Abstract
Agonistic encounters among carnivores can be potentially avoided or minimized by shifts in daily activity patterns. Here, we investigated the temporal ecology of mesocarnivores which co-occur in a semiarid area where top predators are virtually absent. More specifically, we (i) describe the daily activity patterns of six mesocarnivore species, (ii) evaluate possible seasonal changes in their daily activity patterns, (iii) examine patterns of temporal overlap among mesocarnivores, and (iv) test the overlap in daily activity between mesocarnivores and their potential prey. Using camera-trapping data (13,976 camera-days) and circular and overlapping analyses, we studied six out of the seven mesocarnivore species recorded. Striped hog-nosed skunk and the crab-eating raccoon were nocturnal, crab-eating fox and northern tiger cat were nocturnal-crepuscular, ocelot was mainly nocturnal, and jaguarundi was diurnal. With the exception of jaguarundi, we fail to find strong temporal segregation among mesocarnivore and interspecific interactions did not vary seasonally, but we observed separation in their activity peaks and significant difference in their activity distributions. This partial temporal segregation can potentially contribute to interspecific coexistence, reducing the chances of interspecific killing, mainly in relation to the dominant species (ocelot). Mesocarnivores did not exhibit a significant synchrony of their activity with any of the preys evaluated, with the exception of jaguarundi, which significantly overlapped its distribution of activity with some preys. Temporal segregation contributes, but does not seem to be the only mechanism behind the coexistence of mesocarnivores in Caatinga dry forest; thus, other strategies such as spatial and dietary segregation should be considered.
Similar content being viewed by others
References
Andrade EM, Aquino DN, Chaves LCG, Lopes FB (2017) Water as capital and its uses in the Caatinga. In: Silva JC, Leal I, Tabarelli M (eds) Caatinga: the largest tropical dry forest region in South America. Springer, Cham, pp 281–302
Antongiovanni M, Venticinque EM, Fonseca CR (2018) Fragmentation patterns of the Caatinga drylands. Landsc Ecol 33:1353–1367. https://doi.org/10.1007/s10980-018-0672-6
Astete S, Marinho-Filho J, Kajin M, Penido G, Zimbres B, Sollmann R, Jácomo ATA, Tôrres NM, Silveira L (2017a) Forced neighbours: coexistence between jaguars and pumas in a harsh environment. J Arid Environ 146:27–34. https://doi.org/10.1016/j.jaridenv.2017.07.005
Astete S, Marinho-Filho J, Machado RB, Zimbres B, Jácomo ATA, Sollmann R, Tôrres NM, Silveira L (2017b) Living in extreme environments: modeling habitat suitability for jaguars, pumas, and their prey in a semiarid habitat. J Mammal 98:464–474. https://doi.org/10.1093/jmammal/gyw184
Azevedo FC, Lemos FG, Almeida LB, Campos CB, Beisiegel BDM, Paula RC, Crawshaw Junior PG, Ferraz KMP, Barros M, De Oliveira TG (2013) Avaliação do risco de extinção da onça-parda Puma concolor (Linnaeus, 1771) no Brasil. Biodiv Brasil 3:107–121
Bennie JJ, Duffy JP, Inger R, Gaston KJ (2014) Biogeography of time partitioning in mammals. Proc Natl A Sci 111:13727–13732. https://doi.org/10.1073/pnas.1216063110
Bianchi RC, Olifiers N, Gompper ME, Mourão G (2016) Niche partitioning among pesocarnivores in a Brazilian Wetland. PLoS One 11:e0162893. https://doi.org/10.1371/journal.pone.0162893
Bu H, Wang F, McShea WJ, Lu Z, Wang D, Li S (2016) Spatial co-occurrence and activity patterns of mesocarnivores in the temperate forests of Southwest China. PLoS One 11:e0164271. https://doi.org/10.1371/journal.pone.0164271
Cabús R (2015) Tropsolar 5.0. Grupo de Pesquisa em Iluminação (GRILU). http://www.ctec.ufal.br/grupopesquisa/gril. Accessed 15 April 2019
Carmignotto AP, Astúa D (2017) Mammals of the Caatinga: diversity, ecology, biogeography, and conservation. In: Silva JC, Leal I, Tabarelli M (eds) Caatinga: the largest tropical dry forest region in South America. Springer, Cham, pp 211–254
Carothers JH, Jaksic FM (1984) Time as a niche difference: the role of interference competition. Oikos 42:403–406. https://doi.org/10.2307/3544413
Cavalcanti GN, Alfaro-Alvarado LD, Rodrigues FHG (2014) Home range and activity of Conepatus semistriatus (Carnivora, Mephitidae) in Emas National Park, Brazil. Anim Biol 64:151–162. https://doi.org/10.1163/15707563-00002436
Cheida CC, Rodrigues FHG, Beisiegel BM (2013) Avaliação do risco de extinção do Guaxinim Procyon cancrivorus (Cuvier, 1798) no Brasil. Biodiv Brasil 3:283–290
Crooks KR, Soulé ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566. https://doi.org/10.1038/23028
De Angelo C, Paviolo A, Di Blanco Y, Di Bitetti M, Chiappe A (2015) Guía de huellas de los mamíferos de Misiones y otras áreas del subtrópico de Argentina. Ediciones del Subtrópico, Tucumán
Di Bitetti MS, De Angelo CD, Di Blanco YE, Paviolo A (2010) Niche partitioning and species coexistence in a Neotropical felid assemblage. Acta Oecol 36:403e412. https://doi.org/10.1016/j.actao.2010.04.001
Dias DM, Bocchiglieri A (2015) Dieta de carnívoros (Mammalia, Carnivora) em um remanescente de Caatinga, Nordeste do Brasil. Bioikos 29:13–19
Dias DM, Bocchiglieri A (2016) Trophic and spatio-temporal niche of the crab-eating fox, Cerdocyon thous (Linnaeus, 1766) (Carnivora: Canidae), in a remnant of the Caatinga in northeastern Brazil. Mammalia 80:281–291. https://doi.org/10.1515/mammalia-2014-0108
Dias DM (2017) Spatiotemporal ecology of the striped hog-nosed skunk Conepatus semistriatus (Carnivora, Mephitidae) in a seasonally dry forest of northeastern Brazil. Anim Biol 2:119–131. https://doi.org/10.1163/15707563-00002525
Dias DM, Campos CB, Rodrigues FHG (2018) Behavioural ecology in a predator-prey system. Mamm Biol 92:30–36. https://doi.org/10.1016/j.mambio.2018.04.005
Dias DM, Massara RL, Campos CB, Rodrigues FHG (2019) Feline predator-prey relationships in a semi-arid biome in Brazil. J Zool 307:282–291. https://doi.org/10.1111/jzo.12647
Emsens WJ, Hirsch BT, Kays R, Jansen PA (2013) Prey refuges as predator hotspots: ocelot (Leopardus pardalis) attraction to agouti (Dasyprocta punctata) dens. Acta Theriol 59:257–262. https://doi.org/10.1007/s13364-013-0159-4
Feijó A, Langguth A (2013) Mamíferos de médio e grande porte do Nordeste do Brasil: distribuição e taxonomia, com descrição de novas espécies. Rev Nord Biol 22:3–225
Fonseca CR, Antongiovanni M, Matsumoto M, Bernard E, Venticinque EM (2017) Conservation opportunities in the Caatinga. In: Silva JC, Leal I, Tabarelli M (eds) Caatinga: the largest tropical dry forest region in South America. Springer, Cham, pp 429–443
Foster VC, Sarmento P, Sollmann R, Tôrres N, Jácomo ATA, Negrões N, Fonseca C, Silveira L (2013) Jaguar and puma activity patterns and predator-prey interactions in four Brazilian biomes. Biotropica 45:373–379. https://doi.org/10.1111/btp.12021
Gaynor KM, Hojnowski CE, Cater NH, Bashares JS (2018) The influence of human disturbance on wildlife nocturnality. Science 360:1232–1123. https://doi.org/10.1126/science.aar7121
Giordano AJ (2016) Ecology and status of the jaguarundi Puma yagouaroundi: a synthesis of existing knowledge. Mammal Rev 46:30–43. https://doi.org/10.1111/mam.12051
Gómez H, Wallace RB, Ayala G, Tejada R (2005) Dry season activity periods of some Amazonian mammals. Stud Neotropical Fauna Environ 40:91–95. https://doi.org/10.1080/01650520500129638
Goulart FVB, Cáceres NC, Graipel ME, Tortato MA, Ghizoni IR Jr, Oliveiras-Santos LGR (2009) Habitat selection by large mammals in a southern Brazilian Atlantic Forest. Mamm Biol 74:182–190. https://doi.org/10.1016/j.mambio.2009.02.006
Kasper CB, Leuchtenberger C, Bornholdt R, Pontes ARM, Beisiegel BM (2013) Avaliação do risco de extinção do furão Galictis cuja (Molina, 1782) no Brasil. Biodiv Brasil 3:203–210
Linkie M, Ridout MS (2011) Assessing tiger-prey interactions in Sumatran rainforests. J Zool 284:224–229. https://doi.org/10.1111/j.1469-7998.2011.00801.x
Lucherini M, Reppucci JI, Walker RS, Villalba ML, Wurstten A, Gallardo G, Iriarte A, Villalobos R, Perovic P (2009) Activity pattern segregation of carnivores in the high Andes. J Mammal 90:1404–1409. https://doi.org/10.1644/09-MAMM-A-002R.1
Marinho PH, Bezerra D, Antongiovanni M, Fonseca CR, Venticinque EM (2018a) Mamíferos de médio e grande porte da Caatinga do Rio Grande do Norte, nordeste do Brasil. Mastozool Neotrop 25:345–362. https://doi.org/10.31687/saremMN.18.25.2.0.15
Marinho PH, Bezerra D, Antongiovanni M, Fonseca CR, Venticinque EM (2018b) Activity patterns of the threatened northern tiger cat Leopardus tigrinus and its potential prey in a Brazilian dry tropical forest. Mamm Biol 89:30–36. https://doi.org/10.1016/j.mambio.2017.12.004
Massara RL, Paschoal AMO, Bailey LL, Doherty PF Jr, Chiarello AG (2016) Ecological interactions between ocelots and sympatric mesocarnivores in protected areas of the Atlantic Forest, southeastern Brazil. J Mammal 97:1634–1644. https://doi.org/10.1093/jmammal/gyw129
Meredith M, Ridout M (2018) Overview of the overlap package. R Project. 1–9. https://cran.r project.org/web/packages/overlap/vignettes/overlap.pdf. Accessed 04 February 2019
MMA (2016) Áreas Prioritárias para conservação, uso sustentável e repartição de benefícios da biodiversidade do bioma Caatinga – 2ª atualização - Portaria N°223, de 21 de junho de 2016 Ministério do Meio Ambiente http://www.mma.gov.br/areas-protegidas/cadastro-nacional-de-ucs/item/10724-resultados-da-2%C2%B0-atualiza%C3%A7%C3%A3o-das-%C3%A1reas-priorit%C3%A1rias.html Accessed 20 December 2018
Monterroso P, Alves PC, Ferreras P (2013) Catch me if you can: diel activity patterns of mammalian prey and predators. Ethology 119:1044–1056. https://doi.org/10.1111/eth.12156
Monterroso P, Aves PC, Ferreras P (2014) Plasticity in circadian activity patterns of mesocarnivores daily activity coexistence. Behav Ecol Sociobiol 68:1403–1417. https://doi.org/10.1007/s00265-014-1748-1
Morato RG, Beisiegel BM, Ramalho EE, Campos CB, Boulhosa RLP (2013) Avaliação do risco de extinção da onça-pintada Panthera onca (Linnaeus, 1758) no Brasil. Biodiv Brasil 3:122–132
Moreno RS, Kays RW, Samudio R Jr (2006) Competitive release in diets of ocelot (Leopardus pardalis) and puma (Puma concolor) after jaguar (Panthera onca) decline. J Mammal 87:808–816. https://doi.org/10.1644/05-MAMM-A-360R2.1
Nagy-Reis MB, Iwakami VHS, Estevo CA, Setz EZF (2019) Temporal and dietary segregation in a Neotropical small-felid assemblage and its relation to prey activity. Mamm Biol 95:1–8. https://doi.org/10.1016/j.mambio.2018.12.005
Nouvellet P, Rasmussen GSA, MacDonald DW, Courchamp F (2012) Noisy clocks and silent sunrises: measurement methods of daily activity pattern. J Zool 286:179–184. https://doi.org/10.1111/j.1469-7998.2011.00864.x
Oliveira TG, Pereira JA (2014) Intraguild predation and interspecific killing as structuring forces of carnivoran communities in South America. J Mamm Evol 21:427–436. https://doi.org/10.1007/s10914-013-9251-4
Oliveira-Santos LGR, Graipel ME, Tortato MA, Zucco CA, Cáceres NC, Goulart FVB (2012) Abundance changes and activity flexibility of the northern tiger cat, Leopardus tigrinus (Carnivora: Felidae), appear to reflect avoidance of conflict. Zoologia 29:115–120. https://doi.org/10.1590/S1984-46702012000200003
Olmos F (1993) Notes on the food habitats of Brazilian “Caatinga” carnivores. Mammalia 57:126–130
Pita R, Mira A, Beja P (2011) Circadian activity rhythms in relation to season, sex and interspecific interactions in two Mediterranean voles. Anim Behav 81:1023–1030. https://doi.org/10.1016/j.anbehav.2011.02.007
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) Annotated checklist of Brazilian mammals. 2nd edition. Occas Pap Conserv Biol 6:1–76
Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. Am Nat 153:492–508. https://doi.org/10.1086/303189
Penido G, Astete S, Jácomo ATA, Sollmann R, Tôrres N, Silveira L, Marinho Filho J (2017) Mesocarnivore activity patterns in the semiarid Caatinga: limited by the harsh environment or affected by interspecifc interactions? J Mammal 98:1732–1740. https://doi.org/10.1093/jmammal/gyx119
Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330. https://doi.org/10.1146/annurev.es.20.110189.001501
Porfirio G, Foster VC, Fonseca C, Sarmento P (2016) Activity patterns of ocelots and their potential prey in the Brazilian Pantanal. Mamm Biol 81:511–517. https://doi.org/10.1016/j.mambio.2016.06.006
Projeto Caatinga Potiguar (2015) Projeto Caatinga Potiguar – Cartograma. WCS-Brazil/UFRN. http://programs.wcs.org/brazil/Lugares-naturais/Projeto-Caatinga.aspx. Accessed 02 November 2017
Prugh LR, Golden CD (2014) Does moonlight increase predation risk? Meta-analysis reveals divergent responses of nocturnal mammals to lunar cycles. J Anim Ecol 83:504–514. https://doi.org/10.1111/1365-2656.12148
Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Bashares JS (2009) The rise of the mesopredator. Bioscience 59:779–791. https://doi.org/10.1525/bio.2009.59.9.9
R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/ Accessed 30 April 2018
Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998. https://doi.org/10.1111/j.1461-0248.2009.01347.x
Roemer GW, Gompper ME, Valkenburgh BV (2009) The ecological role of the mammalian mesocarnivore. BioScience 59:165–173. https://doi.org/10.1525/bio.2009.59.2.9
Ridout MS, Linkie M (2009) Estimating overlap of daily activity patterns from camera trap data. J Agr Biol Envir St 14:322–337. https://doi.org/10.1198/jabes.2009.08038
Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39. https://doi.org/10.1126/science.185.4145.27
Silva JMC, Barbosa LCF, Leal I, Tabarelli M (2017) The Caatinga: understanding the challenges. In: Silva JC, Leal I, Tabarelli M (eds) Caatinga: the largest tropical dry forest region in South America. Springer, Cham, pp 3–19
Stoner K, Timm RM (2011) Seasonally dry tropical forest mammals: adaptations and seasonal patterns. In: Dirzo R, Young HS, Mooney HA, Ceballos G (eds) Seasonally dry tropical forests: ecology and conservation. Island Press, Washington, pp 85–106
Terrien J, Perret M, Aujard F (2011) Behavioral thermoregulation in mammals: a review. Front Biosci 16:1428–1444. https://doi.org/10.2741/3797
Tomasella J, Silva RMPV, Barbosa AA, Rodriguez DA, Oliveira MS, Sestini MF (2018) Desertification trends in the Northeast of Brazil over the period 2000–2016. Int J Appl Earth Obs 73:197–206. https://doi.org/10.1016/j.jag.2018.06.012
Vanak AT, Fortin D, Thaker M, Ogden M, Owen C, Greatwood S, Slotow R (2013) Moving to stay in place: behavioral mechanisms for coexistence of African large carnivores. Ecology 94:2619–2631. https://doi.org/10.1890/13-0217.1
Velloso AL, Sampaio EVSB, Pareyn FGC (2002) Ecorregiões propostas para o Bioma Caatinga. Associação Plantas do Nordeste, Instituto de Conservação Ambiental, The Nature Conservancy do Brasil, Recife
Valeix M, Chamaillé-Jammes S, Fritz H (2007) interference competition and temporal niche shifts – elephants and herbivore communities at waterholes. Oecologia 153:739–748. https://doi.org/10.1007/s00442-007-0764-5
Wang E (2002) Diets of Ocelots (Leopardus pardalis), Margays (L. wiedii), and Oncillas (L. tigrinus) in the Atlantic rainforest in Southeast Brazil. Stud Neotrop Fauna E 37:207–212. https://doi.org/10.1076/snfe.37.3.207.8564
Wang Y, Allen ML, Wilmers CC (2015) Mesopredator spatial and temporal responses to large predators and human development in the Santa Cruz Mountains of California. Biol Conserv 190:23–33. https://doi.org/10.1016/j.biocon.2015.05.007
Woodroffe R, Ginsberg JR (1998) Edge effects and the extinction of populations inside protected areas. Science 280:2126–2128. https://doi.org/10.1126/science.280.5372.2126
Ximenez A (1982) Notas sobre felidos neotropicales viii observaciones sobre el contenido estamacal y el comportamiento alimentar de diversas espécies de felinos. Rev Nord Biol 5:89–91
Acknowledgments
We are grateful to João B. de Lima (Seu João) and Joana Darque for the field assistance and hospitality, and to Eugenia C. Schmidt, Juan C. V. Mena, Felipe Marinho, Raul dos Santos, Maria L. Falcão, V. Paixão, and T. Oliveira for field or analysis assistance. We would like to thank two anonymous reviewers who helped to improve the work.
Funding
This study was partially supported by Restaurante Camarões and The Mohamed bin Zayed Species Conservation Fund (#172516360). PHM, PS, and CF would like to thank the University of Aveiro and FCT/MEC for the financial support to CESAM RU (UID/AMB/50017) through national funds and co-financed by the FEDER, within the PT2020 Partnership Agreement. EMV (308040/2017-1) and CRF (305304/2013-5; 306812/2017-7) were supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and PHM was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES; financing code 001) and Santander Universities (Santander Mundi scholarship).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 769 kb)
Rights and permissions
About this article
Cite this article
Marinho, P.H., Fonseca, C.R., Sarmento, P. et al. Temporal niche overlap among mesocarnivores in a Caatinga dry forest. Eur J Wildl Res 66, 34 (2020). https://doi.org/10.1007/s10344-020-1371-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10344-020-1371-6