Report on a short study of the wet season feeding ecology and habitat preferences of the golden-backed uacari or bicó, Cacajao melanocephalus ouakary, in Jaú National Park, Brazil. No. 1 of the Igapó Study Project Report Series

Prepared for: Fundação Vitória Amazônica (Manaus), IBAMA (Manaus), Mammal Society (London), Margot Marsh Biodiversity Foundation (Washington, DC), Percy Sladen Memorial Fund (London) and University of Surrey Roehampton (London). Bryn Mawr, PA, U.S.A. October 1999.

Adrian A. Barnett Dept. of Life Sciences University of Surrey Roehampton West Hill, London SW15 3SN, England [email protected] [email protected]

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Other Reports in the Series: No. 1

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No. 3

Report on a Short Study of the Wet Season Feeding Ecology and Habitat Preferences of the Golden-Backed Uacari or Bicó, Cacajao melanocephalus ouakary, on the Lower Rio Jaú, Amazonas, Brazil. Report on a Short Study of the Dry Season Feeding Ecology and Habitat Preferences of the Golden-Backed Uacari or Bicó, Cacajao melanocephalus ouakary (Cebidae:Pitheciinae), on the Lower Rio Jaú, Amazonas, Brazil. Preliminary Results of a Technical Visit to Survey the Bat Species Present in Jaú National Park, Amazonas, Brazil.

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Akodon Ecological Consulting 951 Bancroft Road, #111A Concord, CA 94518 USA 925/280-7685

Map of study location .................................................

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Abstract ....................................................................... Introduction ................................................................

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Methods .......................................................................

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Results ..........................................................................

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primates other mammals

Discussion ....................................................................

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uacaris other primatespecies

Conclusions .................................................................

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Acknowledgements .....................................................

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References ................................................................... Appendices ..................................................................

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Table 1. Latin and local names (phonetic) for fruits reported to be eaten by Cacajao melanocephalus ouakary. Table 2: GPS points for some of the encounters mentioned in the text.

II. Revision of identifications of insects mentioned in the text. (Added September 2000, following arrival of identifications from the Smithsonian Institution).

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Report on a short study of the wet season feeding ecology and habitat preferences of the golden-backed uacari or bicó, Cacajao melanocephalus ouakary, in Jaú National Park, Brazil.

Adrian A. Barnett No. 1 of the Igapó Study Project Report Series

Abstract In an eight-day field excursion, during the wet season of 1999, golden-backed uacaris Cacajao melanocephalus ouakary were encountered five times at three locations in Jaú National Park, Amazonas. Observed group size varied from two to 16. Uacaris were observed eating two fruit species, and two more were found bearing characteristic uacari teeth marks. Local guides identified a further 21 species as being eaten by uacaris. Evidence of active and passive insectivory by uacaris was recorded. Six other primate species were observed during the visit.

A. Barnett: Uacaris in Jaú, wet season 1999

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Introduction The primates of Jaú are little known. Previous work consists of a short inventory by Anthony Rylands (Rylands 1992) and a more recent questionnaire-based survey (Neri & Borges 1998). This has not adequately covered the park and further primate work is considered to be a management plan priority (FVA/IBAMA 1998).

Methods As part of Fundação Vitória Amazônica's (FVA) "Windows of Biodiversity" programme for the Park, I accompanied an FVA excursion to the lower Jaú river, in the area of the village of Seringalzinho. Fieldwork lasted from 19 August -26 August 1999. The surveys aims were to: * assess the density of populations of the golden-backed uacari, Cacajao melanocephalus ouakary * gain information on the habitat use, diet and group size of C. m. ouakary. * considering the logistics of the site and the uacaris' reactions to observers, to assess the feasibility of the area for long-term studies of C. m. ouakary ecology. * record the types and densities of other species of primates in the area. Fieldwork focused on meeting uacari-based objectives. In reviewing uacari ecology Barnett & BrandonJones (1997) believed this monkey to spend much of its time in blackwater flooded forest (or igapó – Prance 1979). Accordingly, this flooded forest type formed the focus of the fieldwork. As this was a preliminary survey, and time was limited, no standard transects were cut through the igapó. Instead short visits were made to several large areas of igapó identified from aerial photographs in FVA's possession. With Sr. Antenor Anicácio, the Captain of Seringalzinho, acting as guide and boatman, these were surveyed by paddled canoe. Within the igapó areas procession was guided by the direction major waterways (igarapés), which were followed until auditory or visual contact was made with a primate group. Primates were searched for from shortly after dawn to near mid-day for 7 days. Additional afternoon searches were conducted on 3 days. For two mornings (19 and 26 August) a terrestrial 5 km transect was walked. The track cuts through both terra firme (never-flooded high-canopied rainforest) and campinaranha (species-poor white sand vegetation with trees) vegetation types. While paddling, opportunities were taken to qualitatively record the characteristics of the vegetation types and to collect from Antenor information on the fruits known by him to be eaten by C. m. ouakary. Evidence of recent feeding bouts (chewed and broken fruits, both floating and on the tree), were also recorded as encountered. Faeces could not be collected due to the nature of the habitat. In addition, I questioned Antenor about the annual movements and habitat use of the uacaris and other primates in the region. When a group of primates was encountered number, sex, age, inter-individual distance, group spread, height above the water and type (local name) of tree were recorded, along with subsequent behaviour. Contacts were too transient to usefully apply the classic quantitative behavioural sampling methods of Altman (1974); effectively we took what we could get from whichever animals were visible. Observations were made with a 7x35 binoculars. GIS locations of encounter points and of feeding sites were recorded using a Garmin GPS. This was also used for recording other significant wildlife encounters.

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Samples of eaten fruits and other items, and of trees in which animals were seen were collected, made into herbarium exicates and, through the kindness of Carolina V. de Castilho deposited at the INPA Herbarium, Manaus. In addition, all botanical specimens were photographed.

Results primates: In a total of 25 hrs. 30 mins of search time, uacaris were encountered 5 times at 3 locations. Group size varied from 2 to 16, though one contact was thought to be the rump of a much larger (30+ group) seen in the region before our visit. Contacts with the uacaris were always brief, with the animals appearing to flee immediately on hearing or seeing humans and no observations on social or feeding behaviour were obtained. No warning vocalizations, threat displays (throwing of fruit or faeces), or piloerection were observed. In four cases side-to-side tail wagging was observed as animals moved off. This behaviour is considered a low-intensity threat display in uacaris (see Barnett & Brandon-Jones 1997). No juveniles or young were observed. Local people reported May as the time to see uacaris with babies. Maximum group size was reported to be around 30 at this time of year, with a group occupying an area estimated to be around 200m across. The groups were reported not to have exclusive home ranges, moving in the same area without rancor. The uacaris were observed eating two different types of fruits (Leopoldinina pulchra: Acecaceae; Sloania obtusa: Eleocarpaceae) and in another two species broken fruits with characteristic marks of uacari teeth were found (Pouteria: sp.: Sapotaceae; Eschweilera tenuifolia: Lecythidaceae). A further 21 species were identified as forming part of their diet (Table One). In the igapó bordering Lago Catipirí, a recently-broken nest of Polistes wasps (Hymenoptera) was found in large chunks, floating on the waters. This damage was attributed by Antenor to uacaris, which are said to eat the larvae. On the upper Rio Negro uacaris are known to visit sandbanks and eat the eggs of Podocnemis terrapins. I was informed that this is not the case at Jaú, although Cebus albifrons has been seen to do this in the dry season when nesting occurs. Eschweilera is said to be a major food item of the uacari. In addition some of the collected food fruits had insects in them. Because this may represent an important, but so-far little-considered, food source for uacaris, some care was taken with these collateral specimens. Notable were the fruits of Parkia discolor (Leg.: Mim.) which were found to contain numerous seed beetles (Bruchidae) some 3-4 mm long and a smaller number of tiny weevils (Curculionidae?) some 2 mm long. The single-seeded fruits of Sloanea (Eliocarpaceae) had each been hollowed out by a lepidopteran larvae (probably of a torticid moth). The infestation appeared intense, effecting nine of the eleven fruits examined. One fruit of an Inga (Leg.: Mim.) contained a lepidopteran larvae. The caterpillars were preserved in alcohol, and the beetles frozen. All have been sent to the Smithsonian Institution, Washington DC, for identification (see Appendix II). The igapó habitat in the region appears divided into four distinct types: i) a on open form, dominated by Eschweilera with occasional Hevea (Euphorbiaceae), which appears as scrubby islands of vegetation above the water level, ii) a dense closed forest type with thin-trunked trees probably some 6-8m tall, which include the sapotaceous tree eaten by the uacaris, iii) a more open taller forest type (canopy to 8-12m) with larger more widely-spaced trees. These three occur, in reverse order, from the terra firme to the open water of the river. The fourth vegetation type occurs along the boundaries of the igarapes, and is characterized by palms (incl. Leopoldinia pulchra) and Sloanea (Eleocarpaceae) trees. According to local informants (A. Anicácio and others) by August there are few uacaris left in the igapó, because it now contains few fruits that they like; most have already migrated to the nearby terra firme forests. Here they stay, within a few hundred meters of the waters' edge until the October rains bring a new flush of fruits to the igapó trees. Then they return, even though there is little water in the igapó at that time. Over the annual cycle of inundation they move from igapó type (i) through (ii) to (iii) before entering the terra firme again.

A. Barnett: Uacaris in Jaú, wet season 1999

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In addition to the uacaris, the following primates were seen: Aotus sp., night monkey - seen by a FVA team member one evening while out fishing in igapó near the park headquarters at the mouth of the Rio Jaú. This species has not been recorded before for the park. According to data in Emmons & Feer (1997) the species in the region should be A. vociferans. Callicebus torquatus, yellow-handed titi - seen by myself and Sérgio Borges on the trail back from the campinha bird study site on the morning of 26 August. A single individual was seen in a Mauritia palm in campinharana in proximity to a large squirrel. Though a clear view was not obtained of the diagnostically coloured hands, it is considered to be this species based on colour, shape and behaviour. Its presence is a new record for the park and confirms the reports to Neri & Borges (1998) that this species existed within the park boundaries. The record is a slight westward range extension, within the Negro-Solimões interfluvial basin (see Emmons & Feer 1997). Saimiri sciureus, squirrel monkey - a large group was seen in the trees among the ruins of Velho Airaõ. Cebus apella, brown capuchin monkey - a group of four was seen in the igapó near Seringalzinho. In addition, a juvenile was seen being kept as a pet on a riverboat moored near Lago Miratucú. Cebus albifrons, white-fronted capuchin - observed by Carlos in the Campinharana. Alouatta seniculus, howler monkey - Two adults (1m, 1f) were seen on 24 August in igapó at Lake Miratucú. The animals moved off quickly after the sighting and no behavioural or feeding observations were possible. other mammals: A pair of giant otter (Pteroneura brasiliensis) were seen 20 August in the water in the vegetation at the side of an igarapé at a distance of around 10m. A clear view of the chest pattern was obtained. A second animal was lurking further in, under cover. Later that day, a second sighting, probably of the same animals, was made by a fisherman in the same area of igapó.

Discussion uacaris:

The reported importance of Eschweilera fruits in the diet of C. m. ouakary agrees with studies elsewhere on other members of the genus (Aquino 1995 on C. c. ucayalii; Ayres 1989 on C. c. calvus). Aquino also noted Pouteria (Sapotaceae) as an important food plant, a genus also recorded as a food plant in Jaú. However, neither species was reported as important in the diet of C. m. ouakary on the upper Rio Negro, despite the abundance of E. tenuifolia in the igapós of the region (Barnett & da Cunha 1991, da Cunha & Barnett 1990). The number of reported food plants is less than has been reported for other taxa (Ayres 1986, 100 for C. c. calvus; Aquino 1995, 50 for C. c. ucayalii), but future work may well add to the list. Ayres (1989) considered that C. c. calvus adopted a mixed-feeding strategy to maximize nutrient intake, and minimize toxification and handling times. Little attention was paid to protein intake. The current work has raised the interesting possibility that diet selection may involve the use of infested fruits as a source of dietary protein. This has also been shown to be important for Old World fruitbats (Courts 1998), and in the European brown bear Ursos arctos (O'Hanlon & Widstrand 1999). As in U. arctos this may be especially important in weaning individuals, an age stage where protein requirements are particularly high (O'Hanlon & Widstrand 1999). Insect action on fruit walls might also weaken, allowing the inclusion in the diet of younger, smaller individuals, of fruits which, allometrically, they would not otherwise have the jaw power to break open. These notions must remain conjectural until further studies are undertaken. However, it should be noted that Ayres (1986) recorded seasonal use of leaf-eating caterpillars by C. c. calvus which Barnett & Brandon-Jones (1997) have interpreted as a store of protein.

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It is unclear why the uacaris at Jaú are so shy. Previous studies on the upper Rio Negro found them phlegmatic in their approach to human presence, with observers being treated to short bouts of low-level threat displays before feeding was resumed (Barnett & da Cunha 1991, da Cunha & Barnett 1990). This was an area where uacaris were subject to low-level hunting. On the other hand, the uacaris at Jaú are considered too small to be hunted (though they have been hunted 20-30 years ago). It is to be hoped that it will prove possible to habituate one or more groups to permit more detailed ecological studies. Of the 25 uacari food fruits collected or recorded, only eight were noticeably hard-shelled. This runs against the commonly-held notion that Cacajao is a specialist on hard-shelled fruits (Barnett & BrandonJones 1997). However, these data do not take into account the relative frequency with which the fruits are eaten. This awaits further quantitative studies. The lack of territoriality between 'groups' (reported above) may reflect the fission-fusion sociality postulated for uacaris by Barnett & Brandon-Jones (1997). other primate species:

It is unusual for Alouatta to use igapó and it would be interesting to know if this is a common occurrence within the park or a serendipitous encounter with an infrequent event. Jau's known primate diversity (8 species) is in line with the biogeographic patterns of primate distribution and species diversity reported by Emmons and Voss (1996). There are, however, a number of species which, with varying degrees of certainty, could occur within the Park and for which more detailed searches need to be conducted. These include: the small dark monkey (also that its been reported to us on Rio Curicuriari), for bare-faced tamarin Saguinus bicolor, the red uacari (Cacajao calvus rubicundus) and the woolly monkey (Lagothrix lagotricha).

Conclusion Primates in the surveyed area appear to be common, and the area has the moderate species diversity expected of the region. In a very short period we saw seven of the nine species reported in interviews to Neri & Borges (1998). The ease and frequency with which species were encountered indicates that the Park would form a good base for future primatological research. In particular: * more primate work needs to be done - to assess species densities and to gain information on synecology and autecology. * remote areas need to be surveyed, especially to check the possibility of populations of Saguinus inustus and for reports of the small black monkey. * white-water areas should be surveyed for Cacajao calvus rubicundus. * field work on the uacari seems to be feasible - a medium-term study should be conducted to investigate the feasibility of longer-term work. Such work should include quantitative botanical studies and detailed studies of the phenology of the igapó flora.

A. Barnett: Uacaris in Jaú, wet season 1999

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Acknowledgements I would like to acknowledge the kindness, good guidance and knowledge of Sr. Antenor Anicácio, who acted as my guide and chief informant during the fieldwork. Carolina V. de Castilho kindly took charge of the plants and arranged for them to be identified at the INPA Herbarium, whose staff I also thank. Funding was provided by the Roehampton Institute London (now University of Surrey Roehampton), by Fundação Vitória Amazônica and by grants from the Mammal Society (London), Margot Marsh Biodiversity Foundation (Washington DC) and the Percy Sladen Memorial Trust (London). I would like to thank Sérgio Borges for the invitation to accompany the FVA team into the field and to all the FVA team for kindness, consideration and tolerance of my version of Portuguese.

References Altmann J. 1974. Observational study of behaviour: sampling methods. Behaviour 49: 227-267. Aquino R. 1995. Concervacion de Cacajao calvus ucayalii en la Amazonía Peruana. Neotropical Primates 1995 (3): 40-42. Ayres M.J. 1986. The White Uakaris and the Amazonian Flooded Forests. PhD Thesis, Cambridge University. Ayres M.J. 1989. Comparative feeding ecology of the uakari and bearded saki, Cacajao and Chiropotes. Journal of Human Evolution 18: 697-716. Barnett A.A. & da Cunha A.C. 1991. The golden-backed uacari on the upper Rio Negro, Brazil. Oryx 25: 80-88. Barnett A.A. & Brandon-Jones D. 1997. The ecology, biogeography and conservation of the uakaris, Cacajao (Pitheciinae). Folia Primatologia 68: 223-235. Courts S.E. 1998. Dietary strategies of Old World fruit bats (Megachiroptera, Pteropodidae): how do they obtain sufficient protein? Mammal Review 28: 185-193. da Cunha A.C. & Barnett A.A. 1990. Sightings of the golden-backed uacari, Cacajao melanocephalus ouakary, on the upper Rio Negro, Amazonas, Brazil. Primate Conservation 11: 8-11. Emmons L.H. & Feer F. 1997. Neotropical Rainforest Mammals: a field guide. Chicago: Chicago University Press. 2nd edition. FVA/IBAMA, 1998. Parque Nacional do Jaú: Plano de Manejo - versão 8. Manaus: FVA and IBAMA. Neri F. & Borges S., 1998. Relatório de primatologia no rio Unini, Parque Nacional.do Jaú. Unpublished report to Fundação Vitóra Amazônica, Manaus. O'Hanlon E. & Widstrand S. 1999. Babes in the wood. BBC Wildlife 17 (9): 50-55. Rylands, A.B. 1992. Relatório de viagem ao Parque Nacional do Jaú. Unpublished report to Fundação Vitória Amazônica, Manaus. Voss R.S. & Emmons L.H. 1996. Mammalian diversity in Neotropical lowland rainforests: a preliminary assessment. Bulletin of the American Museum of Natural History No. 230: 1-115.

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Appendix I Table 1. Latin and local names (phonetic) for fruits reported to be eaten by Cacajao melanocephalus ouakary.

Coll. No. 01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 16 17 18 19 20 21

Latin Name Parkia discolor(Fab.: Mim.) Duroia cf. eriophila (Rubiaceae) Maprounea brasiliensis (Euphorbiaceae) Mabea cf. nitida (Euphorbiaceae) Leopoldinia pulchra (Arecaceae) Pouteria paraensis (Sapotaceae) Pouteria elegans (Sapotaceae) Sclerolobium sp.(Fab.:Caes.) Tococa coronata (Melastomataceae) Acosmium nitens (Fab.:Pap.) Byrsonima cf. punctulata (Malphigiaceae) Cybianthus spicatus (Myrsinaceae) ? Macrolobium acaciifolium (Fab.: Caes.) Hydrochorea marginata var. marginata (Fab.) Buchenavia oxycarpa (Combretaceae) Myrcia sp. ? (Myrtaceae) Sloanea obtusa (Elaeocarpaceae) Macrolobium multijugum (Fab.: Caes.) Duroia macrophylla (Rubiaceae) Marlierea umbraticola (Myrtaceae)

Local Name Para-tucupí Par-ru-í Abuilzinho Taquar-rí Ja-ra Wishí Abilzinho Tashí Abushasoo Tauberana Morta Olho de piexe Muri-çí Araparí Inga de macaco Teni-bucca Ara-sa ? ? ? Pour-to-í

Eschweilera tenuifolia (Lecthyidaceae) was reported, and indirectly observed, to be eaten, but was not collected. The fruit of an epiphytic aroid ('ann-be', Philodendron sp. ? - fruiting but inaccessible), a spiny palm ('jow-a-ree', ? = Astrocaryium jauari) and of a tree ('acachí' neither flowering nor in fruit at the time) were reported as bicó food items, but were also not collected.

Table 2: GPS points for some of the encounters mentioned in the text.

Cacajao melanocephalus M 0681818, UTM 9787121 M 0642197, UTM 9789185 M 0652984, UTM 9791814 Pteronura. brasiliensis M 0652985, UTM 9791826

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Appendix II Revision of identifications of insects mentioned in the text. (Added September 2000, following arrival of identifications from the Smithsonian Institution). For the Bruchidae (seed beetles) from Parkia discolor seeds; there are three species represented, in what appear to be two genera. The lepidoptera larva associated with fruits of plant #18, considered on the label as possibly in the family Tortricidae, is in reality a specimen of the family Pyralidae. I am grateful to Dr. Gary Hevel of the Smithsonian’s Dept. of Entomology for arranging for the determinations by John Kingsolver (U.S.D.A.'s Systematic Entomology Lab, retired: Bruchids) and John W. Brown of the U.S.Dept. of Agriculture's Systematic Entomology Lab at the Smithsonian (lepidoptera).

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