Pulp Fiction: why some populations of ripe-fruit specialists Ateles chamek and A. marginatus prefer insect-infested foods

Article


dos Santos-Barnett, T., Cavalcante, T., Boyle, S., Matte, A., Bezerra, B., de Oliveira, T. and Barnett, A. 2022. Pulp Fiction: why some populations of ripe-fruit specialists Ateles chamek and A. marginatus prefer insect-infested foods. International Journal of Primatology. 43 (3), pp. 384-408. https://doi.org/10.1007/s10764-022-00284-0
TypeArticle
TitlePulp Fiction: why some populations of ripe-fruit specialists Ateles chamek and A. marginatus prefer insect-infested foods
Authorsdos Santos-Barnett, T., Cavalcante, T., Boyle, S., Matte, A., Bezerra, B., de Oliveira, T. and Barnett, A.
Abstract

Fruit pulp is an easily handled energy source for many frugivorous species but generally has little protein. Accordingly, ripe-fruit specialist primate species with diets dominated by fruit pulp risk protein deficiency. While some species use leaf and flower buds, young leaves, and arthropods as an alternative protein supplement, highly frugivorous spider monkeys (Ateles spp.) use protein-rich young leaves and/or fig fruits. However, not all spider monkey populations have access to abundantly available figs. Comparing infestation frequencies of fruits on trees with those eaten by spider monkeys, we tested the hypothesis that, under such circumstances, spider monkeys preferentially choose those nonfig fruits with pulp infested by insect larvae (a highly protein-rich resource). We predicted that: (i) a large proportion of plant species eaten by Ateles would have insect larvae-infested fruits; and (ii) Ateles would actively select infested fruits. We tested these predictions with Ateles chamek and Ateles marginatus on the banks of the Tapajós River, Brazil. Across a 13-month sampling period, we recorded 27 plant species in the diet of the 2 Ateles species. Of these, 23 (85%) had larvae-infested fruits when sampled; 11 species (40%) had high levels of individual fruits infested (35-78%). We used Ivlev Values to quantify selectivity for infested/uninfested fruits in 20 plant species. Infested fruits were positively selected in 12 species (60%), while aversion to infested fruits occurred in 4 species (20%). This covert carnivory/faunivory in spider monkeys is a largely overlooked aspect of their feeding ecology. This situation would be nearly impossible to ascertain from behavioral observations alone, showing the value of integrated, multimethod approaches. The strategy used by Ateles spp. on the banks of the Tapajós highlights the flexibility of primate foraging choices and the importance of indirect source of protein to ripe-fruit specialist primates.

KeywordsAteles; Entomophagy; Figs; Protein; South American primates
Sustainable Development Goals15 Life on land
Middlesex University ThemeSustainability
Research GroupBehavioural Biology group
LanguageEnglish
PublisherSpringer
JournalInternational Journal of Primatology
ISSN0164-0291
Electronic1573-8604
Publication dates
Online22 Mar 2022
PrintJun 2022
Publication process dates
Submitted13 Aug 2021
Accepted03 Feb 2022
Deposited19 Feb 2024
Output statusPublished
Publisher's version
File Access Level
Restricted
Digital Object Identifier (DOI)https://doi.org/10.1007/s10764-022-00284-0
Permalink -

https://repository.mdx.ac.uk/item/zxyvv

Restricted files

Publisher's version

  • 27
    total views
  • 3
    total downloads
  • 2
    views this month
  • 0
    downloads this month

Export as

Related outputs

Eat the fruit earlier: Sakis (Pithecia chrysocephala) show enhanced temporal fruit resource access compared with squirrel monkeys (Saimiri sciureus) in an urban forest fragment in Brazil
Take, M., Yumoto, T., Barnett, A., Onizawa, K. and Spironello, W. 2024. Eat the fruit earlier: Sakis (Pithecia chrysocephala) show enhanced temporal fruit resource access compared with squirrel monkeys (Saimiri sciureus) in an urban forest fragment in Brazil. American Journal of Primatology. 86 (2), pp. 1-20. https://doi.org/10.1002/ajp.23575
Pied tamarins change their vocal behavior in response to noise levels in the largest city in the Amazon
Sobroza, T.V., Gordo, M., Dunn, J.C., Pequeno, P.A.C.L., Naissinger, B.M. and Barnett, A 2024. Pied tamarins change their vocal behavior in response to noise levels in the largest city in the Amazon. American Journal of Primatology. https://doi.org/10.1002/ajp.23606
When partitioning is not an option: Resource availability predicts intraguild interactions in two isolated Amazonian primate assemblages
Cavalcante, T., Mourthé, Í., Barnett, A. and Bicca-Marques, J. 2023. When partitioning is not an option: Resource availability predicts intraguild interactions in two isolated Amazonian primate assemblages. Biotropica. 55 (4), pp. 839-848. https://doi.org/10.1111/btp.13233
When food fights back: Cebid primate strategies of larval paper wasp predation and the high‐energy yield of high‐risk foraging.
Barnett, A., Stone, A., Shaw, P., Ronchi-Teles, B., dos Santos-Barnett, T., Pimenta, N., Kinap, N., Spironello, W., Bitencourt, A., Penhorwood, G., Umeed, R., de Oliveira, T., Bezerra, B., Boyle, S., Ross, C. and Wenzel, J. 2023. When food fights back: Cebid primate strategies of larval paper wasp predation and the high‐energy yield of high‐risk foraging. Austral Ecology: A Journal of Ecology in the Southern Hemisphere. 48 (4), pp. 719-742. https://doi.org/10.1111/aec.13287
A life in fragments: the ecology, behavior, and conservation of the recently described Parecis Plateau titi monkey (Plecturocebus parecis)
Mattos, F., de Alencar, T., Boyle, S., Fleck, G., Koolen, H., Pohlit, A., Silva-Diogo, O., Gusmão, A. and Barnett, A. 2023. A life in fragments: the ecology, behavior, and conservation of the recently described Parecis Plateau titi monkey (Plecturocebus parecis). International Journal of Primatology. 45, pp. 176-202. https://doi.org/10.1007/s10764-023-00370-x
Beans with bugs: Covert carnivory and infested seed selection by the red-nosed cuxiú monkey
Barnett, A., dos Santos-Barnett, T., Muir, J., Tománek, P., Gregory, T., Matte, A., Bezerra, B., de Oliveira, T., Norconk, M. and Boyle, S. 2023. Beans with bugs: Covert carnivory and infested seed selection by the red-nosed cuxiú monkey. Biotropica. 55 (3), pp. 579-593. https://doi.org/10.1111/btp.13207
Do pied tamarins increase scent-marking in response to urban noise?
Sobroza, T., Dunn, J., Gordo, M. and Barnett, A. 2023. Do pied tamarins increase scent-marking in response to urban noise? Ethology Ecology and Evolution. https://doi.org/10.1080/03949370.2023.2248591
Knowledge shortfalls for titi monkey: A poorly known clade of small-bodied South American primates
Souza-Alves, J., Boyle, S. and Barnett, A. 2023. Knowledge shortfalls for titi monkey: A poorly known clade of small-bodied South American primates. Biological Conservation. 286. https://doi.org/10.1016/j.biocon.2023.110256
Records of Crab-eating fox (Cerdocyon thous Linnaeus, 1766, Carnivora, Canidae) in Rondônia, Brazil: range extension, threats and conservation
Ferreira, D., Oliveira, M., Goebel, L., Andriolo, A., Pommer-Barbosa, R., Mattos, F. and Barnett, A. 2023. Records of Crab-eating fox (Cerdocyon thous Linnaeus, 1766, Carnivora, Canidae) in Rondônia, Brazil: range extension, threats and conservation. Mammalia. 87 (6), pp. 577-582. https://doi.org/10.1515/mammalia-2023-0011
Searching for food in a concrete jungle: feeding ecology of a Psittacine assemblage (Aves, Psittacidae) in a major Amazonian city
Soares, C., Barnett, A., Scudeller, V. and Borges, S. 2023. Searching for food in a concrete jungle: feeding ecology of a Psittacine assemblage (Aves, Psittacidae) in a major Amazonian city. Anais da Academia Brasileira de Ciências. 95 (3). https://doi.org/10.1590/0001-3765202320220606
AMAZONIA CAMTRAP: A dataset of mammal, bird, and reptile species recorded with camera traps in the Amazon forest
Antunes, A., Montanarin, A., Gräbin, D., Monteiro, E., de Pinho, F., Alvarenga, G., Ahumada, J., Wallace, R., Ramalho, E., Barnett, A., Bager, A., Lopes, A., Keuroghlian, A., Giroux, A., Herrera, A., Correa, A., Meiga, A., Jácomo, A., Barban, A., Antunes, A., Coelho, A., Camilo, A., Nunes, A., Gomes, A., Zanzini, A., Castro, A., Desbiez, A., Figueiredo, A., de Thoisy, B., Gauzens, B., Oliveira, D., de Lima, C., Peres, C., Durigan, C., Brocardo, C., da Rosa, C., Zárate-Castañeda, C., Monteza-Moreno, C., Carnicer, C., Trinca, C., Polli, D., Ferraz, D., Lane, D., da Rocha, D., Barcelos, D., Auz, D., Rosa, D., Silva, D., Silvério, D., Eaton, D., Nakano-Oliveira, E., Venticinque, E., Junior, E., Mendonça, E., Vieira, E., Isasi-Catalá, E., Fischer, E., Castro, E., Oliveira, E., de Melo, F., Muniz, F., Rohe, F., Baccaro, F., Michalski, F., Paim, F., Santos, F., Anaguano, F., Palmeira, F., Reis, F., Aguiar-Silva, F., Batista, G., Zapata-Ríos, G., Forero-Medina, G., Neto, G., Alves, G., Ayala, G., Pedersoli, G., Bizri, H., do Prado, H., Mozerle, H., Costa, H., Lima, I., Palacios, J., Assis, J., Boubli, J., Metzger, J., Teixeira, J., Miranda, J., Polisar, J., Salvador, J., Borges-Almeida, K., Didier, K., Pereira, K., Torralvo, K., Gajapersad, K., Silveira, L., Maioli, L., Maracahipes-Santos, L., Valenzuela, L., Benavalli, L., Fletcher, L., Paolucci, L., Zanzini, L., da Silva, L., Rodrigues, L., Benchimol, M., Oliveira, M., Lima, M., da Silva, M., Junior, M., Viscarra, M., Cohn-Haft, M., Abrahams, M., Benedetti, M., Marmontel, M., Hirt, M., Tôrres, N., Junior, O., Alvarez-Loayza, P., Jansen, P., Prist, P., Brando, P., Perônico, P., Leite, R., Rabelo, R., Sollmann, R., Beltrão-Mendes, R., Ferreira, R., Coutinho, R., Oliveira, R., Ilha, R., Hilário, R., Pires, R., Sampaio, R., Moreira, R., Botero-Arias, R., Martinez, R., Nóbrega, R., Fadini, R., Morato, R., Carneiro, R., Almeida, R., Ramos, R., Schaub, R., Dornas, R., Cueva, R., Rolim, S., Laurindo, S., Espinosa, S., Fernandes, T., Sanaiotti, T., Alvim, T., Dornas, T., Piña, T., Andrade, V., Santiago, W., Magnusson, W., Campos, Z. and Ribeiro, M. 2022. AMAZONIA CAMTRAP: A dataset of mammal, bird, and reptile species recorded with camera traps in the Amazon forest. Ecology. 103 (9). https://doi.org/10.1002/ecy.3738
Combining geospatial abundance and ecological niche models to identify high-priority areas for conservation: The neglected role of broadscale interspecific competition
Cavalcante, T., Weber, M.M. and Barnett, A. 2022. Combining geospatial abundance and ecological niche models to identify high-priority areas for conservation: The neglected role of broadscale interspecific competition. Frontiers in Ecology and Evolution . 10, pp. 1-20. https://doi.org/10.3389/fevo.2022.915325
Biotic indicators for ecological state change in Amazonian floodplains
Correa, S.B., van der Sleen, P., Siddiqui, S.F., Bogotá-Gregory, J.D., Arantes, C.C., Barnett, A., Couto, T.B.A., Goulding, M. and Anderson, E.P. 2022. Biotic indicators for ecological state change in Amazonian floodplains. BioScience. 72 (8), pp. 753-768. https://doi.org/10.1093/biosci/biac038
Factors influencing terrestriality in primates of the Americas and Madagascar
Eppley, T.M., Hoeks, S., Chapman, C.A., Ganzhorn, J.U., Hall, K., Owen, M.A., Adams, D.B., Allgas, N., Amato, K.R., Andriamahaihavana, M., Aristizabal, J.F., Baden, A.L., Balestri, M., Barnett, A., Bicca-Marques, J.C., Bowler, M., Boyle, S.A., Brown, M., Caillaud, D., Calegaro-Marques, C., Campbell, C.J., Campera, M., Campos, F. A., Cardoso, T.S., Carretero-Pinzón, X., Champion, J., Chaves, Ó.M., Chen-Kraus, C., Colquhoun, I.C., Dean, B., Dubrueil, C., Ellis, K.M., Erhart, E.M., Evans, K.J.E., Fedigan, L.M., Felton, A.M., Ferreira, R.G., Fichtel, C., Fonseca, M.L., Fontes, I.P., Fortes, V.B., Fumian, I., Gibson, D., Guzzo, G.B., Hartwell, K.S., Heymann, E.W., Hilário, R.R., Holmes, S.M., Irwin, M.T., Johnson, S.E., Kappeler, P.M., Kelley, E.A., King, T., Knogge, C., Koch, F., Kowalewski, M.M., Lange, L.R., Lauterbur, M.E., Louis, E.E., Lutz, M.C, Martínez, J., Melin, A.D., de Melo, F.R., Mihaminekena, T.H., Mogilewsky, M.S., Moreira, L.S., Moura, L.A., Muhle, C.B., Nagy-Reis, M.B., Norconk, M.A., Notman, H., O’Mara, M. T., Ostner, J., Patel, E.R., Pavelka, M.S.M., Pinacho-Guendulain, B., Porter, L.M., Pozo-Montuy, G., Raboy, B.E., Rahalinarivo, V., Raharinoro, N.A., Rakotomalala, Z., Ramos-Fernández, G., Rasamisoa, D.C., Ratsimbazafy, J., Ravaloharimanitra, M., Razafindramanana, J., Razanaparany, T.P., Righini, N., Robson, N.M., Gonçalves, J.R., Sanamo, J., Santacruz, N., Sato, H., Sauther, M.L., Scarry, C.J., Serio-Silva, J.C., Shanee, S., Lins, P., Smith, A.C., Smith Aguilar, S.E., Souza-Alves, J.P., Stavis, V.K., Steffens, K.J.E., Stone, A.I., Strier, K.B., Suarez, S.A., Talebi, M., Tecot, S.R., Tujague, M.P., Valenta, K., Van Belle, S., Vasey, N., Wallace, R.B., Welch, G., Wright, P. C., Donati, G. and Santini, L. 2022. Factors influencing terrestriality in primates of the Americas and Madagascar. Proceedings of the National Academy of Sciences. 119 (42), pp. 1-10. https://doi.org/10.1073/pnas.2121105119