Skip to main content

Advertisement

SpringerLink
Log in

Environmental Factors Influencing the Occurrence of Unhealthy Tapirs in the Southern Yucatan Peninsula

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Information about the effects of environmental degradation on the health of terrestrial forest wildlife is limited, especially for rare species. In this study, we analyse the influence of ecological factors such as landscape characteristics and seasonality on the health status of Baird’s tapirs in Calakmul, Mexico. We collected georeferenced photographic records of healthy (n = 32) and unhealthy (n = 22) tapirs from 2008 to 2019 and characterized landscape composition around each record at three spatial scales (circular buffers of 1, 2 and 3-km radii according to Baird’s tapir home ranges). Our logistic model building process consisted in selecting the best spatial scale for each landscape cover class, before including them along with distance to human settlements and seasonality in a full model. The model that best explained the occurrence of unhealthy tapirs included the percentage of agriculture within a 1-km radius. This study hints at the negative effect that land-use change to agriculture occurring in Calakmul might have on tapir health, with 95.45% of unhealthy tapirs recorded in such landscapes. Further studies should investigate the proximate determinants of tapir health in anthropogenic landscapes, which might be linked to stress or to contact with domestic animals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Acevedo-Whitehouse K, Duffus ALJ (2009) Effects of environmental change on wildlife health. Philosophical Transactions of the Royal Society B: Biological Sciences 364:3429–3438. doi:10.1098/rstb.2009.0128

    Article  Google Scholar 

  • Achard F, Eva HD, Stibig H-J, Mayaux P, Gallego J, Richards T, Malingreau JP (2002) Determination of deforestation rates of the world’s humid tropical forests. Science 297:999–1002. doi:10.1126/science.1070656

    Article  CAS  PubMed  Google Scholar 

  • Becker DJ, Streicker DG, Altizer S (2015) Linking anthropogenic resources to wildlife-pathogen dynamics: a review and meta-analysis. Ecology letters 18:483–495. doi:10.1111/ele.12428

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22:95–102. doi:10.1016/j.tree.2006.11.001

    Article  PubMed  Google Scholar 

  • Burgman MA, Ferson S, Akcakaya HR (1993) Risk assessment in conservation biology. London: Chapman and Hall

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: A practical information-theoretic approach. New York: Springer

    Google Scholar 

  • Ceballos G, Chávez C, Rivera A, Manterola C (2002) Tamaño poblacional y conservación del jaguar en la reserva de la biosfera de Calakmul, Campeche, México. In: El jaguar en el nuevo milenio, Medellín RA, Equihua CA, Chetkiewicz CL, Crawshaw P, Rabinowitz A, Redford KH, Robinson JG, Sanderson EW, Taber A (editors), México: Fondo de cultura económica FCE-Universidad Nacional Autónoma de México UNAM-Wildlife Conservation Society, pp. 403–417

    Google Scholar 

  • Chapman CA, Balcomb SR, Gillespie TR, Skorupa JP, Struhsaker TT (2000) Long-term effects of logging on African primate communities: a 28-year comparison from Kibale National Park, Uganda. Conservation Biology 14:207–217

    Article  Google Scholar 

  • Comisión Nacional del Agua (CONAGUA) (2019) Servicio Meteorológico Nacional. Reporte Meteorológico para la Agricultura, 2019. Available: https://smn.conagua.gob.mx/tools/DATA/Formularios/Reporte%20Meteorol%C3%B3gico%20para%20la%20Agricultura/Reporte%20Meteorol%C3%B3gico%20para%20la%20Agricultura_1136.pdf [accessed August 17, 2019]

  • Cottontail VM, Wellinghausen N, Kalko EKV (2009) Habitat fragmentation and haemoparasites in the common fruit bat, Artibeus jamaicensis (Phyllostomidae) in a tropical lowland forest in Panama. Parasitology 136:1133–1145. doi:10.1017/S0031182009990485

    Article  CAS  PubMed  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife threats to biodiversity and human health. Science 287:443–449. doi:10.1126/science.287.5452.443

    Article  CAS  PubMed  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78:103–116. doi:10.1016/s0001-706x(00)00179-0

    Article  CAS  Google Scholar 

  • Deem SL, Karesh WB, Weisman W (2001) Putting theory into practice: wildlife health in conservation. Conservation Biology 15:1224–1233. doi:10.1111/j.1523-1739.2001.00336.x

    Article  Google Scholar 

  • Dupuy-Rada JM, Durán-García R, García-Contreras G, Arellano-Morín J, Acosta-Lugo E, Méndez-González ME, et al. (2015) Conservation and use. In: Biodiversity and Conservation of the Yucatán Peninsula, Islebe GA, Calmé S, León-Cortés JL, Schmook B (editors), Switzerland: Springer, pp. 169–196

    Chapter  Google Scholar 

  • Easterling DR, Meehl GA, Parmesan C, Chagnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074. doi:10.1126/science.289.5487.2068

    Article  CAS  PubMed  Google Scholar 

  • Ericson J, Freudenberger MS, Boege E (1999) Population dynamics, migration, and the future of the Calakmul Biosphere Reserve. Program on Population and Sustainable Development (PSD), American Association for the Advancement of Science (AAAS)

  • ESRI (2014) ArcGIS Desktop: release 10.3. Redlands: Environmental Systems Research Institute

    Google Scholar 

  • Fernandes-Santos RC, Medici EP, Testa-Jose C, Micheletti T (2020) Health assessment of wild lowland tapirs (Tapirus terrestris) in the highly threatened Cerrado biome, Brazil. Journal of Wildlife Diseases 56:34–46. doi:10.7589/2018-10-244

    Article  CAS  PubMed  Google Scholar 

  • Foerster CR, Vaughan C (2002) Home range, habitat use, and activity of Baird’s tapir in Costa Rica. Biotropica 34:423–437. doi:10.1111/j.1744-7429.2002.tb00556.x

    Article  Google Scholar 

  • Fox J, Weisberg S, Adler D, Bates D, Baud-Bovy G, Ellison S, et al. (2016) Package ‘Car.’ Available:https://cran-r.project.org/web/packages/car/car.pdf [accesed July 13, 2019]

  • Furtado MM, Jácomo ATA, Kashivakura CK, Torres NM, Marvulo MFV, Ragozo AMA, et al. (2010) Serologic survey for selected infectious diseases in free-ranging Brazilian tapirs (Tapirus terrestris) in the Cerrado of Central Brazil. Journal of Zoo and Wildlife Medicine 41:133–136

    Article  Google Scholar 

  • García M, Jordan C, O'Farril G, Poot C, Meyer N, Estrada N, et al. (2016) Tapirus bairdii. The IUCN Red List of Threatened Species, e.T21471A45173340. https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T21471A45173340.en

  • García-Gil G, Palacio JL, Ortiz MA (2002) Reconocimiento geomorfológico e hidrográfico de la Reserva de la Biosfera Calakmul, México. Investigaciones Geográficas 48:7–23

    Google Scholar 

  • Gonzalez-Abraham A, Schmook B, Calmé S (2007) Spatio-temporal distribution of forest extractive activities in Caoba ejido, Quintana Roo. Investigaciones Geográficas 62:69–86

    Google Scholar 

  • Goodrich JM, Seryodkin I, Miquelle DG, Bereznuk SL (2011) Conflicts between Amur (Siberian) tigers and humans in the Russian Far East. Biological Conservation 144:584–592. doi:10.1016/j.biocon.2010.10.016

    Article  Google Scholar 

  • Hernandez-Divers S, Bailey J, Aguilar R, Loria D, Foerster C (2005) Health evaluation of a radiocollared population of free-ranging baird’s tapirs (Tapirus bairdii) in Costa Rica. Journal of Zoo and Wildlife Medicine 36:176–187

    Article  Google Scholar 

  • Hoberg EP, Polley L, Jenkins EJ, Kutz SJ, Veitch AM, Elkin BT (2008) Integrated approaches and empirical models for investigation of parasitic diseases in northern wildlife. Emerging Infectious Diseases 14:10–17. doi:10.3201/eid1401.071119

    Article  PubMed  PubMed Central  Google Scholar 

  • Instituto Nacional de Estadística Geografía e Informática (INEGI) (2013) Uso de Suelo y Vegetación, Serie V., Escala 1: 250,000. México. Available: https://www.conabio.gob.mx/informacion/metadata/gis/usv250s5ugw.xml?_httpcache=yes&_xsl=/db/metadata/xsl/fgdc_html.xsl&_indent=no [accesed April 13, 2018]

  • Instituto Nacional de Estadística Geografía e Informática (INEGI) (2015) Conteo socio-económico del 2015. Estado de Campeche, Campeche, México. Available: https://www.snieg.mx/contenidos/espanol/inegi_coord/Informe/Informe2015_Actividades_y_Resultados.pdf [accesed April 13, 2018]

  • Irwin MT, Junge RE, Raharison JL, Samonds KE (2010) Variation in physiological health of diademed sifakas across intact and fragmented forest at Tsinjoarivo, Eastern Madagascar. American Journal of Primatology 72:1013–1025. doi:10.1002/ajp.20847

    Article  PubMed  Google Scholar 

  • Jones DM (1982) Conservation in relation to animal disease in Africa and Asia. Symposia of the Zoological Society of London 50:271–285

    Google Scholar 

  • Junge RE, Barrett MA, Yoder AD (2011) Effects of anthropogenic disturbance on Indri (Indri indri) health in Madagascar. American Journal of Primatology 73:632–642. doi:10.1002/ajp.20938

    Article  PubMed  Google Scholar 

  • Kerr JT, Currie DJ (1995) Effects of human activity on global extinction. Conservation Biology 9:1528–1538. doi:10.1046/j.1523-1739.1995.09061528.x

    Article  Google Scholar 

  • Laurance WF (2007) Have we overstated the tropical biodiversity crisis? Trends in Ecology and Evolution 22:65–70. doi:10.1016/j.tree.2006.09.014

    Article  PubMed  Google Scholar 

  • Magrin G, Gay-García C, Cruz-Choque D, Gímenez JC, Moreno AR, Nagy GJ, et al. (2007) Latin América. In: Climate change 2007: Impacts, adaptability and vulnerability. Contribution of working group II to the fourth assessment report of the Intergovernmental panel on climate change, Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (editors), Cambridge: Cambridge University Press, pp 581–615

  • Mangini PR, Medici EP, Fernandes-Santos RC. 2012. Tapir health and conservation medicine. Integrative Zoology 7:331–345. doi:10.1111/j.1749-4877.2012.00323.x

    Article  PubMed  Google Scholar 

  • Márdero S, Nickl E, Schmook B, Schneider L, Rogan J, Christman Z, et al. (2012) Sequías en el sur de la Península de Yucatán: análisis de la variabilidad anual y estacional de la precipitación. Investigaciones Geográficas 78:19–33

    Article  Google Scholar 

  • Mazerolle MJ (2017) Package “AICcmodavg.” AICcmodavg: model selection and multimodel inference based on (Q) AIC (c) CRAN R Project

  • Medici EP, Mangini PR, Fernandes-Santos RC (2014) Health assessment of wild lowland tapir (Tapirus terrestris) populations in the Atlantic forest and Pantanal biomes, Brazil (1996–2012). Journal of Wildlife Diseases 50:817–828. doi:10.7589/2014-02-029

    Article  PubMed  Google Scholar 

  • Murray M, Edwards MA, Abercrombie B, St. Clair CC (2015) Poor health is associated with use of anthropogenic resources in an urban carnivore. Proceedings of the Royal Society B 282:20150009. doi:10.1098/rspb.2015.0009

    Article  PubMed  Google Scholar 

  • Naranjo E (2009) Ecology and conservation of Baird’s tapir in Mexico. Tropical Conservation Science 2:140–158. doi:10.1177/194008290900200203

    Article  Google Scholar 

  • O’Farrill G, Gauthier-Schampaert K, Rayfield B, Bodin Ö, Calmé S, Sengupta R, et al. (2014) The potential connectivity of waterhole networks and the effectiveness of a protected area under various drought scenarios. PLoS ONE 9(5): e95049. doi:10.1371/journal.pone.0095049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Owen-Smith RN (1992) Megaherbivores: The influence of very large body size on ecology. Cambridge: Cambridge University Press

    Google Scholar 

  • Pence DB, Windberg LA (1994) Impact of a sarcoptic mange epizootic on a coyote population. The Journal of Wildlife Management 58:624–633. doi:10.2307/3809675

    Article  Google Scholar 

  • Pérez-Flores J, Calmé S, Reyna-Hurtado R (2016) Scoring body condition in wild Baird’s tapir (Tapirus bairdii) using camera traps and opportunistic photographic material. Tropical Conservation Science 9:1–12. doi:10.1177/1940082916676128

    Article  Google Scholar 

  • Porter-Bolland L, Drew AP, Vergara-Tenorio C (2006) Analysis of a natural resources management system in the Calakmul Biosphere Reserve. Landscape and Urban Planning 74:223–241. doi:10.1016/j.landurbplan.2004.09.005

    Article  Google Scholar 

  • Primack RB (2002) Essentials of Conservation Biology. Sunderland: Sinauer Associates

    Google Scholar 

  • Pullin AS (2002) Conservation Biology. Cambridge: Cambridge University Press

    Book  Google Scholar 

  • R Core Team (2019) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available:https://www.R-project.org

  • Ramírez-Delgado JP, Christman Z, Schmook B (2014) Deforestation and fragmentation of seasonal tropical forests in the southern Yucatán, Mexico (1990–2006), Geocarto International 29:822–841. doi:10.1080/10106049.2013.868039

    Article  Google Scholar 

  • Reyna-Hurtado R, Rojas-Flores E, Tanner GW (2009) Home range and habitat preferences of white-lipped peccary groups (Tayassu pecari) in a seasonal tropical forest of the Yucatan Peninsula, Mexico. Journal of Mammalogy 90:1199–1209. doi:10.1644/08-MAMM-A-246.1

    Article  Google Scholar 

  • Reyna-Hurtado R, Sanvicente-López M, Pérez-Flores J, Carrillo-Reyna N, Calmé S (2016) Insights into the multiannual home range of a Baird’s tapir (Tapirus bairdii) in the Maya Forest. Therya 7:271–276. doi:10.12933/therya-16-348

    Article  Google Scholar 

  • Ripple W, Newsome T, Wolf C, Dirzo R, Everatt KT, Galetti M, et al. (2015) Collapse of the world’s largest herbivores. Science Advances 1:e1400103. doi:10.1126/sciadv.1400103

    Article  PubMed  PubMed Central  Google Scholar 

  • Rueda X (2010) Understanding deforestation in the southern Yucatán: insights from a sub-regional, multi-temporal analysis. Regional Environmental Change 10:175–189. doi:0.1007/s10113-010-0115-7

    Article  Google Scholar 

  • Scott ME (1988) The impact of infection and disease on animal populations: implications for conservation biology. Conservation Biology 2:40–56

    Article  Google Scholar 

  • Solomon S, Qin D, Manning M, Marquis M, Averyt K (2007) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge: Cambridge University Press

  • Stephen C (2013) Toward a new definition of animal health: Lessons from the Cohen Commission and the SPS agreement. Optimum Online: Journal of Public Sector Management 43:1

    Google Scholar 

  • Stephen C (2014) Toward a modernized definition of wildlife health. Journal of Wildlife Diseases 50:427–430. doi:10.7589/2013-11-305

    Article  PubMed  Google Scholar 

  • Towns L, Derocher AE, Stirling I, Lunn NJ, Hedman D (2009) Spatial and temporal patterns of problem polar bears in Churchill, Manitoba. Polar Biology 32:1529–1537. doi:10.1007/s00300-009-0653-y

    Article  Google Scholar 

  • Vester H, Lawrence D, Eastmant J, Turner R, Calmé S, Dickson R, et al. (2007) Land change in the southern Yucatán and Calakmul Biosphere Reserve: effects on habitat and biodiversity. Ecological Applications 17:989–1003. doi:10.1890/05-1106

    Article  PubMed  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. New York: Springer

    Book  Google Scholar 

  • Wilke CO (2017) Cowplot: Streamlined Plot Theme and Plot Annotations for 'ggplot2', R package version 0.9.2. Available: https://CRAN.R-project.org/package=cowplot [accesed July 13, 2019]

  • Wittrock J, Duncan C, Stephen C (2019) A determinants of health conceptual model for fish and wildlife health. Journal of Wildlife Diseases 55:285–297. doi:10.7589/2018-05-118

    Article  PubMed  Google Scholar 

  • Zimmerman DM, Hernandez S (2015) Tapiridae. In: Fowler’s Zoo and Wild Animal Medicine volume 8, Miller RE, Fowler ME (editors), United States of America: Elsevier Saunders, pp. 547–559

    Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1:3–14. doi:10.1111/j.2041-210X.2009.00001.x

    Article  Google Scholar 

Download references

Acknowledgements

We thank Fernando Contreras Moreno, Georgina O’Farril, Rafael Reyna Hurtado, Marcos Briceño, Mauro Sanvicente López, Cesar Noh Canche, Claudio López Díaz, Alberto Villaseñor Farías, Juan Alberto Villaseñor Pérez and José Arnoldo Villaseñor Pérez for sharing materials. Special thanks go to Jaime Dionisio Cuevas Domínguez and Edwin Hernández Pérez for their help with the statistical analyses. An earlier version of this manuscript benefited from early comments by Rafael Reyna Hurtado and David González Solís. Special thanks are due to the authorities of the Calakmul Biosphere Reserve for their support in this research. JPF was supported by a scholarship (361517) granted by the Mexican government through CONACYT.

Author information

Authors and Affiliations

  1. El Colegio de La Frontera Sur, Ave. Centenario Km 5.5 Carretera Calderitas, 77900, Chetumal, Quintana Roo, Mexico

    Jonathan Pérez Flores, Holger Weissenberger & Sophie Calmé

  2. Pronatura Península de Yucatán, A.C., Calle 32 número 269 Av. Francisco I. Madero, Colonia Santa Lucía, San Francisco de Campeche, 24020, Campeche, Mexico

    Antonio López-Cen

  3. Faculté Des Sciences, Université de Sherbrooke, 2500 Boulevard de l’Université, Sherbrooke, QC, Canada

    Sophie Calmé

Authors
  1. Jonathan Pérez Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Holger Weissenberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antonio López-Cen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sophie Calmé
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan Pérez Flores.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez Flores, J., Weissenberger, H., López-Cen, A. et al. Environmental Factors Influencing the Occurrence of Unhealthy Tapirs in the Southern Yucatan Peninsula. EcoHealth 17, 359–369 (2020). https://doi.org/10.1007/s10393-020-01496-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-020-01496-7

Keywords

Search

Navigation