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What do we know about parasites of wildlife in high biodiversity areas with anthropogenic disturbance? The special case of Mexico

Published online by Cambridge University Press:  26 January 2019

C. I. Muñoz-García ,
E. Berriatua  and
C. Martínez-Carrasco
C. I. Muñoz-García*
Affiliation:
Departamento de Sanidad Animal, Facultad de Veterinaria, Regional Campus of International Excellence “Campus Mare Nostrum”, Universidad de Murcia, 30100 Murcia, Spain Departamento de Producción Agrícola y Animal, Universidad Autónoma Metropolitana, Calzada del Hueso 1100, Col. Villa Quietud, Delegación Coyoacán, 04960 Ciudad de México, Mexico
E. Berriatua
Affiliation:
Departamento de Sanidad Animal, Facultad de Veterinaria, Regional Campus of International Excellence “Campus Mare Nostrum”, Universidad de Murcia, 30100 Murcia, Spain
C. Martínez-Carrasco
Affiliation:
Departamento de Sanidad Animal, Facultad de Veterinaria, Regional Campus of International Excellence “Campus Mare Nostrum”, Universidad de Murcia, 30100 Murcia, Spain
*
Author for correspondence: C. I. Muñoz-García, Departamento de Sanidad Animal, Facultad de Veterinaria, Regional Campus of International Excellence “Campus Mare Nostrum”, Universidad de Murcia, 30100 Murcia, Spain. E-mail: [email protected]
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Abstract

The continual rise of anthropogenic disturbance of ecosystems has been associated with an increasing incidence of emerging diseases. The largest amount of data on emerging diseases relates to bacterial and viral pathogens, but there is a lack of parasite data, especially from wildlife. Monitoring wildlife parasitic diseases should be considered a priority, especially in high biodiversity regions with strong anthropogenic impacts, like Mexico, where the wildlife/livestock/human interface is associated with increased risk of disease transmission. Mexico belongs to the top-ten megadiverse countries and is located between two biogeographic regions. This situation makes Mexico a favourable region for the spillover of animal pathogens to human beings, causing pandemics, such as the one recently caused by influenza virus A (H1N1). The current state of knowledge of Mexican wildlife parasites is scarce and focuses mainly in Neotropical fauna. Moreover, this knowledge is heterogeneous for different parasite groups, especially concerning their pathologic effects and epidemiology. The goals of this review are to compile information on Mexican wildlife parasites and to identify knowledge gaps in order to stimulate research on pending epidemiological, public health, ecological and pathological areas, and to encourage the creation of more specialized groups from the perspective of the One-Health concept.

Keywords

Biodiversityemerging diseasesextinctionmegadiverseOne healthzoonoses
Type
Review Article
Information
Animal Health Research Reviews , Volume 19 , Issue 2 , December 2018 , pp. 155 - 161
Copyright
Copyright © Cambridge University Press 2019 

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References

Abbott, I (2006) Mammalian faunal collapse in Western Australia, 1875–1925: the hypothesised role of epizootic disease and a conceptual model of its origin, introduction, transmission, and spread. Australian Journal of Zoology 33, 530–561.Google Scholar
Acosta-Gutiérrez, R (2014) Biodiversidad de Siphonaptera en México. Revista Mexicana de Biodiversidad 85, 345–352.Google Scholar
Barnes, TS, Morton, JM and Coleman, GT (2007) Clustering of hydatid infection in macropodids. International Journal for Parasitology 37, 943–952.Google Scholar
Berzunza-Cruz, M, Rodríguez-Moreno, Á, Gutiérrez-Granados, G, González-Salazar, C, Stephens, CR, Hidalgo-Mihart, M, Marina, CF, Rebollar-Téllez, EA, Bailón-Martínez, D, Domingo-Bacells, C, Ibarra-Cerdeña, CN, Sánchez-Cordero, V and Becker, I (2015) Leishmania (L.) mexicana infected bats in Mexico: novel potential reservoirs. PLoS Neglected Tropical Diseases 9, e0003438.Google Scholar
Brearley, G, Rhodes, J, Bradley, A, Baxter, G, Seabrook, L, Lunney, D, Liu, Y and Mcalpine, C (2013) Wildlife disease prevalence in human-modified landscapes. Biological Reviews 88, 427–442.Google Scholar
Chomel, BB (2008) Control and prevention of emerging parasitic zoonoses. International Journal for Parasitology 38, 1211–1217.Google Scholar
Davidson, R, Simard, M, Kutz, SJ, Kapel, CMO, Hamnes, IS and Robertson, LJ (2011) Arctic parasitology: why should we care? Trends in Parasitology 27, 239–245.Google Scholar
Flores-Rangel, JA (2015) Infraestructura carretera: construcción, financiamiento y resistencia en México y América. Latina. Revista Transporte y Territorio 13, 122–148.Google Scholar
García-Prieto, L, García-Varela, M, Mendoza-Garfias, B and Pérez-Ponce de León, G (2010) Checklist of the Acanthocephala in wildlife vertebrates of Mexico. Zootaxa 2419, 1–50.Google Scholar
Gómez, A and Nichols, E (2013) Neglected wild life: parasitic biodiversity as a conservation target. International Journal for Parasitology: Parasites and Wildlife 2, 222–227.Google Scholar
Gordillo-Chávez, EJ, Mata-Zayas, EE, García-Morales, R, Morales-Garduza, MA, Villanueva-García, C and Valdez-Leal, JD (2015) Mastofauna del humedal Chaschoc-Sejá en Tabasco, México. Therya 6, 535–544.Google Scholar
Gottdenker, NL, Streicker, DG, Faust, CL and Carroll, CR (2014) Anthropogenic land use change and infectious diseases: a review of the evidence. EcoHealth 11, 619–632.Google Scholar
Graczyk, TK, DaSilva, AJ, Cranfield, MR, Nizeyi, JB, Kalema, GRNN and Pieniazek, N (2001) Cryptosporidium parvum genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. Parasitology Research 87, 368–370.Google Scholar
Graczyk, TK, Bosco-Nizeyi, J, Ssebide, B, Thompson, RCA, Read, C and Cranfield, MR (2002) Anthropozoonotic Giardia duodenalis genotype (assemblage) A infections in habitats of free-ranging human-habituated gorillas, Uganda. Journal of Parasitology 88, 905–909.Google Scholar
Grogan, LF, Berger, L, Rose, K, Grillo, V, Cashins, SD and Skerratt, LF (2014) Surveillance for emerging biodiversity diseases of wildlife. PLoS Pathogens 10, e1004015.Google Scholar
Grosselet, M, Villa-Bonilla, B and Michael, GR (2009) Afectaciones a vertebrados por vehículos motores en 1.2 km de carretera en el Istmo de Tehuantepec. Proceedings of the Fourth International Partners in Flight Conference: Tundra to Tropics, pp. 271–231.Google Scholar
Guberti, V, Stancampiano, L and Ferrari, N (2014) Surveillance, monitoring and surveys of wildlife diseases: a public health and conservation approach. Hystrix 25, 3–8.Google Scholar
Hidalgo-Mihart, MG, Contreras-Moreno, FM, de la Cruz, AJ, Jiménez-Domínguez, D, Juárez-López, R, Oporto-Peregrino, R and Ávila-Flores, R (2016) Mammals of Tabasco, Mexico. In Briones-Salas, M, Hortelano-Moncada, Y, Magaña-Cota, G, Sánchez-Rojas, G and Sosa-Escalante, JE (eds), Riqueza y Conservación de los Mamíferos en México a Nivel Estatal. México: Ciudad de México, pp. 441–472.Google Scholar
Hotez, PJ, Brindley, PJ, Bethony, JM, King, CH, Pearce, EJ and Jacobson, J (2008) Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 1311–1321.Google Scholar
Íñigo, E (1999) Los buitres mexicanos. CONABIO. Biodiversitas 22, 1–8.Google Scholar
Interinstitutional Group of Mexican Postgraduate Students (2017) CONACYT's freeze on postgraduate fellowships in Mexico. The Lancet 389, 2373–2374.Google Scholar
Jaramillo, M, Rohrer, S and Parker, PG (2017) From Galapagos doves to passerines: spillover of Haemoproteus multipigmentatus. International Journal for Parasitology: Parasites and Wildlife 6, 155–161.Google Scholar
Kerr, CL, Bhattacharyya, T, Xavier, SCC, Barros, JH, Lima, VS, Jansen, AM and Miles, MA (2016) Lineage-specific serology confirms Brazilian Atlantic forest lion tamarins, Leontopithecus chrysomelas and Leontopithecus rosalia, as reservoir hosts of Trypanosoma cruzi II (TcII). Parasites & Vectors 9, 584.Google Scholar
Kutz, SJ, Hoberg, EP, Nagy, J, Polley, L and Elkin, B (2004) ‘Emerging’ parasitic infections in arctic ungulates. Integrative and Comparative Biology 44, 109–118.Google Scholar
Labruna, MB, Costa, FB, Port-Carvalho, M, Oliveira, AS, Souza, SLP and Castro, MB (2018) Lethal fascioliasis in capybaras (Hydrochoerus hydrochaeris) in Brazil. The Journal of Parasitology 104, 173–176.Google Scholar
Lafferty, KD (2014) Biodiversity loss and infectious diseases. In Verdad, LM, Lyra-Jorge, MC and Piña, CI (eds), Applied Ecology and Human Dimensions in Biological Conservation. New York: Springer Berlin Heidelberg, pp. 73–89.Google Scholar
Lafferty, KD, Allesina, S, Arim, M, Briggs, CJ, De Leo, G, Dobson, AP, Dunne, JA, Johnson, PTJ, Kuris, AM, Marcogliese, DJ, Martinez, ND, Memmott, J, Marquet, PA, McLaughlin, JP, Mordecai, EA, Pascual, M, Poulin, R and Martinez, ND (2008) Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.Google Scholar
Lawson, B, Petrovan, SO and Cunningham, AA (2015) Citizen science and wildlife disease surveillance. EcoHealth 12, 693–702.Google Scholar
Martin, RW, Handasyde, KA and Skerratt, LF (1998) Current distribution of sarcoptic mange in wombats. Australian Veterinary Journal 76, 411–414.Google Scholar
Martínez-Hernández, F, Rendón-Franco, E, Gama-Campillo, LM, Villanueva-García, C, Romero-Valdovinos, M, Maravilla, P, Alejandre-Aguilar, R, Rivas, N, Córdoba-Aguilar, A, Muñoz-García, CI and Villalobos, G (2014) Follow up of natural infection with Trypanosoma cruzi in two mammals species, Nasua narica and Procyon lotor (Carnivora: Procyonidae): evidence of infection control? Parasites & Vectors 7, 405.Google Scholar
Martínez-Hernández, F, López-Díaz, O, Bello-Bedoy, R, Villalobos, G, Muñoz-García, CI, Alejandre-Aguilar, R, Córdoba-Aguilar, A, Gutiérrez-Cabrera, AE, Suzán, G, Villanueva-García, C, Gama-Campillo, LM, Díaz-Negrete, MT and Rendón-Franco, E (2016) Possible differences in the effects of Trypanosoma cruzi on blood cells and serum protein of two wildlife reservoirs. Vector Borne and Zoonotic Diseases 16, 709–716.Google Scholar
Mey, E and González-Acuña, D (2000) A new genus and species of Ischnocera (Insecta, Phthiraptera) of Chimango Caracara Milvago chimango from Chile with annotated checklist of chewing lice parasitizing caracaras (Aves, Falconiformes, Falconidae). Rudolstädter Naturhistorische Schriften 10, 59–73.Google Scholar
Miller, RS, Farnsworth, ML and Malmberg, JL (2013) Diseases at the livestock–wildlife interface: status, challenges, and opportunities in the United States. Preventive Veterinary Medicine 110, 119–132.Google Scholar
Mörner, T, Obendorf, DL, Artois, M and Woodford, MH (2002) Surveillance and monitoring of wildlife diseases. Revue Scientifique Et Technique 21, 67–76.Google Scholar
Morse, SS, Mazet, JA, Woolhouse, M, Parrish, CR, Carroll, D, Karesh, WB, Zambrana-Torrelio, C, Lapkin, WI and Daszak, P (2012) Prediction and prevention of the next pandemic zoonosis. The Lancet 380, 1956–1965.Google Scholar
Olson, DM, Dinerstein, E, Wikramanayake, ED, Burgess, ND, Powell, GV, Underwood, EC, D´Amico, JA, Itoua, I, Strand, HE, Morrison, JC, Loucks, CJ, Allnutt, TF, Ricketts, TH, Kura, Y, Lamoreux, JF, Wettengel, WW, Hedao, P and Kassem, KR (2001) Terrestrial ecoregions of the world: a new map of life on earth a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience 51, 933–938.Google Scholar
Paknia, O, Rajaei, S and Koch, A (2015) Lack of well-maintained natural history collections and taxonomists in megadiverse developing countries hampers global biodiversity exploration. Organisms Diversity & Evolution 15, 619–629.Google Scholar
Pedersen, AB and Fenton, A (2015) The role of antiparasite treatment experiments in assessing the impact of parasites on wildlife. Trends in Parasitology 31, 200–211.Google Scholar
Pérez-Padilla, R, de La Rosa-Zamboni, D, Ponce de Leon, S, Hernandez, M, Quiñones-Falconi, F, Bautista, E, Ramirez-Venegas, A, Rojas-Serrano, J, Ormsby, CE, Corrales, A, Higuera, A, Mondragon, E and Cordova-Villalobos, JA (2009) Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico. The New England Journal of Medicine 361, 680–689.Google Scholar
Pérez-Ponce de León, G and García-Prieto, L (2001) Los parásitos en el contexto de la biodiversidad y la conservación. Biodiversitas: Journal of Biological Diversity 34, 11–15.Google Scholar
Pérez-Ponce de León, G, García-Prieto, L and Razo-Mendivil, U (2002) Species richness of helminth parasites in Mexican amphibians and reptiles. Diversity & Distribution 8, 211–218.Google Scholar
Pérez-Ponce de León, G, García-Prieto, L and Mendoza-Garfias, B (2007) Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534, 1–238.Google Scholar
Pérez-Ponce de León, G, García-Prieto, L and Mendoza-Garfias, B (2011) Describing parasite biodiversity: the case of the helminth fauna of wildlife vertebrates in Mexico. In Grill, O and Gianfranco, V (eds), Changing Diversity in Changing Environment. Rijeka, Croatia: InTech, pp. 33–54.Google Scholar
Phillips, RB, Cooke, BD, Carrión, V and Snell, HL (2012) Eradication of rock pigeons, Columba livia, from the Galápagos Islands. Biological Conservation 147, 264–269.Google Scholar
Pinkus-Rendón, MJ and Contreras-Sánchez, A (2012) Impacto socioambiental de la industria petrolera en Tabasco: el caso de la Chontalpa. LiminaR. Estudios Sociales y Humanísticos 10, 122–144.Google Scholar
Pomerantz, J, Rasambainarivo, FT, Dollar, L, Rahajanirina, LP, Andrianaivoarivelo, R, Parker, P and Dubovi, E (2016) Prevalence of antibodies to selected viruses and parasites in introduced and endemic carnivores in western Madagascar. Journal of Wildlife Diseases 52, 544–552.Google Scholar
Pozo-Montuy, G and Pozo-Juárez, F (2008) Las carreteras y su impacto sobre la fauna silvestre en una región de la cuenca baja del río Usumacinta. In Sánchez, AJ, Hidalgo-Mihart, MG, Arriaga-Weiss, SL and Contreras-Sánchez, WM (eds), Zoología Mexicana. Villahermosa, Mexico: DACBiol-Universidad Juárez Autónoma de Tabasco, pp. 253–265.Google Scholar
Presupuesto de Egresos de la Federación para el Ejercicio Fiscal 2014 (2014) Diario Oficial. Tercera Sección, pp. 1–112.Google Scholar
Randall, NJ, Blitvich, BJ and Blanchong, JA (2012) Efficacy of wildlife rehabilitation centers in surveillance and monitoring of pathogen activity: a case study with West Nile Virus. Journal of Wildlife Diseases 48, 646–653.Google Scholar
Rendón-Franco, E, Caso, A, Jiménez-Sánchez, NJ, Carvajal-Villareal, S and Zepeda-López, H (2014 a) Frequency of antibodies against Toxoplasma gondii in wild carnivores and marsupials in northeast Mexico. Neotropical Helminthology 8, 473–478.Google Scholar
Rendón-Franco, E, Muñoz-García, CI, Romero-Callejas, E, Moreno-Torres, K and Suzán, G (2014 b) Effect of host species diversity on multiparasite systems in rodent communities. Parasitology Research 113, 447–450.Google Scholar
Rendón-Franco, E, Xocoténcatl-García, L, Rico-Torres, CP, Muñoz-García, CI, Caso-Aguilar, A, Suzán, G, Correa, D and Caballero-Ortega, H (2014 c) Toxoplasmosis seroprevalence in wild small rodents, potentially preys of ocelots in north-eastern Mexico. Parasite 21, 57.Google Scholar
Rhyan, JC and Spraker, TR (2010) Emergence of diseases from wildlife reservoirs. Veterinary Pathology 47, 34–39.Google Scholar
Rovirosa-Hernández, MDJ, Cortes-Ortíz, L, García-Orduña, F, Guzmán-Gómez, D, López-Monteon, A, Caba, M and Ramos-ligonio, A (2013) Seroprevalence of Trypanosoma cruzi and Leishmania mexicana in free-ranging howler monkeys in Southeastern Mexico. American Journal of Primatology 75, 161–169.Google Scholar
Rózsa, L and Vas, Z (2014) Co-extinct and critically co-endangered species of parasitic lice, and conservation-induced extinction: should lice be reintroduced to their hosts? Oryx 49, 107–110.Google Scholar
Ruiz-Piña, HA and Cruz-Reyes, A (2002) The opossum Didelphis virginiana as a synanthropic reservoir of Trypanosoma cruzi in Dzidzilché, Yucatán, México. Memórias do Instituto Oswaldo Cruz 97, 613–620.Google Scholar
Santiago-Alarcon, D, Outlaw, DC, Ricklefs, RE and Parker, PG (2010) Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove. International Journal for Parasitology 40, 463–470.Google Scholar
Shi, H, Singh, A, Kant, S, Zhu, Z and Waller, E (2005) Integrating habitat status, human population pressure, and protection status into biodiversity conservation priority setting. Conservation Biology 19, 1273–1285.Google Scholar
Sleeman, JM, Brand, CJ and Wright, SD (2012) Strategies for wildlife diseases surveillance. In Aguirre, AA, Ostfield, RS and Daszak, P (eds), New Directions in Conservation Medicine: Applied Cases in Ecological Health. New York: Oxford University Press, pp. 539–551.Google Scholar
Sukhdeo, MVK (2012) Where are the parasites in food webs? Parasites & Vectors 5, 239.Google Scholar
Suzan, G and Ceballos, G (2005) The role of feral mammals on wildlife infectious disease prevalence in two nature reserves within Mexico City limits. Journal of Zoo and Wildlife Medicine 36, 479–484.Google Scholar
Thompson, RA (2013) Parasite zoonoses and wildlife: one health, spillover and human activity. International Journal for Parasitology 43, 1079–1088.Google Scholar
Thompson, RC, Kutz, SJ and Smith, A (2009) Parasite zoonoses and wildlife: emerging issues. International Journal of Environmental Research and Public Health 6, 678–693.Google Scholar
Vander Wal, E, Garant, D, Calmé, S, Chapman, CA, Festa-Bianchet, M, Millien, V, Rioux-Paquette, S and Pelletier, F (2014) Applying evolutionary concepts to wildlife disease ecology and management. Evolutionary Applications 7, 856–868.Google Scholar
Vargas-Sanchez, GB, Romero-Valdovinos, M, Ramirez-Guerrero, C, Vargas-Hernandez, I, Ramirez-Miranda, ME, Martinez-Ocaña, J, Valadez, A, Ximenez, C, Lopez-Escamilla, E, Hernandez-Campos, ME, Villalobos, G, Martinez-Hernandez, F and Maravilla, P (2015) Blastocystis isolates from patients with irritable bowel syndrome and from asymptomatic carriers exhibit similar parasitological loads, but significantly different generation times and genetic variability across multiple subtypes. PLoS ONE 10, e0124006.Google Scholar
Villanueva-Garcia, C, Gordillo-Chavez, EJ, Lopez-Escamilla, E, Rendon-Franco, E, Muñoz-Garcia, CI, Gama, L, Martinez-Flores, WA, Gonzalez-Rodriguez, N, Romero-Valdovinos, M, Diaz-Lopez, H and Galian, J (2017 a) Clarifying the cryptic host specificity of Blastocystis spp. isolates from Alouatta palliata and A. pigra howler monkeys. PLoS ONE 12, e0169637.Google Scholar
Villanueva-García, C, Gordillo-Chávez, EJ, Baños-Ojeda, C, Rendón-Franco, E, Muñoz-García, CI, Carrero, JC, Córdoba-Aguilar, A, Maravilla, P, Galian, J, Martínez-Hernández, F and Villalobos, G (2017 b) New Entamoeba group in howler monkeys (Alouatta spp.) associated with parasites of reptiles. Parasitology Research 116, 2341–2346.Google Scholar
Weston, MK and Memon, MA (2009) The illegal parrot trade in Latin America and its consequences to parrot nutrition, health and conservation. Bird Populations Journals 9, 76–83.Google Scholar
Whitaker, JO Jr and Morales-Malacara, JB (2005) Ectoparasites and other associates (Ectodytes) of mammals of Mexico. In Sánchez-Cordero, V and Medellín, RA (eds), Contribuciones mastozoológicas en homenaje a Bernardo Villa. México, DF: Instituto de Biología e Instituto de Ecología, Universidad Nacional Autónoma de México y Conabio, pp. 535–666.Google Scholar
Zamora-Ledesma, S, Hernández-Camacho, N, Villagrán-Herrera, ME, Sánchez-Moreno, M, Concha-Valdez, FG, Jones, RW, Moreno-Pérez, A and Camacho-Macías, B (2016) Presence of trypanosomatid antibodies in gray foxes (Urocyon cinereoargenteus) and domestic and feral dogs (Canis lupus familiaris) in Queretaro, Mexico. Veterinary Parasitology Regional Studies and Case Reports 5, 25–30.Google Scholar