supplementary information: observational and …10.1007... · web viewsupplemental information:...

Supplemental Information: Observational and Experimental Studies of Anthropogenic Land Use Change and Infectious Disease

Disease Pathogen name Pathogen type

Multi or Single Host

Main Host Land Use Type Continent TransmissionType

Citation

Ectoparasites, lizard Eutrombicula arthropod MHP lizards forest fragmentation

S. America

direct Rubio and Simonetti (2009)

Ectoparasites, bat Bat fly arthropod MHP Bats Human settlement

S. America

direct (Pilosof, Dick et al. 2012)

Tick-borne zoonotic bacteria

Anaplasma, Rickettsia,

bacteria MHP wildlife, birds and mammals

forest fragmentation

N. America, S. America

VB (Halos, Bord et al. 2010, Ogrzewalska, Uezu et al. 2011)

Lyme disease Borellia burgdorferi

bacteria MHP White-footed mice, mammals, birds, reptiles

deforestation, forest fragmentation, agricultural development, urbanization

N. America,Eurasia

VB (Glass, Amerasinghe et al. 1994, Allan, Keesing et al. 2003, LoGiudice, Ostfeld et al. 2003, Brownstein, Skelly et al. 2005, Linard, Lamarque et al. 2007, Diuk-Wasser, Vourc'h et al. 2010, Li, Hartemink et al. 2012, Tack, Madder et al. 2012)

Campylobacter Campylobacter spp

bacteria MHP human /livestock

agricultural development

Oceania direct (Eyles, Brooks et al. 2006)

enteric bacterial pathogens

E. coli bacteria MHP human and nonhuman primates


Africa direct (Goldberg, Gillespie et al. 2008)

Waterborne enteric pathogens

Cryptosporidium, Giardia, Salmonella, Campylobacter, Listeria, E.coli

bacteria MHP humans, other mammals, amphibians, reptiles, birds


N. America

direct (Wilkes, Edge et al. 2011)

Ehrlichiosis and Anaplasmosis

Ehrlichia chafeensis, Anaplasma phagocytophilum

bacteria MHP deer reservoir (Ehrlichia)

forest fragmentation, urbanization, suburbanization, forest park management

N. America

VB (Wimberly, Yabsley et al. 2008, Foley, Nieto et al. 2009, Allan, Dutra et al. 2010)


meningococcal meningitis

group A meningococci

bacteria SHP human desertification, loss of vegetation cover

Africa direct (Molesworth, Cuevas et al. 2003)

leptospirosis Leptospira canis serovar pomona, Leptospira spp.

bacteria MHP mammals Agricultural development-urbanization

S. America, N. America

direct (Barcellos, Lammerhirt et al. 2003, Ghneim, Viers et al. 2007)

bovine tuberculosis Mycobacterium bovis

bacteria MHP bovine, wild ungulates

woodland management

Eurasia direct (Vicente, Hofle et al. 2007)

Buruli ulcer Mycobacterium ulcerans

bacteria MHP human agricultural development

Africa direct (Wagner, Benbow et al. 2008, Wagner, Benbow et al. 2008)

Chromoblastomycosis Cladiophialophora carrionii

fungus MHP human deforestation Africa direct (Esterre, Andriantsimahavandy et al. 1997)

Chytridiomycosis Batrachochytrium dendrobatidis

fungus MHP amphibian deforestation, forest fragmentation

N. America, S. America

direct (Becker and Zamudio 2011, Hartson, Orlofske et al. 2011)

intestinal helminth, bobwhite quail

Raillietina spp., Aproctella sp.Cheilospirura,Cyrnea sp. Dispharynx sp. Heterakis sp. Tetrameres Trichostrongylus

helminth (nematode, cestode)

MHP and SHP

bobwhite quail


N. America

direct and trophic

(Davidson, Kellogg et al. 1991)

Echinococcus Echinococcus multilocularis

helminth (cestode)

MHP rodent/ carnivore

deforestation Eurasia trophic (Craig, Giraudoux et al. 2000, Giraudoux, Pleydell et al. 2006, Reperant, Hegglin et al. 2007, Robardet, Giraudoux et al. 2011)

Balysascaris Balysascaris procyonis

helminth (nematode)

MHP raccoons, mammals

urbanization N. America

trophic (Page, Gehrt et al. 2008, Kellner, Page et al. 2012, Samson, Dubay et al. 2012)

endoparasitism, wild GI nematodes helminth MHP/ wild rodents forest S. direct and (Puttker, Meyer-Lucht


rodents (nematode)

SHP fragmentation America trophic et al. 2008)

endoparasites, bobcat CryptosporidiumGiardia sp.Ancylostoma, Uncinaria, Toxacara cati

Protozoa and helminth

MHP Bobcats, mammals

Urbanization N. America

direct and trophic

(Carver, Scorza et al. 2012)

mermithid nematodes Mermithidae helminth (nematode)

MHP spiders habitat fragmentation

N. America

trophic (Vandergast and Roderick 2003)

intestinal helminth and cestode rabbit

nematode- Trichostrongylus retortaeformis, and cestode-Mosgovoyia pectinata

helminth (nematode)

SHP /MHP rabbit forestry management

Eurasia direct and trophic

(Hulbert and Boag 2001)

onchocerchiasis Onchocerca volvularis

helminth (nematode)

SHP/MHP human deforestation, human settlement (immigration)

Africa VB (Muro and Mziray 1990, Fischer, Garms et al. 1997, Traore, Diarrassouba et al. 1997, Wilson, Cheke et al. 2002)

amphibian trematodiasis- echinostomiasis

Echinostoma trivolvis

helminth (trematode)

MHP amphibian-(Rana sylvatica and Hyla versicolor) duck, snail, canid

aquatic eutrophication, urbanization, agricultural development

N. America

trophic (Belden 2006, Koprivnikar, Baker et al. 2006, King, McLaughlin et al. 2007, Skelly, Bolden et al. 2007)

amphibiantrematodiasis

Riberoia ondatrae


MHP amphibian larvae, snail, bird

aquatic eutrophication

N. America

trophic (Johnson, Chase et al. 2007)

Amphibian helminth communities

Multiple species of amphibian trematodes and nematodes

helminth (trematode and nematode)

MHP amphibian Rana pipiens

wetland and agricultural development

N. America

trophic and direct

(Schotthoefer, Rohr et al. 2011)

schistosomiasis Schistosoma japonicum


MHP human, mammals

agricultural development, rice and

Eurasia trophic (Spear, Seto et al. 2004, Leonardo, Rivera et al. 2005,


irrigation, deforestation

Yang, Vounatsou et al. 2005, Wang, Chen et al. 2009)

schistosomiasis Schistosoma mansoni, Schistosoma hematobium


MHP human, snail

deforestation,urbanization, agricultural development (irrigation, rice), deforestation, dam building, land reclamation

Africa trophic (Muigai, Wasunna et al. 1989, el Sayed, Rizkalla et al. 1995, de Clercq, Vercruysse et al. 2000, Umeh, Amali et al. 2001, Njiokou, Yimta Tsemo et al. 2004, Yapi, Briet et al. 2005, Matthys, Vounatsou et al. 2006)

trematode communities-general

trematode helminth (trematode)

MHP avian, snail restoration of salt marshes

N. America

trophic (Huspeni and Lafferty 2004)

schistosomiasis and hookworm

Schistosoma sp and Ancylostoma

helminth (trematode, cestode)

MHP/ SHP

human, mammals, snail

urban farming, agricultural

Africa trophic and direct

(Matthys, Tschannen et al. 2007)

amphibian trematodiasis and nematodiasis

trematodes and nematodes, different species

helminth (trematode, cestode)

MHP/ SHP amphibian deforestation, agricultural development

N. America

trophic, direct (McKenzie 2007)

endoparasites, primates

Oesophagostomum sp, Cryptosporidum, Giardia, Strongyloides spp., Trichuris spp, Ascaris sp., Colobenterobius sp., cestode (Bertellia sp.),

helminth, protozoa

MHP Primates-colobus and red-tailed guenons

forest fragmentation, selective logging

Africa direct and trophic

(Gillespie and Chapman 2004, Gillespie, Chapman et al. 2005, Gillespie and Chapman 2006, Salzer, Rwego et al. 2007, Gillespie and Chapman 2008, Mbora, Wieczkowski et al. 2009, Bonnell, Sengupta et al. 2010, Hodder and Chapman 2012)

endoparasites, primates

Giardia spp., pinworm, helminth,

helminth, protozoa

MHP/ SHP howler monkey


N. America

direct and trophic

(Vitazkova and Wade 2006, Trejo-Macias, Estrada et al. 2007,


coccidia, trematode

Valdespino, Rico-Hernandez et al. 2010, Kowalewski, Salzer et al. 2011, Trejo-Macias and Estrada 2012)

Ectoparasites and endoparasites, and health, primates

Parasites, general Lice, helminth,bacteria

SHP/MHP Primate, Inri indri

Forest disturbance

Africa, Madagascar

direct, trophic (Junge, Barrett et al. 2011)

Endoparasites, deer Helminths, general

Helminth SHP/MHP Roe deer habitat fragmentation, agricultural development

Eurasia direct (Navarro-Gonzalez, Verheyden et al. 2011)

Chronic wasting disease

prion prion MHP deer (mule, white-tailed)

suburban development

N. America

direct (Farnsworth, Wolfe et al. 2005)

"Old World" leishmaniasis

Leismania major, L. turanica, L. gerbilli

protozoa MHP Wild and domestic mammals, humans

agricultural development, woodland use, agricultural development-deforestation and irrigation

Africa and Eurasia

VB (Ashford, Chance et al. 1976, Elhassan, Zijlstra et al. 1995, Thomson, Elnaiem et al. 1999, Wasserberg G 2003, Bhunia, Kesari et al. 2012)

Leishmaniasis, 'New World'

Leishmania mexicana, L. braziliensis L. chagasi L. panamensis, L. donovani

protozoa MHP Wild and domestic mammals

deforestation, urbanization, agricultural development, land resettlement

S.America, N. America

VB (Ready, Lainson et al. 1983, Mouchet, Le Pont et al. 1994, Kawa and Sabroza 2002, Costa, Werneck et al. 2005, Guerra, Ribeiro et al. 2006, Salomon, Sosa-Estani et al. 2006, Chaves, Cohen et al. 2008, Salomon, Acardi et al. 2009, Quintana, Salomon et al. 2010, Fernandez, Lestani et al. 2012)

Perkinsus Perkinsus marinus

protozoa MHP oysters urbanization N. America

direct (Gray, Bushek et al. 2009)

malaria vectors, general

Plasmodium protozoa SHP vertebrates deforestation, urbanization,

Oceania VB (Leisnham, Lester et al. 2006)


pastoralizationmalaria Plasmodium

falciparum, Plasmodium vivax, Plasmodium ovale, Plasmodium malariae

protozoa SHP human agricultural development(including irrigation and orchard) , deforestation,construction,social factors, rice plantation, human settlement, brick making, road building, wetland development, urbanization

N.America, S.America Africa, Eurasia, Oceania, Africa

VB (Lee, Atmosoedjono et al. 1980, Amerasinghe and Ariyasena 1990, Rosenberg, Andre et al. 1990, Amerasinghe, Amerasinghe et al. 1991, Ramasamy, De Alwis et al. 1992, Singh, Singh et al. 1996, Singh, Mehra et al. 1999, Lindblade K.A., Walker E. D. et al. 2000, Nanda, Yadav et al. 2000, Ataka, Ohtsuka et al. 2001, Conn, Wilkerson et al. 2002, Jacob, Regens et al. 2003, Carlson, Byrd et al. 2004, Keiser, Utzinger et al. 2004, Klinkenberg, van der Hoek et al. 2004, Mutero, Kabutha et al. 2004, Afrane, Lawson et al. 2005, Antonio-Nkondjio, Simard et al. 2005, Kebede, McCann et al. 2005, Krishnamoorthy, Jambulingam et al. 2005, Leonardo, Rivera et al. 2005, Sattler, Mtasiwa et al. 2005, Afrane, Zhou et al. 2006, de Castro, Monte-MÃ³r et al. 2006, Grieco, Johnson


et al. 2006, Munga, Minakawa et al. 2006, Vasconcelos, Novo et al. 2006, Vittor, Gilman et al. 2006, Yanoviak, Paredes et al. 2006, Afrane, Zhou et al. 2007, Vanwambeke, Lambin et al. 2007, Yasuoka and Levins 2007, Zhou, Munga et al. 2007, Klinkenberg, McCall et al. 2008, Turell, Sardelis et al. 2008, Saraiva, Amorim et al. 2009, Olson, Gangnon et al. 2010, Wayant, Maldonado et al. 2010, Krefis, Schwarz et al. 2011)

Trypanosomiasis, African

Trypanosoma brucei, other Trypanosoma spp

protozoa MHP mammals anthropogenic land use and agricultural development

Africa VB (Dagnogo, Yapi et al. 1997, bde La Rocque, Augusseau et al. 2001, Cecchi, Mattioli et al. 2008, Ducheyne, Mweempwa et al. 2009)

Trypanosomiasis American (Chagas disease)

Trypanosoma cruzi

Protozoa MHP mammals forest fragmentation, deforestation, agricultural development, urbanization

S. America, N. America

VB (Teixeira, Monteiro et al. 2001, Ceballos, Cardinal et al. 2006, Vaz, D'Andrea et al. 2007, Abad-Franch, Ferraz et al. 2010, Maloney, Newsome et al. 2010, Gottdenker, Calzada et al. 2011, Gottdenker, Chaves et


al. 2012, Moreno, Hoyos et al. 2012)

Trypanosomes, bats Trypanosoma spp.

protozoa MHP bats forest fragmentation

N. America

VB (Cottontail, Wellinghausen et al. 2009)

Trypanosomiasis, wild and domestic animals

Trypanosomiasis, wild and domestic animals

protozoa MHP mammals cattle ranching S. America

VB (Herrera, Rademaker et al. 2007)

Hemoparasites-reptile hemogregarine protozoa NS Reptile-lizard

forest degradation

Eurasia VB (Amo, Lopez et al. 2007)

hemoparasites, avian Plasmodium, Haemoproteus

protozoa MHP/ SHP passerine birds

deforestation, urbanization

N. America, Africa

VB (Geue and Partecke 2008, Bonneaud, Sepil et al. 2009, Chasar, Loiseau et al. 2009, Fokidis, Greiner et al. 2009)

Toxoplasmosis Toxoplasma gondii

protozoa MHP vertebrate- felids reservoirs affecting sea otters

agricultural development, urbanization, runoff

N. America

trophic (Miller, Miller et al. 2008, Lehrer, Fredebaugh et al. 2010)

MSX and dermo Dermo –Perkinsus marinum, MSX- Haplosporidium nelsoni

protozoa MHP Oysters

habitat loss

N. America

direct (Wilberg, Livings et al. 2011)

Cryptosporidiosis Cryptosporidium spp.

protozoa MHP cattle, other mammals


N. America

direct (Ziegler, Wade et al. 2007)

malaria and schistosomiasis

Plasmodium and Schistosoma

protozoa and trematode

SHP/ MHP human agricultural development

Eurasia VB and trophic

(Leonardo, Rivera et al. 2005)

diarrheal pathogens, general

Giardia, E.coli, rotaviruses

protozoa, bacteria, virus

SHP/ MHP human road building S. America

direct (Eisenberg, Cevallos et al. 2006)

Malaria and dengue Plasmodium spp., dengue virus

protozoa, virus

SHP human agricultural development

Eurasia VB (Vanwambeke, Lambin et al. 2007)

Yellow fever arbovirus, Flavivirus

virus MHP human and nonhuman

deforestation S. America

VB (Ribeiro and Antunes 2009)


primatesDengue Dengue virus Virus SHP Humans Horticulture, rice

paddies, agricultural development

Eurasia VB (Vanwambeke, Bennett et al. 2011, Sarfraz, Tripathi et al. 2012)

West Nile Virus Flaviviridae, Flavivirus

virus MHP vertebrates urbanization, suburbanization, deforestationeri

N. America

VB (Gibbs, Wimberly et al. 2006, Bradley, Gibbs et al. 2008, Gomez, Kilpatrick et al. 2008, Ozdenerol, Bialkowska-Jelinska et al. 2008, Wimberly, Hildreth et al. 2008, Gates and Boston 2009, Eisen, Barker et al. 2010, Trawinski and Mackay 2010, Bowden, Magori et al. 2011, LaDeau, Calder et al. 2011, Liu, Weng et al. 2011, Rochlin, Turbow et al. 2011, Chuang, Hockett et al. 2012, Hamer, Lehrer et al. 2012, Johnson, Munafo et al. 2012)

Tick borne encephalitis

Flavivirus virus MHP small rodents, livestock

forest fragmentation, logging

Eurasia VB (Vanwambeke, Sumilo et al. 2010)

Louping ill Flavivirus Virus MHP Sheep, red grouse, humans

habitat fragmentation

Eurasia VB (Jones, Webb et al. 2011)

Hantavirus hantavirus virus MHP wild rodents habitat fragmentation, forest fragmentation, agricultural development, deforestation

N. America

direct (Langlois, Fahrig et al. 2001, Ruedas, Salazar-Bravo et al. 2004, Savory, Cuevas et al. 2006, Suzan, Giermakowski et al. 2006, Suzan, Marce et al. 2008)


Rabies rhabdovirus virus MHP bats, mammals

agricultural development, forest fragmentation

S. America

direct (Gomes, Monteiro et al. 2010)

Venezuelan equine encephalitis

Togaviridae, alphavirus

virus MHP mammals, birds

deforestation S. America

VB (Barrera, Torres et al. 2001)

Eastern equine encephalitis

Togaviridae, alphavirus

Virus MHP Birds, mammals

Natural resource extraction/forestry

N. America

VB (Kelen, Downs et al. 2012)

Chikungunya Chikungunya virus

virus MHP Multiple species

Deforestation, human settlement, agricultural development

Africa VB (Diallo, Sall et al. 2012)

Ross river virus Togaviridae Alphavirus

Virus MHP Mammals Agricultural development, land clearing

Oceania VB (Jardine, Speldewinde et al. 2008)

Crimean-congo hemorrhagic fever

Bunyaviridae, Nairovirus

virus MHP multiple species wild and domestic animals

fragmentation of agricultural land between forests and shrubs, forest fragmentation

Eurasia VB (Estrada-Pena, Zatansever et al. 2007, Estrada-Pena, Vatansever et al. 2010)

Bluetongue virus Orbivirus Virus MHP ruminants agricultural development

N. America

VB (Mayo, Gardner et al. 2012)

Feline Immunodeficiency virus

Retrovirus Virus MHP Felids urbanization, habitat fragmentation

N. America

Direct (Lee, Ruell et al. 2012)

Sea-turtle fibropapillomatosis

Herpesvirus-associated

virus MHP (sea turtles)

sea turtle urbanization, aquatic eutrophication

Oceania direct (Van Houtan, Hargrove et al. 2010)

Avian pox Poxvirus Virus MHP avian Agricultural development

Galapagos Direct and VB (Zylberberg, Lee et al. 2013)

Avian Influenza, Highly Pathogenic

influenza, Orthomyxovirus

virus MHP avian agricultural development

Eurasia direct (Gilbert, Xiao et al. 2007)

Hendravirus Hendravirus Virus MHP Bat Urbanization Oceania direct (Plowright, Foley et al. 2011)

Puumala virus Puumala virus virus MHP bank vole forest Eurasia direct (Linard, Tersago et al.


fragmentation, deforestation

2007, Tersago, Schreurs et al. 2008)

Rabies lyssavirus virus MHP Mammals-raccoons

deforestation N. America

direct (Jones, Curns et al. 2003, Recuenco, Eidson et al. 2008)

Mosquito-borne disease-general

various virus, protozoa

MHP/ SHP vertebrates agricultural development, rice cultivation and irrigation, deforestation, irrigation

S. America, Eurasia

VB (Amerasinghe and Ariyasena 1991, Forattini, Kakitani et al. 1993, Forattini and Massad 1998, Mukhtar, Herrel et al. 2003, Jacups, Warchot et al. 2012, Steiger, Johnson et al. 2012)

MHP-multihost pathogen, SHP-single host pathogen.


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