Abstract
Coastal areas prone to flooding are relatively neglected in primate studies. Eight out of 29 known populations of Critically Endangered Sapajus flavius occur in areas very close to, or containing, mangrove and várzea (i.e., tidal forests) forests, suggesting that these habitats are important for the species. We monitored Sapajus flavius in a mosaic of mangrove forest, estuarine várzea forest, and terra firme forest (i.e., nonfloodable forest) in northeastern Brazil. We carried out the study through direct observations of the animals, tracking their signs and baited camera trapping, between January and December 2016. Direct observations and signs provided 292 records of Sapajus flavius: 61% in terra firme, 36% in várzea, and 3% in mangrove. We recorded 26 food items consumed: 17 plants and 9 animals. Camera trapping provided 396 records of the animals: 21% in terra firme, 73% in várzea, and 6% in mangrove. Concurrent visits to more than one camera trap station suggested fission–fusion behavior in Sapajus flavius. We recorded carried infants throughout 2016, suggesting the absence of reproductive seasonality in the species. Adult females carried infants on 68% of occasions, suggesting that they play a key role in infant care. Sapajus flavius was largely diurnal but showed some crepuscular activity. Agonistic behaviors, although rare, were positively related to the quantity of food available in the baited camera trap stations, while play behaviors were negatively related to food availability. Coastal areas prone to flood are used by Sapajus flavius, especially várzea, and thus they should receive wide attention from researchers and protection from the government to avoid local extinctions of Sapajus flavius and other primates inhabiting such areas in Brazil.
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References
Alfaro, A. C. (2010). Effects of mangrove removal on benthic communities and sediment characteristics at Mangawhai harbour, northern New Zealand. ICES Journal of Marine Science, 67, 1087–1104.
Alongi, D. M. (2002). Present state and future of the world's mangrove forests. Environmental Conservation, 29, 331–349.
Alongi, D. M. (2008). Mangrove forest: Resilience, protection from tsunamis, and responses to global change. Estuarine, Coastal and Shelf Science, 76, 1–13.
Alongi, D. M. (2015). The impact of climate change on mangrove forests. Current Climate Change Reports, 1, 30–39.
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.
Anderson, J., Rowcliffe, J., & Cowlishaw, G. (2007). Does the matrix matter? A forest primate in a complex agricultural landscape. Biological Conservation, 135, 212–222.
Araújo, H., Mariano, E., Toledo, G., Filho, A., & Hernández, M. (2010). Avifauna de floresta de restinga em um complexo de mineração no litoral norte da Paraíba, Brasil. Revista Nordestina de Zoologia, 4, 46–56.
Asensio, N., Korstjens, A., Schaffner, C., & Aureli, F. (2008). Intragroup aggression, fission-fusion dynamics and feeding competition in spider monkeys. Behaviour, 145, 983–1001.
Aureli, F., & Schaffner, C. (2007). Aggression and conflict management at fusion in spider monkeys. Biology Letters, 3, 147–149.
Aureli, F., Schaffner, C., Boesch, C., Bearder, S., Call, J., et al (2008). Fission-fusion dynamics: New research frameworks. Current Anthropology, 49, 627–654.
Bastos, M., Souto, A., Jones, G., Eason, P., Bione, C., Schiel, N., & Bezerra, B. (2015). Vocal repertoire of wild blonde capuchins (Sapajus flavius) and contextual use of calls. American Journal of Primatology, 77, 605–617.
Bastos, M., Medeiros, K., Jones, G., & Bezerra, B. (2018). Small but wise: Common marmosets (Callithrix jacchus) use acoustic signals as cues to avoid interactions with blonde capuchin monkeys (Sapajus flavius). American Journal of Primatology, 80, e22744–e22710.
Bastos, M., Medeiros, K., Souto, A., Jones, G., & Bezerra, B. (2019). Use of mangrove habitats by Sapajus flavius assessed by vocalisation surveys. In A. Barnett, K. Nowak, & I. Matsuda (Eds.), Primates of flooded habitats (pp. 64–67). Cambridge: Cambridge University Press.
Beltrão-Mendes, R., Cunha, A., & Ferrari, S. (2011). New localities and perspectives on the sympatry between two endangered primates (Callicebus coimbrai and Cebus xanthosternos) in northeastern Brazil. Mammalia, 75, 103–105.
Bernard, H., Matsuda, I., Hanya, G., & Ahmad, A. (2011). Characteristics of night sleeping trees of proboscis monkeys (Nasalis larvatus) in Sabah, Malaysia. International Journal of Primatology, 32, 259–267.
Bessa, J., Sousa, C., & Hockings, K. (2015). Feeding ecology of chimpanzees (Pan troglodytes verus) inhabiting a forest-mangrove-savanna-agricultural matrix at Caiquene-Cadique, Cantanhez National Park, Guinea Bissau. American Journal of Primatology, 77, 651–665.
Bezerra, B. M., Bastos, M., Souto, A., Keasey, M., Eason, P., Schiel, N., & Jones, G. (2014). Camera trap observations of nonhabituated critically endangered wild blonde capuchins, Sapajus flavius (formerly Cebus flavius). International Journal of Primatology, 35, 895–907.
Blake, J., Guerra, J., Mosquera, D., Torres, R., Loiselle, B., & Romo, D. (2010). Use of mineral licks by white-bellied spider monkeys (Ateles belzebuth) and red howler monkeys (Alouatta seniculus) in eastern Ecuador. International Journal of Primatology, 31, 471–483.
Chapman, C. A., & Chapman, L. J. (2000). Determinants of group size in primates: The importance of travel costs. In S. Boinski & P. A. Garber (Eds.), On the move: How and why animals travel in groups (pp. 24–42). Chicago: University of Chicago Press.
Coelho, C. G., Falótico, T., Izar, P., Mannu, M., Resende, B. D., Siqueira, J. O., & Ottoni, E. B. (2015). Social learning strategies for nut-cracking by tufted capuchin monkeys (Sapajus spp.). Animal Cognition, 18, 911–919.
Couzin, I., & Laidre, M. (2009). Fission-fusion populations. Current Biology, 19, R633–R635.
CPB (Centro Nacional de Pesquisa e Conservação de Primatas Brasileiros). (2014). Áreas importantes para a conservação de primatas no Centro de Endemismo Pernambuco. João Pessoa - PB, Brazil: Instituto Chico Mendes de Conservação da Biodiversidade, Ministério do meio ambiente. https://www.ibama.gov.br/sophia/cnia/livros/Areas_Importantes_MAPA.PDF. Accessed 8 Feb 2017.
Cutrim, F. (2013). Padrão comportamental e uso de ferramentas em macacos-prego (Sapajus libidinosus) residentes em manguezal. PhD thesis, Universidade de São Paulo.
Di Bitetti, M. S., & Janson, C. H. (2001). Reproductive socioecology of tufted capuchins (Cebus apella nigritus) in northeastern Argentina. International Journal of Primatology, 22, 127–142.
Dinerstein, E., Olson, D., Graham, D., Webster, A., Primm, S., et al (1995). Conservation assessment of the terrestrial ecoregions of Latin America and the Caribbean. Washington: The World Wildlife Fund.
Fernandes, M. (1991). Tool use and predation of oysters (Crassostrea rhizophorae) by the tufted capuchin, Cebus apella apella, in brackish water mangrove swamp. Primates, 32, 529–531.
Fernandes, M., & Aguiar, N. (1993). Evidências sobre a adaptação de primatas neotropicais às áreas de mangue com ênfase no macaco-prego Cebus apella apella. In M. Yamamoto & M. Sousa (Eds.), A primatologia no Brasil IV (pp. 67–80). Natal, RN: Editora Universitária.
Fialho, M., Valença-Montenegro, M., Silva, T., Ferreira, J., & Laroque, P. (2014). Ocorrência de Sapajus flavius e Alouatta belzebul no centro de Endemismo Pernambuco. Neotropical Primates, 21, 214–218.
Field, C., Osborn, J., Hoffman, L., Polsenberg, J., Ackerly, D., et al (1998). Mangrove biodiversity and ecosystem function. Global Ecology and Biogeography Letters, 7, 3–14.
Flesher, K. M. (2015). The distribution, habitat use, and conservation status of three Atlantic Forest monkeys (Sapajus xanthosternos, Callicebus melanochir, Callithrix sp.) in an agroforestry/forest mosaic in southern Bahia, Brazil. International Journal of Primatology, 36, 1172–1197.
Fragaszy, D. M. (2012). Community resources for learning: How capuchin monkeys construct technical traditions. Biological Theory, 6, 231–240.
Fragaszy, D., Visalberghi, E., & Fedigan, L. (2004). The complete capuchin: The biology of the genus Cebus. Cambridge: Cambridge University Press.
Francisco, P., Medeiros, R., Santos, D., & Matos, R. (2015). Classificação climática de Köppen e Thornthwaite para o estado da Paraíba. Revista Brasileira de Geografia Física, 8, 1006–1016.
Freese, C., & Oppenheimer, J. (1981). The capuchin monkeys, genus Cebus. In A. F. Coimbra-Filho & R. A. Mittermeier (Eds.), Ecology and behavior of Neotropical primates (pp. 331–390). Rio de Janeiro: Academia Brasileira de Ciências.
Galat, G., & Galat-Luong, A. (1976). La colonisation de la mangrove par Cercopithecus aethiops sabaeus au Senegal. Extrait de la Terre et la Vie, Revue d’Écologie Appliquée, 30, 3–30.
Gardner, C. (2016). Use of mangroves by lemurs. International Journal of Primatology, 37, 317–332.
Giri, C., Ochieng, E., Tieszen, L., Zhu, Z., Singh, A., et al (2011). Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecology and Biogeography, 20, 154–159.
Godoy, M., & Lacerda, L. (2015). Mangroves response to climate change: A review of recent findings on mangrove extension and distribution. Anais da Academia Brasileira de Ciências, 87, 651–667.
Gumert, M. D., & Malaivijitnond, S. (2012). Marine prey processed with stone tools by burmese long-tailed macaques (Macaca fascicularis aurea) in intertidal habitats. American Journal of Physical Anthropology, 149, 447–457.
Hill, A. (2006). Why be diurnal? Or, why not be cathemeral? Folia Primatologica, 77, 72–86.
Holmes, S., Gordon, A., Louis, E., & Johnson, S. (2016). Fission-fusion dynamics in black-and-white ruffed lemurs may facilitate both feeding strategies and communal care of infants in a spatially and temporally variable environment. Behavioral Ecology and Sociobiology, 70, 1949–1960.
Hutchings, P., & Saenger, P. (1987). Ecology of mangroves. Queensland: University of Queensland Press.
ICMBio. (2011). Sumário executivo do Plano de Ação Nacional para a Conservação dos Primatas do Nordeste. João Pessoa – PB, Brazil: Instituto Chico Mendes de Conservação da Biodiversidade, Ministério do Meio Ambiente. http://www.icmbio.gov.br/portal/images/stories/docs-plano-de-acao/pan-primatas-caatinga/sumario-primatas-nordeste-web.pdf. Accessed 15 March 2017.
Isbell, L. (1991). Contest and scramble competition: Patterns of female aggression and ranging behavior among primates. Behavioral Ecology, 2, 143–155.
Izar, P., Verderane, M., Peternelli-dos Santos, L., Mendonça-Furtado, O., Presotto, A., et al (2012). Flexible and conservative features of social systems in tufted capuchin monkeys: Comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. American Journal of Primatology, 74, 315–331.
Izawa, K. (1980). Social behavior of the wild black-capped capuchins (Cebus apella). Primates, 21, 443–467.
Jones, T., Glass, L., Gandhi, S., Ravaoarinorotsihoarana, L., Carro, A., et al (2016). Madagascar’s mangroves: Quantifying nation-wide and ecosystem specific dynamics, and detailed contemporary mapping of distinct ecosystems. Remote Sensing, 8, 1–31.
Kappeler, P., & van Schaik, C. (2002). Evolution of primate social systems. International Journal of Primatology, 23, 707–740.
Kathiresan, K., & Rajendran, N. (2005). Coastal mangrove forests mitigated tsunami. Estuarine, Coastal and Shelf Science, 65, 601–606.
Kierulff, M., Santos, G., Canale, G., Guidorizzi, C., & Cassano, C. (2004). The use of camera-traps in a survey of the buff-headed capuchin monkey, Cebus xanthosternos. Neotropical Primates, 12, 56–59.
Koenig, A. (2002). Competition for resources and its behavioral consequences among female primates. International Journal of Primatology, 23, 759–783.
Luecke-Bridgeman, L. (2012). Diet of the black howler monkey (Alouatta pigra) in mangrove and the phytochemistry of mangrove plants. American Journal of Physical Anthropology, 147, 71–104.
Majolo, B., Ventura, R., Koyama, N., Hardie, S., Jones, B., et al (2009). Analysing the effects of group size and food competition on Japanese macaque social relationships. Behaviour, 146, 113–137.
Majumder, J., Lodh, R., & Agarwala, B. K. (2012). Fish feeding adaptation by rhesus macaque Macaca mulatta (Cercopithecidae) in the Sundarban mangrove swamps, India. Journal of Threatened Taxa, 4, 2539–2540.
MapBiomas. (2017). Projeto de mapeamento anual da cobertura e uso do solo no Brasil. http://mapbiomas.org/. Accessed 5 May 2017.
Markham, A. C., Gesquiere, L. R., Alberts, S. C., & Altmann, J. (2015). Optimal group size in a highly social mammal. Proceedings of the National Academy of Sciences of the USA, 112, 14882–14887.
McKinney, T. (2011). The effects of provisioning and crop raiding on the diet and foraging activities of human commensal white faced capuchins (Cebus capucinus). American Journal of Primatology, 73, 439–448.
Meijaard, E., & Nijman, V. (2000). Distribution and conservation of the proboscis monkey (Nasalis larvatus) in Kalimantan, Indonesia. Biological Conservation, 92, 15–24.
Milton, K., & Mittermeier, R. (1977). A brief survey of the primates of Coiba Island, Panama. Primates, 18, 931–936.
Nowak, K. (2008). Frequent water drinking by Zanzibar red colobus (Procolobus kirkii) in a mangrove forest refuge. American Journal of Primatology, 70, 1081–1092.
Nowak, K. (2012). Mangrove and peat swamp forests: Refuge habitats for primates and felids. Folia Primatologica, 83, 361–376.
Nowak, K., & Coles, R. (2019). Worldwide patterns in the ecology of mangrove-living monkeys and apes. In K. Nowak, A. Barnett, & I. Matsuda (Eds.), Primates in flooded habitats: Ecology and conservation (pp. 45–53). Cambridge: Cambridge University Press.
O’Brien, T. G., & Robinson, J. G. (1991). Allomaternal care by female wedge-capped capuchin monkeys: Effects of age, rank and relatedness. Behaviour, 119, 30–50.
Oliveira, M., & Langguth, A. (2006). Rediscovery of Marcgrave’s capuchin monkey and designation of a neotype for Simia flavia Schreber, 1774 (Primates, Cebidae). Boletim do Museu Nacional, 523, 1–16.
Oliveira, M. M., Boubli, J. P., & Kierulff, M. C. (2015). Sapajus flavius. The IUCN red list of threatened species 2015: e.T136253A70612549. https://doi.org/10.2305/IUCN.UK.2015.RLTS.T136253A70612549.en. Accessed 11 April 2017.
Olson, D., & Dinerstein, E. (2002). The global 200: Priority ecoregions for global conservation. Annals of the Missouri Botanical Garden, 89, 199–224.
Olson, E., Marsh, R., Bovard, B., Randrianarimanana, H., Ravaloharimanitra, M., et al (2012). Arboreal camera trapping for the critically endangered greater bamboo lemur Prolemur simus. Oryx, 46, 593–597.
Perry, S., & Rose, L. (1994). Begging and transfer for coati meat by white-faced capuchin monkeys, Cebus capucinus. Primates, 35, 409–415.
Port-Carvalho, M., Ferrari, S., & Magalhães, C. (2004). Predation of crabs by tufted capuchins (Cebus apella) in eastern Amazonia. Folia Primatologica, 75, 154–156.
Prance, G. T. (1979). Notes on the vegetation of Amazonia III. The terminology of Amazonian forest types subject to inundation. Brittonia, 31, 26–38.
Ribeiro-Júnior, M., Ferrari, S., Lima, J., Silva, C., & Lima, J. (2016). Predation of a squirrel monkey (Saimiri sciureus) by an Amazon tree boa (Corallus hortulanus): Even small boids may be a potential threat to small-bodied platyrrhines. Primates, 57, 317–322.
Robb, C. K. (2014). Assessing the impact of human activities on British Columbia’s estuaries. PLoS One, 9, 1–11.
Robins, P., Skov, M., Lewis, M., Giménez, L., Davies, A., et al (2016). Impact of climate change on UK estuaries: A review of past trends and potential projections. Estuarine, Coastal and Shelf Science, 169, 119–135.
Robinson, J. (1984). Diurnal variation in foraging and diet in the wedge-capped capuchin Cebus olivaceus. Folia Primatologica, 43, 216–228.
Rodrigues, N., & Martinez, R. (2014). Wildlife in our backyard: Interactions between Wied's marmoset Callithrix kuhlii (Primates: Callithrichidae) and residents of Ilhéus, Bahia, Brazil. Wildlife Biology, 20, 91–96.
Rog, A., Clarke, R., & Cook, C. (2016). More than marine: Revealing the critical importance of mangrove ecosystems for terrestrial vertebrates. Biodiversity Review, 23, 221–230.
Santos, R. (2010). Uso de ferramentas por macacos-prego em manguezais. PhD thesis, Universidade Federal do Rio Grande do Norte.
Schaeffer-Novelli, Y., Soriano-Sierra, E., Vale, C., Bernini, E., Rovai, A., et al (2016). Climate changes in mangrove forests and salt marshes. Brazilian Journal of Oceanography, 64, 37–52.
Shapiro, A., Trettin, C., Küchly, H., Alavinapanah, S., & Bandeira, S. (2015). The mangroves of the Zambezi Delta: Increase in extent observed via satellite from 1994 to 2013. Remote Sensing, 7, 16504–16518.
Snaith, T., & Chapman, C. (2007). Primate group size and interpreting socioecological models: Do folivores really play by different rules? Evolutionary Anthropology: Issues, News, and Reviews, 16, 94–106.
Soley, F., Chacón, I., & Soley-Guardia, M. (2017). Extraction of hermit crabs from their shells by white-faced capuchin monkeys (Cebus capucinus). Primates, 58, 25–29.
Son, V. (2003). Diet of Macaca fascicularis in a mangrove forest, Vietnam. Laboratory Primate Newsletter, 42, 1–5.
Son, V. (2004). Time budgets of Macaca fascicularis in a mangrove forest, Vietnam. Laboratory Primate Newsletter, 43, 1–4.
Southwick, C. (1967). An experimental study of intragroup agonistic behavior in rhesus monkeys (Macaca mulatta). Behaviour, 28, 182–209.
Stevenson, P., & Vargas, I. (2008). Sample size and appropriate design of fruit and seed traps in tropical forests. Journal of Tropical Ecology, 24, 95–105.
Symington, M. (1990). Fission-fusion social organization in Ateles and Pan. International Journal of Primatology, 11, 47–61.
Tan, C., Yang, Y., & Niu, K. (2013). Into the night: Camera traps reveal nocturnal activity in a presumptive diurnal primate, Rhinopithecus brelichi. Primates, 54, 1–6.
Vannucci, M. (2001). What is so special about mangroves? Brazilian Journal of Biology, 61, 599–603.
Vogel, E. R., & Janson, C. H. (2011). Quantifying primate food distribution and abundance for socioecological studies: An objective consumer-centered method. International Journal of Primatology, 32, 737–754.
Zhang, K., Liu, H., Li, Y., Xu, H., Shen, J., Rhome, J., & Smith III, T. (2012). The role of mangrove in attenuating storm surges. Estuarine, Coastal and Shelf Science, 102, 11–23.
Acknowledgments
The present study is in accordance with the Brazilian law under the permit # 25727-1 MMA, ICMBio, and SISBIO to Bruna Bezerra. We are thankful to Tronox Pigmentos do Brasil SA (former Cristal Mineração do Brasil Ltda), Sr. Geraldo Moraes, Sr. Virgílio Pinto, Rodrigo Costa, Severino Ramos, and Cristiano Lira for essential logistical support at the study site. M. Bastos and K. Medeiros were funded by FACEPE (Pernambuco Foundation to Support Science and Technology) scholarships (IBPG-0544-2.05/13, IBPG-0225-2.04/15). We thank Carla Castro, Monica Montenegro, Paulo Carvalho, Antonio Souto, and João Pedro Souza Alves for fruitful discussions over the course of this study. We thank Hevana Lima for the drawings in Fig. 2. This is a new contribution from our blonde capuchin research conservation project funded by Mohamed bin Zayed Species Conservation Fund, Margot Marsh Biodiversity Foundation, Rufford Foundation, FACEPE (APQ-1534-2.04/10, APQ-0143-2.04/14, BFT-01602.04), and CNPq (The Brazilian National Council for Scientific and Technological Development, Universal 445071/2014-1).
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KM and BB conceived and designed the study; KM conducted the fieldwork and analysed all camera trap images; KM and BB performed data analysis. KM, MB, GJ and BB wrote the manuscript.
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Medeiros, K., Bastos, M., Jones, G. et al. Behavior, Diet, and Habitat Use by Blonde Capuchin Monkeys (Sapajus flavius) in a Coastal Area Prone to Flooding: Direct Observations and Camera Trapping. Int J Primatol 40, 511–531 (2019). https://doi.org/10.1007/s10764-019-00103-z
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DOI: https://doi.org/10.1007/s10764-019-00103-z