VITAL RATES, THEIR VARIATION AND NATURAL SELECTION: A CASE FOR AN ATLANTIC FOREST MARSUPIAL

Authors

  • Maja Kajin University of Oxford, United Kingdom; University of Ljubljana, Slovenia https://orcid.org/0000-0001-9996-5897
  • Rosana Gentile
  • Paulo Jose Leitão de Almeida
  • Marcus Vinicius Vieira
  • Rui Cerqueira

DOI:

https://doi.org/10.4257/oeco.2023.2702.03

Keywords:

life cycle, life history, matrix population model, sensitivity of sensitivity, selection pressures

Abstract

Evolutionary theory predicts that viable wild populations confront environmental variation by maintaining the variance of the most important vital rates low, a phenomenon also known as demographic buffering. However, patterns diverging from the demographic buffering hypothesis have also been reported. Here we used Population Matrix Models to test the hypothesis of buffering in the early survival of an Atlantic Forest marsupial. We used sensitivity analyses, which allow quantifying the effects that perturbations in specific vital rates could have on the population’s growth rate. We obtained the sensitivities, elasticities, and second-order derivatives of the discrete population growth rate with respect to different vital rates for a population of the black-eared opossum (Didelphis aurita, Marsupialia, Didelphidae) in a preserved Atlantic Forest, the state of Rio de Janeiro, Brazil. The second-order derivatives offer an insight into the selection forces occurring during the life cycle, clarifying the processes behind the common pattern of early-survival importance. We found evidence of buffering in early survival, however, in one of the cohorts, early survival displayed evidence of opposed behavior to the expected under demographic buffering, thus revealing that established life-history patterns can be quickly modified by a small change in one vital rate.

References

Almeida, P. J. L. de, Vieira, M. V., Prevedello, J. A., Kajin, M., Forero-Medina, G., & Cerqueira, R. 2015. What if it gets crowded? Density-dependent tortuosity in individual movements of a Neotropical mammal. Austral Ecology, 40(7), 758–764. DOI: 10.1111/aec.12250

Bergallo, H. G. 1994. Ecology of a small mammal community in an Atlantic forest area in southeastern Brazil. Studies on Neotropical Fauna and Environment, 29(4), 197–217.

Burnham, K., & Anderson, D. R. 1998. Model selection and multimodel inference. A practical information-theoretic approach. NY: Springer.

Caceres, N. C., & Monteiro-Filho, E. L. A. 2001. Food Habits, Home Range and Activity of Didelphis aurita (Mammalia, Marsupialia) in a Forest Fragment of Southern Brazil. Studies on Neotropical Fauna and Environment, 36(2), 85–92. DOI: 10.1076/snfe.36.2.85.2138

Caswell, H. 2018. Matrix Population Models: Construction, Analysis, and Interpretation. Second Second ed.Sinauer Associates Inc. Publishers, Sunderland, Massachusetts, USA.

Caswell, H. 1996. Second Derivatives of Population Growth Rate: Calculation and Applications. Ecology, 77(3), 870–879. DOI: 10.2307/2265507

Caswell, H. 2019. Sensitivity Analysis: Matrix Methods in Demography and Ecology.p. 299.

Cerqueira, R., Fernandez, F. A. S., & Quintela, F. M. 1990. Mamíferos da restinga de Barra de Maricá, Rio de Janeiro. Papeis Avulsos de Zoologia/Museu de Zoologia Da Univ. de Sao Paulo.

Cerqueira, R., Gentile, R., Fernandez, F. A. S., & Andrea, P. S. D. 1993. A five-year population study of an assemblage of small mammals in Southeastern Brazil.

Cerqueira, R., & Lemos, B. 2000. Morphometric differentiation between Neotropical black-eared opossums, Didelphis marsupialis and D. aurita (Didelphimorphia, Didelphidae). Mammalia, 64, 319–327.

Cerqueira, R. 1985. The distribution of Didelphis in South America (Polyprotodontia, Didelphidae). Journal of Biogeography, 12, 135–145.

Cerqueira, R. 2005. Fatores ambientais e a reprodução de marsupiais e roedores no leste do brasil. Arquivos Do Museu Nacional, Rio de Janeiro, 63(1), 29–39.

Coulson, T., Benton, T. G., Lundberg, P., Dall, S. R. X., & Kendall, B. 2016. Putting evolutionary biology back in the ecological theatre : a demographic framework mapping genes to communities. Evolutionary Ecology Research, 8(7), 1155–1171.

Coulson, T., Tuljapurkar, S., & Childs, D. 2010. Using evolutionary demography to link life history theory, quantitative genetics and population ecology. Journal of Animal Ecology, 79(6), 1226–1240. DOI: 10.1111/j.1365-2656.2010.01734.x

Cunha, A. A., & Vieira, M. V. 2002. Support diameter, incline, and vertical movements of four didelphid marsupials in the Atlantic forest of Brazil. Journal of Zoology, 258(4), 419–426. DOI: 10.1017/S0952836902001565

Dinerstein, E., Olson, D., Graham, D., Webster, A., Primm, S., Bookbinder, M., & Ledec, G. 1995. A Conservation Assessment of the Terrestrial Ecoregions of Latin America and the Caribbean. WashWashington (DC): World Bank.

Ebert, T. 1999. Plant and animal populations: Methods in demography.Academis Press, San Diego, CA, USA.

Ferreira, M., Kajin, M., Vieira, M., Zangrandi, P., Cerqueira, R., & Gentile, R. 2013. Life history of a neotropical marsupial: Evaluating potential contributions of survival and reproduction to population growth rate. Mammalian Biology - Zeitschrift Fur Saugetierkunde, 78(6), 406–411.

Fisher, D. O., Owens, I. P. F., & Johnson, C. N. 2013. The Ecological Basis of Life History Variation in Marsupials., 82(12), 3531–3540.

Fonseca, G. A. B., & Robinson, J. G. 1990. Forest size and structure: Competitive and predatory effects on small mammal communities. Biological Conservation, 53(4), 265–294. DOI: 10.1016/0006-3207(90)90097-9

Gaillard, J.-M., & Yoccoz, N. 2003. Temporal Variation in Survival of Mammals: a Case of Environmental Canalization? Ecology, 84(12), 3294–3306. DOI: 10.1890/02-0409

Gentile, R., & Fernandez, F. A. S. 1999. Influence of habitat structure on a streamside small mammal Community in a Brazilian rural area. Mammal Review, 63(1), 29–40.

Gentile, R., Finotti, R., Rademaker, V., & Cerqueira, R. 2004. Population dynamics of four marsupials and its relation to resource production in the Atlantic forest in southeastern Brazil. Mammalia, 68(2–3), 109–119.

Gentile, R., D’Andrea, P., Cerqueira, R., & Maroja, L. S. 2000. Population dynamics and reproduction of marsupials and rodents in a Brazilian rural area : a five-year study. Studies on Neotropical Fauna and Environment, 35, 1–9.

Hilde, C. H., Gamelon, M., Sæther, B.-E., Gaillard, J.-M., Yoccoz, N. G., & Pélabon, C. 2020. The Demographic Buffering Hypothesis: Evidence and Challenges. Trends in Ecology & Evolution, 35(6), 523–538. DOI: 10.1016/j.tree.2020.02.004

Kajin, M., Cerqueira, R., Vieira, M. V, & Gentile, R. 2008. Nine-year demography of the black-eared opossum Didelphis aurita (Didelphimorphia: Didelphidae) using life tables. Revista Brasileira de Zoologia, 25(2), 206–213.

Kawano, S. 2020. Selection Gradients. In: D. J. Futuyma (Ed.), Evolutionary Biology.Oxford University Press.

Koons, D. N., Pavard, S., Baudisch, A., & Jessica E. Metcalf, C. 2009. Is life-history buffering or lability adaptive in stochastic environments? Oikos, 118(7), 972–980. DOI: 10.1111/j.1600-0706.2009.16399.x

Lande, R. 1982. A Quantitative Genetic Theory of Life History Evolution. Ecology, 63(3), 607–615. DOI: 10.2307/1936778

McCarthy, D., Townley, S., & Hodgson, D. 2008. On second order sensitivity for stage-based population projection matrix models. Theoretical Population Biology, 74(1), 68–73. DOI: 10.1016/j.tpb.2008.04.008

McDonald, J. L., Franco, M., Townley, S., Ezard, T. H. G., Jelbert, K., & Hodgson, D. J. 2017. Divergent demographic strategies of plants in variable environments. Nature Ecology & Evolution, 1(2), 0029. DOI: 10.1038/s41559-016-0029

Mendel, S., Vieira, M., & Cerqueira, R. 2008. Precipitation, litterfall, and the dynamics of density and biomass in the black-eared opossum, Didelphis aurita. Journal of Mammalogy, 89(1), 159–167.

Mendel, S., & Vieira, M. V. 2003. Movement distances and density estimation of small mammals using the spool-and-line technique. Acta Theriologica, 48(3), 289–300.

Moura, M. C., Vieira, M. V., & Cerqueira, R. 2009. Occasional intraguild predation structuring small mammal assemblages: the marsupial Didelphis aurita in the Atlantic Forest of Brazil. Austral Ecology, 34(5), 481–489. DOI: 10.1111/j.1442-9993.2009.01948.x

Nilsen, E. B., Gaillard, J.-M., Andersen, R., Odden, J., Delorme, D., van Laere, G., & Linnell, J. D. C. 2009. A slow life in hell or a fast life in heaven: demographic analyses of contrasting roe deer populations. The Journal of Animal Ecology, 78(3), 585–94. DOI: 10.1111/j.1365-2656.2009.01523.x

Nimer, E. 1989. Climatologia do Brasil.IBGE, Departamento de Recursos Naturais e Estudos Ambientais, Rio de Janeiro, Brazil.

Paglia, A. P., Rylands, A. B., Herrmann, G., Aguiar, L. M. S., Chiarello, A. G., Leite, Y. L. R., Costa, L. P., & Siciliano, S. 2012. Lista Anotada dos Mamíferos do Brasil.

Pfister, C. 1998. Patterns of variance in stage-structured populations: Evolutionary predictions and ecological implications. Proceedings of the National Academy of Sciences, 95(1), 213–218. DOI: 10.1073/pnas.95.1.213

Phillips, P. C., & Arnold, S. J. 1989. Visualising multivariate selection. Evolution, 43(6), 1209–1222.

Reed, A. W., & Slade, N. a. 2012. Buffering and plasticity in vital rates of oldfield rodents. The Journal of Animal Ecology, 81(5), 953–9. DOI: 10.1111/j.1365-2656.2012.01976.x

Salguero-Gómez, R., & de Kroon, H. 2010. Matrix projection models meet variation in the real world. Journal of Ecology, 98(2), 250–254. DOI: 10.1111/j.1365-2745.2009.01635.x

Santori, R. T., Lessa, L. G., & Astúa, D. 2012. Alimentação, nutrição e adaptações alimentares de marsupiais brasileiros. In: N. C. Cáceres (Ed.), Os Marsupiais do Brasil: Biologia, Ecologia e Evolução. pp. 385–406. 2nd ed. Campo Grande: Editora UFMS.

Santos, G. S., Salguero-Gómez, R., Dias, A. T. C., & Kajin, M. 2021. To buffer or to be labile? A framework to disentangle demographic patterns and evolutionary processes. BioRxiv, April 14,. DOI: 10.1101/2021.04.12.439165

Shyu, E., & Caswell, H. 2014. Calculating second derivatives of population growth rates for ecology and evolution. Methods in Ecology and Evolution, 5(5), 473–482. DOI: 10.1111/2041-210X.12179

Sterns, S. 1999. The Evolution of Life Histories.Oxford University Press, Oxford.

Van Tienderen, P. H. 2000. Elasticities and the link between demographic and evolutionary dynamics. Ecology, 81(3), 666–679. DOI: 10.2307/177368

Vieira, E. M., & Monteiro-Filho, E. L. A. 2003. Vertical stratification of small mammals in the Atlantic rain forest of south-eastern Brazil. Journal of Tropical Ecology, 19(5), 501–507. DOI: 10.1017/S0266467403003559

White, G., & Burnham, K. 1999. Program MARK: Survival estimation from populations of marked animals. Bird Study, 46(supplement), 120–138.

Published

2023-06-15