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 immature seeds. However, such items are often low in available proteins, and digestion seeds is further inhibited by tannins. This suggests that overall plant-derived protein intake relatively low. We examined presence insect larvae partially eaten fruits, compared with intact fruit on trees, fecal pellets for larvae. found red-nosed cuxiú (Chiropotes albinasus) individuals may supplement their limited seed-derived ingesting seed-inhabiting insects. Comparison fruits those sampled directly from trees showed insect-containing were positively selected 20 41 C. albinasus diet tested, suggesting infested actively foraging animals. no differences accessibility to seeds, is, husk penetrability between uninfested excluding likelihood insect-infestation results easier access fruits. Additionally, none samples any evidence living pupae or larvae, indicating infesting digested. Our findings raise possibility these seed-predating primates might provide net benefits plant species they feed on, since many plants actions reduce populations seed-infesting Os membros do gênero de primatas neotropicais comem grandes sementes imaturas. No entanto, esses itens geralmente são baixos em proteínas disponíveis e a digestão das é ainda mais inibida pelos taninos. Isso sugere que ingestão geral derivadas plantas relativamente baixa. Examinamos presença larvas insetos frutas parcialmente consumidas, comparação com intactas nas árvores, examinamos grânulos fecais para larvas. Descobrimos os indivíduos nariz vermelho podem complementar sua limitada sementes, ingerindo inabitados às sementes. A consumidas por suas as amostradas diretamente árvores mostrou frutos contendo foram selecionados positivamente dos dieta testados, sugerindo infestadas ativamente selecionadas pela forrageamento animais. Não encontramos diferenças acessibilidade isto é, nenhuma diferença na penetração da casca entre não infestadas, excluindo probabilidade infestação resulte acesso fácil nessas frutas. Além disso, amostras qualquer evidência pupas vivas ou larvas, indicando infestantes digeridas. Nossas descobertas levantam possibilidade prevejam possam fornecer benefícios líquidos espécies vegetais se alimentam, uma vez alimentam muitas ações reduzir populações The family Pitheciidae represents, “a clade more committed eating than other group” (Rosenberger, 2020; 53). especially true sub-family Pitheciinae, which comprises three genera (Cacajao, Chiropotes, Pithecia) all show notable dental cranial specializations accessing extracting non-pulpy, hard-husked (Kinzey, 1992; Püschel et al., 2018). Of genera, Cacajao have most derived suite adaptations Rosenberger, 2020). In addition, annual diets both dominated immature, rather ripe, (Ayres, 1989; Barnett 2012; Norconk, Norconk 2013; Pinto represent 33% 75% (Table 1). These be contained within either dry pulpy husks (pericarp/mesocarp). Fruits 117 reported (2008) being albinasus, 66 (52.8%) dry-husked, remainder having pulp. Whether possessing pulp not, used (53% two sites 2018), when unripe (e.g., 48 65%, respectively: Exploitation beneficial longer periods ripe ones (Boubli, 1999; Shaffer, 2013), feeding competition reduced Ara macaws, Palminteri 2012: primates, Kinzey & 1990). seed-eating presents potential nutritional challenges, tend rich hard-to-metabolize structural proteins poor easily digested storage (Craig, 1988), generally deposited shortly before dispersal (Gallardo 2008; Harborne, 1996; Table 2). Tannin protein-binding capacities also challenge seed eaters. Tannins commonly present high concentrations pulps (Harborne, 1996). While tannin-rich food avoided due astringency (Marks, 1986; Simmen Charlot, 2003), tannins bind pose (Hagerman, 1989), this subsequently render unavailable thus reducing quality (Glander, 1982; Robbins 1987). relationship tannin ingestion negative effects complex (Felton 2009). proline-rich (PRPs) saliva known detoxify some animals, it not yet whether pitheciins produce PRPs if would increase decrease nitrogen digestibility gut (Skopec 2004). Nevertheless, levels condensed hydrolysable indigested significantly availability what small them during (Lambert Garber, 1998). Pitheciins balance risks toxins variety different chemical compositions 2009; Righini, 2017; AA Barnett, unpublished data), although individual still run risk entering deficiency day-to-day foraging. Ingestion protein-rich buds, young leaves, insects compensate (Cacajao: Chiropotes: van Roosmalen only free-living (i.e., habitually inhabiting resources) caterpillars, ants, termites, grasshoppers been considered (Ayres Nessimian, Frazäo, 1991; Mittermeier 1983; 2018; Port-Carvalho Ferrari, 2004; Veiga 2006). When consumption embedded recorded, accidental (Raubenheimer Rothman, 2013). Redford al. (1984) pointed out colonized (Coleoptera, Diptera, Lepidoptera), providing source primates. observation received little attention at time, recent studies Ronchi-Teles, (2017); Silla, (2017) Ballantyne (2018) shown least one pitheciin, golden-backed uacari (Cacajao ouakary; sensu Ferrari 2014), selects insect-infested (termed “covert carnivory” 2017). Selective predation has observed (Bravo, 2012), vertebrates (Alves Drew, 1987; Silvius, 2002; Valburg, 1992). Predation widely host fitness, removing section seed-predator population future effectively enhances reproductive fitness Herrera, Jordano, Furthermore, noted Lambert (2001), additional result insect-damaged become fungi pathogens (Barnett Menendez, 2019), can potentially transfer infestations healthy seedlings, survivorship. Choice losses, increasing (Lambert, 2001). For occur, must survive passage through digestive tract primate, survivorship could (Guix Ruiz, 1995, 1997). studied Chiropotes. dietary profile ecology very similar 2020), plausible benefit covert carnivory. Accordingly, we here study selectivity albinasus). took place middle Rio Tapajós, Pará State, Brazil (Figure Regionally, main forest types tall terra firme (never-flooded) (15–30 m), igapó (Prance, 1979). latter seasonally flooded forest, inundated site January-late April/early May (de Oliveira 2016), nutrient-poor waters Tapajós (Junk, Igapó forms narrow strip (rarely 10 m wide) along banks tributaries. area lies town Itaituba (4°16′33″S, 55°59′02″W), impassable rapids south (upstream) Machado village, first set lower Jamanxim (4°45′23″S, 56°26′15″W; Figure Unlike river basin Alouatta, Aotus, Ateles, Mico, Plecturocebus), (C. albinasus), 2016). arboreal, weighs 3.5 kg, travels groups 20–60, home range exceed 1000 ha (Pinto listed Vulnerable IUCN As part broader series faunal surveys mid-Tapajós 2016; 2017, Oliveira, Todd, Jucá Tománek collected field data October 2013 December 2014. Primate occurred 05:30 18:30 h motorized canoes, 06.00–10.00 14.00–18.00 trails. Using pre-existing trail system conducted observations margins (a 200-km transect) adjacent (five 10-km transects). During surveys, GPS location each tree was in-field taxonomic identification far possible. group seen tree, ascertain bout duration, identity eaten, way processed. study, discontinued after 30 min, unless encounter close end survey session. Monkeys tidy feeders (Howe, 1986), common accumulate below trees. word “ort” material, defined fragment food, fallen table. meal remnant” (https://www.merriam-webster.com/dictionary/ort). usage followed Santos-Barnett (2022), use here. monkeys messy eaters (Zagt, 1997), highly selective (Chapman Clink Consequently, previous ort-based methods composition patterns S1). Thus, while an imperfect measure “selectivity” requires controlled laboratory experiments supportive verification, dropped important information wild remnant orts beneath likely mixed handled without opening, opened discarded consumption. preliminary indicated that, species, whole had same proportions infested/non-infested ground It therefore appeared cuxiús did pluck then reject simply knocked down accidentally movement. material analysis, focused purely fed upon. Fed-at flagged marking tape. Any repeat visits treated independent events. Trees signs (orts discolored and/or oozing sap latex bearing marks characteristic feeding) (see collect based discoloration loss texture, 1–2 h, action ants content greatly, so bias results. husk, addition water content, sclerified fibrous (Cunha Junior Roosmalen, 1985), account frequency infestation insects, (AA data). accounted nearly half (51 Pinto, 2008). (if present) checked resident distinguished visiting scavengers excavated tunnels, frass, larval (rather adult) development stage. To compare levels, analyzed values (orts) branches trimmed feed. expand sample, accurately assay canopies belonging but observed. All 250 feeding. pitheciin region Pithecia mittermeieri) leave large-bodied central (Ateles chamek, Ateles marginatus, Alouatta discolor, nigerrima, Cebus albifrons, Sapajus apella: effect marked morphology means processing taxon pitheciins, P. mittermeieri, unique method “sclerocarpic foraging” (1992)), uses hypertrophied canines penetrate procumbent incisors extract imparting impressions 2) associated mittermeieri rarely smaller body mass making unlikely assigned erroneously. assess searched areas pellets. shape form, resembling coffee bean, allows similar-sized regional lack sections fiber leaf fragments sets apart deer. sampling, stored plastic zip-lock bags labeled orts, fallen-uneaten removed tree. crush-resistant vials. lab 3 collection preserved alcohol. Plants identified lowest possible category using Gentry (1993), Ribeiro (1999), (1985), Flora Mori Prance, 1990), specialist literature Procópio Secco, 2008 Couratari), Harris (2001) Jackson (2004) botanical terminology. Identifications confirmed lists (2008: firme), Ferreira Prance (1998: igapó), comparison photographs flowers (when available), bark, possible) on-line herbarium resources: Herbarium Specimens, New York Botanic Garden, Tropicos, Flore Guyane (https://www.fieldmuseum.org/node/4781; http://sweetgum.nybg.org/science/vh/; https://www.tropicos.org/home, https://floredeguyane.piwigo.com, respectively). test Prediction i (that percentage insects), presence/absence determined fruit, percentages calculated per species. done analyzing retrieved ground. Infestation intensity (measured number total weight) quantified equipment failure. comparability, ensure selection estimates conservative, categories ±0.33 side zero (neutral) occurred; < −0.33 (active avoidance), >+0.33 active selection. fruit-infesting passed alive (Prediction iii), broken thin glass rod. Material washed, sorted, placed petri dish, scrutinized 10x hand-lens. paid particular invertebrate fragments, (the because masticated size). apparently prodded seeker tip vitality. determine force needed covering less whose non-infested status left pericarps iv), tested relative eight indehiscent (Couratari stellata, Couratari cf. tenuicarpa, Eschweilera alba, obversa, Hevea spruceana, Lecythis lurida, Mabea nitida, Macrolobium acaciifolium), hard, indehiscent, (Chaunochiton loranthoides Ternstroemia candolleana). materials failure brittle (dry shell) ductile (pericarp-covered pulp) substances: former, cracks auto-propagate point impact (Mode I fracture: cracking), latter, propagation application continuous III tearing ripping) (Sun Jin, 2012). just bored hole creates zone weakness rigid structure (Bao Wierzbicki, Murdani 2008), bite facilitate post-canine insertion crack propagations non-elastic, husks, ones. Like ouakary opens biting selectively natural (sutures dehiscent fruit) thinness (indehiscent (A.A. following (2015), measured sutures between-suture faces International Ripening Company (Norfolk, VA 23502-2095) FT-011 penetrometer, mounted replica Fridley Fruit Tester (Fridley, 1966), prosthetic cast adult female canine replacing standard plunger head. Single measurements at, between, made, avoid induced mechanical experimentally made holes affecting subsequent measurements. required reach spruceana) second, inner, layer endocarp) harder outer epicarp (Muzik, 1954). Differences comparing single bore/oviposition Mann–Whitney U test). compromising integrity under investigation, use, animals ascertained. Level significance 0.05. Although fungal infections influence vertebrate choice (Buchholz Levey, 1990) negatively (Cipollini Stiles, 1993), investigate variable, excluded rot investigated 4649 130 vines, representing 37 18 families analyzed. 3249 sampled, 1400 orts. vines obtained, 56 direct observation, collections 74 others represented where recently discolored, covered ants; recorded exploited mature (Malouetia flavescens; Tabernaemontana sp. – Apocynaceae; Dalium sp., Swartzia polyphylla Fabaceae; Lecythidaceae; Calytranthus Eugenia Myrtaceae; Duroia Rubiaceae), 45 items, stages (seed: M. flavescens, tenuicarpa) parts (e.g. pod vs aril pod: polyphylla: Only (Iryanthera sagotiana, Myristicaceae) definitively lacked obvious infestation. remaining 44 41. ingested entirety, leaving analysis. 41, (48.8%). 15 (36.6%), parity. 6 (14.6%), parity, appear avoided. terms diet, incidence by-species basis (44 analyzed: 97.8%), leveled greater parity 26 (63.4% analyzed). these, (48.8% 76.9% demonstrated: high) supported, ii preferentially) supported. Analysis 13 nine (69.2%) remains form invertebrate, insectivory stricto There were, however, few 2), head capsules well-sclerotized dermis. Pupal found, (Item 4, 3). iii validated: neither nor pupae, survived albinasus. record intestinal parasites mistaken alimentary canal. Comparative obtained species: six (including indehiscent), there significant (statistical difference examples morphologies Hence, iv validated, penetrated fruit. consumed Selectivity estimated lacking whole. (15%) infested, (49%) preferentially selected. (36%) face suture analyzed, presence, ease access. Larval restricted cases. dry, fibrous, nature pericarp reflected encountered Overall, insects) partial support (within select disproportional availability). (fruit-infesting feces (for given protective infested). fact penetration since, like bites possess T. above, occur current 17 (45.9%: value region, 43.6%). records infested. Penetrometer does make open (we saw spat out) digested, samples. contrasts neotropical eaters, Guix 1997 birds). Indeed, diverse remnants adults 3), (item 5 setae caterpillar skin 2 probably lightly sclerotized, intact. variation select, reject) 2015) spp. (dos 2022). verified explanations r