Abstract
Insectivorous-frugivorous birds have been described to benefit from multiple forms of interspecific feeding associations. Here we present quantitative data on a new feeding association between the black-goggled tanager (Trichothraupis melanops) and an endangered frugivorous-faunivorous neotropical primate, the black lion tamarin (Leontopithecus chrysopygus), at an Atlantic Forest remnant in São Paulo state, Brazil. Using scan data from full day follows with a group of lion tamarins, we investigated if the behaviors displayed by the primates influenced the presence, behavior, and proximity of the tanagers. We observed the black-goggled tanagers to activelly follow the primates during the day, always positioned below the primates, and to capture insects flushed by the lion tamarins’ foraging activities. We found that black-goggled tanagers associated significatively more with black lion tamarins in the early hours of the day (i.e., from 6:00 to 8:59 a.m.) and when the primates were feeding/foraging. We found no evidence that the black lion tamarin benefits or incurs costs from associating with the tanagers, suggesting a new record of commensalism.
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
BirdLife International (2016) Trichothraupis melanops. The IUCN Red List of threatened species 2016: e.T22722406A94765253. https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22722406A94765253.en. Accessed 27 August 2021
Boinski S, Scott PE (1988) Association of birds with monkeys in Costa Rica. Biotropica 20:136–143. https://doi.org/10.2307/2388186
Esquivel A, Peris S (2008) Influence of time of day, duration and number of counts in point count sampling of birds in an Atlantic Forest of Paraguay. Ornitol Neotrop 19:229–242
Faria CMA, Rodrigues M (2009) Birds and army ants in a fragment of the Atlantic Forest of Brazil. J Field Ornithol 80:328–335. https://doi.org/10.1111/j.1557-9263.2009.00238.x
Fávaro FL, Anjos L (2005) Microhabitat of Habia rubica (Vieillot) and Trichothraupis melanops (Vieillot) (Aves, Emberizidae, Thraupinae) in an Atlantic Forest, southern Brazil. Rev Bras Zool 22:213–217. https://doi.org/10.1590/S0101-81752005000100026
Gomes G, Freitas TC, Cunha HC, Jacobs F, Spenst Wall M (2020) New records and range extension of black-goggled tanager, Trichothraupis melanops (Vieillot, 1818) (Passeriformes, Thraupidae), in extreme southern Brazil. Check List 16:67–73. https://doi.org/10.15560/16.1.67
Hankerson SJ, Dietz JM, Raboy BE (2006) Associations between golden-headed lion tamarins and the bird community in the Atlantic Forest of southern Bahia. Int J Primatol 27:487–495. https://doi.org/10.1007/s10764-006-9025-4
Heymann EW, Hsia SS (2015) Unlike fellows—a review of primate-non-primate associations. Biol Rev 90:142–156. https://doi.org/10.1111/brv.12101
Hilty S (2020) Black-goggled tanager (Trichothraupis melanops). In: Del Hoyo J, Elliott A, Sargatal J, Christie DA, De Juana E (eds) Birds of the world. Cornell Lab of Ornithology, Ithaca, NY, USA
Kuniy A, Morais JM, Gomes E (2003) Associação do arapaçu-verde (Sittasomus griseicapillus, Vieillot, 1818) com o mico leão dourado (Leontopithecus rosalia, Linnaeus, 1766), Reserva Biológica União, Rio das Ostras, Brasil. Acta Biol Leopold 25:261–264
Lescano CH, Oliveira IP, Lima FF, Baldivia DS, Justi PN, Cardoso CAL, Raposo Júnior JL, Sanjinez-Argandoña EJ (2018) Nutritional and chemical characterizations of fruits obtained from Syagrus romanzoffiana, Attalea dubia, Attalea phalerata and Mauritia flexuosa. J Food Meas Charact 12:1284–1294. https://doi.org/10.1007/s11694-018-9742-3
Maldonado-Coelho M, Durães R (2003) The black-goggled tanager (Trichothraupis Melanops): an occasional kleptoparasite in mixed-species bird flocks and ant swarms of southeastern Brazil. Ornitol Neotrop 14:397–404
Maldonado-Coelho M, Marini MA (2000) Effects of forest fragment size and successional stage on mixed-species bird flocks in southeastern Brazil. Condor 102:585–594. https://doi.org/10.1093/condor/102.3.585
Manhães MA, Loures-Ribeiro A, Dias MM (2010) Diet of understorey birds in two Atlantic Forest areas of southeast Brazil. J Nat Hist 44:469–489. https://doi.org/10.1080/00222930903380947
Martínez AE, Parra E, Gomez JP, Vredenburg VT (2021) Shared predators between primate groups and mixed species bird flocks: the potential for forest-wide eavesdropping networks. Oikos, Online Version. https://doi.org/10.1111/oik.08274
Moro-Rios RF, Silva-Pereira JE, Ludwig G, Barriento FG (2018) Interspecific associations between two woodcreeper species (Dendrocolaptinae) and a group of black-faced lion tamarins (Primates, Callitrichinae). Ardeola 65:299. https://doi.org/10.13157/arla.65.2.2018.sc3
Passos FC (1997) A foraging association between the olivaceous woodcreeper Sittasomus griseicapillus and the black lion tamarin Leontopithecus chrysopygus in south-east Brazil. Cienc Cult 49:144–145
Pizo MA, Melo AS (2010) Attendance and co-occurrence of birds following army ants in the Atlantic Rain Forest. Condor 112:571–578. https://doi.org/10.1525/cond.2010.090057
R Core Team (2020) R: a language and environment for statistical computing. In. R Foundation for Statistical Computing, Vienna, Austria
Rezende GC, Knogge C, Passos FC, Ludwig G, Oliveira LC, Jerusalinsky L, Mittermeier RA (2020) Leontopithecus chrysopygus. The IUCN Red List of threatened species 2020: e.T11505A17935400. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T11505A17935400.en. Accessed 17 July 2020.
Robbins CS (1981) Effect of time of day on bird activity. Stud Avian Biol 6:275–286
Rodrigues M, Machado CG, Suzana MRA, Galetti M (1994) Association of the black-goggled tanager (Trichothraupis melanops) with flushers. Biotropica 26:472–475. https://doi.org/10.2307/2389245
Siegel CE, Hamilton JM, Castro NR (1989) Observations of the red-billed ground-cuckoo (Neomorphus pucheranii) in association with tamarins (Saguinas) in northeastern Amazonian Peru. Condor 91:720–722. https://doi.org/10.2307/1368126
Stotz DF, Fitzpatrick JW, Parker TA III, Moskovits DK (1996) Neotropical birds: ecology and conservation. University of Chicago Press
Terborgh J (1983) Five new world primates: a study in comparative ecology. Princeton University Press, Priceton
Willis E (1986) Tanagers, finches, and weavers as ant followers. Gerfaut 76:307–316
Acknowledgements
We thank Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and National Fund for Scientific Research (FRS-FNRS, Belgium) for research fellowships and financial support to this study.
Funding
FB is curently a Ph.D. scholarchip holder from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, 443489/2020-3), and during the development of this study received a Ms.C. scholarship from CNPq (133172/2018-0). OK receives a fellowship from the National Fund for Scientific Research (FRS-FNRS, Belgium). RGA reseaved a fellowship from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, 2019/11102-5) and currently is a scholarship holder from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). This research was financed by a Young Investigator grant from FAPESP given to LC (#2014/14739-0).
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FB, RGA, OK, and LC designed the study and investigated the data; RGA and OK performed fieldwork; FB analyzed the data; FB wrote the original draft; and all authors contributed to the final version of the manuscript.
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Permits for this project were granted by Instituto Chico Mendes da Conservação da Biodiversidade (SISBIO, #65113, #68253) and by the Comitê de Ética no Uso Animal–IB, UNESP, Rio Claro (CEUA, #6581).
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The authors declare no competing interests.
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Communicated by Cristiano Azevedo (Associate Editor)
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Bufalo, F., Amaral, R.G., Kaisin, O. et al. A new feeding association between black-goggled tanagers (Tachyphoninae) and black lion tamarins (Primates, Callitrichinae). Ornithol. Res. 30, 216–220 (2022). https://doi.org/10.1007/s43388-022-00099-w
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DOI: https://doi.org/10.1007/s43388-022-00099-w