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

Abstract

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.
Abstract in Portuguese is available with online material.

Full text

Biotropica. 2023;00:1–15.
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1wileyonlinelibrary.com/journal/btp
Received: 21 Januar y 2022
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Revised: 24 September 2022
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Accepted: 7 December 2022
DOI: 10.1111/btp.13207
ORIGINAL ARTICLE
Beans with bugs: Covert carnivory and infested seed selection
by the red- nosed cuxiú monkey
Adrian A. Barnett1,2,3 | Tereza Cristina dos Santos- Barnett4 | Jen Muir5 |
Pavel Tománek6 | Tremaine Gregory7 | Ana Luiza L. Matte1 | Bruna M. Bezerra1 |
Tadeu de Oliveira8 | Marilyn Norconk9 | Sarah A. Boyle10
1Department of Zoology, Federal
University of Pernambuco, Recife, Brazil
2Amazon Mammal Research Group,
National Amazon Research Institute,
Manaus, Amazonas, Brazil
3Animal and Agricultural Sciences,
Hartpury University, Gloucester, UK
4Department of Nutrition, Manaus
Central University- FAMETRO, Manaus,
Amazonas, Brazil
5School of Life Sciences, Anglia Ruskin
University, Cambridge, UK
6Department of Etholog y, Czech
University of Life Sciences- Prague,
Prague, Czech Republic
7Center for Conser vation and
Sustainability, Smithsonian National
Zoo and Conservation Biology Institute,
Washington, District of Columbia, USA
8Department of Biology, Maranhão State
University, São Luís, Maranhão, Brazil
9Department of Anthropology, Kent State
University, Kent, Ohio, USA
10Department of Biology and
Environmental Studies and Sciences
Program, Rhodes College, Memphis,
Tennessee, USA
Correspondence
Adrian A . Barnett, Department of Zoology,
Federal University of Pernambuco, Recife,
Brazil.
Email: adrian.barnett.biology2010@gmail.
com
Associate Editor: Jennifer Powers
Handling Editor: Laurence Culot
Abstract
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 supple-
ment 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 ac-
cess 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 spe-
cies of plants and their actions may reduce the populations of seed- infesting insects.
Abstract in Portuguese is available with online material.
KEYWORDS
bearded saki, pitheciid, protein, seed predation, tannin
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2023 The Authors. Biotropica published by Wiley Periodicals LLC on behalf of Association for Tropical Biology and Conservation.

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1 | INTRODUCTION
The family Pitheciidae represents, “a clade more committed to eat-
ing seeds than any other primate group” (Rosenberger, 2020; 53).
This is especially true of the sub- family Pitheciinae, which com-
prises three genera (Cacajao, Chiropotes, and Pithecia) all of which
show notable dental and cranial specializations for accessing and
extracting seeds from non- pulpy, hard- husked fruits (Kinzey, 1992;
Püschel et al., 2018). Of these genera, Cacajao and Chiropotes have
the most derived suite of adaptations for such a diet (Kinzey, 199 2;
Rosenberger, 2020). In addition, the annual diets of both genera
are often dominated by seeds from immature, rather than ripe,
fruits (Ayres, 1989; Barnett et al., 2012; Norconk, 2020; Norconk
et al., 2013; Pinto et al., 2020). In the genus Chiropotes, such im-
mature seeds may represent between 33% and 75% of the diet
(Table 1). These seeds may be contained within fruits with either
dry or pulpy husks (pericarp/mesocarp). Fruits of 117 plant spe-
cies were reported by Pinto (2008) as being eaten by C. albinasus,
of these 66 (52.8%) were dry- husked, the remainder having pulp.
Whether possessing pulp or not, most fruit species are used for
their seeds (53% and 75% of diet for the two sites reported on by
Pinto et al., 2018), with the seeds eaten when unripe (e.g., 48 and
65%, respectively: Pinto et al., 2018).
Exploitation of such seeds is beneficial in that unripe fruits
are available for longer periods than ripe ones (Boubli, 1999;
Norconk, 2020; Shaffer, 2013), and feeding competition with other
species may be reduced (e.g., Ara macaws, Palminteri et al., 2012:
other primates, Kinzey & Norconk, 1990). However, seed- eating
presents potential nutritional challenges, since unripe seeds tend
to be rich in hard- to- metabolize structural proteins and poor in
the more easily digested storage proteins (Craig, 198 8), which are
generally deposited shortly before dispersal (Gallardo et al., 2008;
Harborne, 1996; Table 2).
Tannin protein- binding capacities may also provide a nutritional
challenge to seed eaters. Tannins are commonly present in high con-
centrations in both unripe fruit pulps and seeds (Harborne, 1996).
While tannin- rich food items are often avoided due to their astrin-
gency (Marks, 1986; Simmen & Charlot, 2003), that tannins bind with
proteins may also pose a challenge (Hagerman, 1989), since this sub-
sequently render such proteins unavailable for digestion thus reduc-
ing food quality (Glander, 1982; Robbins et al., 1987). The relationship
between tannin ingestion and their potential negative effects is com-
plex (Felton et al., 2009). While proline- rich proteins (PRPs) in saliva
are known to bind with and detoxify tannins in some animals, it is not
yet known whether pitheciins produce PRPs or if they would increase
or decrease nitrogen digestibility in the gut (Skopec et al., 2004).
Nevertheless, the high levels of condensed and hydrolysable tannins
in the immature seeds indigested by C. albinasus may significantly re-
duce the availability of what small levels of proteins are available from
them during digestion (Lambert & Garber, 1998 ).
Pitheciins may balance the risks of ingesting high concen-
trations of tannins and toxins by ingesting a variety of fruits with
different chemical compositions (Felton et al., 2009; Righini, 2017;
AA Barnett, unpublished data), although individual Cacajao and
Chiropotes may still run the risk of entering protein deficiency during
day- to- day foraging. Ingestion of protein- rich buds, young leaves,
and insects may compensate for this (Cacajao: Barnett et al., 2013;
Chiropotes: van Roosmalen et al., 1988), However, for insect in-
gestion only free- living insects (i.e., not those habitually inhabiting
fruits, their seeds, or other food resources) such as caterpillars, ants,
termites, and grasshoppers have generally been considered (Ayres
& Nessimian, 1982; Frazäo, 1991; Mittermeier et al., 1983; Pinto
et al., 2018; Port- Carvalho & Ferrari, 2004; Veiga & Ferrari, 2006).
When consumption of insects embedded in fruit or seeds is recorded,
their ingestion is generally considered accidental (Raubenheimer &
Rothman, 2013).
Redford et al. (1984) pointed out that seeds are often colo-
nized by insect larvae (Coleoptera, Diptera, and Lepidoptera),
providing a potential source of protein for seed- eating primates.
While this observation received little attention at the time, more
recent studies by Barnett, Ronchi- Teles, et al. (2017); Barnet t,
Silla, et al. (2017) and Ballantyne (2018) have shown that at least
one pitheciin, the golden- backed uacari (Cacajao ouakary; sensu
Ferrari et al., 2014) , ac tivel y selec t s fruit with insect- inf ested seeds
(termed “covert carnivory” by Barnett, Ronchi- Teles, et al., 2017;
Barnett, Silla, et al., 2017).
Selective predation of infested fruits has been observed in
primates (Bravo, 2012), and other vertebrates (Alves et al., 2018;
Drew, 1987; Silvius, 2002; Valburg, 19 92). Predation of seed- eating
insects is widely considered to be beneficial to host plant fitness,
since removing a section of the insect seed- predator population
of future seeds effectively enhances the reproductive fitness of
the individual plants (Bravo, 2008; Herrera, 1989; Jordano, 1987).
Furthermore, as noted by Lambert (2001), additional benefits may
result from the predation of insect- damaged seeds since such seeds
often become infested by fungi and other pathogens (Barnett
et al., 2012; Menendez, 20 19), which can potentially transfer in-
festations to healthy seeds and seedlings, reducing their survivor-
ship. Choice of infested fruits and seeds by seed- eating primates
may reduce such losses, increasing overall plant reproductive fit-
ness (Lambert, 2001). For this to occur, insect larvae and pupae
must not survive passage through the digestive tract of a seed-
eating primate, as survivorship could result in their dispersal (Guix
& Ruiz, 1995, 1997).
Selective predation of infested fruits has not been studied in
Chiropotes. However, as they have a dietary profile and feeding
ecology very similar to Cacajao (Ayres, 19 89; Norconk, 2020), it is
plausible that Chiropotes may also benefit from covert carnivory.
Accordingly, we present here a study of infested fruit selectivity in
the red- nosed cuxiú (Chiropotes albinasus).
We tested the hypothesis that C. albinasus preferentially se-
lect fruits whose seeds are infested with larval insects, these being
protein- rich (Rothman et al., 2014) and relatively easy to digest. We
predicted that:

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BARNETT et a l.
TAB LE 1 Infestation levels and selectivitya based on Ivlev Values for 45 diet items from 37 species eaten by Chiropotes albinasus on the
middle Rio Tapajós, Pará State, Brazil.b,c
Scientific name
No. of
treesdHabitate
Part eaten and
maturation statef
Tree: Infested/
uninfested fruits
(% on tree with
infested seeds)
Diet: Infested/
uninfested fruits
(% in diet sample
with infested
seeds)
Electivity
index
Selection
typeg
Annonaceae
Xylopia cf. fructescens 4h,iIg Am 40/98 (40.8) 2/17 (11.8) −0.55 A
Apocynaceae
Malouetia flavescens 7hIg Si 27/117 (23.1) 28/37 (75.7) 0.53 P
Malouetia flavescens 3Ig Sm 9/46 (19.6) 12/25 (48.0) 0.42 P
Tabernaemontana sp. 7h,jIg Si 6/28 (21.4) 12/21 (57.1) 0.45 P
Tabernaemontana sp. 4 Ig Sm 5/23 (21.7) 9/14 (64.3) 0.52 P
Chrysobalanaceae
Licania cf. canescens 2iTf Si 14/89 (15.7) 14/22 (63.7) 0.60 P
Euphorbiaceae
Hevea spruceana 8hIg Si 7/58 (12.1) 18/40 (45.0) 0.58 P
Mabea nitida 3hIg Si 21/60 (35.0) 2/23 (8.7) −0.61 A
Fabaceae
Inga alba 5hTf Am 63/199 (31.7) 3/47 (6.4) −0.64 A
Inga heterophylla 2hIg Am 46/122 (39.4) 2/50 (4.0) −0.79 A
Dalium sp. 3Ig Pm 4/37 (10.8) 6/16 (37.5) 0. 55 P
Dalium sp. 2Ig Si 9/19 (47.3) 2/16 (12.5) −0.58 A
Macrolobium
acaciifolium
8Ig Si 17/100 (17.0) 9/46 (19.6) 0.07 O
Swartzia polyphylla 2Ig Wo27/85 (31.8) 19/23 (82.6) 0.44 P
Swartzia polyphylla 2Ig Am 8/40 (20.0) 3/17 (17.7) −0.06 O
Humiriaceae
Endopleura uchi 1iTf Pi 4/31 (12.9) 2/19 (10. 5) − 0.10 O
Lecythidaceae
Couratari stellata 2TF Sm 22/207 (10.6) 5/44 (11.7) 0.05 O
Couratari cf. tenuicarpa 3Ig Si 16/221 (7.2) 4/52 (7.7) 0.03 O
Couratari cf. tenuicarpa 2Ig Sm 24/194 (12.4) 6/63 (9.5) −0.13 O
Eschweilera albiflora 5hIg Si 28/74 (37.8) 34/49 (79.6) 0.36 P
Eschweilera obversa 3hTF Si 61/227 (26.9) 57/94 (60.6) 0.43 P
Lecythis lurida 1hTF Si 55/80 (67.8) 20/37 (54.1) −0.11 O
Menispermaceae
Abuta cf. panurensis 1TF Pmk7/34 (20.6) 26/41 (63.4) 0 . 51 P
Moraceae
Brosimum parinarioides 3iTf Wm 2/78 (2.6) – – n/a
Myristicaceae
Iryanthera sagotiana 1Tf Am 0/23 – – n/a
Myrtaceae
Calyptranthes sp. 5iIg. Si 14/34 (41.2) 17/27 (62.9) P
Calyptranthes sp. 3iIg Wm 26/35 (74.3) – – n /a
Eugenia sp. 11iIg Si 82/100 (82.0) 36/47 (76.6) −0.03 O
Eugenia sp. 4iIg Wm 36/50 (72.0) – – n/a
(Continues)

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BARNETT et a l.
Scientific name
No. of
treesdHabitate
Part eaten and
maturation statef
Tree: Infested/
uninfested fruits
(% on tree with
infested seeds)
Diet: Infested/
uninfested fruits
(% in diet sample
with infested
seeds)
Electivity
index
Selection
typeg
Olacaceae
Chaunochiton
loranthoides
4Ig Si 12/52 (23.1) 13/19 (68.4) 0.49 P
Passifloraceae
Passiflora cf. costata 5i,jIg Pm, Sm 10/29 (34.5) 8/11 (72.3) 0.35 P
Polygalaceae
Moutabea guianensis 5i,lTf Si 14/63 (21.5) 19/33 (57.6) 0.46 P
Securidaca sp. 378/100 (78.0) 21/29 (72.4) −0.03 O
Rubiaceae
Duroia sp. 7 Ig Wi 4/47 (8.5) 2/16 (12.5) 0.19 O
Duroia sp. 4 Ig Wm 4/34 (11.8) 2/19 (10.5) −0.05 O
Salicaceae
Casearia sp. 3mIg Wm 39/56 (69.6) 9/15 (60.0) −0.07 O
Sapotaceae
Chromolucuma cf.
rubriflora
2mIg Si 25/43 (58.1) 39/61 (63.9) 0.05 O
Chrysophyllum sp. 2mTF Si 14/49 (28.6) 22/31 (70.1) 0.42 P
Elaeoloma glabrescens 3mIg Si 8/29 (27.6) 15/23 (65.2) 0.41 P
Manilkara bidentata 2mIg Si 11/44 (25.0) 54/86 (62.7) 0.40 P
Pouteria bilocularis 1mTf Si 13/35 (37.1) 7/20 (35.0) −0.03 O
Pouteria cf. cuspidata 1mIg Si 19/64 (29.7) 36/56 (64.3) 0.36 P
Pouteria gomphiifolia 3mIg Si 17/41 (41. 5) 22/27 (81.4) 0.32 P
Pouteria cf. macrophylla 2mTF Si 39/50 (78.0) 21/28 (75.0) −0.02 O
Theaceae
Ternstroemian
candolleana
1Ig Si 8/27 (29.7) 25/39 (64.1) 0.37 P
aElectivity Index = (Oi − Ti)/(Oi + Ti). Electivity Index data are given for each diet item and is based on all analyzed individuals of the species concerned
for which a particular morphological part was consumed. If a different part was consumed, and that was the only part ingested, then that was treated
as a separate diet item from any others of the same species (e.g., whole young pods and arils from mature pods of Swartzia polyphylla). If the same
part was eaten at two different maturational stages (e.g., seeds from immature and mature fruits of Malouetia flavescens), this too was treated as two
distinct diet items, and the electivit y indexes calculated separately combined (different maturation states treated separately).
bC. albinasus was seen feeding on seeds of three species of tree that could not be sampled for logistical reasons (Acosmium sp., Aldina [heterophylla?],
Swartzia sp., all Fabaceae).
cC. albinasus was also seen eating flowers and young leaves, these data will be reported elsewhere.
dIn all eight cases of multi- use, the same trees were visited.
eHabitat: Tf = terra firme, Ig = igapó.
fPart eaten: A = aril/sarcotesta, P = pulp, S = seed, W = whole fruit, maturation state: m = mature, i = immature.
gSelection type: P = positive, A = avoidance, and O = none; where species that were avoided had some fruits with infested seeds (or fruit parts
eaten), these were always very lightly infested, so that it is possible that any induced zootropic phytochemicals may not have been present or were
present at very low levels.
hMulti- seeded fruits, selectivity estimated for individual seeds.
iFruit species had a pulpy pericarp, and there was insect infestation in both the pericarp and seeds.
jA vine with N = number of clumps; the vine was growing on a flooded bank at the time of feeding.
kIn this species, the layer of pulp is thinner as than the exocarp is thick, and infesting insects appeared to be feeding on both.
lA vine, but the true number of individuals was not ascertained.
mFruit species had a pulpy pericarp, and there was insect infestation only in the seeds.
nThe genus Ternstroemia considered by some to belong to the Pentaphylaceae (or its own family Ternstromeaceae).
oVery immature pods.
TAB LE 1 (Continued)

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BARNETT et a l.
(i) a high percentage of the fruits eaten by Chiropotes albinasus
would be infested by larval insects;
(ii) foraging C. albinasus would select such infested fruits at a fre-
quency disproportionate to their availability;
(iii) fruit- infesting larvae would not be found intact and alive in the
feces of C. albinasus;
Finally, because larval infestations generally create holes and
tunnels in fruit pericarp and/or seed coats (see images in Barnett
et al., 2016), this could, potentially, make the fruit husk, and/or that
of the shell of the seed within, easier to break, resulting in a me-
chanical advantage to their exploitation. Thus, to test whether me-
chanical rather than nutritional benefits underpinned any recorded
preferences, we also predicted that:
(i) for any given species, the force needed to penetrate the protec-
tive covering of the part eaten by C. albinasus would be less in
infested than in uninfested fruits.
2 | METHODS
2.1 | Study site and species
The study took place on middle Rio Tapajós, Pará State, Brazil
(Figure 1). Regionally, the ma in forest ty pes are tall terra firme (never-
flooded) forest (15– 30 m), and igapó (Prance, 1979). The latter is a
seasonally flooded forest, inundated at the study site from January-
late April/early May (de Oliveira et al., 2016), by the nutrient- poor
waters of the Rio Tapajós (Junk, 2013). Igapó forest forms a narrow
strip (rarely more than 10 m wide) along the banks of the Tapajós
and tributaries. The study area lies between the town of Itaituba
(4°16′33″S, 55°59′02″W), the impassable rapids on the Tapajós
south (upstream) of Machado village, and the first set of impass-
able rapids on the lower Rio Jamanxim (4°45′23″S, 56°26′15″W;
Figure 1).
Unlike many primate genera in the Tapajós river basin (e.g.,
Alouatta, Aotus, Ateles, Mico, and Plecturocebus), the species of
TAB LE 2 Content of red- nosed cuxiú (Chiropotes albinasus) fecal pellets, Rio Tapajós, Pará State, Brazil.
Pellet # Plant material present Animal material present Comments
1Pollen, leaf frag, stamens Some legs (of beetles?), beetle elytra –
2No identifiable material Spiders, caterpillar headcapsules, setae Possible consumption of the same kind of
caterpillars as reported by Veiga and
Ferrari (2006)
3No identifiable material No identifiable material No identifiable remains, gray- pink matrix
appeared smooth and homogeneous
4 Strands of fiber (palm fruit?) Spiders, beetle elytra (some ver y small) Very small elytra could be from seed beetles
(Bruchinae)
5No identifiable material Winged ant remains (~25% of pellet by
volume)
Based on thorax fragments, ants would
have been around 1.25 cm long. Ferreira
et al. (2021) repor t ant- eating very common
in South American primates.
6Three intact Duroia seeds, plus
testa fragments
No identifiable remains – some material
that might be larval skin
Two seeds germinateda
7No identifiable material Beetle wings and elytra (some very small),
spiders, termite wings.
As above, possible bruchinids from seeds?
8Possible bud scales, pollen, a petal
fragment
Remains of several stingless bees, small
irregular shapes (possible remnants of
nest resin)
Moura (2016) reports Chiropotes sagulatus
raiding stingless bee nests
9Leaf fragments, bud scales (?) Leg fragments (possibly from beetle
imagos)
Young leaf?
10 No identifiable material Some termite wings, beetle legs, and elytra
(some very small)
As above, possible bruchinids?
11 – – No identifiable remains, gray- pink matrix
appeared smooth, and homogeneous
12 No identifiable material Grasshopper remains; dense, non- plant,
material – possibly from a spider egg
case?
Spider egg case eating reported by Moura (2016)
for Chiropotes sagulatus
13 – – No identifiable remains, pinkish- gray matrix
appeared smooth, and homogeneous
aThree Duroia seeds were found intact in one pellet. Since previous studies had found D. velutina seeds in germinated from feces of Cacajao, a close
Chiropotes relative (Barnett et al., 2012), the seeds were placed on local soil in a plastic pot covered with netting, and watered to keep the soil moist,
two seeds sprouted (9 and 11 days after sowing).

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BARNETT et a l.
Chiropotes, the red- nosed cuxiú (C. albinasus), is found on both
banks (de Oliveira et al., 2016). The species is arboreal, weighs some
3.5 kg, travels in groups of 20– 60, has a home range that may exceed
1000 ha (Pinto et al., 2020), and is listed as Vulnerable by the IUCN
(Pinto et al., 2020).
2.2 | Data collection
2.2.1 | Field surveys
As part of a broader series of faunal surveys in the mid- Tapajós (de
Oliveira et al., 2016; Barnett & de Oliveira 2018; Barnett, Ronchi-
Teles, et al., 2017; Barnett, Silla, et al., 2017, Barnett, de Oliveira,
et al., 2018; Barnett, Todd, & de Oliveira, 2018; Jucá et al., 2020;
Tománek et al., 2020), we collected field data on C. albinasus be-
tween October 2013 and December 2014. Primate surveys oc-
curred between 05:30 and 18:30 h from motorized canoes, and from
06.00– 10.00 h and 14.00– 18.00 h on trails. Using a pre- existing trail
system (de Oliveira et al., 2016), we conducted primate observa-
tions and collected data on the margins of the igapó (a 200- km
transect) and in adjacent terra firme forest (five 10- km transects).
During these surveys, the GPS location of each feeding tree was
recorded, and in- field taxonomic identification of individual trees
was conducted as far as possible. When a C. albinasus group was
seen entering a feeding tree, the group was observed to ascertain
feeding bout duration, plant species identity and part eaten, and
the way it was processed. As the study was par t of a broader faunal
st udy, su ch ob servations were discontinue d after 30 min , unl ess th e
encounter was close to the end of a survey session.
2.2.2 | Sample form
Monkeys are not tidy feeders (Howe, 1986), and it is common for
large volumes of partially eaten fruits to accumulate below feeding
trees. Barnett, Ronchi- Teles, et al. (2017); Barnett, Silla, et al. (2017)
used the word “ort” for such material, a word defined as “a frag-
ment of food, fallen from a table. A meal remnant” (https://www.
m e r r i a m - w e b s t e r . c o m / d i c t i o n a r y / o r t ). This usage was followed by
Ballantyne (2018) and dos Santos- Barnett et al. (2022), and we use
it here.
While monkeys can be messy eaters (Zagt, 1997), they are
also often highly selective feeders (Chapman et al., 2012; Clink
et al., 2017). Consequently, many previous studies have used ort-
based methods to study diet composition and patterns of selectivity
(Table S1). Thus, while an imperfect measure of dietary “selectivity”
that requires controlled laboratory experiments for supportive veri-
fication, dropped fruit is often an important source of information in
studies of wild primates.
The feeding remnant orts collected from beneath feeding trees
are likely to be mixed with fruits handled and dropped without
opening, and those opened and discarded without consumption.
However, preliminary studies indicated that, for all sampled spe-
cies, fallen whole fruits had the same proportions of infested/non-
infested fruits on the ground as in the trees. It therefore appeared
that cuxiús did not pluck then reject infested material, and that such
fruits had simply been knocked down accidentally by movement.
Accordingly, such material was not used in analysis, which focused
purely on material that had been fed upon.
2.2.3 | Sample collection
Fed- at trees were flagged with marking tape. Any repeat vis-
its by C. albinasus to individual trees were treated as independ-
ent events. Trees with very recent feeding signs (orts that were
not discolored and/or still oozing sap or latex and bearing dental
marks characteristic of Chiropotes feeding) were also sampled (see
Figure 2). We did not collect orts or seeds that, based on discol-
oration or loss of texture, were considered likely to have been on
the ground for longer than 1– 2 h, since the action of foraging ants
could have reduced insect content of such material greatly, and so
bias results.
FIGURE 1 Map illustrating the location
of the study area and positions of land and
water transects.

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BARNETT et a l.
2.2.4 | Defining and collecting insect- infected fruits
Members of the genus Chiropotes have diets dominated by imma-
ture seeds from hard- husked fruits (Pinto et al., 2018). In such fruits,
the husk, in addition to a low water content, is often rich in tan-
nins and highly sclerified or fibrous (Cunha Junior et al., 2020; van
Roosmalen, 1985), which may account for low frequency of their
infestation by insects, compared to pulp or seeds (A A Barnett, un-
published data). However, pulpy fruits accounted for nearly half the
species eaten (51 of the 117 species reported for the C. albinasus
diet by Pinto, 2008). Consequently, both seeds and pulp (if present)
were checked for the presence of resident infesting insects. We dis-
tinguished these from visiting scavengers by their presence in exca-
vated tunnels, presence of frass, and individuals being at the larval
(rather than adult) development stage.
To compare infestation levels, we analyzed values from fallen
fruits (orts) with feeding marks and those from fruits on branches
trimmed from trees C. albinasus had been observed to feed. To ex-
pand the sample, and more accurately assay the potential range of
infestation levels, we collected fruit from the canopies of other in-
dividual trees belonging to known food tree species, but in which
feeding had not been observed. All such trees were within 250 m of
a tree in which C. albinasus had been observed feeding.
2.2.5 | Determining which primate species had
deposited the collected orts
The two pitheciin species in the region (C. albinasus and Pithecia
mittermeieri) leave different dental marks on orts than the other
large- bodied primates of the central Tapajós (Ateles chamek, Ateles
marginatus, Alouatta discolor, Alouatta nigerrima, Cebus albifrons, and
Sapajus apella: de Oliveira et al., 2016), an effect of the marked dif-
ferences in dental morphology and means of food processing of each
taxon (Rosenberger, 2020). As pitheciins, C. albinasus and P. mitter-
meieri, have a unique feeding method (termed “sclerocarpic foraging”
by Kinzey (1992)), which uses hypertrophied canines to penetrate
fruit husks and procumbent incisors to extract seeds imparting char-
acteristic dental impressions (see Figure 2) on fruit husks and any
associated pulp. Pithecia mittermeieri was rarely seen and is smaller
in body mass than C. albinasus, making it unlikely that orts from the
two species would be assigned erroneously.
2.2.6 | Determining larval gut passage survivorship
To assess gut passage survivorship of larvae, we actively searched
feeding areas for fecal pellets. Chiropotes pellets have a characteris-
tic shape and form, resembling a large coffee bean, that allows them
to be easily distinguished from those of similar- sized regional pri-
mates. The lack of sections of fiber and leaf fragments sets them
apart from deer.
During sampling, fruit and seeds were stored in plastic zip- lock
bags and labeled either as orts, fallen- uneaten fruits, or fruits re-
moved from the tree. We stored fecal material in crush- resistant
vials. All fruits, seeds, and fecal pellets were analyzed in a field lab
within 3 h of collection and then preserved in alcohol.
2.2.7 | Plant species identification
Plants were identified to lowest possible taxonomic category
using Gentry (1993), Ribeiro et al. (1999), van Roosmalen (1985),
Neotropical Flora volumes (e.g., Mori & Prance, 1990), specialist
literature (e.g., Procópio & Secco, 2008 for Couratari), and Harris
and Harris (2001) and Jackson (2004) for botanical terminology.
Identifications were confirmed using species lists in Pinto (2008:
terra firme), Fe r rei r a & Pr a n ce (1998: igapó), and comparison of photo-
graphs of fruits, seeds, leaves, flowers (when available), bark, whole
tree (when possible) with on- line herbarium resources: Neotropical
Herbarium Specimens, New York Botanic Garden, Tropicos, and
Flore de Guyane (https://www.field museum.org/node/4781; ht tp://
sweet gum.nybg.org/scien ce/vh/; https://www.tropi cos.org/home,
https://flore deguy ane.piwigo.com, respectively).
2.3 | Data analysis
To test Prediction i (that a high percentage of the fruits eaten by
C. albinasus would be infested by insects), the presence/absence of
infestation was determined for the seeds in each individual fruit, and
percentages were then calculated per plant species. This was done
by analyzing orts discarded by C. albinasus and retrieved from the
ground. Infestation intensity (measured as number of larvae or their
total weight) was not quantified due to equipment failure.
To establish on- tree levels of infestation (key for Prediction ii,
that foraging C. albinasus would select such infested fruits at a fre-
quency disproportionate to their availability), fruits/seeds were sec-
tioned, and the presence of insect larvae and/or damage associated
with them (tunnels, bore- holes, frass, and discoloration) was noted.
For each species, infestation was quantified using only fruits at the
same maturation level as those eaten by C. albinasus. Following
Barnett, Ronchi- Teles, et al. (2017); Barnett, Silla, et al. (2017) and
Felton et al. (2008), we tested for selectivity of insect- infected fruit
(Prediction ii) obtain from tree canopies using Electivity Indices
(Ivlev, 1961) for each fruit species, such that:
where Oi = percent of orts with insect- infestation, and Ti = percent of
on- tree fruit insect- infestation. Electivity values range from −1 to +1,
where +1 indicates complete selection, −1 indicates complete avoid-
ance, and 0 indicates no preference (larvae- infested fruits selected at
ambient value).
(
Oi−Ti
)
∕
(
Oi+Ti
)

8
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BARNETT et a l.
To provide comparability, and to ensure selection estimates were
conservative, we used the same categories as Barnett, Ronchi- Teles,
et al. (2017); Barnett, Silla, et al. (2017); values ±0.33 to either side
of zero (neutral) indicated no selection had occurred; values < −0.33
indicated negative selection (active avoidance), and values >+0.33
indicated active selection.
To assess whether fruit- infesting larvae passed intact and alive
through the C. albinasus digestive sy stem (Prediction iii), fec al pellet s
were broken apart with a thin glass rod. Material was then washed,
sorted, placed in a petri dish, and scrutinized with a 10x hand- lens.
We paid particular attention to the presence of invertebrate frag-
ments, intact insect larvae, and pupae (the latter because they may
not have been masticated due to small size). Any apparently intact
individuals were prodded with a seeker tip to test for vitality.
To determine whether the force needed to penetrate the cov-
ering of the part eaten by C. albinasus is less for infested fruits than
those whose non- infested status has left their pericarps intact
(Prediction iv), we tested relative penetrability of the eight species
with hard- husked indehiscent fruit (Couratari stellata, Couratari cf.
tenuicarpa, Eschweilera alba, Eschweilera obversa, Hevea spruceana,
Lecythis lurida, Mabea nitida, Macrolobium acaciifolium), and two
species with hard, but indehiscent, fruit (Chaunochiton loranthoides
and Ternstroemia candolleana). We used only hard- husked fruits,
due to the differences in materials failure in brittle (dry shell) and
ductile (pericarp- covered pulp) substances: in the former, cracks
auto- propagate from the point of impact (Mode I fracture: cracking),
while in the latter, propagation requires the application of contin-
uous force (Mode III fracture: tearing or ripping) (Sun & Jin, 2012).
Thus, just as a bored hole create s a zone of weakness in a rigid struc-
ture (Bao & Wierzbicki, 2004; Murdani et al., 2008), a bite is only
likely to facilitate post- canine insertion crack propagations in hard,
non- elastic, husks, and not pulpy ones.
Like C. ouakary (Barnett et al., 2016), C. albinasus opens hard-
husked fruits by biting selectively at areas of natural weakness
(sutures of dehiscent fruit) or thinness (indehiscent fruit) (A.A.
Barnett, unpublished data). Accordingly, following Barnett
et al. (2015), Barnett, Ronchi- Teles, et al. (2017); Barnett, Silla,
et al. (2017) we measured penetrability values at sutures and on
between- suture faces using an International Ripening Company
(Norfolk, VA 23502- 2095) FT- 011 fruit penetrometer, mounted on
a replica Fridley Fruit Tester (Fridley, 1966), with the prosthetic
cast of an adult female C. albinasus canine replacing the standard
plunger head. Single measurements at, and between, sutures were
made, to avoid the possibility of induced mechanical weakness
induced by experimentally made holes affecting the values of
subsequent measurements. We measured the force required not
just to penetrate the husk, but also to reach the seed since some
species (e.g., Hevea spruceana) have a second, inner, layer (the en-
docarp) harder than the outer epicarp (Muzik, 1954). Differences
in penetrability were tested by comparing single measurements
from the sutures and the areas between them for 10 infested and
10 uninfested fruits of each species (i.e., fruits with and without
insect bore/oviposition holes using a Mann– Whitney U test). To
avoid compromising the very structural integrity under investiga-
tion, al l tested fruit s were opened only af ter use , and the presence
of infesting animals then ascertained. Level of significance was set
at 0.05.
Although fungal infections have been shown to influence ver-
tebrate choice of fruits, either positively (Buchholz & Levey, 1990 )
or negatively (Cipollini & Stiles, 199 3), we did not investigate this
variable, and excluded fruits with fungal rot from the data sets of all
investigated species.
3 | RESULTS
A total of 4649 fruits from 130 trees or vines, representing 37 spe-
cies in 30 genera and 18 families were analyzed. A total of 3249
fruits from trees were sampled, and 1400 fruits were sampled as
orts. Of the 130 trees or vines from which fruits were obtained, 56
were sampled as a result of direct observation, while collections
from 74 others represented sites where feeding had occurred very
recently (e.g., fruit not discolored, and/or covered in ants; Table 1).
Of the 37 species recorded as eaten by C. albinasus, eight were
exploited when both immature and mature (Malouetia flavescens;
Tabernaemontana sp. – both Apocynaceae; Dalium sp., Swartzia
polyphylla – both Fabaceae; Couratari cf. tenuicarpa, Lecythidaceae;
Calytranthus sp ., Eugenia s p . – bot h My rt ace a e ; Duroia s p., Rubi a c e ae),
providing a total of 45 diet items, with either the same part being
eaten in both stages (seed: M. flavescens, Tabernaemontana sp., C.
cf. tenuicarpa) or different parts of the fruit (e.g. whole immature
pod vs aril in mature pod: Swartzia polyphylla: Table 1). Only one
(Iryanthera sagotiana, Myristicaceae) definitively lacked any obvious
FIGURE 2 A Sapotaceae fruit eaten by Chiropotes, showing the
curved insertion point of the dental arc of the procumbent incisors,
and the lateral rips subsequently made by the robust, splayed,
and canines. Photo Credit: Justin A . Ledogar of fruit bitten by
Chiropotes sagulatus in Suriname.

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9
BARNETT et a l.
insect infestation. Of the remaining 44 species, selectivity could be
determined for 41. For the other three species, fruits were ingested
in their entirety, leaving no orts for analysis. Of the 41, fruits with
infested seeds were positively selected in 20 (48.8%). In 15 of the
41 species (36.6%), fruits with infested and uninfested seeds were
eaten at parity. In 6 species (14.6%), fruits with infested seeds were
eaten at less than parity, and so appear to have been avoided.
Thus, in terms of the overall diet, the incidence of infestation
on by- species basis was high (44 of the 45 diet items analyzed:
97.8%), as were leveled for many species (Table 1). Additionally,
within species, selectivity was relatively high with infested fruits
being eaten at a greater frequency than parity for 26 species
(63.4% of the 41 for which selectivity could be analy zed). Of these,
20 were positively selected (48.8% of analyzed species, and 76.9%
of species for which selectivity was demonstrated: Table 1). Thus,
Prediction i (that infestation would be high) is supported, and
Prediction ii (that infested fruits would be eaten preferentially) is
partially supported.
Analysis for living larvae and pupae was conducted on 13 C. al-
binasus fecal pellets (Table 2). Of these, nine (69.2%) contained the
remains of some form of invertebrate, most likely the result of insec-
tivory sensu stricto (Ayres & Nessimian, 1982; Frazäo, 1991; Pinto
et al., 2018). There were, however, no living larvae and few larval re-
mains (Table 2), apart from head capsules and other well- sclerotized
parts and some areas of dermis. Pupal remains were also found, but
none were intact (Item 4, Figure 3). Thus, Prediction iii is validated:
neither insect larvae, nor pupae, survived passage through the gut
of C. albinasus. We did not record any intestinal parasites that might
have been mistaken for seed- inhabiting larvae that had survived
passage through the alimentary canal.
Comparative penetrability data for sutures and faces of fruits
that were and were not infested were obtained for 10 species: eight
with hard- husked dehiscent fruits, and two hard- husked indehiscent
species (Table 3). For six of the tested species (including the two
indehiscent), there were no significant differences between the pen-
etrability faces of infested and uninfested fruits (statistical results
are in Table 3). We also found no significant difference between the
force needed to penetrate sutures for infested and uninfested ex-
amples of any of the eight fruits with dehiscent morphologies (sta-
tistical results are in Table 3). Hence, Prediction iv is not validated,
and infested fruits were not more easily penetrated than uninfested
fruit.
4 | DISCUSSION
Infestation levels were high in the fruit tested since of the 45 items
from 37 species of fruits seen to be consumed by the monkeys only
one lacked evidence of infestation. Selectivity could be estimated
for 41 of the 44 infested items, with selectivity data lacking for three
which were eaten whole. Of the 41, six (15%) appeared to have been
avoided when infested, while in 20 (49%) fruits with infested seeds
appeared to have been preferentially selected. Fruits of 15 species
(36%) were eaten at parity. Furthermore, none of the fecal samples
showed any evidence of living pupae or larvae.
We found no difference in the penetrability of the husk face or
suture for any of the 10 species analyzed, indicating that infested
fruit choice was based on insect presence, rather than relative ease
of access. Larval infestation was restricted to seeds in all studied
cases. This is likely due to the dry, fibrous, tannin- rich nature of the
pericarp of the species investigated and means that the obtained
penetrabilit y values therefore refle cted thos e of likely to be encoun-
tered by a foraging C. albinasus.
Overall, Prediction i (a high percentage of the species eaten by
Chiropotes albinasus would have seeds infested by insects) was sup-
ported, while partial support was obtained for Prediction ii (within
species, C. albinasus would select infested fruits at a frequency dispro-
portional to their availability). Additionally, support was found for
Prediction iii (fruit- infesting larvae would not be found whole and alive
in the feces of C. albinasus), but not for Prediction iv (for any given
species, the force nee ded to penetrate the protective covering of the part
eaten by C. albinasus would be greater for fruits with uninfested seeds
than those where seeds were infested). The fact that there was no dif-
ference between penetration force values at the suture for any of
the tested species is significant since, like Cacajao ouakary (Barnett
et al., 2016), C. albinasus selectively bites at the sutures when fruits
possess them (AA Barnett & T. de Oliveira, unpublished data).
As noted above, infesting insects may occur in both the pulp or
seeds of fruit. In the current study, 17 of the 37 species of fruits
recorded in the diet had pulpy pericarp (45.9%: a value close to that
recorded by Pinto (2008) in the same region, 43.6%). Of these, eight
FIGURE 3 Invertebrate remains from a fecal pellet of Chiropotes
albinasus, showing fragments of spiders, and adult insects, but no
larval insects associated with fruit infestation or their pupal stages.
1 = termite wings, 2 = caterpillar skin, 3 = elytra of small beetles,
4 = empty Dipteral pupal cases, 5 = caterpillar head capsules,
6 = body of a spider. Each square is 0.5 × 0.5 cm. Photo Credit:
Adrian A Barnett.

10
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BARNETT et a l.
had records of infestation in both the pericarp and seeds, while in
nine only the seeds were infested (Table 1). No eaten fruit had only
pulp infested.
Penetrometer values showed insect presence does not make
it easier to open a hard- husked fruit. Furthermore, the insects in-
gested (we saw no evidence that they were spat out) appear to have
been digested, since none appeared as living larvae or pupae in fecal
samples. The lack of living insects in C. albinasus fecal samples con-
trasts with those of other neotropical seed eaters, where living lar-
vae and pupae of fruit- infesting insects have been found (see Guix &
Ruiz, 1995, 1997 for birds). Indeed, while diverse remnants of adults
occurred in the analyzed C. albinasus fecal samples (see Table 3), lar-
val material was represented by just a few head capsules (item 5 in
Figure 3), setae and material resembling caterpillar skin (item 2 in
Figure 3). This probably occurred because larvae are generally very
lightly sclerotized, so that most parts would be unlikely to survive
the digestive passage intact.
The variation recorded here in C . albinasus sele ctivi ty of fr uit wi th
infested seeds (i.e., select, parity, and reject) has also been reported
for C. ouakary (Barnett et al., 2015) and Ateles spp. (dos Santos-
Barnett et al., 2022). As with these species, experimentally verified
explanations for this range of responses is lacking. However, cases
where infested items are selected at parity may reflect some form
of frequency- dependent selection, where the chance of encounter-
ing an item is sufficiently large that the extra time spent in active
searching is not compensated for in enhanced returns. Meanwhile,
cases where fruits with infested seeds are selected at parity may
be due to avoidance of chemicals synthesized as part of the plant's
defensive response to seed infestation, including those where plants
selectively accumulate toxic compounds within such infested seeds
(Ibanez et al., 2009), as well as insect countermeasures where larvae
sequester such compounds for their own defense (Ferro et al., 2006).
Some responses by C. albinasus clearly showed fine adjustments
in foraging techniques. For example, very young pods of Swartiza
polyphylla (Fabaceae) were eaten in their entirety (as humans would
eat petit pois), while in more mature fruits only the sarcotesta is
eaten. By weight, the sarcotesta is a very small proportion of the
entire seed (less than 5%), an aspect that might well have influenced
the selectivity pattern observed. In species where infested seeds
were generally avoided, a few were recorded as being eaten (e.g.,
Inga). However, under such circumstances, the missing (i.e., eaten)
portions appeared not to have insect- bored galleries continuing
into them. Given the lack of the kind of direct action by insects that
would induce a phytochemical response, we consider it probable
that such areas did not have higher levels of toxic chemicals than
other parts of the seeds of conspecifics.
Infestation was common with 44 of the 45 food items (98%) hav-
ing some individuals that were infested. Of the infested items, 20
(45%) were positively selected. We attribute this to the nutritional
benefits of insect consumption. Although we have focused here on
the potential benefits of larvae as supplements in an immature seed-
dominated diet potentially deficient in protein (Bukkens, 1997),
it should be noted that insect larvae can also function as sources
TAB LE 3 Comparative penetrability (kg/mm2) of faces and sutures of hard- husked fruits with infested and uninfested seeds eaten by red- nosed cuxiú (Chiropotes albinasus) on the Rio
Tapajós, Pará State, Brazil.
Species
Uninfested face:
Mean ± SD (range)a
Infested face:
Mean ± SD (range)aSignificance
Uninfested suture:
Mean ± SD (range)a
Infested suture:
Mean ± SD (range)aSignificant difference?
Chaunochiton loranthoides 2.09 ± 0.07 (2.0– 2.1) 2.07 ± 0.05 (2.0– 2.2) No (U = 41.5; p = .52) n/abn/a n /a
Couratari stellata 9.6 8 ± 0.12 (9.4– 9.8) 9.48 ± 0.21 (9.1– 9.7) Yes (U = 20.0; p = .020) 6.27 ± 0.32 (5.8– 6.6) 6.28 ± 0.27 (5.9– 6.7) No (U = 48.5; p = .91)
Couratari cf. tenuicarpa 2.27 ± 0.16 (2.0– 2.5) 1.89 ± 0.20 (1.5– 2.2) Yes (U = 5.0; p = .0 01) 1.70 ± 0.13 (1.5– 1.9) 1.73 ± 0.11 (1.6– 1.9) No (U = 46.0; p = .75)
Eschweilera albiflora 4.74 ± 0.83 (3.3– 5.8) 3.79 ± 0.95 (2.5– 5.0) No (U = 25.0; p = .058) 3.08 ± 0.33 (2.6– 3.7) 3.06 ± 0.55 (2.3– 3.7) No (U = 48.0; p = .91)
Eschweilera obversa 5.77 ± 0.91 (4.3– 7.2) 4.68 ± 0.83 (3.3– 6.0) Yes (U = 19. 0; p = .019) 3.04 ± 0.55 (2.4– 4.0) 3.03 ± 0.52 (2.5– 3.9) No (U = 50.0; p = 1.00)
Hevea spruceana 3.01 ± 0.73 (1.7– 3.8) 3.00 ± 0.64 (1.8– 3.7) No (U = 49.0; p = .94) 1.75 ± 0.24 (1.3– 2.1) 1.74 ± 0.22 (1.3– 2.0) No (U = 47.0; p = .82)
Lecythis lurida 5.64 ± 0.41 (5.0– 6.3) 5.20 ± 0.56 (4.3– 5.9) No (U = 30.0; p = .13) 5.20 ± 0.30 (4.8– 5.8) 5.21 ± 0.27 (4.9– 5.6) No (U = 47.5; p = .85)
Mabea nitida 2.73 ± 0.34 (2.1– 3.3) 2.13 ± 0.47 (1.5– 3.1) Yes (U = 15.0 ; p = .008) 1.86 ± 0.26 (1.5– 2.4) 1.89 ± 0.17 (1.7– 2.2) No (U = 43.5; p = .62)
Macrolobium acaciifolium 3.03 ± 0.21 (2.7– 3.4) 3.07 ± 0.29 (2.7– 3.6) No (U = 42.0; p = .54) 5.37 ± 0.39 (4.8– 6.0) 5.35 ± 0.49 (4.8– 6.2) No (U = 48.5; p = .91)
Ternstroemia candolleana 1.84 ± 0.22 (1.5– 2.2) 1.67 ± 0.31 (1.3– 2.1) No (U = 34.5; p = .24) n/abn /a n/a
aSample size is 10.
bIndehiscent fruit.

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11
BARNETT et a l.
of minerals, amino acids, and vitamins (Drew, 198 8; Finke, 2013).
Indeed, accessing such supplements from insect larvae may be par-
ticularly efficient, since the generally low levels of sclerotization
of larval exoskeletons results in their being more easily digested
than those of imagoes (Hopkins & Kramer, 1992; Raubenheimer
& Rothman, 2013). Furthermore, since infesting larvae are con-
centrated within the boundaries of the seed, they also represent
a clustered resource whose exploitation is more time/energy effi-
cient than the more spatially dispersed adults (Barnett et al., 2020;
McNamara & Houston, 1987 ). This may be significant since, in some
fruits, infesting insects can constitute up to 35% of the total mass
(Barnett et al., 2022; Barnett, Ronchi- Teles, et al., 2017; Barnett,
Silla, et al., 2017 ).
However, this foraging approach is not without risks since dam-
aged seeds may contain aflatoxins, which are inimical to mammals
(Janzen, 1977; Massey et al., 1995). Accordingly, the avoidance of
some plant species may be a reflection of aflatoxin avoidance. In ad-
dition, such fruits may have already had a substantial proportion of
their material consumed – potentially offsetting the energetic gains
obtained from animal material ingestion (Muñoz & Bonal, 2008).
Thus, we have shown that while it is a species already known
to eat large free- ranging adult insects (Ayres & Nessimian, 1982 ;
Frazäo, 1991; Mittermeier et al., 1983; Veiga & Ferrari, 2006), as well
as large spiders and their egg sacs (Moura, 2016), C. albinasus also
appears to practice covert carnivory (sensu Barnett, Ronchi- Teles,
et al., 2017; Barnett, Silla, et al., 2017), eating insects concealed
within seeds, and appearing to actively select infested seeds when
doing so.
Chiropotes is a pitheciin, a group of neotropical primates that are
generally considered to be seed predators and thus a group whose
dietary strategies work in opposition to the reproductive interests
of the plant species on which they feed. However, since many of the
plant species involved have fruiting periods long enough to support
several sequential generations of seed- predating insects (e.g., multi-
voltine species: Janzen, 1976), the apparent capacity of C. albinasus
(and presumably other members of the clade) to digest larvae, could
act as a source of population control for such insects. This may be
especially pertinent given that fruits with infected seeds are prefer-
entially selected. Combined with observations that pitheciin species
can also act as seed dispersers (Barnett et al., 2012), this under-
scores the fact that not all pitheciin intersections with plants in their
diet are predatory.
Covert carnivory may also be underestimated in other plant
forms. Other potential insect- rich sources include buds, develop-
ing flowers, and young shoots (dos Santos- Barnett unpublished
data), while young, unopened, leaves may house concealed cat-
erpillars (Barnett, de Oliveira, et al., 2018; Barnett, Todd, & de
Oliveira, 2018). Many primates, including Chiropotes spp., are also
known to eat buds (stem, leaf, and flower) and flowers (Boyle
et al., 2012; Di Fiore et al., 2008; Felton et al., 2008; Gregory, 2011;
Russo et al., 2005). Given the ub iquit y of bud- bor ers (Hanover, 1975;
Sugiura & Yamazaki, 2009), and the often extensive presence of lar-
val insects in budding and open leaves (Liu et al., 2015), and flowers
(e.g., Barnett et al., 2020 for Eschweilera tenuifolia, Lecythidaceae),
it is possible that covert carnivory occurs here too. Along with
observing insectivory on 18 occasions over a year- long study of
Chiropotes sagulatus, Gregory (2011) observed frequent (101 bouts)
consumption of Lecythidaceae flowers, and found that most of the
fallen flowers inspected on the ground were infested with a variety
of insect larvae. Additionally, older Pradosia caracasana (Sapotaceae)
fruit opened by C. chiropotes in Venezuela had (bruchid) beetle emer-
gence holes (M Norconk, unpublished data).
Furthermore, while Chiropotes spp. are known to eat the suc-
culent leaf- bases and central stems of epiphytes, this may not be
a source of water, as commonly supposed for primates (Galetti &
Pedroni, 1994; Peres, 2000; Wright, 2004). Instead, they may be
consuming insects, since such areas are commonly colonized by
Dryophthorid weevils of the genus Metamasius (Cave et al., 2006),
which are bromeliad- tissue specialists and can reach high densities
(Frank, 1999). Ad dit ionally, Pint o et al. (2018) re ported 39 in stan ces
of leaf galls being eaten by C. albinasus (though insect type was not
identified). Galls can be important sources of insect- derived pro-
tein (Milton & Nessimian, 1984) and are known to be eaten by a
range of other primates (e.g., indri lemur, Indri: Britt et al., 2002;
patas monkey, Erythrocebus patas: Isbell, 1998; Hanuman lan-
gur, Presby tis entellus: Srivastava, 1991; chimpanzee, Pan trog-
lody tes: Tutin & Fernandez, 19 93; Rio Mayo titi, Plecturocebus
oenanthe: Deluycker, 2012; Chamek spider monkey, Ateles chamek:
Wallace, 2005). Thus, it is possible that such ingestion again ser ves
as a supplemental source of insect- derived protein. In addition,
Shaffer (2013) noted that C. sagulatus would eat adult beetles pres-
ent within Fabaceae pods, but not in the seeds. Though this was
observed in fieldwork for the current study and may represent a
source of additional protein, beetle presence was not quantified.
Given the large number of small beetle- like legs and small elytra
that were present in the fecal pellets (item 3, Figure 3), it seems
likely that such taxa also form part of the C. albinasus diet.
Of the 37 species of fruits studied, 17 had a pulpy exterior, and
in eight this area was also infested with insects. Thus, it is possible
that they, rather than the insects in the seeds, alerted and attracted
the foraging monkeys. Irrespective of this, the fact that covert car-
nivory occurs in C. albinasus remains unaltered. Together, this and
the information above support the original contention of Redford
et al. (1984) who were the first to propose that primates might gain
protein from eating larval insects in food items, but whose insight
was widely overlooked until recently.
ACKNOWLEDGMENTS
AAB thanks Maracajá Ecological Consulting for the invitation to
conduct the primate survey work. TCS- B thanks the Department
of Nutrition at University Central Manaus- FAMETRO. TdeO wishes
to thank CNEC/WorleyParsons and ELETROBRÁS for financial
support of the mammal survey in the Tapajós river basin. We col-
lectively thank Daniela Zappi and John VanderPlank for identifying
the Passiflora. AAB was supported by PNPD/CAPES (Process no.
8887.470331/2019- 00), ALLM is supported by Capes (Finance code

12
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BARNETT et a l.
0001), BMB is partially supported by a CNPq- Productivity grant
(309256/2019- 4). This paper is contribution 54 from the Amazonian
Mammals Research Group, and contribution number 63 from the
Igapó Study Project. We thank the anonymous reviewers and the
journal editor, Laurence Culot, for their helpful comments, and
to Wendy Martin for her kind assistance. We also thank Justin A
Ledogar for providing the image for Figure 2.
CONFLICT OF INTEREST STATEMENT
No potential conflict of interest was reported by the authors.
DATA AVAIL AB ILI T Y STAT E MEN T
The data that support the findings of this study are openly avail-
able in the Dryad Digital Repository: https://doi.org/10.5061/dryad.
fn2z3 4v0b (Barnett et al., 2022).
ORCID
Adrian A. Barnett https://orcid.org/0000-0002-8829-2719
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SUPPORTING INFORMATION
Additional supporting information can be found online in the
Supporting Information section at the end of this article.
How to cite this article: Barnett, A. A., dos Santos-Barnett, T.
C., Muir, J., Tománek, P., Gregory, T., Matte, A. L. L., Bezerra,
B. M., de Oliveira, T., Norconk, M., & Boyle, S. A. (2023).
Beans with bugs: Covert carnivory and infested seed
selection by the red-nosed cuxiú monkey. Biotropica, 00,
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