Beans with bugs: Covert carnivory and infested seed selection by the red‐nosed cuxiú monkey

Members of the Neotropical primate genus Chiropotes eat large volumes of immature seeds. However, such items are often low in available proteins, and digestion of seeds is further inhibited by tannins. This suggests that overall plant‐derived protein intake is relatively low. We examined the presence of insect larvae in partially eaten fruits, compared with intact fruit on trees, and examined fecal pellets for the presence of larvae. We found that red‐nosed cuxiú (Chiropotes albinasus) individuals may supplement their limited seed‐derived protein intake by ingesting seed‐inhabiting insects. Comparison of fruits partially eaten for their seeds with those sampled directly from trees showed that fruits with insect‐containing seeds were positively selected in 20 of the 41 C. albinasus diet items tested, suggesting that fruits with infested seeds are actively selected by foraging animals. We found no differences in accessibility to seeds, that is, no differences in husk penetrability between fruits with infested and uninfested seeds excluding the likelihood that insect‐infestation results in easier access to the seeds in such fruits. Additionally, none of the C. albinasus fecal samples showed any evidence of living pupae or larvae, indicating that infesting larvae are digested. Our findings raise the possibility that these seed‐predating primates might provide net benefits to the plant species they feed on, since they feed from many species of plants and their actions may reduce the populations of seed‐infesting insects.

[1]  B. Bezerra,et al.  Pulp Fiction: Why Some Populations of Ripe-Fruit Specialists Ateles chamek and A. marginatus Prefer Insect-Infested Foods , 2022, International Journal of Primatology.

[2]  E. Heymann,et al.  Myrmecovory in Neotropical primates , 2021, Primates.

[3]  L. Redd,et al.  International Union for Conservation of Nature , 2010, Permanent Missions to the United Nations, No. 309.

[4]  Sarah A. Boyle,et al.  Buds, Bugs and Bienniality: The Floral Biology of Eschweilera tenuifolia (O. Berg) Miers in a Black-Water Flooded Forest, Central Amazonia , 2020, Forests.

[5]  P. Tománek,et al.  Calls for concern: Matching alarm response levels to threat intensities in three Neotropical primates , 2020 .

[6]  A. Rosenberger New World Monkeys: The Evolutionary Odyssey , 2020 .

[7]  P. Tománek,et al.  Being hunted high and low: do differences in nocturnal sleeping and diurnal resting sites of howler monkeys (Alouatta nigerrima and Alouatta discolor) reflect safety from attack by different types of predator? , 2020 .

[8]  M. Norconk Historical antecedents and recent innovations in pitheciid (titi, saki, and uakari) feeding ecology , 2020, American journal of primatology.

[9]  Jéssica Badolato Corrêa da Silva,et al.  Brazilian Amazon Plants: An Overview of Chemical Composition and Biological Activity , 2020, Natural Resources Management and Biological Sciences.

[10]  Marcelo Menezes Alves Parkia multijuga (fabaceae): interações multi-espécie e estratégias que maximizam a sobrevivência nos estágios iniciais de sua história de vida , 2019 .

[11]  W. Sellers,et al.  Analyzing the sclerocarpy adaptations of the Pitheciidae mandible , 2018, American journal of primatology.

[12]  M. Ribeiro,et al.  Queen palm fruit selection and foraging techniques of squirrels in the Atlantic Forest , 2018 .

[13]  P. Tománek,et al.  Honest error, precaution or alertness advertisement? Reactions to vertebrate pseudopredators in red‐nosed cuxiús (Chiropotes albinasus), a high‐canopy neotropical primate , 2018 .

[14]  N. Righini Recent advances in primate nutritional ecology , 2017, American journal of primatology.

[15]  Christopher Dillis,et al.  Dietary diversity, feeding selectivity, and responses to fruit scarcity of two sympatric Bornean primates (Hylobates albibarbis and Presbytis rubicunda rubida) , 2017, PloS one.

[16]  E. Setz,et al.  Run, hide, or fight: anti-predation strategies in endangered red-nosed cuxiú (Chiropotes albinasus, Pitheciidae) in southeastern Amazonia , 2017, Primates.

[17]  A. Barnett,et al.  Nonvolant Mammal Megadiversity and Conservation Issues in a Threatened Central Amazonian Hotspot in Brazil , 2016 .

[18]  A. MacLarnon,et al.  Foraging with finesse: A hard-fruit-eating primate selects the weakest areas as bite sites. , 2016, American journal of physical anthropology.

[19]  Viviane Sodré Moura Variação sazonal e longitudinal na ecologia alimentar de Chiropotes sagulatus Trail, 1821 na Amazônia brasileira , 2016 .

[20]  B. Jackson Dictionary of botanical names and terms , 2016 .

[21]  X. Dai,et al.  Influences of leaf-mining insects on their host plants: A review , 2015 .

[22]  B. Bezerra,et al.  An Improved Technique Using Dental Prostheses for Field Quantification of the Force Required by Primates for the Dental Penetration of Fruit , 2015, Folia Primatologica.

[23]  S. Ferrari,et al.  Reconsidering the taxonomy of the Black-Faced Uacaris, Cacajao melanocephalus group (Mammalia: Pitheciidae), from the northern Amazon Basin. , 2014, Zootaxa.

[24]  D. Raubenheimer,et al.  Nutritional contributions of insects to primate diets: implications for primate evolution. , 2014, Journal of human evolution.

[25]  C. Shaffer,et al.  Feeding Ecology of Northern Bearded Sakis (Chiropotes sagulatus) in Guyana , 2013, American journal of primatology.

[26]  D. Raubenheimer,et al.  Nutritional ecology of entomophagy in humans and other primates. , 2013, Annual review of entomology.

[27]  G. Powell,et al.  Advantages of granivory in seasonal environments: feeding ecology of an arboreal seed predator in Amazonian forests , 2012 .

[28]  W. Spironello,et al.  Implications of habitat fragmentation on the diet of bearded saki monkeys in central Amazonian forest , 2012 .

[29]  S. P. Bravo From which Ocotea diospyrifolia trees does Alouatta caraya (Primates, Atelidae) eat fruits? , 2012, Journal of Tropical Ecology.

[30]  Anneke M. DeLuycker Insect Prey Foraging Strategies in Callicebus oenanthe in Northern Peru , 2012, American journal of primatology.

[31]  L. Després,et al.  Plant chemical defence: a partner control mechanism stabilising plant - seed-eating pollinator mutualisms , 2009, BMC Evolutionary Biology.

[32]  D. Lindenmayer,et al.  Nutritional goals of wild primates , 2009 .

[33]  Anggit Murdani,et al.  Stress concentration at stop-drilled holes and additional holes , 2008 .

[34]  Richard D. Thompson,et al.  Reserve accumulation in legume seeds. , 2008, Comptes rendus biologies.

[35]  S. P. Bravo Seed Dispersal and Ingestion of Insect‐Infested Seeds by Black Howler Monkeys in Flooded Forests of the Parana River, Argentina , 2008 .

[36]  D. Lindenmayer,et al.  Diet and Feeding Ecology of Ateles chamek in a Bolivian Semihumid Forest: The Importance of Ficus as a Staple Food Resource , 2008, International Journal of Primatology.

[37]  R. Bonal,et al.  Seed choice by rodents: learning or inheritance? , 2008, Behavioral Ecology and Sociobiology.

[38]  E. Setz,et al.  Ecologia alimentar do cuxiu-de-nariz-vermelho Chiropotes albinasus (Primates : Pitheciidae) na Floresta Nacional do Tapajos, Para , 2008 .

[39]  Patrick S. Duetting,et al.  Biology of Metamasius mosieri (Coleoptera: Dryophthoridae), with a Description of Larval and Pupal Stages , 2006 .

[40]  P. Guimarães,et al.  Why do larvae of Utetheisa ornatrix penetrate and feed in pods of Crotalaria species? Larval performance vs. chemical and physical constraints , 2006 .

[41]  S. Ferrari,et al.  Predation of arthropods by southern bearded sakis (Chiropotes satanas) in Eastern Brazilian Amazonia , 2006, American journal of primatology.

[42]  P. Stevenson,et al.  A Multi-Forest Comparison of Dietary Preferences and Seed Dispersal by Ateles spp , 2005, International Journal of Primatology.

[43]  R. Wallace Seasonal Variations in Diet and Foraging Behavior of Ateles chamek in a Southern Amazonian Tropical Forest , 2005, International Journal of Primatology.

[44]  W. Karasov,et al.  Do Salivary Proline-Rich Proteins Counteract Dietary Hydrolyzable Tannin in Laboratory Rats? , 2004, Journal of Chemical Ecology.

[45]  B. Simmen,et al.  A comparison of taste thresholds for sweet and astringent-tasting compounds in great apes. , 2003, Comptes rendus biologies.

[46]  A. Britt,et al.  Diet and Feeding Behaviour of Indri indri in a Low-Altitude Rain Forest , 2002, Folia Primatologica.

[47]  K. Silvius Spatio-temporal patterns of palm endocarp use by three Amazonian forest mammals: granivory or ‘grubivory’? , 2002, Journal of Tropical Ecology.

[48]  J. Lambert Red-Tailed Guenons (Cercopithecus ascanius) and Strychnos mitis: Evidence for Plant Benefits Beyond Seed Dispersal , 2001, International Journal of Primatology.

[49]  C. Peres Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods , 2000, Journal of Tropical Ecology.

[50]  J. Boubli Feeding Ecology of Black-headed Uacaris (Cacajao melanocephalus melanocephalus) in Pico da Neblina National Park, Brazil , 1999, International Journal of Primatology.

[51]  Ghillean T. Prance,et al.  Species richness and floristic composition in four hectares in the Jaú National Park in upland forests in Central Amazonia , 1998, Biodiversity & Conservation.

[52]  J. Guix,et al.  Weevil Larvae Dispersal by Guans in Southeastern Brazil 1 , 1997 .

[53]  S. Bukkens The nutritional value of edible insects , 1997 .

[54]  R. Zagt Pre-dispersal and early post-dispersal demography, and reproductive litter production, in the tropical tree Dicymbe altsonii in Guyana , 1997, Journal of Tropical Ecology.

[55]  J. Guix,et al.  TOUCANS AND THRUSHES AS POTENTIAL DISPERSERS OF SEED-PREDATORY WEEVIL LARVAE IN SOUTHEASTERN BRAZIL , 1995 .

[56]  T. Massey,et al.  Biochemical and Molecular Aspects of Mammalian Susceptibility to Aflatoxin B1 Carcinogenicity , 1995, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[57]  James G. Harris,et al.  Plant Identification Terminology: An Illustrated Glossary , 1994 .

[58]  M. Galetti,et al.  Seasonal diet of capuchin monkeys (Cebus apella) in a semideciduous forest in south-east Brazil , 1994, Journal of Tropical Ecology.

[59]  M. Cipollini,et al.  Fruit rot, antifungal defense, and palatability of fleshy fruits for frugivorous birds , 1993 .

[60]  Lisa K. Valburg Feeding preferences of common bush-tanagers for insect-infested fruits: avoidance or attraction? , 1992 .

[61]  W. Kinzey Dietary and dental adaptations in the Pitheciinae. , 1992, American journal of physical anthropology.

[62]  E. Gdoutos,et al.  Fracture Mechanics , 2020, Encyclopedic Dictionary of Archaeology.

[63]  Edson da R. Frazäo Insectivory in free-ranging bearded saki (Chiropotes satanas chiropotes) , 1991, Primates.

[64]  A. Srivastava Insectivory and its significance to langur diets , 1991, Primates.

[65]  D. Levey,et al.  The evolutionary triad of microbes, fruits, and seed dispersers: an experiment in fruit choice by cedar waxwings, Bombycilla cedrorum , 1990 .

[66]  J. Ayres Comparative feeding ecology of the Uakari and Bearded Saki, Cacajao and Chiropotes , 1989 .

[67]  C. Herrera Frugivory and seed dispersal by carnivorous mammals, and associated fruit characteristics, in undisturbed Mediterranean habitatsFrugivory and seed dispersal by carnivorous mammals, and associated fruit characteristics, in undisturbed Mediterranean habitats , 1989 .

[68]  R. A. I. Drew,et al.  Amino acid increases in fruit infested by fruit flies of the family Tephritidae , 1988 .

[69]  P. Jordano Avian Fruit Removal: Effects of Fruit Variation, Crop Size, and Insect Damage. , 1987, Ecology.

[70]  A. Houston,et al.  Partial preferences and foraging , 1987, Animal Behaviour.

[71]  Charles C. Schwartz,et al.  Role of Tannins in Defending Plants Against Ruminants: Reduction in Protein Availability , 1987 .

[72]  M. Roosmalen Fruits of the Guianan flora , 1986 .

[73]  K. Redford,et al.  The relationship between frugivory and insectivory in primates , 1984, Primates.

[74]  R. Mittermeier,et al.  Further evidence of insect consumption in the bearded saki monkey,Chiropotes satanas chiropotes , 1983, Primates.

[75]  B. Styles,et al.  Tropical trees : variation, breeding, and conservation , 1978 .

[76]  D. Janzen Why Fruits Rot, Seeds Mold, and Meat Spoils , 1977, The American Naturalist.

[77]  V. S. Ivlev,et al.  Experimental ecology of the feeding of fishes , 1962 .

[78]  A. MacLarnon,et al.  Covert Carnivory? A Seed-Predating Primate, the Golden- Backed Uacari, Shows Preferences for Insect-Infested Fruits , 2017 .

[79]  M. Finke Complete nutrient content of four species of feeder insects. , 2013, Zoo biology.

[80]  C. Chapman,et al.  Chapter 7 Food as a Selective Force in Primates , 2013 .

[81]  M. Norconk,et al.  Evolutionary Biology and Conservation of Titis, Sakis and Uacaris: Morphological and ecological adaptations to seed predation – a primate-wide perspective , 2013 .

[82]  T. Defler,et al.  Evolutionary Biology and Conservation of Titis, Sakis and Uacaris: Cacajao ouakary in Brazil and Colombia: patterns, puzzles and predictions , 2013 .

[83]  L. Gregory SOCIOECOLOGY OF THE GUIANAN BEARDED SAKI, CHIROPOTES SAGULATUS , 2011 .

[84]  Shinji Sugiura,et al.  Gall-attacking behavior in phytophagous insects, with emphasis on Coleoptera and Lepidoptera , 2009 .

[85]  G. Prance Notes on the vegetation of amazonia III. The terminology of amazonian forest types subject to inundation , 2008, Brittonia.

[86]  R. Secco,et al.  A importância da identificação botânica nos inventários florestais: o exemplo do "tauari" (Couratari spp. e Cariniana spp. - Lecythidaceae) em duas áreas manejadas no estado do Pará , 2008 .

[87]  L. Prestes,et al.  INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA , 2006 .

[88]  T. Wierzbicki,et al.  On fracture locus in the equivalent strain and stress triaxiality space , 2004 .

[89]  B. Wright Ecological Distinctions in Diet, Food Toughness, and Masticatory Anatomy in a Community of Six Neotropical Primates in Guyana, South America , 2004 .

[90]  L. G. Lohmann,et al.  Flora da Reserva Ducke. Guia de identificacao das plantas vasculares de uma floresta de terra-firme na Amazonia Central , 1999 .

[91]  L. Isbell Diet for a small primate: Insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus) , 1998, American journal of primatology.

[92]  P. Garber,et al.  Evolutionary and ecological implications of primate seed dispersal. , 1998, American journal of primatology.

[93]  W. Junk General aspects of floodplain ecology with special reference to Amazonian floodplains , 1997 .

[94]  Rudolf Schmid,et al.  A field guide to the families and genera of woody plants of northwest South America (Colombia, Ecuador, Peru), with supplementary notes on herbaceous taxa , 1993 .

[95]  C. Tutin,et al.  Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the lopé reserve, gabon , 1993, American journal of primatology.

[96]  K. Kramer,et al.  Insect Cuticle Sclerotization , 1992 .

[97]  W. Kinzey,et al.  Hardness as a basis of fruit choice in two sympatric primates. , 1990, American journal of physical anthropology.

[98]  A. Hagerman Chemistry of Tannin-Protein Complexation , 1989 .

[99]  J. Fleagle,et al.  Diet of the northern bearded saki (Chiropotes satanas chiropotes): A neotropical seed predator , 1988, American journal of primatology.

[100]  S. Craig Structural Aspects of Protein Accumulation in Developing Legume Seeds , 1988 .

[101]  R. Drew Reduction in fruit fly (Tephritidae: Dacinae) populations in their endemic rainforest habitat by frugivorous vertebrates , 1987 .

[102]  J. Nessimian,et al.  Evidence for insectivory in two primate species (Callicebus torquatus lugens and Lagothrix lagothricha lagothricha) from northwestern Amazonia , 1984, American journal of primatology.

[103]  K. Glander The impact of plant secondary compounds on primate feeding behavior , 1982 .

[104]  J. W. Hanover Physiology of Tree Resistance to Insects , 1975 .

[105]  T. Muzik DEVELOPMENT OF FRUIT, SEED, EMBRYO, AND SEEDLING OF HEVEA BRASILIENSIS , 1954 .