Abstract
Social behavior studies in mammals are commonly found in the literature. However, nothing is known on the hierarchical relationships of American marsupials, which are mainly composed of cryptic, nocturnal species. We aim to examine the existence of a domination and subordination relationship among Didelphis aurita females. For such purpose, we used capture and recapture data of five resident female individuals in a forest patch for 1 year. Comparative analyses among females were performed in relation to the temporal variation in body size, the spatial segregation in their home ranges, and the individual differences in their diets, all focusing on hierarchical relationships. Behavioral differences were observed between the hypothetically dominant female and other resident females, corroborating the hypothesis of hierarchy among D. aurita females. The dominant female presented larger home range, larger territory, stronger dominance over the patch center, and a mostly different diet regarding young females. Its diet changed from specific food items to a more diversified strategy in the following season, possibly due to the increased competition among adult females during the breeding season. After the disappearance of the dominant female, the central patch area was invaded by another large-sized, well-conditioned, and older female that lived in peripheral areas of the patch. Although the data are from a limited number of individuals and while we think that dominance hierarchy is the most likely explanation for the patterns observed, other interpretations are also possible, and further studies with more data and individuals are needed, to confirm the existence of dominance hierarchy in this species.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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The codes used in our analyses are available from the corresponding author on reasonable request.
References
Abrams PA (1984) Foraging time optimization and interactions in food webs. Am Nat 124:80–96
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Astúa D, Carvalho RA, Maia PF, Magalhães AR, Loretto D (2015) First evidence of gregarious denning in opossums (Didelphimorphia, Didelphidae), with notes on their social behaviour. Biol Lett 11:20150307
Belcher CA, Darrant JP (2004) Home range and spatial organization of the marsupial carnivore, Dasyurus maculatus maculatus (Marsupialia: Dasyuridae) in South-eastern Australia. J Zool 261:271–280
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57:289–300
Burt WH (1943) Territoriality and home range concepts as applied to mammals. J Mammal 24:346–352
Cáceres NC (2003) Use of the space by the opossum Didelphis aurita Wied-Newied (Mammalia, Marsupialia) in a mixed forest fragment of Southern Brazil. Rev Bras Zool 20(2):315–322
Cáceres NC, Machado AF (2013) Spatial, dietary and temporal niche dimensions in ecological segregation of two sympatric, congeneric marsupial species. Open Ecol J 6:10–23
Cáceres NC, Monteiro-Filho ELA (1998) Population dynamics of the common opossum, Didelphis marsupialis (Mammalia, Marsupialia), in southern Brazil. Z Säugetierkd 63:169–172
Cáceres NC, Monteiro-Filho ELA (2001) Food habits, home range and activity of Didelphis aurita (Mammalia, Marsupialia) in a forest fragment in Southern Brazil. Stud Neotrop Fauna E 36:85–92
Cáceres NC, Monteiro-Filho ELA (2007) Germination in seed species ingested by opossums: implications for seed dispersal and forest conservation. Braz Arch Biol Technol 50(6):921–928
Cáceres NC, Dittrich VAO, Monteiro-Filho ELA (1999) Fruit consumption, distance of seed dispersal and germination of solanaceous plants ingested by the common opossum (Didelphis aurita) in Southern Brazil. Rev Ecol (terre Vie) 54:225–234
Cáceres NC, Weber MM, Melo GL, Meloro C, Sponchiado J, Carvalho RS, Bubadué JM (2016) Which factors determine spatial segregation in the South American opossums (Didelphis aurita and D. albiventris)? An ecological niche modelling and geometric morphometrics approach. PLoS One 11(6):1–19
Cáceres NC, Delciellos AC, Prevedello JA, Brum M, Albanese MS (2022) Movement, habitat selection, and home range of American marsupials. In: Cáceres NC, Dickman CR (eds) American and Australasian marsupials: an evolutionary, biogeographical, and ecological approach. Springer, Cham
Cáceres NC (2000) Diet, feeding adaptation, and seed dispersal by marsupials in southern Brazil. Ph.D. dissertation, Universidade Federal do Paraná
Calenge C (2006) The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519
Ceotto P, Finotti R, Santori R, Cerqueira R (2009) Diet variation of the marsupials Didelphis aurita and Philander frenatus (Didelphimorphia, Didelphidae) in a rural area of Rio de Janeiro state, Brazil. Mastozool Neotrop 16(1):49–58
Cerboncini RAS, Passamani M, Braga TV (2011) Use of space by the black-eared opossum Didelphis aurita in a rural area in southeastern Brazil. Mammalia 75:287–290
Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67
Cleveland SW (1979) Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc 74:829–836
Clutton-Brock T, Huchard E (2013) Social competition and its consequences in female mammals. J Zool 289:151–171
Dolnik OV, Hoi H (2010) Honest signalling, dominance hierarchies and body condition in House Sparrows Passer domesticus (Aves: Passeriformes) during acute coccidiosis. Biol J Linn Soc 99(4):718–726
Draud M, Lynch PAE (2002) Asymmetric contests for breeding sites between monogamous pairs of convict cichlids (Archocentrus nigrofasciatum, Cichlidae): pair experience pays. Behaviour 139:861–873
Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol 16:257–333
Ferreira MS, Kajin M, Cerqueira R, Vieira MV (2016a) Marsupial population dynamics in a tropical rainforest: intraspecific competition and nonlinear effect of rainfall. J Mammal 97(1):121–127
Ferreira MS, Vieira MV, Cerqueira R, Dickman CR (2016b) Seasonal dynamics with compensatory effects regulate populations of tropical forest marsupials: a 16-year study. Oecologia 182:1095–1106
Fisher DO, Owens IPF (2000) Female home range size and the evolution of social organization in macropod marsupials. J Anim Ecol 69:1083–1098
Fleming TH (1972) Aspects of the population dynamics of three opossums in the Panama Canal Zone. J Mammal 53:619–623
Gagliardi-Seeley J, Leese J, Santangelo N, Itzkowitz M (2009) Mate choice in female convict cichlids (Amatitlania nigrofasciata) and the relationship between male size and dominance. J Ethol 27(2):249–254
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleon-tological statistics software package for education and data analysis. Palaeontol Electr 4:9
Harcourt AH (1987) Dominance and fertility among female primates. J Zool 213:471–487
Hodge SJ, Manica A, Flower TP, Clutton-Brock TH (2008) Determinants of reproductive success in dominant female meerkats. J Anim Ecol 77:92–102
Holand O, Gjostein H, Losvar A, Kumpula J, Smith ME, Roed KH, Nieminem M, Weladji RB (2004) Social rank in female reindeer (Rangifer tarandus): effects of body mass, antler size and age. J Zool 263:365–372
Holmes DJ (1991) Social behavior in captive Virginia opossums, Didelphis virginiana. J Mammal 72(2):402–410
Hossler RJ, McAninch JB, Harder JD (1994) Maternal denning behavior and survival of juveniles in opossums in southeastern New York. J Mammal 75(1):60–70
Huchard E, English S, Bell MBV, Thavarajah N, Clutton-Brock TH (2016) Competitive growth in a cooperative mammal. Nature 533:532–534
Kaufmann JH (1983) On the definitions and functions of dominance and territoriality. Biol Rev 58:1–20
Kelt DA, Van Vuren DH (2001) The ecology and macroecology of mammalian home range area. Am Nat 157:637–645
Koskela E, Mappes T, Ylonem M (1997) Territorial behavior and reprodutive sucess of bank vole Clethrionomys glareolus females. J Anim Ecol 66:341–349
Labocha MK, Hayes JP (2012) Morphometric indices of body condition in birds: a review. J Ornith 153:1–22
Lea AJ, Learn NH, Theus MJ, Altmann J, Alberts SC (2014) Complex sources of variance in female dominance rank in a nepotistic society. Anim Behav 94:87–99
Leiner NO, Silva WR (2009) Territoriality in females of the slender opossum (Marmosops paulensis) in the Atlantic Forest of Brazil. J Trop Ecol 25:671–675
Lessa LG, Costa FN (2010) Diet and seed dispersal by five marsupials (Didelphimorphia: Didelphidae) in a Brazilian cerrado reserve. Mamm Biol 75:10–16
Lindstorm J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14(9):343–348
Loretto D, Vieira MV (2005) The effects of reproductive and climatic seasons on movements in the black-eared opossum (Didelphis aurita Wied-Neuwied, 1826). J Mammal 86(2):287–293
Mazerolle MJ (2019) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.2-2. https://cran.r-project.org/package=AICcmodavg
McManus JJ (1970) Behavior of captive opossums, Didelphis marsupialis virginiana. J Mammal 84(1):144–169
Mendel SM, Vieira MV, Cerqueira R (2008) Precipitation, litterfall, and the dynamics of density and biomass in the black-eared opossum, Didelphis aurita. J Mammal 89(1):159–167
Miller EJ, Eldridge MDB, Cooper DW, Herbert CA (2010) Dominance, body size and internal relatedness influence male reproductive success in eastern grey kangaroos (Macropus giganteus). Reprod Fert Dev 22:539–549
Mohr CO, Stumpf WA (1966) Comparison of methods for calculating areas of animal activity. J Wildl Manage 30:293–304
Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10(2):58–62
Ostfeld RS (1990) The ecology of territoriality in small mammals. Trends Ecol Evol 5(12):411–415
Paglia AP, Fonseca GAB, Rylands AB, Herrmann G, Aguiar LMS, Chiarello AG, Leite YLR, Costa LP, Siciliano S, Kierulff MCM, Mendes SL, Tavares VC, Mittermeier RA, Patton JL (2012) Lista anotada dos mamíferos do Brasil/Annotated checklist of Brazilian mammals. 2. ed. Arlington, Conservation International (Occasional Papers in Conservation Biology, no. 6)
Pinheiro J, Bates D, DebRoy S, Sarkar D (2020) _nlme: linear and nonlinear mixed effects models_R package version 3.1-147. https://CRAN.R-project.org/package=nlme
Pires AS, Fernandez FAS (1999) Use of space by the marsupial Micoureus demerarae in small Atlantic Forest fragments in south-eastern Brazil. J Trop Ecol 15:279–290
Poulos DE, McCormick MI (2015) Asymmetries in body condition and order of arrival influence competitive ability and survival in a coral reef fish. Oecologia 179:719–728
Powell RA, Proulx G (2003) Trapping and marking terrestrial mammals for research: integrating ethics, performance criteria, techniques, and common sense. ILAR J 44(4):259–276
Pruetz JD, Isbell LA (2000) Correlations of food distribution and patch size with agonistic interactions in female vervets (Chlorocebus aethiops) and patas monkeys (Erythrocebus patas) living in simple habitats. Behav Ecol Sociobiol 49:38–47
R Development Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. https://www.R-project.org/
Rosvall KA (2011) Intrasexual competition in females: evidence for sexual selection? Behav Ecol 22:1131–1140
Russell EM (1984) Social behaviour and social organization of marsupials. Mammal Rev 14(3):101–154
Russell AF, Carlson AA, McIlrath GM, Jordan NR, Clutton-Brock T (2004) Adaptive size modification by dominant female meerkats. Evolution 58:1600–1607
Ryser J (1992) The mating system and male mating success of the Virginia opossum (Didelphis virginiana) in Florida. J Zool 228:127–139
Ryser J (1995) Activity, movement and home range of Virginia opossum (Didelphis virginiana) in Florida. Bull Florida Mus Nat Hist 38:177–194
Schradin C, Schmohl G, Rödel HG, Schoepf I, Treffler SM, Brenner J, Bleeker M, Schubert M, König B, Pillay N (2010) Female home range size is regulated by resource distribution and intraspecific competition: a long-term field study. Anim Behav 79:195–203
Schulte-Hostedde AI, Millar JS, Hickling GJ (2001) Evaluating body condition in small mammals. Can J Zool 79:1021–1029
Sikes RS, Thompson TA, Bryan JA II (2019) American Society of Mammalogists: raising the standards for ethical and appropriate oversight of wildlife research. J Mammal 100(3):763–773
Stockley P, Bro-Jorgensen J (2011) Female competition and its evolutionary consequences in mammals. Biol Rev 86:341–366
Sunquist ME, Eisenberg JF (1993) Reproductive strategies of female didelphis. Bull Florida Mus Nat Hist 36(4):109–140
Toni P, Forsyth DM, Festa-Bianchet M (2020) Forage availability and maternal characteristics affect costs of reproduction in a large marsupial. Oecologia 193:97–107
Tucker MA, Ord TJ, Rogers TL (2014) Evolutionary predictors of mammalian home range size: body mass, diet and the environment. Glob Ecol Biogeogr 23:1105–1114
Tyndale-Biscoe CH, Mackenzie RB (1976) Reproduction in Didelphis marsupialis and D. albiventris in Colombia. J Mammal 57(2):249–265
Vieira EM, Camargo NF (2013) Uso do espaço vertical por marsupiais brasileiros. In: Cáceres NC (ed) Os marsupiais do Brasil: Biologia, ecologia e conservação. Editora UFMS, Campo Grande, pp 365–383
Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2020) gplots: various R programming tools for plotting data. R package version 3.1.1. https://CRAN.R-roject.org/package=gplots
Wilder SM, Le Couteur DG, Simpson SJ (2013) Diet mediates the relationship between longevity and reproduction in mammals. Age 35:921–927
Wolff JO (1993) Why are female small mammals territorial? Oikos 68(2):346–370
Woodroffe R, MacDonald DW (1995) Female/female competition in European badgers Meles meles: effects on breeding success. J Anim Ecol 64:12–20
Worton BJ (1989) Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70(1):164–168
Acknowledgements
We thank the Companhia Paranaense de Energia (COPEL) for the authorization to use the study area at Curitiba during the master dissertation research of Nilton Cáceres at UFPR. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001 to MNB. NCC is a Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ) research fellow in Brazil (process number 313.191/2018-2).
Funding
This study was financed in part by the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brazil (CAPES)”-Finance Code 001 to MNB. Nilton Cáceres is supported by the “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ)” in Brazil (research fellow, process number 313.191/2018-2).
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NCC and MNB contributed to the study conception and design. Data collection was performed by NCC. Material preparation was performed by MNB. Analyses were performed by MNB and GLM. All authors read and approved the final manuscript.
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All applicable international and/or national guidelines for the care and use of animals were followed (Sikes et al. 2019). Although there was no institutional ethical committee (this was created only in 2003: http://www.bio.ufpr.br/portal/ceua/home/) during the time animals were sampled (1995), the authors (NCC) followed the best practices of animal care (e.g., when capturing and marking) during the animal manipulation (see Sikes el al. 2019). These included shelter over traps to protect captured animals from environmental conditions, revision of traps during early morning (because the focal species is nocturnal), gently handling the animals for data record, and assuring a safe animal release after handling.
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Brum, M.d., Melo, G.L. & Cáceres, N.C. Ecological evidence of hierarchy and competition in Didelphis aurita females. Mamm Biol 102, 1709–1721 (2022). https://doi.org/10.1007/s42991-022-00269-9
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DOI: https://doi.org/10.1007/s42991-022-00269-9