Arthropod Predation by a Specialist Seed Predator, the Golden-backed Uacari (Cacajao melanocephalus ouakary, Pitheciidae) in Brazilian Amazonia
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- Barnett, A.A., Ronchi-Teles, B., Almeida, T. et al. Int J Primatol (2013) 34: 470. doi:10.1007/s10764-013-9673-0
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Morphological adaptations related to food processing generally reflect those elements of the diet that represent the greatest biomechanical challenge or that numerically dominate the diet. However, in periods of the annual cycle when the availability of such foods is low, items to which a species has low apparent morphological adaptation may be included in the diet. Here we test the responses of a diet-specialist primate to limitations in the supply of the resource it is specialized to exploit. Uacaris are primarily predators of immature seeds, in seasonally flooded forests in Amazonian Brazil, and have dental specializations to open hard-shelled fruits. We investigated the importance of arthropods in the diet of golden-backed uacaris (Cacajao melanocephalus ouakary), examining their seasonal importance in the uacari diet, and the ways C. m. ouakary used to access them. Using scan and ad libitum sampling of feeding and phenology from botanical study plots to assess fruit availability, we conducted an 18-mo study in Jaú National Park, Amazonas State, Brazil. We recorded arthropod predation 298 times, with Cacajao melanocephalus ouakary feeding on 26 invertebrate taxa in ≥11 families and 9 different orders. Uacaris extracted wood-boring beetles dentally from rotting wood and smaller larvae from twigs, stems, and petioles, but this food class did not predominate. This food class (encapsulated foods) constituted 23.4 % of the arthropod records. The majority of arthropod food items were either manually removed from substrates (ants, beetle larvae, caterpillars, fulgorid bugs, grasshoppers, mayflies, spiders, termites, wasps, and a whip-scorpion) or plucked from the air (volant Lepidoptera). Uacaris appeared to avoid toxic caterpillars. Insectivory was most frequent when fruit and seeds were least available. Arthropods seem to be seasonally important to this primate, supplementing or making up for shortfalls in the hard fruits and immature seeds for which uacaris have highly developed dental, and possibly intestinal, adaptations.
Morphological adaptations related to food processing generally reflect those elements of the diet that represent the greatest biomechanical challenge or that numerically dominate the diet (Rosenberger 1992). However, in periods of the annual cycle when the availability of such foods is low, items to which a species has low apparent morphological adaptation may be included in the diet (fallback foods: sensu Robbins et al. 2006). Based on Jarman-Bell metabolic scaling (Gaulin 1979), the maximum theoretical adult body mass for primate to have a diet dominated by invertebrates is 500 g (Redford et al. 1984). Known as Kay’s Threshold (Kay and Simons 1980), this maximum mass is rarely surpassed, although patas monkeys (Erythrocebus patas) may be a notable exception (Isbell 1998). However, many primates surpassing this threshold consume insects frequently (McGrew 2001), and the amount eaten often may be underestimated (Chivers 1969). For such larger primates, the energy- and protein-rich packages that arthropods represent are generally exploited either as fallback foods (sensu Robbins et al.2006), in times of need (Cebus apella: Galetti and Pedroni 1994; Ateles: Link 2003), or when insects are superabundant (Erythrocebus patas: Isbell 1998; Presybtis entellus: Srivastava 1991; Cercopithecus lhoesti, Ce. mitis: Tashiro 2006).
Although the existence and ecological importance of insectivory in primates >2 kg is well studied for generalist species such as capuchins (Cebus and Sapajus spp.: Izawa 1979; Melin et al.2007; Thorington 1967), knowledge is still sparse about the nature and importance of insectivory in primate species that have traditionally been regarded as highly dependent on the first trophic level. This includes members of the Pitheciinae: uacaris, genus Cacajao and cuxiú (or bearded sakis), genus Chiropotes. This subfamily possesses dental specializations for extracting seeds from hard-husked fruits, including robust hypertrophied canines and prognathous incisors (Deane 2012; Kinzey 1992; and Fig. 1.2 in Kay et al.2013), and at least some species have an enlarged hindgut (MacLarnon et al.1986), which may be an adaptation for seed-eating (J. M. Ayres and D. J. Chivers, pers. comm.). Researchers have recorded a diet consisting almost entirely of immature seeds and fruit, supplemented by flowers, leaves, and buds, for several uacaris (Cacajao calvuscalvus: Ayres 1986; Cacajao c. ucayalii: Bowler and Bodmer 2011; Cacajao melanocephalus melanocephalus: Boubli 1997; C. m. ouakary: Barnett et al. 2005). However, there is good evidence that arthropods can be seasonally important in the closely related genus Chiropotes, especially in seasons of fruit dearth: for example, insects constitute between 17.8 % (Frazão 1991) and 20.8 % (Peetz 2001) of diet items for Chiropotes chiropotes. Insects may even dominate briefly: Chiropotes satanas fed nearly exclusively on caterpillars over a 3-d period (Veiga and Ferrari 2006). Researchers have recorded seasonal peaks in arthropod consumption of 5.8 % diet and 10.5 % of foraging time in Chiropotes satanas (Veiga and Ferrari 2006). In Cacajao calvus calvus caterpillars briefly constituted nearly 20 % of the diet (Ayres 1986). In addition, there are scattered records of insect consumption in Cacajao including ants, caterpillars, grasshoppers, katydids, and termites (Cacajao calvus calvus: 5.2 %, including some periods during which caterpillars dominated daily diet; C. c. ucayalii, Ayres 1986: 1.7 % of total diet, including removal of commensal ants from hollow terminal stems of Couroupita guianense [Lecythidaceae] and the catching of flying termites; Bowler 2007).
Here we present the first investigation of arthropod predation in golden-backed uacaris (Cacajao melanocephalus ouakary), a species traditionally regarded as gaining sustenance purely from various forms of plant matter (Barnett 2005; Barnett and Brandon-Jones 1997; Norconk 2011; Veiga and Ferrari 2006). We report on which arthropods are eaten and how they are accessed. Based on the hypothesis that a species may exploit foods whose defenses it is not specifically adapted to overcome when those to which it is well adapted are in shorter supply, we test three predictions: 1) that arthropods never dominate the annual overall diet of golden-backed uacaris, but may seasonally form part of it; 2) the season when insectivory is greatest will be that when fruit and seed availability is lowest; and 3) that, given the high level of dental specialization in this primate, the methods by which it accesses arthropods will use the same biomechanical characteristics as those used to access seeds, i.e., dental extraction from a hard-surfaced structure.
Taxonomic note: The precise appellation for some members of the genus Cacajao is currently disputed (vide Boubli et al.2008; Figueiredo 2006; Ferrari et al.2010). Therefore, in this article, the Latin names used for Cacajao species follow Hershkovitz (1987). The use of the common name cuxiú for Chiropotes follows Barnett, Pinto et al.(2012).
A. A. Barnett, T. Almeida, and W. Souza Silva conducted a field study between October 2006 and April 2008 in Jaú National Park, Amazonas, Brazil, between Cachoeira do Jaú (01°53.21′ ′ S, 61°40.43′ ′ W) and Patuá village (01°53.16′ ′ S, 61°44.31′ ′ W), and quantified incidences of arthropod predation. The study was preceded by a series of preliminary visits in 1999, 2000, and 2005 by A. A. Barnett, A. Deveny, and V. Schiel-Baracuhy (Barnett et al. 2005, 2011; Barnett, Boyle et al. 2012, Barnett, Shaw et al. 2012). During all these studies we recorded the identity of ingested arthropods whenever uacaris were observed feeding on them. In all years, we conducted fieldwork in both terra firme (never-flooded lowland rain forest) and igapó (blackwater seasonally flooded forest, sensu Prance 1979). These habitats comprise, respectively 85 % and 12 % of the park’s 2,700,000 ha (Borges et al.2004). Flooding of igapó is greatest between June and July when water depths can exceed 7 m (Ferreira 1997).
We recorded phenology once each month from 1587 trees in 6 study plots, 3 each in terra firme and igapó using presence/absence of fruits, flowers, and new leaves in the canopy of each individual. We assessed the availability of fruit resources to uacaris based on fruit abundance (sensu Chapman et al. 1992) from 20 igapó tree species and 9 tree species from terra firme and from monthly phenology data. Based on these data, we distinguished three phases of resource availability at Jaú (Barnett 2010): Terra Firme Fruit Phase (November–February), fruit abundant in terra firme but sparse in igapó; Igapó Fruit Phase (March–June), flowers, then fruit, abundant in igapó, declining in terra firme; Few Fruit Phase (July–October), fruit availability sparse in both igapó and terra firme, new leaves and shoots available in igapó only. This pulsing of resource availability occurs because tree species in this community most commonly possess hydrochoreous and/or ichthychorous dispersal syndromes (Kubitzki and Ziburski 1994), and peak fruit production occurs when water levels are highest (Parolin et al. 2004). Consequently, March–June is the period both of maximum inundation and of highest fruit production in igapó (the Igapó Fruit Phase).
Uacaris at Jaú migrate seasonally between igapó and terra firme forest, spending the flooded season in the former and visiting the latter for the brief part of the year when igapó is dry (Barnett 2010; Barnett, Pinto et al.2012). We report incidences of predation on arthropods by uacaris recorded during the short visits in 1999, 2000, and 2005 as supplementary observations. The main body of the results comes from fieldwork conducted between 2006 and 2008, when A. A. Barnett and T. Almeida searched for uacaris on foot in terra firme forest, and with paddled wooden canoes in flooded igapó. To maximize the information that could be gained from encounters (Ferrari 1988), we recorded uacari behaviors with both instantaneous scan and ad libitum sampling (Altmann 1974). Uacaris have a social ecology with high fission–fusion dynamics (Bowler and Bodmer 2009), and group sizes in Cacajao melanocephalus ouakary change seasonally, ranging from 5 to 50+ individuals (Barnett 2010). We scan sampled a maximum of three individuals every 30 s for 5 min, choosing the three individuals nearest to the observer. Immediately after each scanning block, we recorded behavior ad libitum for the nearest visible member of the group for 1 min continually, before undertaking the next 5-min block of scans. We used ad libitum sampling to record all behaviors, not just feeding, and followed a scan sampling session with ad libitum sampling whether or not feeding was observed during the scan session. Scanning allowed us to estimate the proportion of feeding bouts devoted to insectivory, while ad libitum sampling provided information on bout duration and how uacaris captured and processed the invertebrates they ate.
For both scan and ad libitum observations we defined a single feeding event as the placing of an edible object in the mouth, followed by processing and ingestion (if observed). We counted this as “one” irrespective of the size of the food item or the time taken to process it. Because floodwaters in igapó cover understory vegetation, visibility was good and did not differ between seasons. As it was rarely possible to sex or individually identify individuals, we combined results from all adult individuals.
When we observed uacaris feeding on animals, we collected the body parts and partial individuals that fell below feeding uacaris to provide material for identification, scooping them up from the water surface with a net and placing the remains in labeled tubes. We retrieved from the water surface stems and small branches from which uacaris had extracted tunneling insect larvae. We also collected examples of those insects that were abundant, i.e., either seen every day or present in localized aggregations where density exceeded five visible individuals per m2, but that the uacaris acted as if they were actively avoiding, either by foraging in an adjacent conspecific tree, not touching or feeding upon the insects even when they fed in the same tree, or coming close to the insects and then turning away from them; see Table III. If we observed extraction from a stem we counted it as one item. We rarely achieved identified larvae beyond class, so we collected similar stems to try and hatch out imagoes from the larvae within. We did not monitor arthropods for seasonal resource availability because the arthropod taxa uacaris ate were unknown before this study and habitat-wide monitoring of annual patterns of general arthropod abundance was not logistically feasible.
If an arthropod specimen could not be identified by B. Ronchi-Teles or colleagues at the Department of Entomology, Instituto National de Pesquisas da Amazonia (INPA), Manaus, we sent digital images to other experts. W. Souza Silva identified plants using Gentry (1993), Ribeiro et al. (1999), and by comparing field-collected material with exiccates in the INPA Herbarium. Though fruits containing adult and larval insects are known to be eaten by uacaris, we did not quantify their percentage contribution to the uacari diet.
We tested prediction 1 by calculating the annual percentage of arthropods in the diet across the year during each of the three phases of resource abundance. We tested for differences in the frequency of insectivory between phases with a χ2 test. We tested prediction 2 by comparing the proportions of arthropods in the diet with the phenological data for fruit availability (a proxy for seed availability for these predominantly seed-eating individuals), and prediction 3 by examining the number of feeding records in which arthropods were encapsulated in hard structures with those that were in soft structures (such as leaves) or free-moving.
In 171 d of field work we recorded uacaris feeding on 26 invertebrate taxa in ≥11 families and 9 different orders. We give their identities and a description of how they were eaten in Table II. During this time we obtained 12,199 feeding records, of which 297 (3 %) involved insects and other arthropods that were freely-moving, i.e., highly motile and neither inside a burrow or nest nor on a web. Overall, caterpillars were the most common category eaten (37.4 %). Most prey items were small, with few (11.5 %) >2 cm in length. Twenty-eight of the 297 records (9.42 %) came from scan samples and the remainder from ad libitum samples (see Table II). With the exception of one occasion, we observed insectivory only in flooded igapó forest. All avoided insects were caterpillars.
We observed uacaris eating invertebrates that moved out of concealment when the primates passed close to them. Animals eaten in this way included the Amazon tailless whip-scorpion (Heterophrynus batesii, Phrynidae), other smaller unidentified invertebrates, and a treefrog (probably Hyla boans, Hylidae). We also saw uacaris attempt to grab butterflies and moths from the air with their hands (N = 9) and to search piles of dead leaves (N = 9). We observed no attempts to predate small vertebrates such as lizards, nestlings, or birds’ eggs.
Predictions 1 and 2: Arthropods will not dominate the diet and the season when insectivory is greatest will be that when fruit and seed availability is lowest.
Seasonal variation in the faunal component of golden-backed uacari diet, in Jaú National Park, Brazil, October 2006–April 2008
N of animal taxa eaten per phase
N of faunal feeding observations and % of all feeding observations (N = total)
Terra firme fruit
98, 3.9 % (N = 2452)
Stem borers (48.9 %, 48), leaf-boring caterpillars (22/2*), Clusia petiole borers (7), Ephemeroptera (7), unidentified on branch (5/2*) beetles in dead wood (3), Polybia wasps (2 nests).
55, 0.7 % (N = 7765)
Ephemeroptera (29.1 %, 15/1*), unidentified 10*, caterpillars (on branches and leaves) 5/1*, ants 5, spiders 4/1*, Orthoptera (adult) 2/1*, Isoptera 3, Polybia wasps (3 nests), Orthoptera (instar) 2, insects in leaves 1/1*
146, % (N = 1685)
Larval Lepidoptera in leaves (58.2 %, 82/2*), Coleoptera 7/2*, ants (adults) 6, Isoptera 6, Orthoptera (adults) 6, Opthoptera (juvs.) 5/1*, unidentified within live leaves 5, spiders 2/3*, insects in dead leaves 3/1*, Polybia wasps (4 nests), ants (larvae) 3, fulgorids 3, stem borers 3, larval Lepidoptera (free-moving) 1/1*
Prediction 3: Uacaris will use the same biomechanical characteristics to access arthropods as those used to access seeds.
Few (3 %) feeding records were from hard-surfaced structures such as dead wood and twigs. However, 61 records (20.5 %) were from stems and petioles, where the invertebrates would also have been encapsulated in a hard covering. In neither case did we retrieve the arthropods involved directly, but we collected dead wood bearing dental impressions across the central frass-filled lumen, the width and spacing of which was characteristic of the genus Cacajao, as were the canine marks on retrieved stems. In all nine cases involving dead wood, the diameter of the tunnel was ≥0.5 cm (max. 1.4 cm), indicating the presence of substantial larval animals (probably those of Cerambycid or Scarabidae beetles). We retrieved Scarabid beetle larvæ from three dead wood sections of the same size and species (Sclerolobium sp., Fabaceae) as those eaten by the uacaris. For stems and petioles, samples of the same host species yielded beetle and lepidopteran larvae. In all cases, damage patterns indicated that uacaris opened the arthropod-containing structures with the tip of a canine. Although specialized dental extraction of larvae is not the only way by which uacaris obtain arthropods, such records did form 23.4 % of all recorded insectivory.
Feeding in arthropods made up a small proportion of feeding records (7.8 % of feeding records), in line with prediction 1. However, we observed increased insect consumption by uacaris in the No Fruit Phase) when fruit availability is lowest, supporting prediction 2.
Support for Prediction 3 was equivocal: Uacaris do extract beetle larvae from rotting branches and from petioles and twigs, all structurally defended resources similar in form to seeds in hard husks, but they also exploit a variety of other arthropods, many of which are soft-bodied and not defended in this way, and they capture them with a great variety of foraging techniques. The dominant means by which arthropods were obtained did not resemble the way they fed for the rest of the year, i.e., extracting larvae from such structurally defended resources as twigs. Instead, in 76.6 % of feeding records, uacaris ate surface-dwelling arthropods, which they apparently encountered opportunistically. Extractive feeding on arthropods from plant material has been recorded in only one other primate species, the aye-aye (Daubentonia madagascariensis), which is, like uacaris, a specialist feeder on structurally defended resources (Erickson 1994; Farris et al. 2011; Sterling 1994). It may be that other Neotropical primates simply cannot access this resource, and only the robust dentition of Cacajao, adapted for sclerocarpic foraging, can break open the relatively thick branches inhabited by such large insects. The tough outer covering surrounding a soft interior entity is not dissimilar to a hard-husked seed, whose body, like a seed itself, is soft and pulpy. In addition, unlike any other primate, uacaris use the tips of their canines to open fruits (Barnett 2010), a behavior that could also be deployed to open stems and access burrowing insects.
Although other pitheciines also show seasonal variation of insectivory (Veiga and Ferrari 2006), there are differences between the arthropod exploitation observed in Cacajao melanocephalus ouakary and other pitheciines, particularly Cacajao and Chiropotes species. For example, with the exception of occasional large (≥6 cm long) larval Automeris sp. (Saturniidae: Helimeucinae), Cacajao melanocephalus ouakary at Jaú appear to have concentrated on small (≤7.5 mm in length) leaf-mining and leaf-burrowing caterpillars. No records paralleled those for Cacajao calvus calvus (Ayres 1986) and Chiropotes satanas (Veiga 2006), where individuals visited tree canopies specifically to feed on large aggregations of caterpillars (those eaten by Chiropotes satanas were ≥3 cm in length; L. Veiga, pers. comm.). In addition, several arthropod taxa eaten by Cacajao melanocephalus ouakary have not previously been recorded in pitheciine diets (see Table II). However, there are several instances in which consumption of the same insect taxon has been recorded in other pitheciids, often with very similar behaviors. For example, observations of Cacajao melanocephalus ouakary extracting Tortricid moth larvæ from Swartzia acuminata leaflets are similar to those for Chiropotes satanas, where individuals removed moth larvæ from young, still folded (L. Veiga, pers. comm.) leaves of Berthollettia excelsa (Lecythidaceae: Veiga and Ferrari 2006). However, whereas other pithecines eat caterpillars from families that are often either toxic (noctuids, Cacajao calvus calvus: Ayres 1986) or highly irritant (notodontids, Chiropotes satanus: Veiga and Ferrari 2006), the current study recorded seven instances in which caterpillars appeared to have been actively avoided. In five these, the caterpillars involved have strong physical or chemical defenses (Table III).
Like Cacajao melanocephalus ouakary, other Cacajao species have been recorded eating small insects such as termites, ants, and Orthoptera (Ayres 1986; Boubli 1997; Bowler 2007), as have other pitheciines (Cacajao and Chiropotes: Ayres and Nessimian 1982; Pithecia: Harrison-Levine 2003; Heymann and Bartecki 1990; Chiropotes and Pithecia: Kinzey and Norconk 1993). Chiropotes satanas also eats ants (Veiga and Ferrari 2006), with, as we also recorded, both alates and workers being eaten. Because alate ant emergences are difficult to predict, their exploitation is likely an example of opportunistic foraging.
Uacaris did not systematically search epiphytes for animal prey, unlike the region’s capuchins (Defler 1979; Gómez-Posada 2012; Janson and Boinski 1992; Rosenberger 1992). Instead, we observed traveling uacaris foraging only on invertebrates that they seemed to have encountered opportunistically. This may be a common pattern in pitheciines: Cacajao melanocephalus melanocephalus and Cacajao calvus ucayalii also do this (Boubli 1997; Bowler 2007, respectively), grabbing at passing Lepidoptera and Orthoptera and plucking spiders from the substrate while traveling (Boubli 1997; Bowler 2007), and Chiropotes satanas have also been recorded plucking insects from spiders’ webs (as we observed), plus searching dry dehisced Eschweilera pyxidia for edible arthropods (Veiga and Ferrari 2006).
The specific use of xylophageous coleopteran larvae as food items has not been recorded in previous reviews of uacari diets (Aquino and Encarnatión 1999; Ayres 1986; Boubli 1997; Bowler and Bodmer 2011). However, the extreme dental specializations in Cacajao for extracting seeds from hard-husked fruits (Kinzey 1992, Norconk 2011) are also suited for extracting this energy-rich (Dufour 1987) resource. Consumption of beetle larvae is widely reported for Neotropical primates, e.g., Chiropotes (Mittermeier et al. 1983; Veiga and Ferrari 2006), but not deep wood-tunneling forms.
Our results suggest that arthropods are probably seasonally important for this 3.5-kg primate and its dental specializations may be useful for exploiting resources above the first trophic level. In addition, because fruits are generally protein poor (Norconk 2011), whereas arthropods are rich in both fat and protein (Dufour 1987), the nutritional importance of insects may be much greater than the small percentages indicate. Thus, uacaris may adopt a mixed foraging strategy with respect to arthropods: Although foraging for them appears opportunistic at all times of year, uacaris may use arthropods primarily as a nutrient supplement in phases during which fruit dominates and as a potentially important source of energy when fruit availability is restricted.
The study was undertaken under CNPq-IBAMA Protected Area Study License 138/2006 issued to W. Souza Silva, and the study written while A. A. Barnett was a Visiting Scientist at the Instituto National de Pesquisas de Amazônia (under PCI-INPA initiative and CNPq Bolsa de Curta Duração [BEV] grant no. 680.004/2009-2). IBAMA-Manaus issued monthly park research permits to A. A. Barnett. Funding was generously provided by American Society of Primatologists, Columbus Zoo Conservation Fund, Sophie Danforth Conservation Fund, LSB Leakey Foundation (U.S.), Leakey Fund (U.K.), Laurie Shapley, Margot Marsh Foundation, Oregon Zoo Conservation Fund, Percy Sladen Memorial Fund, Pittsburgh Zoo and Aquarium Conservation Fund, Primate Action Fund, Primate Conservation Inc., Roehampton University, and Wildlife Conservation Society. Technical assistance and advice were provided by Fundação Vitória Amazônica, Manaus. A. A. Barnett and T. Almeida thank Eliana dos Santos Andrade, Eduardo do Souza, Maria de Bom Jesus, Roberto Morreira, and the IBAMA staff at Jaú. The following kindly identified specimens: Ambylopygids: Linda Raynor (Cornell University), Ephemeroptera: Eduardo Domínguez and Carlos Molineri (Universidad Nacional de Tucumán, Argentina), Lepidoptera: Dick Vane-Wright (University of Kent Canterbury), and Orthoptera: George Beccaloni and Judith Marshall (The Natural History Museum, London). This is Contribution 19 from the Igapó Study Project. We thank Joanna Setchell and Jessica Rothman and two anonymous reviewers, all of whose comments greatly improved the manuscript.