Accessible Requires Authentication Published by De Gruyter February 4, 2020

Population viability analysis of common marsupials, Didelphis marsupialis and Didelphis virginiana, in a scenario of constant loss of native vegetation

Bárbara Cruz-Salazar ORCID logo and Lorena Ruiz-Montoya ORCID logo
From the journal Mammalia

Abstract

We studied the population viability of two common marsupials, Didelphis marsupialis and Didelphis virginiana, based on field data and published ecological and genetic information. Using the VORTEX v. 10. 2.6 program, a 100-year simulation was performed with 1000 iterations for five populations of D. marsupialis and six of D. virginiana. A low probability of extinction was observed in both species, particularly for D. virginiana (0.000–0.007). Population size is higher considering a metapopulation dynamics approach versus individual populations for the two marsupials: 498.25 individuals for D. marsupialis and 367.41 individuals for D. virginiana. The estimated mean genetic diversity was high for both D. marsupialis (He = 0.77–0.78) and D. virginiana (He = 0.79–0.82). The survival of both species over time could be expected to increase if a metapopulation dynamics is favored over the coming decades, despite a 1.3% loss rate of forest cover. The monitoring of population size and genetic diversity is highly recommended to validate the trends suggested by the model; this is especially true for D. marsupialis, a species associated with conserved areas that are becoming progressively less abundant. This research provides information on the responses of common mammalian species to environmental changes such as deforestation.

Acknowledgments

We wish to thank Alfonso Ortiz Moreno, Wenceslao Bonifáz, Carlos Molina, Eugenia Sántiz, and Trinidad Alejandro Guillén for their assistance in fieldwork. This work was part of the doctoral thesis of Bárbara Cruz Salazar (Consejo Nacional de Ciencia y Tecnología scholarship number 175336, Funder Id: http://dx.doi.org/10.13039/501100003141). María Elena Sánchez-Salazar translated the manuscript into English.

References

Adler, G.H., J.J. Arboledo and B.L. Travi. 1997. Population dynamics of Didelphis marsupialis in Northern Colombia. Stud. Neotrop. Fauna E. 32: 7–11. Search in Google Scholar

Andersen, L.H., P. Sunde, I. Pellegrino, V. Loeschcke and C. Pertoldi. 2017. Using population viability analysis, genomics, and habitat suitability to forecast future population patterns of Little Owl Athene noctua across Europe. Ecol. Evol. 7: 10987–11001. Search in Google Scholar

Aranda, M. 2000. Huellas y otros rastros de los mamíferos grandes y medianos de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Instituto de Ecología, A. C., Xalapa, Veracruz, Mexico. pp. 212. Search in Google Scholar

Beasley, J.C., W.S. Beatty, Z.H. Olson and O.E. Rhodes. 2010. A genetic analysis of the Virginia opossum mating system: evidence of multiple paternity in a highly fragmented landscape. J. Hered. 101: 368–373. Search in Google Scholar

Beatty, W.S., J.C. Beasley, G. Dharmarajan and O.E. Rhodes. 2012. A genetic structure of a Virginia opossum (Didelphis virginiana) population inhabiting a fragmented agricultural ecosystem. Can. J. Zool. 90: 101–109. Search in Google Scholar

Beatty, W.A., J.C. Beasley and O.E. Rhodes. 2014. Habitat selection by a generalist mesopredator near its historical range boundary. Can. J. Zool. 92: 41–48. Search in Google Scholar

Begon, M., C.R. Towsend and J.L. Harper. 2006. Ecology: from individuals to ecosystems. Blackwell, Oxford. pp. 738. Search in Google Scholar

Bozek, C.K., S. Prange and S.D. Gehrt. 2007. The influence of anthropogenic resources on multi-scale habitat selection by raccoons. Urban Ecosyst. 10: 413–425. Search in Google Scholar

Brook, B.W., M.A. Burgman and R. Frankham. 2000. Differences and congruencies between PVA package the importance of sex ratio for predictions of extinction risk. Conserv. Ecol. 4: 6–18. Search in Google Scholar

Burgman, M.A., S. Ferson and H.R. Akcakaya. 1993. Risk assessment in conservation biology. Chapman and Hall, London, UK. pp. 292. Search in Google Scholar

Cabello, D.R. 2006. Reproduction of Didelphis marsupialis (Didelphimorphia: Didelphidae) in the Venezuelan Andes. Acta Theriol. 51: 427–433. Search in Google Scholar

Cáceres, N.C. and E.L.A. Monteiro-Filho. 1998. Population dynamics of the common opossum, Didelphis marsupialis (Mammalia, Marsupialia), in southern Brazil. J. Mammal. Biol. 63: 169–172. Search in Google Scholar

Cancino, J., R. Rodríguez-Estrella and P. Miller. 2010. Using population viability analysis for management recommendations of the endangered endemic peninsular pronghorn. Acta Zool. Mex. 26: 173–189. Search in Google Scholar

Cairns, M.A., R. Dirzo and F. Zadroga, 1995. Forests of Mexico. J. For. 93: 21–24. Search in Google Scholar

Carim, K.J., Y. Vindenes, L.A. Eby, C. Barfoot and L.A. Vollestad, 2017. Life history, population viability, and the potential for local adaptation in isolated trout populations. Glob. Ecol. Conserv. 10: 93–102. Search in Google Scholar

Ceballos, G. and G. Oliva. 2005. Los mamíferos silvestres de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad: Fondo de Cultura Económica, Mexico. pp. 986. Search in Google Scholar

Clark, T.W., G.N. Backhouse and R.C. Lacy. 1991. Report of a workshop on population viability assessment as a tool for threatened species management and conservation. Aust. Zool. 27: 28–35. Search in Google Scholar

Cruz-Salazar, B., L. Ruiz-Montoya, D. Navarrete-Gutiérrez, E. Espinoza-Medinilla, E. Vázquez-Domínguez and L.-B. Vázquez. 2014. Diversidad genética y abundancia relativa de Didelphis marsupialis y Didelphis virginiana en Chiapas, México. Rev. Mex. Biodivers. 85: 251–261. Search in Google Scholar

Cruz-Salazar, B., L. Ruiz-Montoya, E. Vázquez-Domínguez, D. Navarrete-Gutiérrez, E.E. Espinoza-Medinilla and L.-B. Vázquez. 2016a. Genetic diversity of Didelphis virginiana related to different levels of disturbance in the Highlands and the Central Depression regions of Chiapas, Mexico. J. Trop. Ecol. 32: 146–157. Search in Google Scholar

Cruz-Salazar, B., L. Ruiz-Montoya, D. Navarrete-Gutiérrez and L.-B. Vázquez. 2016b. Influence of the composition and structure of modified landscapes on abundance of two marsupials during the dry season. Therya 7: 393–406. Search in Google Scholar

Dreschsler, M. and K. Johst. 2010. Rapid viability analysis for metapopulations in dynamic habitat networks. Proc. R. Soc. B. 277: 1889–1897. Search in Google Scholar

Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34: 487–515. Search in Google Scholar

Frankham, R., J.D. Ballou and K.H. McInnes. 2004. A primer of conservation genetics. University of Cambridge, Cambridge. pp. 236. Search in Google Scholar

Gardner, A.L. 1973. The systematics of the genus Didelphis (Marsupialia: Didelphidae) in North and Middle America. Spec. Publ. Mus. Tex. Tech. Univ. 4: 1–81. Search in Google Scholar

Gardner, A.L. and M.E. Sunquist. 2003. Opossum, Didelphis virginiana. In: (G.A. Feldhamer, B.C. Thompson and J.A. Chapman, eds.) Wild mammals of North America. The Johns Hopkins University Press, Baltimore. pp. 3–29. Search in Google Scholar

Gaston, K.J. 2010. Valuing common species. Ecology 327: 154–155. Search in Google Scholar

Gaston, K.J. and R.A. Fuller. 2007a. Biodiversity and extinction: losing the common and the widespread. Prog. Phys. Geogr. 31: 213–225. Search in Google Scholar

Gaston, K.J. and R.A. Fuller. 2007b. Commonness, population depletion and conservation biology. Trends Ecol. Evol. 23: 14–18. Search in Google Scholar

Gaston, K.J., T.M. Blackburn, J.J.D. Greenwood, R.D. Gregory, R.M. Quinn and J.H. Lawton. 2000. Abundance-occupancy relationships. J. Appl. Ecol. 37: 39–59. Search in Google Scholar

Gehrt, S.D., D.E. Clark and E.K. Fritzell. 1997. Population dynamics and ecology of Virginia opossums in southern Texas. Southwest Nat. 42: 170–176. Search in Google Scholar

Gillete, L.N. 1980. Movement patterns of radio-tagged opossums in Wisconsin. Amer. Midl. Naturalist. 27: 171–176. Search in Google Scholar

González-Espinosa, M., N. Ramírez-Marcial, G. Méndez-Dewar, L. Galindo-Jaimes and D. Golicher. 2005. Riqueza de especies de árboles en Chiapas: variación espacial y dimensiones ambientales asociadas al nivel regional. In: (M. González-Espinosa, N. Ramírez-Marcial and L. Ruiz-Montoya, eds.) Diversidad biológica en Chiapas. Ecosur, Cocytech, Plaza y Valdez Editores, México. pp. 81–125. Search in Google Scholar

González-Espinosa, M., N., Ramírez-Marcial and J.M. Rey-Benayas. 2008. Variación Espacial de la diversidad arbórea de Chiapas: patrones regionales y jerarquía de factores determinantes. In: (L.R. Sánchez-Velásquez, J. Galindo-González and F. Díaz-Fleischer, eds.) Ecología, manejo y conservación de los ecosistemas de montaña en México. Mundi-Prensa Mexico, S. A. de C. V. Ciudad de México, México. pp. 147–166. Search in Google Scholar

Greenwald, K.R. 2010. Genetic data in population viability analysis: case studies with ambystomatid salamanders. Anim. Conserv. 13: 115–122. Search in Google Scholar

Gutiérrez, D. 2002. Metapoblaciones: un pilar básico en biología de conservación. Ecosistemas 11: 1–3. Search in Google Scholar

Harding, K.C. and J.M. McNamara. 2002. A unifying framework for metapopulation dynamics. Am. Nat. 160: 173–185. Search in Google Scholar

Hennessy, C., C.C. Tsai, J.C. Beasley, W.S. Beatty, P.A. Zollner and O.E. Rhodes. 2015. Elucidation of population connectivity in synanthropic mesopredators: using genes to define relevant spatial scales for management of raccoons and Virginia opossums. J. Wildl. Manage. 79: 112–121. Search in Google Scholar

Hughes, J., K. Goudkamp, D. Hurwood, M. Hancock and S. Bunn. 2003. Translocation causes extinction of a local population of the freshwater shrimp Paratya australiensis. Conserv. Biol. 17: 1007–1012. Search in Google Scholar

Kelly, M.J. and T. Caro. 2003. Low density of small mammals at Las Cuevas, Belize. Mamm. Biol. 68: 372–386. Search in Google Scholar

Keyghobadi, N. 2007. The genetic implications of habitat fragmentation for animals. Can. J. Zool. 85: 1049–1064. Search in Google Scholar

Kim, B.-J., B.-K. Lee, H. Lee and G.-S. Jang. 2016. Considering threats to population viability of the endangered Korean long-tailed goral (Naemorhedus caudatus) using VORTEX. Anim. Cells Syst. 20: 52–59. Search in Google Scholar

Krabbe, B.M. and C. Rahbek. 2010. Causality of the relationship between geographic distribution and species abundance. Q. Rev. Biol. 85: 3–25. Search in Google Scholar

Lacy, R.C. and J.P. Pollak. 2017. VORTEX: a stochastic simulation of the extinction process. Version 10.2.3. Chicago Zoological Society, Brookfield, Illinois, USA. Search in Google Scholar

Lindenmayer, D.B., R.C. Lac and M.L. Pope. 2000. Testing a simulation model for population viability analysis. Ecol. Appl. 10: 580–597. Search in Google Scholar

Lindermayer, D., R.K. Hobbs, R. Montague-Drake, J. Alexandra, A. Bennett, M. Burgman, P. Cale, A. Calhoun, V. Cramer, P. Cullen, D. Driscoll, L. Fahrig, J. Fischer, J. Franklin, Y. Haila, M. Huter, P. Gibbons, S. Lake, G. Luck, C. MacGregor, S. Mcintyre, R. Mac N., A. Manning, J. Miller, H. Mooney, R. Noss, H. Possingham, D. Saunders, F. Schmiegelow, M. Scott, D. Simberloff, T. Sisk, G. Tabor, B. Walker, J. Wiens, J. Woinarski and E. Zavaleta. 2008. A checklist for ecological management of landscapes for conservation. Ecol. Lett. 11: 78–91. Search in Google Scholar

Lu, N. and Y.-H. Sun. 2011. Population viability analysis and conservation of Chinese grouse Bonasa sewerzowi in Lianhuashan Nature Reserve, north-west China. Bird Conserv. Int. 21: 49–58. Search in Google Scholar

MacManus, J.J. 1974. Didelphis virginiana. Mamm. Species 40: 1–6. Search in Google Scholar

Morrison, C., C. Wardle and G. Castley. 2016. Repeatability and reproducibility of Population Viability Analysis (PVA) and the implications for threatened species management. Front. Ecol. Evol, 4: 1–7. Search in Google Scholar

Nicolé, F., E. Brzosko and I. Till-Bottraud. 2005. Population viability analysis of Cypripedium calceolus in a protected area: longevity, stability and persistence. J. Ecol. 93: 716–726. Search in Google Scholar

Norberg, J., M.C. Urban, M. Vellend, C.A. Klausmeier and N. Loeuille. 2012. Eco-evolutionary responses of biodiversity to climate change. Nat. Clim. Chang. 2: 747–751. Search in Google Scholar

Ramírez-Marcial, N., M. González-Espinosa and D. Williams-Linera. 2001. Anthropogenic disturbance and tree diversity in montane rain forests in Chiapas, México. For. Ecol. Manage. 154: 311–326. Search in Google Scholar

Ramírez-Pulido, J., J. Arroyo-Cabrales and A. Castro-Campillo. 2005. Estado actual y relación nomenclatural de los mamíferos terrestres de México. Acta Zool. Mex. (n.s.) 21: 21–82. Search in Google Scholar

Ringier, H.J. 1961. Review of Oligocene Didelphid marsupials. J. Paleontol. 35: 218–228. Search in Google Scholar

Rocha-Loredo, A.G., N. Ramírez-Marcial and M. González-Espinosa. 2010. Riqueza y diversidad de árboles del bosque tropical caducifolio en la Depresión Central de Chiapas. Bol. Soc. Bot. Mex. 87: 89–103. Search in Google Scholar

Rosatte, R., M. Ryckman, K. Ing, S. Proceviat, M. Allan, L. Bruce, D. Donovan and J.C. Davies. 2010. Density, movements, and survival of raccoons in Ontario, Canada: implications for disease spread and management. J. Mammal. 91: 122–135. Search in Google Scholar

Spear, S.F., N. Balkenhol, M-J. Fortin, B.H. Mcrae and K. Scribner. 2010. Use of resistance surfaces for landscape genetics studies: considerations for parameterization and analysis. Mol. Ecol. 19: 3376–3591. Search in Google Scholar

Sunquist, M.E., S.N. Austad and F. Sunquist. 1987. Movement patterns and home range in the common opossum (Didelphis marsupialis). J. Mammal. 68: 173–176. Search in Google Scholar

Templeton, A.R., K. Shaw, E. Routman and S.K. Davis. 1990. The genetic consequences of habitat fragmentation. Ann. Mo. Bot. Gard. 77: 13–27. Search in Google Scholar

Vega, R., E. Vázquez-Domínguez, T.A. White, D. Valenzuela- Galván and J.B. Searle. 2017. Population genomics applications for conservation: the case of the tropical dry forest dweller Peromyscus melanophrys. Conserv. Genet. 18: 313–326. Search in Google Scholar

Whitaker Jr., J.O. and R.E. Mumford. 2009. Mammals of Indiana. Indiana University Press, Bloomington. pp. 327. Search in Google Scholar

Whitlock, M.C. and D.E. Mccauley. 1999. Indirect measures of gene flow and migration. Heredity 82: 117–125. Search in Google Scholar

Wilcox, C., B.J. Cairns and H.P. Possingham. 2006. The role of habitat disturbance and recovery in metapopulation persistence. Ecology 87: 855–863. Search in Google Scholar

Wright, S. 1951. The genetical structure of populations. Ann. Eugen. 15: 323–353. Search in Google Scholar

Received: 2019-10-22
Accepted: 2019-12-17
Published Online: 2020-02-04
Published in Print: 2020-09-25

©2020 Walter de Gruyter GmbH, Berlin/Boston