Seasonal variation in frog predation by black lion tamarins (Leontopithecus chrysopygus, Primates)

Garbino, Guilherme S. T.; Rezende, Gabriela Cabral; Antônio, Daphne Chiara; Bufalo, Felipe; Amaral, Rodrigo Gonçalves; e Silva, Anne-Sophie de Almeida; Kaisin, Olivier; Culot, Laurence

doi:10.1080/00222933.2022.2078242

Request a copy

Article (Scientific journals)

Seasonal variation in frog predation by black lion tamarins (Leontopithecus chrysopygus, Primates)

Garbino, Guilherme S. T.; Rezende, Gabriela Cabral; Antônio, Daphne Chiara et al.

2022 • In Journal of Natural History, 56 (5-8), p. 449 - 461

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/298194

DOI
10.1080/00222933.2022.2078242

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Garbino et al. 2022-Seasonal variation in frog predation by black lion tamarins.pdf

Author postprint (5.97 MB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Anura; Atlantic Forest; Callitrichidae; Hylidae; seasonality; Ecology, Evolution, Behavior and Systematics

Abstract :

[en] Although lion tamarins (Leontopithecus spp.) are known to prey upon frogs, no study has attempted to document the frequency and seasonal patterns of such events. In this study, we compiled data on frog predation by black lion tamarins, Leontopithecus chrysopygus, in south-eastern Brazil between 2014 and 2020. We investigated the effects of seasonality on predation rate and described the behaviour of the lion tamarins. In 1972 observation hours, we recorded 49 frog predation events. Predation was more intense in the beginning (April and May) and the end (August and September) of the dry season, suggesting seasonal variation. The observed pattern may be related to a combination of increased fruit availability in the rainy season and decreased frog activity in the height of the dry season. Compared to Saguinus mystax, the only other tamarin species for which there is available data, predation rate of anurans by black lion tamarins is five times higher. We suggest that frogs are an important item in the diet of black lion tamarins and reinforce the idea that vertebrate predation in some primates is seasonal.

Disciplines :

Zoology

Author, co-author :

Garbino, Guilherme S. T. ; Departamento de Biologia Animal, Museu de Zoologia João Moojen, Universidade Federal de Viçosa, Minas Gerais, Brazil

Rezende, Gabriela Cabral ; Instituto de Biociências, Universidade Estadual PaulistaPrograma de Pós-Graduação em Ecologia, Biodiversidade, Brazil ; Black Lion Tamarin Conservation Program, IPÊ – Instituto de Pesquisas Ecológicas, São Paulo, Brazil ; Laboratory of Primatology, Departamento de Biodiversidade, Instituto de Biociências, Universidade Estadual Paulista, São Paulo, Brazil

Antônio, Daphne Chiara ; Departamento de Biologia Animal, Museu de Zoologia João Moojen, Universidade Federal de Viçosa, Minas Gerais, Brazil

Bufalo, Felipe ; Instituto de Biociências, Universidade Estadual PaulistaPrograma de Pós-Graduação em Ecologia, Biodiversidade, Brazil ; Laboratory of Primatology, Departamento de Biodiversidade, Instituto de Biociências, Universidade Estadual Paulista, São Paulo, Brazil

Amaral, Rodrigo Gonçalves ; Laboratory of Primatology, Departamento de Biodiversidade, Instituto de Biociências, Universidade Estadual Paulista, São Paulo, Brazil ; Graduação em Zoologia, Instituto de Biociências, Universidade Estadual PaulistaPrograma de Pós, São Paulo, Brazil

e Silva, Anne-Sophie de Almeida ; Laboratory of Primatology, Departamento de Biodiversidade, Instituto de Biociências, Universidade Estadual Paulista, São Paulo, Brazil ; Graduação em Zoologia, Instituto de Biociências, Universidade Estadual PaulistaPrograma de Pós, São Paulo, Brazil

Kaisin, Olivier ; Université de Liège - ULiège > Sphères ; Laboratory of Primatology, Departamento de Biodiversidade, Instituto de Biociências, Universidade Estadual Paulista, São Paulo, Brazil

Culot, Laurence ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale ; Laboratory of Primatology, Departamento de Biodiversidade, Instituto de Biociências, Universidade Estadual Paulista, São Paulo, Brazil

Language :

English

Title :

Seasonal variation in frog predation by black lion tamarins (Leontopithecus chrysopygus, Primates)

Publication date :

2022

Journal title :

Journal of Natural History

ISSN :

0022-2933

eISSN :

1464-5262

Publisher :

Taylor and Francis Ltd.

Volume :

Issue :

5-8

Pages :

449 - 461

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.tandfonline.com/doi/pdf/10.1080/00222933.2022.2078242

Funders :

CAPES - Coordenação de Aperfeicoamento de Pessoal de Nível Superior
Rufford Foundation
F.R.S.-FNRS - Fonds de la Recherche Scientifique
FAPESP - Fundação de Amparo à Pesquisa do Estado de São Paulo

Funding text :

GSTG was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (Grant code 001); GCR received fellowships from FAPESP (process no. #2017/11962–9) and CAPES (code 001); FB was supported by CNPq (133172/2018-0 and 443489/2020-3); RGA received a fellowship from FAPESP (process no. #2019/11102–5); ASAS received a fellowship from CNPq (141813/2017-2) and a Small Grant from the Rufford Foundation (29108-1); OK received funding from the National Fund for Scientific Research (FRS-FNRS, Belgium). Fieldwork was financed by a Young Investigator grant from FAPESP given to LC (#2014/14739–0) and by the Disney Conservation Fund and the Sustainable Lush Fund granted to the Black Lion Tamarin Conservation Program. LC receives a Research Productivity Fellowship from CNPq. We are most grateful to José Wilson Alves and Andre P. de Albuquerque for their invaluable assistance in the field. Thank you also to Amandine Lambot, Mirela Alcolea, Miguel Rangel, Yness Messaoudi and Vinicius José Alves Pereira for their assistance in the field. Lisieux Fuzessy and Eduardo Zanette gave useful insights on the subject of the paper. Henrique Costa and Renan Lieto sent important literature on Atlantic Forest anurans. Gustavo Simões Libardi made the drawing in Figure 2.
Young Investigator grant from FAPESP given to LC

Available on ORBi :

since 06 January 2023

Statistics

Number of views

43 (1 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour. 49 (3–4): 227–267. doi: 10.1163/156853974X00534.
Beltrão-Mendes R, Cavalcante CB, Caldas FLS, Ferrari SF. 2016. Hypsiboas albomarginatus (White-edged treefrog). Predation. Herpetol Rev. 47: 110.
Beltrão-Mendes R, Luiz F, Caldas S, Adriano P, Santana DO. 2018. Predation of Boana raniceps (Cope, 1862) by the common marmoset Callithrix jacchus (Linnaeus, 1758) in northeastern Brazil. Herpetol Notes. 11: 1069–1074.
Butynski TM. 1982. Vertebrate predation by primates: a review of hunting patterns and prey. J Hum Evol. 11 (5): 421–430. doi: 10.1016/S0047-2484(82)80095-X.
Cavalcante T, Simões PI, Mourthe I. 2019. Predation of Boana boans (Anura, hylidae) by an opportunistic frugivorous primate. Acta Amaz. 49 (4): 307–310. doi: 10.1590/1809-4392201901430.
Culot L, Griese J, Knogge C, Tonini M, Mulato M, Estevam CG, Lopes BP, Mantovani B, Silva B, Heliodora B, et al. 2015. New records, reconfirmed sites and proposals for the conservation of Black Lion Tamarin (Leontopithecus chrysopygus) in the middle and upper Paranapanema. Neotrop Primates. 22: 32–39.
De Carvalho CT, Albernaz ALKM, De Lucca CAT. 1989. Aspectos da bionomia do mico-leão preto (Leontopithecus chrysopygus Mikan).(Mammalia, Callithricidae). Rev do Inst Florestal São Paulo. 1: 67–83.
Dietz JM, Peres CA, Pinder L. 1997. Foraging ecology and use of space in wild Golden Lion Tamarins (Leontopithecus rosalia). Am J Primatol. 41 (4): 289–305. doi: 10.1002/(SICI)1098-2345(1997)41:4<289::AID-AJP2>3.0.CO;2-T.
Eterovick PC, Sazima I. 2000. Structure of an anuran community in a montane meadow in southeastern Brazil: effects of seasonality, habitat, and predation. Amphib Reptil. 21 (4): 439–461. doi: 10.1163/156853800300059331.
Ferrari SF. 1993. Ecological differentiation in the Callitrichidae. In: Rylands AB, editor. Marmosets Tamarins Syst Behav Ecol. Oxford: Oxford University Press; p. 314–328.
Garber PA. 1992. Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae. Am J Phys Anthrop. 88 (4): 469–482. doi: 10.1002/ajpa.1330880404.
Garbino GST, Rezende GC, Valladares-Padua C. 2016. Pelage variation and distribution of the Black Lion Tamarin, Leontopithecus chrysopygus. Folia Primatol. 87 (4): 244–261. doi: 10.1159/000450998.
Garbino GST, da Silva LH, Amaral RG, Rezende GC, Pereira VJA, Culot L. 2020. Predation of treefrogs (Anura: Hylidae) with toxic skin secretions by the black lion tamarin (Leontopithecus chrysopygus, Callitrichinae). Primates. 61 (4): 567–572. doi: 10.1007/s10329-020-00818-1.
Heymann EW, Knogge C, Tirado Herrera ER. 2000. Vertebrate Predation by Sympatric Tamarins, Saguinus mystax and Saguinus fuscicollis. Am J Primatol. 51 (2): 153–158. doi: 10.1002/(SICI)1098-2345(200006)51:2<153::AID-AJP5>3.0.CO;2-T.
Keuroghlian A, Passos FC. 2001. Prey foraging behavior, seasonality and time-budgets in black lion tamarins, Leontopithecus chrysopygus (Mikan 1823) (Mammalia, Callitrichidae). Brazilian J Biol. 61 (3): 455–459. doi: 10.1590/S1519-69842001000300015.
Lüffe TM, Tirado ER, Mirjam H, Berles P, Smith AC, Knogge C, Heymann EW. 2018. Seasonal variation and an “ outbreak ” of frog predation by tamarins. Primates. 59 (6): 549–552. doi: 10.1007/s10329-018-0688-1.
Medici P. 2001. Translocação e manejo metapopulacional de mico-leão-preto, Leontopithecus chrysopygus Mikan, 1823 (Callitrichidae - Primates). Belo Horizonte: Universidade Federal de Minas Gerais.
Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC, Zipparro VB. 2000. Phenology of Atlantic rain forest trees: a comparative study. Biotropica. 32 (4b): 811–823. doi: 10.1111/j.1744-7429.2000.tb00620.x.
Morellato LPC, Camargo MGG, Gressler E. 2013. A review of plant phenology in South and Central America, and Schwartz M, editor. Phenology: an Integrative Environmental Science. Dordrecht: Springer; p. 91–113. doi: 10.1007/978-94-007-6925-0_6.
Passos FDC. 1999. Dieta de um grupo de mico-leão-preto, Leontopithecus chrysopygus (Mikan) (Mammalia, Callitrichidae), na Estação Ecológica dos Caetetus, São Paulo. Rev Bras Zool. 16 (suppl 1): 269–278. doi: 10.1590/S0101-81751999000500019.
Passos FDC, Keuroghlian A. 1999. Foraging behavior and microhabitats used by black lion tamarins, Leontopithecus chrysopygus (Mikan) (Primates, Callitrichidae). Rev Bras Zool. 16 (suppl 2): 219–222. doi: 10.1590/S0101-81751999000600022.
Rievers CR, Pires MRS, Eterovick PC. 2014. Habitat, food, and climate affecting leaf litter anuran assemblages in an Atlantic Forest remnant. Acta Oecologica [Internet]. 58: 12–21. doi: 10.1016/j.actao.2014.04.003.
Rolim GS, Camargo MBP, Lania DG, Moraes JFL. 2007. Classificação climática de Köppen e de Thornthwaite e sua aplicabilidade na determinação de zonas agroclimáticas para o Estado de São Paulo. Bragantia. 66 (4): 711–720. doi: 10.1590/S0006-87052007000400022.
Santos TG, Vasconcelos TDS, Rossa-Feres DDC, Haddad CFB. 2009. Anurans of a seasonally dry tropical forest: Morro do Diabo State Park, São Paulo state, Brazil. J Nat Hist. 43 (15–16): 973–993. doi: 10.1080/00222930802702498.
São Paulo. 1988. Decreto Estadual n° 28.169, de 21 de janeiro de 1988. Altera dispositivo do Decreto no 25.342, de 4 de junho de 1986.
Savage JM. 2002. The amphibians and reptilies of Costa Rica: a herpetofauna between two continents, between two seas. Chicago: The University of Chicago Press.
Terborgh J. 1983. Foraging for Prey. In: Terborgh J, editor. Five new world primates a study Comp Ecol. New Jersey: Princeton University Press; p. 96–127.
Toledo LF, Ribeiro RS, Haddad CFB. 2007. Anurans as prey: an exploratory analysis and size relationships between predators and their prey. J Zool. 271 (2): 170–177. doi: 10.1111/j.1469-7998.2006.00195.x.
Valladares-Padua CB. 1993. The ecology, behavior and conservation of the black lion tamarins (Leontopithecus chrysopygus Mikan, 1823). Gainesville: University of Florida.
Vasconcelos TDS, Dos Santos TG, Rossa-Feres DDC, Haddad CFB. 2011. Spatial and temporal distribution of tadpole assemblages (Amphibia, Anura) in a seasonal dry tropical forest of southeastern Brazil. Hydrobiologia. 673 (1): 93–104. doi: 10.1007/s10750-011-0762-9.
Ximenez SS, Tozetti AM. 2015. Seasonality in anuran activity and calling season in a Brazilian subtemperate wetland. Zool Stud. 54 (1): 47. doi: 10.1186/s40555-015-0125-8.