preorbital
vomerine processes well-developed into elongate arches bearing a single row of
280
numerous teeth; columella absent; no tarsal spur evident; phalangeal formulae 1-2-3-2
and 1-2-3-3-2; penultimate phalanges reduced, exceeded in length by terminal
phalanges on digits II, III, and IV of the forelimbs and digits II, III, IV, and V of hind
limbs; terminal phalanges tapered at distal tip, or slightly expanded in digit III of
forelimbs and digit III of the hindlimbs; mesopodial elements not mineralized.
Etymology. The specific epithet references the type locality and tallest mountain
in the Sierra de Agalta, Cerro La Picucha, whose high elevation elfin forests make it one
of the natural wonders of Honduras. The type series was collected on the northwestern
slope of Cerro La Picucha, above the highest basecamp used to access the summit.
Natural history. The type specimens of Nototriton picucha were collected at 1,890
and 1,920 meters in the Lower Montane Wet Forest formation on the north-northwest
slope of Cerro La Picucha (2,354 m) in the Sierra de Agalta. The holotype was collected
near the highest base camp used for accessing the elfin forest atop Cerro La Picucha,
and the paratype was found farther up the ridgeline trail to the peak before the transition
to elfin forest. Both specimens were collected while active underneath leaf litter on the
ground between 21:00 and 00:00 hours on a rainy night. Nototriton picucha is sympatric
with another endemic plethodontid salamander, Bolitoglossa longissima, which was also
found along the same trail.
Conservation Status. Critically Endangered B1ab(iii).
Remarks. Parque Nacional Sierra de Agalta contains the easternmost fragment of
cloud forest (Lower Montane Wet Forest formation) in Nuclear Central America, being
located in Dept. Olancho approximately 180 km to the northeast of Tegucigalpa,
Honduras. The park was established in 1987 to protect an area of approximately of
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73,924 ha under the management of the National Institute of Conservation and Forest
Development, Protected Areas and Wildlife (ICF). There are 75 species of amphibians
and reptiles recorded from Parque Nacional Sierra de Agalta (Castañeda 2006;
McCranie & Cruz 2010); however to date only three species (Bolitoglossa longissima,
Nototriton picucha, and Omoadiphas cannula) are considered to have geographic
distributions completely restricted to this mountain range.
Restriction of the taxon Nototriton barbouri (Schmidt, 1936)
The precise type locality of Nototriton barbouri is a matter of some uncertainty.
The taxon was described by Schmidt (1936: 43) based on material collected by R.E.
Stadelman from ―Portillo Grande, Yoro, Honduras.‖ The type series was collected ―from
bromeliads, and from altitudes between 5000 [=1,524 m] feet (the type), and 6000
[=1,828 m] feet.‖ While there are numerous communities in Yoro named ―El Portillo‖ and
at least one ―Cerro Portillo Grande‖ (maximum elevation approximately 1,020 m), the
only locality with that name and local access to elevations above 1,800 m is El Portillo
(15.095323°N, 87.343902°W), a small community sitting at around 1,300 m elevation on
the northern side of Montaña Macuzal (maximum elevation approximately 1,945 m;
Chapter 3, Figures 3-7G, 3-7H), an isolated karstic mountain supporting a small
fragment of broadleaf cloud forest on its summit. McCranie and Wilson (1995: 137)
suggested that Bolitoglossa porrasorum collected from Portillo Grande by Stadelman
were ―probably from Montaña Macuzal south of this town,‖ and I agree that Montaña
Macuzal indeed represents the only known suitable habitat for cloud forest salamanders
in the vicinity of El Portillo, and, therefore, consider it to be the type locality of N.
barbouri.
282
A single specimen (AMNH 54949) from a locality near Lago de Yojoa (―El Volcán,‖
north slopes of Cerro Azul Meámbar, 860 m elevation [McCranie & Wilson 2002:576]) is
also assigned to this taxon. Given the confirmation that populations of Nototriton from
nearby Cerro Azul Meámbar represent N. limnospectator (Townsend et al. 2011b;
Chapter 4), I consider this single specimen to be representative of N. limnospectator,
and not a distjunct and lower elevation locality for N. barbouri sensu stricto.
Nototriton barbouri (Schmidt 1936)
Oedipus barbouri Schmidt 1936: 43.
Holotype. MCZ 21247, an adult male from Portillo Grande, 1,524 m elevation,
Departamento de Yoro, Honduras; collected 9 May 1934 by R.E. Stadelman.
Paratypes. All females from the vicinity of the holotype, 1,524–1,828 m elevation;
MCZ 21248–50, FMNH 21866–67.
Genetype. UF 156538, an adult female from Montaña Macuzal (15.079455°N,
87.352985° W), 1,760 m elevation, above El Panal to the west of Yorito, Departamento
de Yoro, Honduras; collected 9 April 2008, by J.M. Butler, L. Ketzler, J. Slapcinsky,
N.M. Stewart, J.H. Townsend, and L.D. Wilson; original field number JHT 2420;
GenBank accession numbers GU971733 (16S), GU971734 (cyt b), JN377401 (COI).
Referred specimens. 15; ANSP 28981–85, 28200, Montaña Macuzal S of Pueblo
Viejo; USNM 339700–08, from the eastern slope of Pico Pijol (15.175°N, 87.558°W),
1,920 m elevation, Parque Nacional Pico Pijol, Departamento de Yoro, Honduras.
Distribution and natural history. I consider this taxon to be restricted to the
Sierra de Sulaco in southwestern Departamento de Yoro, where it is known to occur in
the vicinity of the type locality in an unprotected patch of remant cloud forest on the top
of Montaña Macuzal (maximum elevation approximately 1,945 m) at the eastern
283
Figure 5-6. Nototriton barbouri sensu stricto. A and B) Genetype of Nototriton barbouri
sensu stricto (UF 156538), from Montaña Macuzal, Departamento de Yoro, Honduras. Photos © J.H. Townsend.
terminus of the range and in the cloud forests of PN Pico Pijol (maximum elevation
approximately 2,282 m) at the western end of the range. Nototriton barbouri is known to
occur in the Lower Montane Wet Forest formation from 1,520–1,920 m elevation.
Conservation status. Endangered B1ab(iii).
284
Description of unassigned populations from the Cordillera Nombre de Dios
Restriction of the taxon Nototriton barbouri to populations inhabiting the highlands
of southern Yoro (Montaña de Pijol and Montaña de Macuzal) leaves two allopatric
populations from the Cordillera Nombre de Dios without assignment to an existing
taxon. With no referable name present in the synonymy of N. barbouri for these
populations, putatively endemic to highland forests at opposite ends of the Cordillera
Nombre de Dios in Parque Nacional Pico Bonito and Refugio de Vida Silvestre Texiguat
(Figure 5-1), I herein describe these two cryptic species as new taxa. Together, they
form a clade with N. brodiei, a species residing in the Sierra de Omoa and Cordillera de
Merendón in northwestern Honduras and adjacent Guatemala (Figure 5-1).
Nototriton sp. A, sp. nov.
Nototriton barbouri: McCranie 1996a: 28.
Holotype. USNM 497552, an adult female from the south slope of Cerro Búfalo
(15.66°N, 86.79°W), 1,540 m elevation, Parque Nacional Pico Bonito, Departamento de
Atlántida, Honduras; collected 30 May 1996 by S. Gotte and J.R. McCranie; original
field number LDW 10724; GenBank accession number AF199137 (cyt b).
Paratype. USNM 339712, an adult female from Quebrada de Oro (15.64°N,
86.80°W), 1,210 m elevation, Parque Nacional Pico Bonito, Departamento de Atlántida,
Honduras; collected 13 February 1995 by J.R. McCranie & J.C. Rindfleish; original field
number LDW 10378; GenBank accession numbers AF199201 (16S), AF199136 (cyt b).
Measurements of holotype (in mm). SL 33.7; AG 19.5; TW 4.9; HL 6.0; HW 4.1;
TL 39.4; HLL 6.4; FLL 6.0; CLL 12.4; FFW 1.0; HFW 1.9; NL 0.3; eye length 1.7; eye
width 1.2; interorbital distance 1.3; anterior rim of orbit to snout 1.5; distance separating
internal nares 1.1; distance separating external nares 1.6.
285
Distribution and natural history. This species is known only from the vicinity of
Cerro Búfalo in Parque Nacional Pico Bonito, Honduras, 1,210–1,540 m elevation.
Conservation status. Critically Endangered B1ab(iii).
Nototriton sp. B, sp. nov.
Holotype. USNM 578300, an adult male from Cerro El Chino above La Liberación
(15.525394°N, 87.278672°W), 1,420 m elevation, Refugio de Vida Silvestre Texiguat,
Departamento de Atlántida, Honduras; collected 19 June 2010 by E. Aguilar, B.K.
Atkinson, C.A. Cerrato M., A. Contreras, A. Portillo, J.H. Townsend, and L.D. Wilson;
original field number JHT 3159; GenBank accession numbers JN377387 (16S),
JN377391 (cyt b), JN377403 (COI).
Paratypes. USNM 339709–10, about 2.5 km (airline) NNE of La Fortuna, Refugio
de Vida Silvestre Texiguat, Departamento de Yoro, 1,690 m elevation; USNM 339711,
about 2.5 km (airline) NNE of La Fortuna, Refugio de Vida Silvestre Texiguat,
Departamento de Yoro, 1,800 m elevation; USNM 509333, about 2.5 km (airline) NNE
of La Fortuna, Refugio de Vida Silvestre Texiguat, Departamento de Yoro, 1,600 m
elevation.
Measurements of holotype (in mm). SL 31.9; AG 19.1; TW 3.8; HL 6.9; HW 4.2;
TL 41.0; HLL 7.2; FLL 6.4; CLL 13.6; FFW 1.1; HFW 1.5; NL 0.2; eye length 1.8; eye
width 0.9; interorbital distance 1.6; anterior rim of orbit to snout 1.5; distance separating
internal nares 1.4; distance separating external nares 1.8; tip of snout to axilla 9.6.
Distribution and natural history. This species is known only from highland forest
within Refugio de Vida Silvestre Texíguat, 1,420–1,800 m. The holotype was collected
as it crawled out of an arboreal bromeliad approximately 1.5 m above the ground on a
rainy night.
286
Figure 5-7. Nototriton sp. B. A) Holotype of Nototriton sp. B (USNM 578300) in life B) X-
ray radiograph of the holotype of Nototriton sp. B. C) Immediate vicinity of the type locality of Nototriton sp. B, Cerro El Chino, 1,420 m, above La Liberación in Refugio de Vida Silvestre Texíguat. Photos © J.H. Townsend.
Conservation status. Critically Endangered B1ab(iii)+2ab(iii).
Review of the Remaining Species of Nototriton from the Chortís Highlands
The additions of Nototriton picucha, N. tomamorum, N. sp. A, N. sp. B, and N. sp.
C (identified in Chapter 4 and being described elsewhere) brings the total number of
species in the genus to 18, with 10 of these species being endemic to the Chortís
287
Highlands. This is a more than 27% increase in the number of species in this cryptozoic
genus, and a nearly two-fold increase in the number of species known from the Chortís
Highlands.
Nototriton brodiei Campbell & Smith 1998
Holotype. UTA A-50000, an adult female from Cerro Pozo de Agua, 1,125 m
elevation, Sierra de Caral, Municipio de Morales, Izabal, Guatemala.
Distribution and Natural History. Premontane forests of the Cordillera de
Merendón along the Guatemala/Honduras border, from 875–1,140 m elevation. This
species is known from the vicinity of the type locality in the Sierra de Caral, Guatemala,
and the northwestern slope of the Sierra de Omoa, Honduras (Campbell & Smith 1998;
Kolby et al. 2009).
Conservation Status. Critically Endangered B1ab(iii) (Acevedo et al. 2008); the
discovery of this species in a relatively well-protected area of Honduras should
necessitate re-evaluation of this taxon’s conservation status.
Remarks. This species was recently reported from the Sierra de Omoa in
Honduras (Kolby et al. 2009).
Referred Specimens. GUATEMALA: IZABAL: Sierra de Caral, UTA A-50001,
UTA A-51490. HONDURAS: CORTÉS: Parque Nacional Cusuco, MVZ 258034–36.
Nototriton lignicola McCranie & Wilson 1997
Nototriton ―barbouri‖: Espinal et al. 2000: 102.
Holotype. USNM 497539, an adult male from above the Monte Escondido, 1,780
m elevation, Cerro de Enmedio (15°06'N, 86°44'W), Parque Nacional La Muralla,
Olancho, Honduras.
288
Figure 5-8. Nototriton lignicola. A and B) N. lignicola (UF 156543), from Cataguana,
2,020 m, Parque Nacional Montaña de Yoro, Departamento de Francisco Morazán, Honduras. C) Cloud forest habitat at Cataguana. D) Juvenile N. lignicola (UF 156543) from Cataguana, 1,820 m, Parque Nacional Montaña de Yoro, Departamento de Francisco Morazán, Honduras. Photos © J.H. Townsend.
Distribution and Natural History. Lower Montane Wet Forest of northern
Departamento de Francisco Morazán and northwestern Departamento de Olancho,
Honduras, from 1,780–2,020 m elevation.
Conservation Status. Critically Endangered B1ab(iii).
Referred Specimens. HONDURAS: FRANCISCO MORAZÁN: Cataguana, UF
156542–44, OLANCHO: Cerro de Enmedio, USNM 497539–51, 509335 (cleared and
stained).
289
Figure 5-9. A) Nototriton limnospectator (UF 156539), from above Río Varsovia, 1,640
m, Parque Nacional Cerro Azul Meámbar, Departamento de Comayagua, Honduras (Photo © J.H. Townsend). B) Juvenile N. limnospectator (IRL 035) from Cataguana, from above Los Pinos, 900 m, Parque Nacional Cerro Azul Meámbar, Departamento de Cortés, Honduras (Photo © I. Luque).
Nototriton limnospectator McCranie, Wilson, & Polisar 1998
Holotype. UF 98460, an adult female from southwest of San Luís de los Planes
(14°56'N, 88°08'W), 1910 m elevation, northwestern side of Montaña de Santa Bárbara,
Parque Nacional Montaña de Santa Bárbara, Santa Bárbara, Honduras.
Distribution and Natural History. This species is found in Premontane Wet
Forest, Lower Montane Wet Forest, and Montane Wet Forest on both sides of Lago de
Yojoa in central Honduras.
Conservation Status. Endangered B1ab(iii).
290
Referred Specimens. COMAYAGUA: UF 156539–41, IRL 035. CORTÉS: El
Volcán, AMNH 54949. SANTA BARBARA: El Ocotillo, MVZ 225866, USNM 509334
(CS); Montaña de Santa Bárbara, SW of San Luís de Los Planes, UF 98460–66.
Nototriton stuarti Wake & Campbell 2000
Holotype. UTA A-33686, an adult male from 11.6 road km west-southwest of
Puerto Santo Tomás, 744 m elevation, Montañas del Mico (15°38'N, 88°40'W), Izabal,
Guatemala.
Distribution and Natural History. This species is known only from a single
specimen from premontane forest in the Montañas del Mico in eastern Guatemala.
Conservation Status. Data Deficient (IUCN 2011).
291
Table 5-1. Samples used in sequence divergence and phylogenetic analyses, with GenBank accession and museum voucher numbers; CR = Costa Rica, GT = Guatemala, HN = Honduras, NI = Nicaragua.
Taxon Locality GenBank voucher
GenBank Accession Numbers
16S cytb COI
N. barbouri HN: Yoro: Macuzal UF156538 GU971733 GU971734 JN377401
N. brodiei (1) GT: Izabal: Sierra de Caral UTA A-51490 AF199202 AF199139 JN377402
N. brodiei (2) HN: Cortés: Cusuco MVZ258035 JN377384 – –
N. lignicola (1) HN: Olancho: La Muralla USNM497540 AF199204 AF199141 –
N. lignicola (2) HN: Olancho: La Muralla USNM497550 – AF199142 –
N. lignicola (3) HN: Francisco Morazán: Cataguana UF156543 GU971735 GU971736 JN377408
N. limnospectator (1) HN: Santa Bárbara: El Ocotillo MVZ225866 – AF199143 –
N. limnospectator (2) HN: Santa Bárbara: San Luís Planes MVZ263852 JN377383 – –
N. limnospectator (3) HN: Comayagua: Azul Meámbar UF156539 GU971737 GU971738 JN377397
N. limnospectator (4) HN: Comayagua: Azul Meámbar UF156540 GU971739 GU971740 JN377398
N. limnospectator (5) HN: Comayagua: Azul Meámbar UF156541 JN377386 JN377396 JN377399
N. limnospectator (6) HN: Cortés: Azul Meámbar UF-IRL035 JN377385 JN377395 JN377400
N. picucha sp. nov. (1) HN: Olancho: Sierra de Agalta USNM578299 JN377388 JN377392 JN377404
N. picucha sp. nov. (2) HN: Olancho: Sierra de Agalta USNM578298 JN377389 JN377393 JN377405
N. sp. A (1) HN: Atlántida: Quebrada de Oro USNM339712 AF199201 AF199136 –
N. sp. A (2) HN: Atlántida: Cerro Búfalo USNM497552 – AF199137 –
N. sp. B (1) HN: Atlántida: Texíguat USNM578300 JN377387 JN377391 JN377403
N. sp. B (2) HN: Yoro: Texíguat USNM509333 – AF199138 –
N. tomamorum HN: Yoro: Texíguat UF155377 GU971731 GU971732 JN377407
N. saslaya (1) NI: Atlantíco Norte: Saslaya MVZ230241 GU981761 – –
N. saslaya (2) NI: Atlantíco Norte: Saslaya UF156352 JN377390 JN377394 JN377406
292
Table 5-2. Models of nucleotide substitution chosen for phylogenetic analyses of Chortís Highland taxa using Akaike Information Criterion values.
Partition Model AIC lnL
16S GTR+G 2335.9224 -1126.9612 cyt b (1st) HKY+G 1380.1242 -651.0621 cyt b (2nd) HKY+G 1011.5928 -466.7964 cyt b (3rd) GTR+G 2527.2855 -1220.6427 COI (1st) GTR+G 2603.4728 -1270.7364 COI (2nd) K80+I 1010.9648 -481.4824 COI (3rd) HKY 641.4734 -294.7367
Table 5-3. Within and between species sequence divergence (uncorrected p-distance) for Chortís Highland moss salamanders.
Intraspecific Interspecific
Taxon 16S cyt b COI 16S cyt b COI
N. barbouri – – – 0.012–
0.055
0.071–
0.123
0.080–
0.121
N. sp. A – 0.000 – 0.014–
0.059
0.052–
0.142
–
N. sp. B – 0.014 – 0.018–
0.057
0.052–
0.144
0.061–
0.126
N. brodiei 0.000 – – 0.014–
0.061
0.057–
0.123
0.061–
0.133
N. lignicola 0.002 0.005 – 0.023–
0.064
0.082–
0.120
0.105–
0.139
N. limnospectator 0.000–
0.006
0.000–
0.019
0.002–
0.003
0.012–
0.059
0.071–
0.147
0.080–
0.126
N. picucha 0.000 0.008 0.002 0.012–
0.049
0.093–
0.123
0.085–
0.121
N. saslaya 0.006 – – 0.047–
0.064
0.104–
0.147
0.107–
0.136
N. tomamorum – – – 0.035–
0.057
0.095–
0.131
0.115–
0.139
293
Table 5-4. Morphological and morphometric comparison of species of Nototriton; see Material and Methods section for explanation of abbreviations; SVL is given in mm. Comparative morphological data for species other than N. picucha are from Campbell & Smith (1998), McCranie et al. (1998), Wake & Campbell (2000), Köhler (2002), McCranie & Wilson (2002), and Townsend et al. (2010).
Taxon SL HW/SL TL/SL HLL/SL FLL/SL HFW/SL NL/SL MT VT
N. barbouri 30.2–39.9
0.104–0.132
1.031–1.398
0.153–0.200
0.142–0.174
0.037–0.060
0.005–0.011
41–54 12–23
N. brodiei 33.2–34.5
0.120 1.420–1.440
0.166–0.180
0.148–0.151
0.040–0.060
0.004–0.005
60–62 23–24
N. lignicola 28.3–33.9
0.103–0.118
0.840–1.059
0.158–0.181
0.137–0.160
0.029–0.040
0.006–0.009
46–54 16–24
N. limnospectator 33.0–38.2
0.095–0.118
1.027–1.297
0.164–0.211
0.156–0.183
0.048–0.061
0.003 42–55 16–26
N. picucha 25.7–27.9
0.140–0.148
1.143 0.204–0.218
0.179–0.191
0.042–0.043
0.007–0.008
41 16–19
N. saslaya 28.1–34.6
0.133–0.155
0.883–1.255
0.217–0.244
0.194–0.210
0.075–0.091
0.002–0.003
17–22 3–11
N. stuarti 32.6 0.138 1.264 0.178 0.172 0.049 0.012 36 20
N. tomamorum 26.9 0.145 0.911 0.197 0.160 0.037 0.018 26 11
294
CHAPTER 6 INTEGRATING RESEARCH, EDUCATION, AND OUTREACH IN SUPPORT OF
CONSERVATION IN THE CHORTÍS HIGHLANDS
This dissertation represents the first step in developing an accurate picture of
evolutionary diversification and phylogenetic distinctiveness for the Chortís Block. The
region’s amphibian fauna, already known to have a high degree of endemism and to be
facing a comparably high risk of extinction, is herein demonstrated to be greatly
underestimated in terms of taxonomic diversity. Throughout my research in Honduras
and Nicaragua I encountered a series of significant challenges to the continued
documentation of Chortís Block biodiversity, and more importantly to the conservation of
the ecosystems that support Chortís Block biodiversity.
First, outside of the herpetofaunal research that has taken place since 1967
(Townsend & Wilson 2010), there has been no concerted effort to inventory and
document other major biotic components (e.g. mammals, birds, plants) using modern,
molecular-based approaches (but see Matamoros et al. [2009] for details of efforts in
freshwater ichthyology). The majority of endemic herpetofaunal species in the Chortís
Block are found in the highlands, owing to the extreme ecophysiographic heterogeneity
in its 50+ isolated highland forests and interceding dry valleys. Exploration of these
geographically limited, highly threatened mountain-top forests continues apace among
the best known groups, as evidenced by the continued regular discovery of new
amphibians (Chapter 4) and reptiles (Chapter 3). However, integrative taxonomy
inventories are desperately needed for other taxa.
Second, opportunities for recruitment, education, and practical training of aspiring
Honduran systematists and conservation biologists, those representing the next
generation of ―front-line warriors‖ in the effort to document and conserve their national
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biodiversity resources, are increasingly rare. The countries of the Chortís Block are
among the poorest and most underdeveloped in the Americas, and opportunities for
higher education in systematics and related fields are limited to a few small, under-
resourced programs in public universities.
Finally, regional awareness of the unique nature of the endemic Chortís Block
biota is low. To date, little concerted outreach has been targeted at the largest group of
stakeholders in regional conservation: the public. My experience has been that
Hondurans generally are interested in and supportive of conservation of their national
environmental patrimony. However, lacking access to information about endemic
biodiversity limits the ability of individuals and groups to lead, or even support,
conservation efforts.
Below I outline my vision for promoting biodiversity conservation through
education, training, and outreach opportunities generated through a strategic program
to inventory the biodiversity of the Chortís Block. Given that it contains the majority of
the endemism-rich Chortís Highlands and that geopolitical considerations warrant an
initial focus at the national level, I am presenting this strategy as I would see it
implemented in Honduras.
Taxonomic Inventories in Promotion of Education and Extension
As I became aware of these three principal obstacles to biodiversity conservation
in the Chortís Block, I sought avenues to address these issues through my own
research initiatives. Biodiversity inventory and systematics research address the first
challenge, cataloging the biological diversity of the region; however activities associated
with carrying out taxonomic inventory work also offer an excellent opportunity to provide
education and training to multiple groups. My experience in Honduras has
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demonstrated that a virtually untapped talent pool of university students,
parataxonomists, park guards, and conservation practitioners are available for
participation in all levels of inventory-related research.
Taxonomic inventory projects also present frequent opportunities for scientists to
engage with the public across a variety of platforms. In my case, I have had frequent
opportunities to engage the Honduran public through the media, promoting local and
regional biodiversity awareness and endemic species conservation through newspaper
articles and television interviews (Figure 6-1). I was able to provide both planned and
impromptu presentations to municipal governmental leaders, community groups,
schools, and residents in rural areas, often within the buffer zones of the highland
protected areas where I was working (Figure 6-2). Activities such as these should be
promoted as part of any truly ―integrative‖ taxonomic inventory project, and field-based
systematists have the unique opportunity to simultaneously carry out research, engage
the public, and contribute to the development of Honduran capacity in systematic
biology.
As evidenced in this dissertation, Honduras is a country of remarkable
herpetofaunal diversity, having the highest degree of amphibian endemism (i.e.,
percentage of the country’s amphibian species that are found only within its’ borders) of
all Central American countries: 36.2%, compared to 27.1% for Guatemala and 26.6%
for Costa Rica (Wilson & Johnson 2010). With the discovery of more than 30 potentially
new species (Chapter 4), it appears that this high degree of endemism is actually
greatly underestimated, and numerous undiscovered species undoubtedly await
discovery across Honduras.
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Figure 6-1. Print media coverage of the discovery of new endemic species during 2008
and 2009.
As I have emphasized throughout this dissertation, much of the diversity is
attributed to the high number of isolated highland forests that are home to suites of
endemic species. Across Honduras, more than a dozen of these cloud forest ―islands‖
remain virtually unexplored biologically, and likely conceal veritable treasure-troves of
new species from a variety of taxonomic groups. As a consequence of the unique
biogeography of the Chortís Block, Honduras remains a largely unrealized center for
biodiversity in the Americas, overshadowed by more thoroughly studied Central
American countries.
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Opportunities for Training and Education
Currently, the School of Biology at the National Autonomous University of
Honduras (Universidad Nacional Autónoma de Honduras, or UNAH) offers only a single
degree, the Licenciatura en Biología, a degree more comprehensive than a traditional
Bachelor of Science degree but lacking the professional preparation and opportunities
for research typical of a Master of Science program (in 2011–12 UNAH has plans to
launch an Master of Science in Tropical Botany). Biology majors complete a capstone
research design course (BI-025 Seminario de Investigación) as their final class, after
which they must complete an 800-hour professional practicum which can take on a wide
variety of forms. The primary focus of BI-025 is for students to develop a research
proposal, and some highly-motivated students develop proposals to carry out under
direction of a supervising scientist in fulfillment of their 800-hour requirement. Despite
potential synergies between the requirements of BI-025 and the professional practicum,
UNAH faculty do not typically encourage students to attempt linking the two and it is
exceedingly challenging for students to propose and find support for independent, or
even faculty-directed, research projects.
As a result of my time spent in Honduras, I have had the opportunity to work
closely with numerous UNAH biology students, relying on them in innumerable ways
while promoting their professional development through participation in remote
biodiversity surveys. In further support of a few dedicated students, I served in the
supervisory role for their final-year professional practica, assisting in developing
proposals for and carrying out rapid herpetological inventories that, among other things,
led directly to the discovery of a new species of salamander (Townsend et al. 2011a). I
see providing opportunities of this nature for UNAH students to gain practical
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experience is critical to strengthening the national biological community, and the
promotion of UNAH student participation also serves to enhance the Honduran public’s
perception of biodiversity conservation and its practitioners. The excitement and pursuit
of scientific discovery, centered on the collection, identification, and further study of new
and poorly-known species, was and will continue to be the central theme to my efforts to
give students the opportunity to be fully involved in leading-edge systematic research
with real-world applications in the realm of Honduran biodiversity exploration and
conservation.
Pilot Project: Parque Nacional Montaña de Yoro
One of my principal goals in taking an approach that combines biodiversity
inventory work and integrative systematics is to refine our understanding of the patterns
of diversification exhibited in the Chortís Highlands. My initiation of inventory work in
Parque Nacional Montaña de Yoro (Chapter 3) provided an opportunity to do so, and at
the same time develop and practice the educational and outreach-related elements
described above. Parque Nacional Montaña de Yoro was virtually unknown to biologists
prior to my initial trip there in 2006. As a result of limited baseline biodiversity data, this
large area (~50km2) of cloud forest was among the lowest priorities for national level
conservation planning and at one point was recommended for a reduction in its
protected area status (Vreugdenhil et al. 2002; COHECO 2003). During a single rapid
inventory in 2006, we found new species of salamander (Townsend et al. 2009a), anole
lizard (Townsend & Wilson 2009), and spikethumb treefrog (Plectrohyla cf.
guatemalensis; Chapter 4), with all three qualify as Critically Endangered based on
IUCN Red List criteria due to severe threat to their limited distributions. In contrast, we
also found two species of salamanders previously considered to be endemic to Parque
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Figure 6-2. Examples of public outreach and dissemination of results from taxonomic inventories. A) Television interview about the endemic biodiversity in Honduras (Photo © James Austin). B) Presenting the results of work in La Liberación de Texíguat to the Alcalde (mayor) of the municipality that receives its water from the reserve (Photo © Ileana Luque). C) Community members attending a public presentation of results from La Liberación de Texíguat (Photo © J.H. Townsend). D) Ileana Luque and I presenting educational materials on endemic species to children in Jilamito Nuevo, in the buffer zone of Refugio de Vida Silvestre Texíguat (Photo © Yensi Flores).
301
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Nacional La Muralla (Nototriton lignicola and Oedipina kasios) in Parque Nacional
Montaña de Yoro (Chapter 4; Townsend et al. 2011b).
Three expeditions were carried out to Parque Nacional Montaña de Yoro in 2006,
2007, and 2008, each in close coordination with national (Honduran National
Department of Protected Areas and Wildlife [ICF]), municipal (Municipality of Marale,
collaborating with the alcalde (mayor) and the office of rural development), park
administrative (logistics arranged in close collaboration the director of the park), and
community management (were accompanied by the local guardabosque, or park
ranger, and worked out of local homes) levels. The guardabosques were not simply
viewed as local escorts into the park, rather a deliberate attempt was made to engage
them in an active interchange of ecological knowledge, sharing scientific knowledge
about biodiversity in exchange for locally-derived traditional knowledge of the cloud
forest and its inhabitants.
In addition to the participation by guardabosques, expeditions into Montaña de
Yoro included (along with myself and Dr. Larry David Wilson), two graduate students
and one undergraduate from North American universities, two biology students from the
National Autonomous University of Honduras (UNAH), and two Peace Corps
volunteers. None of the participants had previous experience in remote field-based
research in the tropics, but all were able to fully participate and gain experience in a
variety of methods, ranging from expedition planning and wilderness survival to
preparation of tissue samples and specimens.
Following the discoveries in Parque Nacional Montaña de Yoro, a priority became
the public dissemination of information about this virtually unknown area. Scientific
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results were published in peer-reviewed outlets as is standard practice in the field. In
addition, I wrote (with Ileana Luque-Montes) a newspaper article that, with the
assistance of the Zamorano Biodiversity Center, received front page coverage in the
two largest Honduran newspapers (Figure 6-1). Additional undiscovered species almost
certainly occur in this reserve, but intensive survey work is needed immediately to
document Montaña de Yoro’s diversity in support of a plan for conserving its remaining
forests.
Concluding Statement
In this dissertation, I have sought to usher in a new era of biodiversity research in
the Chortís Block region of Central America. By utilizing an integrative framework built
around biodiversity inventory and molecular systematics, I have presented a viable
model for addressing critical unmet goals for biodiversity conservation, through the
taxonomic and molecular inventory of an endemism hotspot, which simultaneously
promotes training for the next generation of Honduran (and Honduras-focused)
biologists and raising public awareness of endemic-rich areas and related conservation
issues through extension and outreach. I am anticipating the opportunity to fully pursue
implementation of this model with even greater intensity and at a broader scale in the
coming years, with the sincere hope that this initiative will catalyze efforts to bring the
Chortís Block biodiversity hotspot to the forefront of regional and global conservation
and to its recognition as one of the planet’s premier regions for localized evolutionary
diversification.
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APPENDIX TAXONOMIC REVIEW OF CAUDATA FROM THE CHORTÍS BLOCK
Below I present a review of the salamander taxa known to occur with the Chortís
Block as of July 2009, the point at which I began writing this dissertation. ―Available
genetic data‖ is indicative of data openly available (i.e., via NCBI) as of July 2009,
summarized in order to provide the context for newly-generated data.
Dwarf salamanders (genus Cryptotriton García-París & Wake 2000)
The genus Cryptotriton contains the six species formerly referred to as the
Nototriton nasalis group (sensu Papenfuss & Wake 1987), but recognized by García-
París & Wake (2000) to represent a cryptic clade distinct from Nototriton. An
undescribed seventh species was identified from the Sierra de Las Minas in Guatemala
by García-París & Wake (2000). Three putative species of Cryptotriton are reported to
occur in the Chortís Highlands; however the status of C. wakei is disputed, with
McCranie & Wilson (2002: 139) making the case that this species is a junior synonym of
C. nasalis, given a lack of morphological distinction between the two and the proximity
of their known distributions. However, genetic material referable to C. wakei is lacking,
and until the status of this taxon can be assessed phylogenetically its taxonomic validity
will remain uncertain.
Cryptotriton monzoni (Campbell & Smith 1998)
Nototriton monzoni Campbell & Smith 1998: 6.
Cryptotriton monzoni: García-París & Wake 2000: 58.
Type locality. ―Cerro Del Mono, near La Unión, Zacapa, Guatemala, 1570 m
elevation (14°58’N, 89°17’W).‖
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Known distribution. Known only from a single specimen from the type locality in
easternmost Guatemala.
Available genetic data. None.
Cryptotriton nasalis (Dunn 1924)
Oedipus nasalis Dunn 1924: 97.
Chiropterotriton nasalis: Meyer & Wilson 1971: 7.
Nototriton nasalis: Wake & Elias 1983: 11.
Cryptotriton nasalis: García-París & Wake 2000: 58.
Type locality. ―Mountains west of San Pedro, Honduras, at 4500 [= 1,371 m] feet
altitude.‖
Known distribution. Restricted to the Sierra de Omoa in northwestern Honduras,
from 1,220–2,200 m elevation.
Available genetic data. Cyt b (1 sample; García-París & Wake 2000).
Cryptotriton wakei (Campbell & Smith 1998)
Nototriton wakei Campbell & Smith 1998: 5.
Cryptotriton wakei: García-París & Wake 2000: 58.
Type locality. ―West slope of Cerro Pozo de Agua, Sierra de Caral, Municipio de
Morales, Izabal, Guatemala, 1150 m elevation (15°22’N, 88°42’W).‖
Known distribution. Known only from a single specimen from the type locality in
easternmost Guatemala, 1,150 m elevation.
Available genetic data. None.
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Bromeliad salamanders (genus Dendrotriton Wake & Elias 1983)
The genus Dendrotriton was proposed to accommodate the species of the
Chiropterotriton bromeliacia group (sensu Lynch & Wake 1975) of Chiropterotriton beta
(Wake & Elias 1983). Of the six species of Dendrotriton, the single Chortís Highlands
species stands as a biogeographic outlier, with the five remaining species restricted to
the highlands of western Guatemala and adjacent Chiapas, México (Wake 1998).
Bromeliad-dwelling salamanders have been known from Cerro Santa Bárbara, and
isolated karstic mountain in central Honduras, since first collected by XXX in XXX.
These salamanders were referred to as Chiropterotriton (and later Nototriton) nasalis
(Meyer & Wilson 1971; Wake & Elias 1983), a species otherwise known only from the
Sierra de Omoa in northwestern Honduras, until being recognized as a distinct species
by McCranie & Wilson ―1996‖ [1997]. Those authors placed the new species in the
genus Nototriton based on its previous assignment to N. nasalis, a member of the N.
nasalis group (Papenfuss & Wake 1987; later referred to the genus Cryptotriton; García-
París & Wake 2000); however, Wake (1998) placed the species in the genus
Dendrotriton based on external and internal morphology.
Dendrotriton sanctibarbarus (McCranie & Wilson “1996” [1997])
Nototriton sanctibarbarus McCranie & Wilson ―1996‖ [1997]: 111.
Dendrotriton sanctibarbarus: Wake 1998: 88.
Type locality. ―Montaña de Santa Bárbara (14 55’N, 88 07’W), 2,100 m elevation,
Departamento de Santa Bárbara, Honduras.‖
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Known distribution. Restricted to Montaña de Santa Bárbara, 1,800–2,744 m
elevation.
Available genetic data. None.
Moss salamanders (genus Nototriton Wake & Elias 1983)
The genus Nototriton included 13 species of miniature salamanders that are
disjunctly distributed across highland forests in Guatemala, Honduras, Nicaragua, and
Costa Rica (AmphibiaWeb, 2 September 2011). This genus was one of two named to
accommodate the species of Chiropterotriton beta (Wake & Elias 1983). Nototriton
sensu Wake & Elias 1983 itself was later shown to be paraphyletic, resulting in
description of the genus Cryptotriton by García-París & Wake (2000). There are three
species groups currently recognized within the genus Nototriton (Papenfuss & Wake
1987; Savage 2002): the N. barbouri group, the N. picadoi group, and the N. richardi
group. These three groups exhibit two discrete patterns of geographic distribution. The
N. barbouri group (five species) is restricted to the Chortís Highlands of Honduras and
Guatemala, and the N. picadoi group (six species) and N. richardi group (two species)
are found in the highlands of Costa Rica, with a single species in the N. picadoi group,
N. saslaya, endemic to a cloud forest in northern Nicaragua (Köhler 2002). This genus
is dealt with in detail in Chapters 4 and 5.
Nototriton barbouri (Schmidt 1936)
Oedipus barbouri Schmidt 1936: 43.
?Pseudoeurycea barbouri: Taylor 1944: 209.
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Chiropterotriton barbouri: Meyer 1969: 106.
Nototriton barbouri: Wake & Elias 1983: 11.
Type locality. ―Portillo Grande, Yoro, Honduras... from altitudes between 5000 [=
1524 m] feet (the type), and 6000 [= 1828 m] feet.‖
Known distribution. Populations assigned to this taxon are known from the vicinity
of Montaña Macuzal and Pico Pijol in Yoro, from Texíguat along the southwestern
border between Atlántida and Yoro, and from Pico Bonito in Atlántida; all localities
1,550–1,990 m elevation. A single specimen (AMNH 54949) from a locality near Lago
de Yojoa at 860 m elevation is also assigned to this taxon.
Available genetic data. 16S (1 sample; García-París & Wake 2000), cyt b (3
samples; García-París & Wake 2000).
Nototriton brodiei Campbell & Smith 1998
Nototriton brodiei Campbell & Smith 1998: 3.
Type locality. ―West slope of Cerro Pozo de Agua, Sierra de Caral, Municipio de
Morales, Izabal, Guatemala, 1125 m elevation (15°22’N, 88°42’W).‖
Known distribution. This species is known only from the Sierra de Caral in
easternmost Guatemala, 875–1,140 m elevation.
Available genetic data. 16S (1 sample; García-París & Wake 2000), cyt b (1
sample; García-París & Wake 2000).
Nototriton lignicola McCranie & Wilson 1997
Nototriton lignicola McCranie & Wilson 1997: 369.
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Nototriton ―barbouri‖: Espinal et al. 2001: 105.
Type locality. ―Cerro de Enmedio (15°06'N, 86°44'W) along the trail above the
Monte Escondido campground, Parque Nacional La Muralla, 1780 m elev.,
Departamento de Olancho, Honduras.‖
Known distribution. Known only from the vicinity of the type locality in the
northwestern corner of Olancho in north-central Honduras, 1,760–1,780 elevation.
Available genetic data. 16S (1 sample; García-París & Wake 2000), cyt b (2
samples; García-París & Wake 2000).
Nototriton limnospectator McCranie, Wilson, & Polisar 1998
Nototriton limnospectator McCranie et al. 1998: 455.
Type locality. ―The northwestern side of Montaña de Santa Bárbara, southwest of
San Luís de los Planes (14°56'N, 88°08'W), 1910 m elevation, Departamento de Santa
Bárbara, Honduras.‖
Known distribution. Apparently restricted to Montaña de Santa Bárbara, 1,640–
1,980 m elevation.
Available genetic data. Cyt b (1 sample; García-París & Wake 2000).
Nototriton saslaya Köhler 2002
Nototriton saslaya Köhler 2002: 205.
Type locality. ―S slope of Cerro Saslaya (13°46.0’N, 85°02.3’W), 1,371 m
elevation, Región Autónoma Atlántico Norte, Nicaragua.‖
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Known distribution. Known only from the vicinity of the type locality in north-central
Nicaragua, 1,280–1,370 m elevation.
Available genetic data. None.
Nototriton stuarti Wake & Campbell 2000
Nototriton stuarti Wake & Campbell 2000: 817.
Type locality. ―11.6 km (road) WSW Puerto Santo Tomás, Montañas del Mico,
Depto. Izabal, Guatemala, 88°40'W, 15°38'N, 744 m elev.‖
Known distribution. Known only from a single specimen from the type locality in
easternmost Guatemala.
Available genetic data. None.
Worm salamanders (genus Oedipina Keferstein 1868)
The taxon Oedipina accommodates some of the mostly morphologically divergent
Neotropical salamanders, a monophyletic clade that is sister to Nototriton (García-París
& Wake 2000). These elongate, attenuate species are the only Neotropical
salamanders to have lengthened their bodies as a result of an increased number of
vertebrae, and along with having greatly reduced limbs and elongate tails (which can be
more than two times the body length in many species) are well adapted for life inside
root masses, leaf litter, rotten logs, and other fossorial microhabitats (Brame 1968).
Oedipina represents an excellent example of a non-adaptive radiation (highly conserved
morphology across three distinct clades) that is adaptive at the clade level (the drastic
change in body form in order to exploit fossorial microhabitats). Eleven species of
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Oedipina are known from the Chortís Highlands, representing all three subgenera:
Oedipina, Oeditriton, and Oedopinola (García-París & Wake 2000, McCranie et al.
2008).
Subgenus Oedipina
This subgenus is represented by six putative species in the Chortís Highlands, two
of which have distributions that extend outside the region, leaving the remaining four as
endemics.
Oedipina cyclocauda Taylor 1952
Oedipina cyclocauda Taylor 1952: 764.
Type locality. ―Los Diamantes (1 mile south of Gúapiles), Costa Rica.‖
Known distribution. Caribbean lowlands of Costa Rica and southern Nicaragua,
60–500 m elevation.
Available genetic data. 16S (2 samples; García-París & Wake 2000), cyt b (2
samples; García-París & Wake 2000).
Oedipina ignea Stuart 1952
Oedipina ignea Stuart 1952: 1.
Type locality. ―Along the Río Las Brisas, just south of Yepocapa, Department of
Chimaltenango, Guatemala. Elevation, about 1450 meters.‖
Known distribution. Pacific versant of south-central Guatemala to southwestern
Honduras, 1,340–1,750 m elevation.
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Available genetic data. As ―O. sp. B,‖ 16S (1 sample; García-París & Wake 2000),
cyt b (1 sample; García-París & Wake 2000).
Oedipina leptopoda McCranie, Vieites, & Wake 2008
Oedipina cyclocauda (in part): Brame 1968: 30.
Oedipina leptopoda McCranie et al. 2008: 13.
Type locality. ―32 km (road) W of Yoro on road to Morazán, 15.267480 N,
87.434820 W, Dept. Yoro, Honduras.‖
Known distribution. Known from three localities in Departamento de Yoro,
Honduras, 700–1,300 m elevation.
Available genetic data. As ―O. sp. C,‖ cyt b (1 sample; García-París & Wake 2000).
Oedipina pseudouniformis Brame 1968
Oedipina uniformis (in part): Taylor 1952: 350.
Oedipina pseudouniformis Brame 1968: 25.
Type locality. ―Cienaga Colorado approximately three kilometers by road east of
Juan Viñas and 6.3 km by road west of Turrialba, Canton de Turrialba, Provincia de
Cartago, Costa Rica, elevation 1035 m (3400 ft).‖
Known distribution. The type series includes a series of eight specimens from
Hacienda La Cumplida, Matagalpa, Nicaragua, 731 m elevation, and is otherwise
known from 19–1,253 m elevation in northern and central Costa Rica.
Available genetic data. 16S (1 sample; García-París & Wake 2000), cyt b (3
samples; García-París & Wake 2000).
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Oedipina stuarti Brame 1968
Oedipina stuarti Brame 1968: 47.
Type locality. ―Amapala, Isla Tigre, in the Golfo de Fonseca, Departamento de
Valle, Honduras.‖
Known distribution. This enigmatic taxon is known from three specimens, two from
Isla El Tigre in the Pacific Ocean, and the third reportedly from Tegucigalpa, 975 m
elevation.
Available genetic data. None.
Oedipina taylori Stuart 1952
Oedipina taylori Stuart 1952: 2.
Type locality. ―4 kilometers east of Hacienda La Trinidad (23 air-line kilometers
southeast of Chiquimulilla, Department of Jutiapa, Guatemala. Elevation, about 100
meters.‖ [Where is the terminal parenthesis supposed to be placed?]
Known distribution. Pacific versant of southeastern Guatemala, El Salvador, and
Honduras, 140–1,140 m elevation. This species also is known from an isolated locality
in the upper Río Motagua Valley in eastern Guatemala.
Available genetic data. None.
Subgenus Oeditriton
Oedipina kasios McCranie, Vieites, & Wake 2008
Oedipina cyclocauda: Espinal et al. 2001: 103.
Oedipina kasios McCranie et al. 2008: 11.
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Type locality. ―Near Quebrada Pinol, 15°07’N, 86°44’W, Parque Nacional La
Muralla, 1,190 m a.s.l., Dept. Olancho, Honduras.‖
Known distribution. Known only from the vicinity of the type locality in the
northwestern corner of Olancho in north-central Honduras, 950–1,780 m elevation.
Available genetic data. 16S (2 samples; McCranie et al. 2008), cyt b (2 samples;
McCranie et al. 2008).
Oedipina quadra McCranie, Vieites, & Wake 2008
Oedipina cyclocauda (in part): Brame 1968: 30.
Oedipina quadra McCranie et al. 2008: 6.
Type locality. ―Urus Tingni Kiamp, 14°55’N, 84°41’W, tributary of upper portion
of Río Warunta, 160 m above sea level (a.s.l.), Dept. Gracias A Dios, Honduras.‖
Known distribution. Considered relatively widespread in the lowlands and
peripheral areas in north-central and eastern Honduras, 70–540 m elevation.
Available genetic data. 16S (1 sample; McCranie et al. 2008), cyt b (1 sample;
McCranie et al. 2008).
Subgenus Oedopinola
Oedipina elongata (Schmidt 1936)
Oedipus elongatus Schmidt 1936: 165.
Oedipina elongata: Taylor 1944: 226.
Type locality. ―Escobas, the site of the water supply for Puerto Barrios, Izabal,
Guatemala.‖
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Known distribution. Caribbean versant from near the Isthmus of Tehuantepec,
México, to northwestern Honduras, 10–770 m elevation.
Available genetic data. 16S (1 sample; García-París & Wake 2000), cyt b (1
sample; García-París & Wake 2000).
Oedipina gephyra McCranie, Wilson, & Williams 1993
Oedipina gephyra McCranie et al. 1993: 385.
Type locality. ―2.5 airline km NNE La Fortuna (15°26’N, 87°18‖W), 1690 m elev.,
Cordillera Nombre de Dios, Departamento de Yoro, Honduras.‖
Known distribution. Known from the vicinity of the type locality around Cerro
Texíguat at the western end of the Cordillera Nombre de Dios and from Cerro Búfalo in
the central portion of the same range in northern Honduras, 1,580–1,810 m elevation.
Available genetic data. 16S (2 samples; García-París & Wake 2000), cyt b (2
samples; García-París & Wake 2000).
Oedipina tomasi McCranie 2006
Oedipina sp.: Townsend et al. 2006: 31.
Oedipina tomasi McCranie 2006: 291.
Type locality. ―Near Sendero de Cantiles, Parque Nacional El Cusuco, 15°30’N,
88°14’W, 1800m elevation, Departamento de Cortés, Honduras.‖
Known distribution. Known only from the vicinity of the type locality in the Sierra de
Omoa in northwestern Honduras, 1,780–1,800 m elevation.
Available genetic data. None.
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Mushroom-tongued salamanders (genus Bolitoglossa Duméril, Bibron, & Duméril
1854)
The most species-rich genus of salamanders at 117 described species and
counting (AmphibiaWeb, 2 September 2011), Bolitoglossa also has the broadest
distribution of any salamander genus, ranging from San Luis Potosí in central México
south through Middle America and into South America to the Amazon Basin and
Bolivian highlands (Parra-Olea et al. 2004). There are 15 species of Bolitoglossa in the
Chortís Highlands, which are spread across four phylogenetically delimited subgenera
(after Parra-Olea et al. 2004): Bolitoglossa, Magnadigita, Nanotriton, and Pachymandra.
The subgenera Bolitoglossa and Nanotriton both are found generally in the lowlands
and peripherally in the highlands, and do not contain any species heretofore considered
endemic to the Chortís Highlands. Pachymandra is represented by a single, giant
species in the Chortís Highlands, B. dofleini, which inhabits premontane elevations and
peripheral areas. Magnadigita represents a diverse highland restricted radiation that is
largely endemic to the Chortís Highlands and includes the morphologically-defined B.
dunni species group (McCranie & Wilson 1993).
Subgenus Bolitoglossa Duméril, Bibron, & Duméril 1854
This diverse and widespread subgenus includes two species in the Chortís
Highlands, both of which are found in the lowlands formations peripheral to the
highlands of the serranía, with one species, B. mexicana, widely occurring at
premontane elevations.
317
Bolitoglossa mexicana Duméril, Bibron, & Duméril 1854
Bolitoglossa mexicana Duméril, Bibron, & Duméril 1854: 93.
Type locality. ―Dolorès peten.‖
Known distribution. Atlantic versant from southern Veracruz, México, to eastern
Honduras, near sea level to 1,400 m elevation.
Available genetic data. 16S (17 samples; García-París et al. 2000a), cyt b (6
samples; García-París et al. 2000a).
Bolitoglossa striatula (Noble 1918)
Oedipus striatulus Noble 1918: 344.
Bolitoglossa striatula: Taylor 1941: 147.
Type locality. ―Cukra, Eastern Nicaragua.‖
Known distribution. Atlantic versant from eastern Honduras to central Costa Rica,
near sea level to 1,050 m elevation.
Available genetic data. 16S (1 sample; García-París et al. 2000a), cyt b (1 sample;
García-París et al. 2000a).
Subgenus Magnadigita Taylor 1944
This subgenus includes the constituent members of the B. dunni species group,
the B. franklini species group, and the B. rostrata species group (Parra-Olea et al.
2004). Only the B. dunni group is found in the region, with 11 putative species endemic
to the Chortís Highlands.
318
Bolitoglossa carri McCranie & Wilson 1993
Bolitoglossa carri McCranie & Wilson 1993: 9.
B. (Magnadigita) carri: Parra-Olea et al. 2004: 336.
Type locality. ―Cerro Cantagallo, near Lepaterique (14°06’N, 87°28’W), 1840 m
elevation, Departamento de Francisco Morazán, Honduras.‖
Known distribution. Known only from the vicinity of the type locality in the
mountains west of Tegucigalpa, Honduras, 1,840–2,070 m elevation.
Available genetic data. 16S (2 samples; Parra-Olea et al. 2004), cyt b (2 samples;
Parra-Olea et al. 2004).
Bolitoglossa celaque McCranie & Wilson 1993
Bolitoglossa dunni (in part): Hidalgo 1983: 6.
Bolitoglossa celaque McCranie & Wilson 1993: 11.
B. (Magnadigita) celaque: Parra-Olea et al. 2004: 336.
Type locality. ―Near the Rio Arcáqual, eastern side of Cerro Celaque, Cordillera de
Celaque (14°32’N‖, 88°40’W), 2480 m elevation, Departamento de Lempira, Honduras.‖
Known distribution. Highland forests across the departments of Lempira, Intibucá,
and La Paz in southwestern Honduras, 1,900–2,620 m elevation.
Available genetic data. 16S (2 samples; Parra-Olea et al. 2004), cyt b (2 samples;
Parra-Olea et al. 2004).
Bolitoglossa conanti McCranie & Wilson 1993
Oedipus morio (in part): Dunn 1926: 387.
319
Oedipus dunni (in part). Schmidt 1933: 16.
Magnadigita dunni (in part): Taylor 1944: 218.
Bolitoglossa dunni (in part): Wake & Brame 1963: 386.
Bolitoglossa conanti McCranie & Wilson 1993: 4.
B. (Magnadigita) conanti: Parra-Olea et al. 2004: 336.
Type locality. ―Quebrada Grande (15°05’N, 88°55’W), 1370 m elevation,
Departamento de Copán, Honduras.‖
Known distribution. Several isolated localities in western Honduras along the
Guatemalan and Salvadoran borders, 1,370–2,000 m elevation.
Available genetic data. 16S (1 sample; Parra-Olea et al. 2004), cyt b (1 sample;
Parra-Olea et al. 2004).
Bolitoglossa decora McCranie & Wilson 1997
Bolitoglossa decora McCranie & Wilson 1997: 367.
B. (Magnadigita) decora: Parra-Olea et al. 2004: 336.
Type locality. ―Along the trail to Cerro de Enmedio along the trail above the Monte
Escondido campground (15°05'N, 86°44'W), Parque Nacional La Muralla, 1440 m elev.,
Departamento de Olancho, Honduras.‖
Known distribution. Known only from the vicinity of the type locality in the
northwestern corner of Olancho in north-central Honduras, 1,430–1,550 m elevation.
Available genetic data. 16S (1 sample; Parra-Olea et al. 2004), cyt b (1 sample;
Parra-Olea et al. 2004).
320
Bolitoglossa diaphora McCranie & Wilson 1995
Bolitoglossa sp. 1: McCranie & Wilson 1994: 147.
Bolitoglossa diaphora McCranie & Wilson 1995: 448.
B. (Magnadigita) diaphora: Parra-Olea et al. 2004: 336.
Type locality. ―Above the visitors center of Parque Nacional El Cusuco, Cerro
Cusuco (15°31’N, 88°12‖W), 5.6 km WSW Buenos Aires, 1550 m elevation, Sierra de
Omoa, Departamento de Cortés, Honduras.‖
Known distribution. Restricted to the Sierra de Omoa in northwestern Honduras,
from 1,470–2,200 m elevation.
Available genetic data. 16S (1 sample; Parra-Olea et al. 2004), cyt b (1 sample;
Parra-Olea et al. 2004).
Bolitoglossa dunni (Schmidt 1933)
Oedipus morio (in part): Dunn 1926: 387.
Oedipus dunni Schmidt 1933: 16 (note: the type series was later shown to contain
more than one species by McCranie & Wilson 1993).
Magnadigita dunni (in part): Taylor 1944: 218.
Bolitoglossa dunni (in part): Wake & Brame 1963: 386.
B. (Magnadigita) dunni: Parra-Olea et al. 2004: 336.
Type locality. ―Mountains west of San Pedro, Honduras. Altitude 4500 feet [=
1,371 m].‖
Known distribution. Several isolated localities in western Honduras along the
Guatemalan border, 1,200–1,600 m elevation.
321
Available genetic data. 16S (1 sample; Parra-Olea et al. 2004), cyt b (1 sample;
Parra-Olea et al. 2004).
Bolitoglossa heiroreias Greenbaum 2004
Magnadigita engelhardti: Mertens, 1952: 20.
Bolitoglossa dunni (in part): Wake and Lynch, 1976: 13.
Bolitoglossa engelhardti (in part): Villa et al., 1988: 3.
Bolitoglossa conanti (in part): McCranie and Wilson, 1993: 8.
Bolitoglossa cf. conanti: Leenders and Watkins-Colwell, 2004: 5.
Bolitoglossa sp. 3: Parra-Olea et al., 2004: 336.
Bolitoglossa heiroreias Greenbaum 2004: 412.
Type locality. ―Camel Cigarettes Field Station at base of Cerro Montecristo, Depto.
Santa Ana, El Salvador, elevation 1880 m… coordinates 14°24’04‖N, 89°21’02‖W.‖
Known distribution. Known from the vicinity of Cerro Montecristo in El Salvador,
Guatemala, and Honduras, 1,840–2,300 m elevation.
Available genetic data. 16S (2 samples; Parra-Olea et al. 2004), cyt b (2 samples;
Parra-Olea et al. 2004).
Bolitoglossa longissima McCranie & Cruz 1996
Bolitoglossa longissima McCranie & Cruz 1996: 195.
B. (Magnadigita) longissima: Parra-Olea et al. 2004: 336.
322
Type locality. ―Along the trail to Pico La Picucha, Sierra de Agalta (14°58’N,
88°55‖W), ca. 10 airline km NNW Catacamas, 1900 m elevation, Departamento de
Olancho, Honduras.‖
Known distribution. Known only from the vicinity of the type locality in the Sierra de
Agalta in eastern Honduras, 1,840–2,240 m elevation.
Available genetic data. 16S (1 sample; Parra-Olea et al. 2004), cyt b (1 sample;
Parra-Olea et al. 2004).
Bolitoglossa oresbia McCranie, Espinal, & Wilson 2005
Bolitoglossa oresbia McCranie et al. 2005: 108.
Type locality. ―Cerro El Zarciadero, 14°43.662’N, 87°53.925’W, 1880 m elevation,
Departamento de Comayagua, Honduras.‖
Known distribution. Known only from the vicinity of the type locality, a 1 hectare
patch of forest on top of an isolated peak in central Honduras, 1,880 m elevation.
Available genetic data. None.
Bolitoglossa porrasorum McCranie & Wilson 1995
Bolitoglossa dunni (in part): Meyer 1969: 95.
Bolitoglossa conanti (in part): McCranie & Wilson 1993: 8.
Bolitoglossa sp.: Holm & Cruz 1994: 20.
Bolitoglossa sp. 2: McCranie & Wilson 1994: 147.
Bolitoglossa porrasorum McCranie & Wilson 1995: 132.
B. (Magnadigita) porrasorum: Parra-Olea et al. 2004: 336.
323
Type locality. ―East slope of Pico Pijol (15°10’N, 87°33'W), Montaña de Pijol
northwest of Tegucigalpita, 1860-1900 m elevation, Departamento de Yoro, Honduras.‖
Known distribution. Populations assigned to this taxon are known from the vicinity
of Montaña Macuzal and Pico Pijol in Yoro, from Texíguat along the border between
Atlántida and Yoro, and from the vicinity of Pico Bonito in Atlántida; 980–1,920 m
elevation
Available genetic data. 16S (1 sample; Parra-Olea et al. 2004), cyt b (1 sample;
Parra-Olea et al. 2004).
Bolitoglossa synoria McCranie & Köhler 1999
Bolitoglossa celaque (in part): McCranie & Wilson 1993: 13.
Bolitoglossa synoria McCranie & Köhler 1999: 226.
B. (Magnadigita) synoria: Parra-Olea et al. 2004: 336.
Type locality. ―Quebrada La Quebradona (14°23.96’N, 89°07.38’W), north slope of
Cerro El Pital, 2150 m elevation, Departamento de Ocotepeque, Honduras.‖
Known distribution. Known only from the vicinity of the type locality on Cerro El
Pital along the border between Honduras and El Salvador, 2,150–2,713 m elevation.
Available genetic data. 16S (1 sample; Parra-Olea et al. 2004), cyt b (1 sample;
Parra-Olea et al. 2004).
Subgenus Nanotriton Parra-Olea, García-París, & Wake 2004
This subgenus accommodates two small species, one of which is currently known
to occur in the Chortís Highlands. The second species, B. occidentalis, has been
324
reported previously from a disjunct locality in Honduras, but a recent review of this
specimen showed to represent a poorly preserved juvenile B. mexicana (T. Papenfuss,
pers. comm.).
Bolitoglossa rufescens (Cope 1869) complex
Oedipus rufescens Cope 1869: 104.
Spelerpes (Oedipus) rufescens: Peters 1873: 617.
Geotriton rufescens: Smith 1877: 76.
Spelerpes rufescens: Boulenger 1882: 71.
Bolitoglossa rufescens: Taylor 1941: 145.
B. (Nanotriton) rufescens: Parra-Olea et al. 2004: 335.
Type locality. ―Orizava…Vera Cruz, México.‖
Known distribution. On the Caribbean versant from central México to central
Honduras, from near sea level to over 1,400 m elevation, although typically in the
lowlands.
Available genetic data. 16S (1 sample; Parra-Olea et al. 2004), cyt b (1 sample;
Parra-Olea et al. 2004).
Subgenus Pachymandra Parra-Olea, García-París, & Wake 2004
This subgenus was erected to contain two very large species of terrestrial
salamanders, one of which occurs in the Chortís Highlands.
Bolitoglossa dofleini (Werner 1903)
325
Spelerpes dofleini Werner 1903: 352.
Oedipus schmidti Dunn 1924: 96.
Bolitoglossa doffleini [lapsus]: Taylor 1944: 219.
B. (Pachymandra) dofleini: Parra-Olea et al. 2004: 337.
Type locality. ―Guatemala.‖
Known distribution. The Caribbean versant of eastern Guatemala, southern Belize,
and northwestern and north-central Honduras, from 650–1,370 m elevation.
Available genetic data. 16S (1 sample; Parra-Olea et al. 2004), cyt b (1 sample;
Parra-Olea et al. 2004).
326
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BIOGRAPHICAL SKETCH
Josiah (Joe) Townsend received his Ph.D. in Interdisciplinary Ecology from the
University of Florida in Fall 2011, and had previously earned his Master of Arts in Latin
American Studies and Bachelor of Science in Wildlife Ecology and Conservation, both
from the University of Florida. Joe was born in Enid, Oklahoma in 1978, the son of
Steve Townsend of Ferriday, Louisiana and Terri Boyd Townsend or Medford,
Oklahoma. After living in Medford for his first year, Joe and his family moved to Kenner,
Louisiana, and then to Sulfur, Louisiana, where they were joined 1981 by his sister,
Katielynn Boyd Townsend. They soon relocated to Bethel Park, a suburb of Pittsburgh,
Pennsylvania, where Joe attended Logan Elementary School. It was here that Joe
spent his childhood and developed his fascination with biological diversity in the halls of
the Carnegie Museum of Natural History and the creeks and woods of southwestern
Pennsylvania. They relocated briefly to Pembroke Pines, Florida in 5th grade, then to
Hauppauge, New York from 6th through 8th grade, and finally to Miami, Florida in 1992,
where they moved the same week that Hurricane Andrew struck. In Miami, Joe
attended Southwood Middle School and Miami Palmetto Senior High School, where he
graduate in 1996. Joe attended Miami-Dade Community College after high school, while
helping to manage a youth hockey league. He began his studies at the University of
Florida in 2000. He married Ileana Rosario Luque-Montes on the 4th of July, 2009, at
his parent’s house in Maryland, and they lived happily ever after.