morphometric analysis of the rio apaporis caiman (reptilia...

ZOOTAXA

ISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)Copyright 2015 Magnolia Press

Zootaxa 4059 (3): 541554 www.mapress.com/zootaxa/

Article

http://dx.doi.org/10.11646/zootaxa.4059.3.6

http://zoobank.org/urn:lsid:zoobank.org:pub:A23EEA5E-1351-40F3-93ED-C3DFED51294E

Morphometric analysis of the Rio Apaporis Caiman

(Reptilia, Crocodylia, Alligatoridae)

ARMANDO H. ESCOBEDO-GALVN1,2,6, JULIN A. VELASCO3, JOS F. GONZLEZ-MAYA4 & ALAN

RESETAR51Centro del Cambio Global y la Sustentabilidad en el Sureste A.C., Centenario del Instituto Jurez s/n, 86080 Villahermosa, Tabasco,

Mxico2Current address: Centro Universitario de la Costa, Universidad de Guadalajara, Av. Universidad 203, 48280 Puerto Vallarta,

Jalisco, Mxico3Laboratorio de Anlisis Espaciales, Instituto de Biologa, Universidad Nacional Autnoma de Mxico, 04360 Mxico D.F., Mxico4 Proyecto de Conservacin de Aguas y Tierras - ProCAT Colombia/Internacional, Carrera 13 # 96-05, Of. 205, Bogot, Colombia &

Instituto de Ecologa, Universidad Nacional Autnoma de Mxico, 04360 Mxico D.F., Mxico5Division of Amphibians and Reptiles, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, IL 60605-2496 USA 6Corresponding author. E-mail: [email protected]

Abstract

Caiman crocodilus apaporiensis has been considered by several authors as an extreme of morphological variation within

the Caiman crocodilus complex. Here, we evaluate its position in the Caiman crocodilus complex morphospace using

morphological traits from head shape. We examined the holotype and seventeen paratypes of Caiman crocodilus apa-

poriensis Medem 1955 deposited at the Field Museum of Natural History. We performed multivariate morphometric anal-

yses: principal component analysis (PCA) and discriminant function analysis (DFA), based on 21 cranial traits of of C. c.

apaporiensis, C. yacare and the C. crocodilus complex (C. c. chiapasius, C. c. fuscus andC. c. crocodilus). We find a no-

table separation of C.c. apaporiensis from C. yacare and C. crocodilus complex in the morphospace. We suggest that geo-

graphic isolation might have driven this morphological separation from the C. crocodilus complex, but further analysis

are necessary to confirm whether these differences are related with genetic differentiation within the complex. In addition,

we suggest that environmental heterogeneity might drive the evolution of independent lineages within the C. crocodilus

complex.

Key words: Caiman crocodilus, Colombia, conservation, cranial shape, morphology

Resumen

El Caimn del Apaporis Caiman crocodilus apaporiensis ha sido considerado por algunos autores como una variacin

extrema en la morfologa del complejo Caiman crocodilus. En este trabajo evaluamos su posicin dentro del complejo

Caiman crocodilus, utilizando caracteres morfolgicos de la forma de la cabeza. Examinamos el holotipo y diecisiete

paratipos de Caiman crocodilus apaporiensis Medem 1955 depositado en el Field Museo de Historia Natural. Se re-

alizaron anlisis morfomtricos multivariados: anlisis de componentes principales (PCA) y anlisis de funcin discrim-

inante (DFA), basado en 21 rasgos craneales de C. c. apaporiensis, C. yacare y C. crocodilus (C. c. chiapasius, C. c. fuscus

and C. c. crocodilus). Se encontr una notable separacin de C. c. apaporiensis respecto a C. yacarey el complejo C. croc-

odilus. Los resultados sugieren que el aislamiento geogrfico podra haber impulsado esta separacin morfolgica del

complejo C. crocodilus, sin embargo futuros anlisis son necesarios para confirmar si estas diferencias estn relacionadas

con la diferenciacin gentica dentro del complejo C. crocodilus. Adems, se sugiere que la heterogeneidad ambiental

podra conducir la evolucin de los linajes independientes dentro del complejo C. crocodilus.

Palabras clave: Caiman crocodilus, Colombia, conservacin, forma del crneo, morfologa

Accepted by S. Carranza: 23 Nov. 2015; published: 23 Dec. 2015 541

Introduction

In 1955, Federico Medem described Caiman crocodilus apaporiensis (= C. sclerops apaporiensis) based on twenty-one specimens from the upper Apaporis River in Colombia between the falls of Jirijirimo and Puerto Yaviya (0 7 N, 71 0 W, approximately), and were deposited at the Field Museum of Natural History, Chicago, Illinois (FMNH). Medem (1955) stated that the specimens showed a noticeable difference from specimens from other localities in the region (Colombian Llanos Orientales and British Guiana), especially in the elongated and comparatively narrow snout and in certain external characteristics. Thereafter, Medem (1981, 1983) found substantial morphological evidence to recognize different lineages with Caiman crocodilus suggesting and proposed four subspecies to be recognized as follows: C. c. fuscus, C. c. chiapasius, C. c. crocodilus and C. c. apaporiensis (Rueda-Almonacid et al. 2007; Venegas-Anaya et al. 2008; Velasco & Ayarzagena 2010). In 1953 and 1954, F. Medem and K.P. Schmidt were writing a manuscript on taxonomic revision of the all genus Caiman, in which the taxonomic status of additional linages within the C. crocodilus complex (C. crocodilus matogrossensis, C. crocodilus paraguayensis and C. crocodilus humboldti) would be discussed. Unfortunately K.P. Schmidt died in 1954, and the manuscript was not published (Medem 1983).

Although Medem (1981, 1983) clarified many taxonomic problems that had been approached by some authors during 200 years (Schneider 1801; Daudin 1802; Spix 1825; Gray 1862; Boulenger 1889; Schmidt 1928; Mertens 1943), recent morphometric studies conducted by Busack & Pandya (2001) did not find support to recognize variation within Caiman crocodilus. However, mtDNA analysis recognized a difference between lineages from Mesoamerica and South America and provided evidence of substantial variation within the C. crocodilus complex (Venegas-Anaya et al. 2008). In addition, mtDNA analysis also revealed that C. crocodilus complex is far more diverse than previously thought, suggesting the existence of evolutionary independent lineages (Venegas-Anaya et al. 2008).

Caiman crocodilus apaporiensis has been controversial in the literature. Some authors consider this species as an extreme of morphological variation of Caiman crocodilus complex (Ayarzagena 1984; Gorzula 1994; Busack & Pandya 2001), but to our knowledge no studies have been conducted to evaluate the morphological position of C. c. apaporiensis within the morphospace of C. crocodilus complex. Here we conducted a morphological analysis of Caiman crocodilus apaporiensis, with emphasis on cranial shape variation of specimens pertaining to Caiman yacare and all recognized subspecies of C. crocodilus from most of its geographical range.

Material and methods

We examined eighteen skulls of C. c. apaporiensis, fifty-five from other subspecies of C. crocodilus, and eight of C. yacare. All this material is deposited in the division of amphibians and reptiles at the FMNH. We measured twenty-one standard morphological variables: dorsal cranial length (DCL), cranial width (CW), snout length (SL), basal snout width (SW), maximal orbital width (OW) minimal interorbital width (IOW), maximal orbital length (OL), length of the postorbital cranial roof (LCR), posterior width of the cranial roof (WCR), maximal width of external nares (WN), ventral cranial length (VCL: anterior tip of snout to posterior surface of occipital condyle), length of upper ramus (UM), length of palatal premaxillary symphysis (PXS), length of palatal maxillary symphysis (MXS), mandible length (ML), length of the mandibular symphysis (LMS), maximal width across the mandibular symphysis (WMS), dentary length (DL), dentary width (DW), surangular width (WSR), and length of lower ramus (LM). We based our analysis on skull morphological variables previously established to distinguish between crocodilian species (Montague 1984; Hall 1989; Hall & Portier 1994; Platt et al. 2009). All measurements were taken using digital calipers to the nearest 0.1 mm, and means standard deviation are provided. All specimens were photographed and measured using a metric tape by the first author (AHEG). We log-transformed data before statistical analysis to control for the possible influence of body size on the other measurements. We performed a first principal component analysis (PCA) with all morphometric traits from adult skulls in order to explore the structure of the morphological data. To remove body size effects from morphological traits, we performed regressions of each morphological trait against dorsal cranial length (DCL) as a proxy of body size. We performed a second PCA with DCL and the rest of traits adjusted by size. In addition, we performed a discriminant analysis using the PCA scores of the first four components to evaluate whether C. c. apaporiensis differ from other

ESCOBEDO-GALVN ET AL.542 Zootaxa 4059 (3) 2015 Magnolia Press

Caiman forms. In addition, we used the derived discriminant functions to quantify the percentage of taxon assignation. We compared C. c. apaporiensis with other lineages within the C. crocodilus complex and C. yacare as external group. Data for coloration in life were adapted from the original description.

Locality records of C. crocodilus complex and C. yacare were geo-referenced from museum voucher specimens in the FMNH, and were mapped using ArcMap 9.3 (ESRI, Inc). All records for C. crocodilus apaporiensis were obtained from Medem (1955), and were geo-referenced with a spatial precision of 0.04 using locality information and national gazetteers.

We followed Romer (1956), Brochu (2006) and Bona & Desojo (2011) for nomenclature of osteology and format description. We measured all morphometric variables in Caiman species and subspecies (see Appendix 1 for a complete list of revised material).

Results

Caiman crocodilus apaporiensis

Rio Apaporis Caiman (fig. 1)

Caiman sclerops apaporiensis MEDEM 1955

Caiman crocodilus apaporiensis MEDEM 1955

Caiman crocodilus apaporiensisNICKEL & AULIYA 2004

Holotype. FMNH 69812, adult male, from upper Rio Apaporis, Amazonas department, Colombia; collected by Federico Medem in February 1952.

Paratypes. FMNH 69813-69832 with the same data as the holotype. Type locality. Colombia: Laguna Inan, the upper Apaporis River, Comisariato Amazonas, 0 7 N, 71 0 W,

approximately.Diagnosis. Differs from other Caiman species by its long skull and large supratemporal fenestrae (Fig. 1). The

snout is relatively long and slender in contrast with the rest of extant Caiman species and subspecies. The snout length (anterior tip of snout to anterior orbital border, measured diagonally) is almost twice the width across the anterior orbital border (SL:SW ranged from 1.8 to 2.2). The SL:SW ratio for the other Caiman species/subspecies ranged from 1.2 to 1.7, with C. c. fuscus as broad-snouted taxa (SL:SW ranged from 1.2 to1.4); while C. c. crocodilus showed the most high variation (ranged from 1.4 to 1.7). The premaxillae completely surround the external naris and extend dorsolaterally back to the level of the fifth maxillary alveoli.

Description of the holotype.

Skull: in dorsal view, the skull of C. crocodilus apaporiensis has an elongated form. The snout is very enlarged and narrow in comparison with other Caiman species (Fig. 1; Table 1).

The premaxillae completely surround the external naris and extend dorsolaterally back to the level of the fifth maxillary alveoli. This condition of the premaxillae extending back would be unique condition among alligatorids but shared by basal globidontans (C. Brochu, pers. comm.). In dorsal view each premaxilla extends beyond this point, forming an acute process on either side of the nasal. Each premaxilla supports five alveoli. The second and fourth are largest, and behind the third alveolus their arrangement is almost linear. The premaxillary-maxillary suture on the palate is W-shaped, with each premaxilla bearing a broad posterior process. The nasals are long and narrow in comparison with other caimanine species (Romer 1956; Bona & Desojo 2011). The nasals broadly contact the premaxillae anteriorly, the maxillae laterally, and lacrimals and prefrontals posterolaterally, and the frontal posteromedially to a small degree. In the anterior part, nasals extend to third maxillary alveolus almost reaching the external naris. In the posterior part, the nasals extend to the level of the posterior end of the maxillae.

The maxillae extend behind the premaxilla and form much of the snout. The maxillae contact the nasals medially and the lacrimals and jugals posteromedially. Contact with the lacrimals is broad. The maxillae and prefrontals are separated by the lacrimal-nasal suture and do not contact each other. The maxillae possess 1921 alveoli.

The lacrimal forms the anterior margin of the orbit and extends rostrally and modestly contacts the nasal.

Zootaxa 4059 (3) 2015 Magnolia Press 543MORPHOLOGY OF RIO APAPORIS CAIMAN

FIGURE 1. Caiman crocodilus apaporiensis, holotype, FMNH 69812. Skull in dorsal, lateral and ventral views. Jaw in dorsal

view.

FIGURE 2. Caiman yacare ( = C. crocodilus yacare), FMNH 9150. Skull in dorsal, lateral and ventral views. Jaw in dorsal

view.


FIGURE 3. Caiman crocodilus chiapasius, FMNH 73709. Skull in dorsal, lateral and ventral views. Jaw in dorsal view.

FIGURE 4. Caiman crocodilus fuscus, FMNH 69849. Skull in dorsal, lateral and ventral views. Jaw in dorsal view.


FIGURE 5. Caiman crocodilus crocodilus, FMNH 26672. Skull in dorsal, lateral and ventral views. Jaw in dorsal view.

The prefrontal forms the anteromedial margin of the orbit. It contacts the lacrimal laterally and the frontal and nasal medially. Posteriorly, between the orbit and frontal, there is a shallow sulcus on the dorsal prefrontal surface.

The frontal is slightly concave between the orbits and flat posteriorly. Anteriorly, it forms an acute process, which contacts the nasals. The frontal contacts the postorbitals posterolaterally and the parietal posteriorly. The posterior margin of the frontal is convex and not involved in the formation of the supratemporal fenestrae.

The postorbital contacts the frontal and parietal in its anteromedial part, and the squamosal posteroventrally. This structure forms the anterior part of the supratemporal fenestrae, the dorsal part of the postorbital bar and pass along the posterior margin of the infratemporal fenestra. The parietal forms the medial walls of the supratemporal fenestrae. The interfenestral bar is dorsally flat. It contacts the squamosals posteromedially. The supratemporal fenestrae are large in comparison with other Caiman species (Fig. 15). The parietal perforates on the medial wall of the fenestra. The squamosal contacts the postorbital anteriorly, forming the posterior wall of the supratemporal fenestrae. In ventral view, the maxillae contact the palatines posteromedially and ectopterygoids posteriorly. The maxillae, premaxilla and palatine form the anterior floor of the nasopharyngeal duct. The palatines are slender and contact one another at the midline, delimiting the suborbital fenestrae medially. The palatines exhibit a slight concavity posteriorly. The pterygoids contact each other along the midline conforming the middle and posterior part of the nasopalatine duct. The secondary choana is located in the middle to posterior part of the pterygoids.

The ectopterygoid delimits the suborbital fenestra posterolaterally and contacts the maxilla anterolaterally, the jugal posterolaterally, the pterygoids medially, and the descending process for the postorbital posteromedially.

Jaw: The dentaries meet at the midline along a symphysis that extends back to the level of the fourth or fifth alveolus. The dentary extends back to 14 alveolus. There are 20 dentary alveoli; most are comparatively small, except the first and fourth which is almost twice the diameter of the other alveoli. The pattern of spacing of alveoli in the dentary is regular, except for the more widely spaced first three and closer third and fourth.

The splenials do not participate in the short mandibular symphysis. They are adjacent to the posteriormost five dentary alveoli. The splenial bears a small foramen in the middle, as all alligatorids (Bona & Desojo 2011). This foramen usually is confused as the foramen intermandibularis oralis, however this foramen is lost in all living alligatorids, excepting Alligator sinensis (C. Brochu, pers. comm.). The splenial makes contact with the coronoid


FIGURE 6. Geographic distribution of Caiman crocodilus apaporiensis, C. crocodilus complex and C. yacare examined.

posterordorsally and angular posteroventrally, delimitating the foramen intermandibularis caudalis. The angular lies below the surangular and forms the ventral margin of the external mandibular fenestra. The angular extends more than the internal mandibular fenestra and encapsulates completely the foramen intermandibularis caudalis. The angular contacts the surangular posteriorly, and it extends posterior to the external mandibular fenestra. The surangular projects posteriorly, forming the posterodoral margin of the external mandibular fenestra. The external


mandibular fenestra is wide and makes visible laterally the foramen intermandibular caudalis. The surangular exhibits ventral and dorsal process in its anterior part similar in length. The articular forms the posterior margin of the internal mandibular fenestra and its dorsal surface is concave, and bears an anterior process ventral to lingual foramen. The retroarticular process projects posterodorsally. The coronoid is ventrally elongated completely surrounds foramen intermandibularis medius. In its anterior part makes contact with splenial and its posterior end makes contact with angular bone.

Coloration in life (adapted from original description). The color description of living specimens is from Medem (1955): the dorsal coloration is bright yellowish-brown, with black spots and vermiculations; spotting more dense on the head, making the top of the head dark brown; tail yellowish on light brown, covered with numerous black vermiculations and spots, with four to six broad dark zones discernible; throat and lower jaws yellowish; flanks in general yellow, gray directly beneath the outer rows of dorsal scutes; keeled scutes of the flanks dark brown or black; several scutes with orange-colored keels on the sides of the neck; extremities dark gray or black.

Distribution and ecology. The current distribution of Rio Apaporis Caiman remains uncertain due to the low herpetological sampling conducted in that area of Colombia. We only made reference to historical information from previous studies (Fig. 6). The first surveys conducted by Medem (1955) were around two hundred kilometers between Puerto Yaviya and the Falls of Jirijimo in the upper of Apaporis River. Subsequently, Medem (1981) observed C. c. apaporiensis in the Ajaju and Macayo Rivers. A specimen was collected in the upper Tacunema. Additional observations provided by local landowners who state that the long-snouted caiman have been observed in some lakes of the upper Mesai, tributaries of Yari River in the Caqueta basin (Fig. 6).

FIGURE 7. Distribution of C. c. apaporiensis, C. crocodilus complex and C. yacare along the first and second principal

components axes.


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TABL

E 1.

Rang

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Conservation status. Assessment of population size, extent of occurrence and occupancy and threats over C. c. apaporiensis are needed to determine the real status of the species, and conservation status definition seems warranted. Speculative and anecdotal information mostly derived from original descriptions of the subspecies by Medem (1955) and our interpretation indicates the sub-species has a likely restricted distribution of no more than

60 km2, is affected by hunting pressure by local communities (Medem 1981) and it is likely suffering from genetic introgression and hybridization. Given these factors, it is likely the species could be assessed at high risk, potentially as Critically Endangered according to the IUCN Red List of Threatened Species criteria; however, information needed to adequately provide a Red List category is still lacking. As a conservative approach, we suggest listing the sub-species as Data Deficient, given the enormous information gaps, and prioritize it for further assessment and assigning an adequate conservation status category.

Morphometric analysis. The principal component analysis shows a separation between C. c. apaporiensis, C.yacare, and other C. crocodilus complex forms (Fig. 7). The first four components explain 63.73% of variance in cranial shape (Table 2). Cranial width variables had the highest loadings in the first component (CW, SW and WMS). Cranial length (DCL, LCR, ML, DL and LM) showed the highest loadings in the second component (Fig. 7); while IOW, OL, VCL, WMS, ML and LMS have the highest loadings in the third and four components. The use of derived discriminant functional analysis (DCL, CW, SL, and SW) showed that between 83.3% and 100% (untransformed and log-transformed data, respectively) was correctly attributed to C. c. apaporiensis. For C. yacare was 87.5% in both cases. For C. c. chiapasius was 29.4% and 52.9%; whereas for C.c. crocodilus and C. c. fuscus was 66.7% and 75.0% in both cases, respectively.

Etymology. The specific name apaporiensis refers to the Apaporis River.

TABLE 2. Results of principal component analysis (the first four PC axes) for 21 morphological characters for adults of

C. apaporiensis, C. yacare and C. crocodilus complex.

Character PC 1 PC 2 PC 3 PC 4

% variation 31.56% 18.85% 7.49% 5.83%

Eigenvalues 6.63 3.96 1.57 1.22

Loadings DCL -0.0061 -0.3696 0.19676 0.10989

CW 0.33396 0.13360 -0.0133 -0.0572

SW 0.35221 0.14270 -0.04259 0.00694

SL -0.25742 0.22898 -0.26551 0.06294

IOW 0.19604 0.06299 0.31611 -0.53937

OW 0.28979 0.14781 -0.18685 0.08006

OL -0.05417 0.14838 -0.30824 -0.37701

LCR 0.02247 -0.34248 -0.09610 -0.01468

WCR 0.29611 0.09828 -0.16889 -0.02210

WN 0.23989 0.26140 -0.00657 0.05309

VCL -0.01741 0.17818 0.23731 0.32292

UM -0.20773 0.27354 -0.01130 0.07901

PXS 0.19011 -0.00713 -0.31627 0.53329

MXS -0.21932 0.22429 0.03451 -0.21158

ML 0.09016 0.32117 0.32824 -0.01387

LMS 0.17563 -0.16035 0.44366 0.11282

WMS 0.35998 0.07722 0.04460 0.00692

DL -0.12403 0.37020 0.17782 0.14424

DW 0.09452 0.05551 0.25935 0.18471

WSR 0.26283 0.04880 -0.22782 -0.14023

LM -0.19334 0.30884 0.07834 0.10204


Discussion

The Rio Apaporis Caiman has been considered by several authors as an extreme of morphological variation within the Caiman crocodilus complex; however, morphological studies had not been carried to clarify the morphospace position within the Caiman crocodilus complex. Recent studies on species delimitation have provided a deeper insight into the implications for systematic and conservation within Crocodylia, showing that there are likely cryptic lineages showing notable diagnostic morphological features, mostly in skull traits (McAliley et al. 2006; Venegas-Anaya et al. 2008; Eaton et al. 2009; Hekkala et al. 2011; Milin-Garca et al. 2011; Shirley et al. 2014). The suite of morphological traits exhibited by C. c. apaporiensis clearly differentiates it from other species within the C. crocodilus complex. Previous morphometric studies suggest that the diversity of rostral shape among extant alligatorids has a strong phylogenetic signal (Piras et al. 2009). Thus, morphological traits of C c. apaporiensiscould be the results of evolutionary history despite to environmental variations. Future molecular analysis will be necessary to evaluate whether morphological differentiation of C. c. apaporiensis is related with genetic differentiation in the C. crocodilus complex. Furthermore, the phylogenetic position of C. c. apaporiensis needs to be evaluated using a combination of morphological and molecular data.

Moreover, we found a greater morphological differentiation between C. c. apaporiensis and the rest of the C. crocodilus complex than between C. yacare and the C. crocodilus complex excluding C. c. apaporiensis. Some phylogenetic studies support the monophyly of Caiman (C. crocodilus, C. yacare and C. latirostris), and shown a distinctiveness between C. yacare and C. crocodilus (Brochu 1999; Densmore 1983; Poe 1996; Brochu & Densmore 2000; White & Densmore 2000; Oaks 2011). Although the divergence time between C. crocodilus and C. yacare, based on fossil and molecular data, took place during the late Miocene (Godschalk 2006), we found strong morphometric similarity between C. yacare, C. crocodilus chiapasius, C. crocodilus fuscus, and C. crocodilus crocodilus. In addition, in some areas where C. yacare and C. crocodilus are sympatric and introgression is common, molecular and morphological data are unclear for distinguishing the species (Busack & Pandya 2001; Hrbek et al. 2008). On the other hand, C. crocodilus could show clinal variation, ranging from longirostrine to broad snout phenotypes, resulting in an overlap of snout morphotypes of C. crocodilus and C. yacare. Nevertheless, this must be studied in more detail in future morphological studies where latitude and altitude limits have been poorly defined between sympatric crocodilians.

Cranial variation within Caiman may reflect differences in diet (Ayarzagena 1984; Monteiro et al. 1997). The new insights regarding allometric cranial shape in crocodilians suggest that bite-force performance varies independently of rostral form, and that changes in body size/bite-force allows access to different prey types (Erickson et al. 2003, 2012; Foth et al. 2015). Despite the limited information about feeding habits of C. c. apaporiensis and other members of the C. crocodilus complex in general, morphological divergence could suggest widespread alimentary habits from durophagous for broad-snout morphotypes to slender-snouted generalist for longirostrine forms (see Erickson et al. 2012). Based on our results, we suggest that despite poorly-known differences on body size and mass between C. c. apaporiensis and the rest of the C. crocodilus complex (Medem 1981; Morales-Betancourt et al. 2013), ecomorphological variation may partially support the separation of ecological niche between C. c. apaporiensis and other Caiman species.

A recently described fossil species, Caiman venezuelensis Fortier and Rincon 2012 from the Pleistocene of Venezuela, might bear on the validity of C. c. apaporiensis. Although limited to a partial premaxilla, it suggests a comparatively slender snout with a premaxilla. The material is insufficient to determine whether C. venezuelensisand C. c. apaporiensis are closely related or even conspecific, but if they are, it suggests a divergence between C. c. apaporiensis and other living species minimally by the early Pleistocene. This, in turn, implies that the lineage including C. c. apaporiensis could have been independent for 2 million years or more. Nevertheless, further study is needed.

Finally, our results suggest that the Rio Apaporis Caiman might be a distinct evolutionary linage from the rest of the C. crocodilus complex, thus, could be considered a different species; however, molecular data is therefore needed for supporting this statement and clearly identify C.c. apaporiensis as a distinct species.

Acknowledgements

This work was supported by Visiting Scholarships Program at Field Museum of Natural History. Centro del


Cambio Global y la Sustentabilidad en el Sureste AC, ProCAT Colombia and Sierra to Sea Institute provided partial support. We deeply thank Stephanie Wear for logistic support. We thank Chistopher Brochu for suggestions and recommendations on this manuscript. We also express our deep thanks to Salvador Carranza and anonymous reviewers for constructive comments and suggestions to improve this paper. JAV is a graduate student at the Posgrado en Ciencias Biolgicas, UNAM, and receive a graduate scholarship from the Consejo Nacional de Ciencia y Tecnologa.

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APPENDIX 1. Additional specimens examined.

Caiman crocodilus-Venezuela: FMNH 13062. Colombia: Meta Intendencia: Cano Manacales, near Talanqueras, FMNH 73438.

Meta Intendencia: Viso de Pinal, Rio Guejar, south from Talanqueras, FMNH 73443. Meta Intendencia: Laguna de

Choriaro, near Rio Guejar & camp "La Macarena", Sabana de San Juan de Arama, FMNH 73443. Meta Intendencia: Rio

Guejar, Playa Dudita, southeast from Finca Talanqueras, FMNH 73440. Meta Intendencia: Upper Rio Cunimia, territory of

Talanqueras, FMNH 73446. Meta Intendencia: Laguna del Penon, Sabana de San Juan, FMNH 73448. Trinidad: San

Rafael, FMNH 53653. Peru: Loreto, FMNH 56179. Loreto, Rio Ucayali, Yarinacocha, FMNH 56189, 56190, 56191,

56192. British Guiana: Demerara: Buxton (E coast), FMNH 26679, 27080.

Caiman crocodilus chiapasius-Colombia: Choc: Golfo de Uraba, Rio Acandi, FMNH 73710, 73724, 73725, 73731. Choc:

Golfo de Uraba, Rio Tolo, FMNH 73714, 73715. Choc: Golfo de Uraba, Rio Arquiti, FMNH 73732, 73739, 73740,

73741, 73744, 73747. Choc: Sautata, lower Rio Atrato, FMNH 73683, 73684, 73686, 73693, 73699, 73701, 73704,

73707, 73708. Choc: Golfo de Uraba, Rio Negro, FMNH 73723. PANAMA: Canal Zone, Barro Colorado Island, FMNH

6126.

Caiman crocodilus fuscus-Colombia: Magdalena: Cienaga Grande, Rio Frio, FMNH 69835, 69840, 69841, 69842, 69844,

69845. Magdalena: Cienaga Grande, FMNH 69851, 69856, 69857. Magdalena: Cienaga Grande, Rio (Cano) Pajaro,

FMNH 69848, 69849. Magdalena: Cienaga Grande, Rio Palenque, FMNH 69862, 69863, 69864, 69865. Magdalena:

Cienaga Grande, Rio Aracataca, FMNH 69847.

Caiman crocodilus yacare: Brazil: Paraguay River, FMNH 9136, 9140, 9141, 9144, 9145, 9146, 9147. Mato Grosso: Paraguay

River below Descalvados, FMNH 9150.

Caiman crocodilus apaporiensis-Colombia: Amazonas Intendencia: Rio Apaporis, FMNH 69812, 69813, 69814, 69816,

69817. Amazonas Intendencia: Rio Apaporis, Laguna del Capitan Mario, FMNH 69818, 69819, 69820, 69821, 69823,

69824. Amazonas Intendencia: Rio Apaporis, Rio Pacoa, FMNH 69825. Amazonas Intendencia, Rio Apaporis, Laguna de

Chirucu, FMNH 69826. Amazonas Intendencia, Rio Apaporis, Laguna Inana N 1, FMNH 69827, 69828, 69830.

Amazonas Intendencia: Rio Apaporis, Laguna Inana N 2, FMNH 69831, 69832.


ResumenIntroductionMaterial and methodsResultsCaiman crocodilus apaporiensisDiscussionAcknowledgementsReferences

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