Effects of hunting on western Amazonian primate communities

Biological Conservation 54 (1990) 47-59

Effects of Hunting on Western Amazonian Primate Communities Carlos A. Peres Nflcleo de Primatologia, Museu Goeldi, Caixa Postal 399, Bel6m, Parfi, Brazil (Received 28 December 1987; revised version received 7 January 1990, accepted 16 January 1990)

A BSTRA CT Transect surveys were carried out in seven western Amazonian upland.forest sites and compared with four additional sites to examine effects of hunting by humans on the structure of species-rich primate communities. Primate body mass was a strong positive correlate of its crude and metabolic population biomass in non-hunted but not in hunted sites. Primate body mass was a good negative correlate of population density in hunted but not in non-hunted sites. Group density was not clearly affected by hunting activity. Large primates had significantly lower group densities than small primates in both hunted and non-hunted sites, These trends are largely a consequence of differences in abundance of large-bodied genera (i.e. Alouatta, Ateles and Lagothrix), accounting for the bulk of the primate biomass in non-hunted sites, but being over-harvested or becoming extinct #l sites hunted by man.

INTRODUCTION Predation can affect the patterns of species abundance in prey communities (MacArthur, 1972), some of which may compete with one another for a common resource. Cases in which natural predation limits the distribution or abundance of a given species have rarely been documented. Human predation (hunting) even at a subsistence level can severely depress the numbers of a target species to the point of driving it locally extinct. This is Present address: Sub-Department of Veterinary Anatomy, Cambridge University, Tennis Court Road, Cambridge CB2 1QS, UK. 47 Biol. Conserv. 0006-3207/90/$03"50 © 1990 Elsevier Science Publishers Ltd, England. Printed in Great Britain

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potentially the case in tropical forests where sustainable hunting is not practised because adequate regulations and their enforcement are often lacking. When the object of hunting is to obtain animal protein, as with subsistence hunters, choice of prey should then depend on (1) the relative profitability of prey, and (2) the costs of obtaining it. Thus, large-bodied prey should always be more profitable than small prey for a given quality of meat. Primates comprise an important source of protein for both indigenous groups and colonists in the Brazilian Amazon (Redford & Robinson, 1987) and elsewhere in the tropics (Mittermeier, 1987). The effects of the primate harvest on the remaining numbers of animals may be examined by comparing sites affected by different degrees of hunting. In this paper, I compare the structure of primate communities in 6 hunted and 5 nonhunted sites, and present evidence of how hunting may affect them. In addition, I discuss the significance of body mass in the relationship between intensity and selectivity of hunting and the resulting primate densities and biomass. METHODS

Survey sites Surveys were conducted during the wet seasons of 1987 and 1988 in seven forest sites of western Brazilian Amazonia (Fig. 1). Three of those sites (Igarapr-A~fi, RUC, and SUC) were entirely undisturbed, and access to them was only possible by helicopter. These sites were located on upland forest on the lower Rio Urucu (4 ° 30'S and 64 ° 29' W), upper Rio Urucu (4°50'S and 65°16'W) and upper Rio Tef~ (4°50'S and 65°26'W), respectively. Prior to this study transects had been cut through primary forest of 25-40 m in height on undulating terrain during seismic operations, to map oil deposits in these sites. Small, clear-water forest streams were common, and levels of structural habitat heterogeneity were low. Local human residents were conspicuously absent in these survey areas, and in extremely low densities in the entire Rio Urucu basin (less than 0-02 inhabitants kin-z). Consequently, the abundance of prime hunting targets, such as large terrestrial mammals (e.g. brocket deer Mazama sp., peccaries Tayassu sp. and tapirs Tapirus terrestris), was relatively high and unaffected by hunters. Primates at these sites had never been hunted. Four other sites surveyed--Lago da Fortuna, S~o Domingos, Jaraqui, and Riozinho--were undisturbed by logging but had been frequently used by hunters for at least 15 years prior to my surveys, or during most of the rubber trade. Hunting effort at these sites was seasonal in intensity because fishing was preferred during the dry season.

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® Fig. 1. Location of western Amazonian sites surveyed. Unhunted sites: (1) RUC; (2) Igarap~-Ac/l; (3) SUC; (4) Aqaituba (Johns, 1986); and (5) Cosha-Cashu (Terborgh, 1983). Hunted sites: (6) Lago da Fortuna; (71Jaraqui; (8) Riozinho; (9) S~o Domingos; (10) Tahuayo (Bodmer el aL, in press); and (11) Ponta da Castanha (Johns, 1986). Circled numbers correspond to sites in Peru.

Lago da Fortuna (5 ° 5' S and 67 ° 10' W) was located on the fringes of an oxbow lake isolated from the main stream of the Juru~i river, the second largest white-water tributary of the Amazon. I surveyed a transect which cut through upland forest and a small portion of dry lower restinga, a type of flooded forest under water for three months annually. A number of families of rubber tappers lived in the upland forest adjacent to the lake. Aquatic sources of protein, including primarily several species of characid fish and aquatic turtles Podocnemis unifilb, were most important when concentrated during months of low water level. During the wet season, however, terrestrial mammals (e.g. pacas Agouti paca, brocket deer, peccaries), large primates (e.g. howler Alouatta seniculus and spider Ateles paniscus monkeys), and large birds (e.g. trumpeters Psophia leucoptera, curassows Crax mitu) supplied most wild meat consumed. Jaraqui (4° 21' S and 66 ° 31' W) and Riozinho (4° 28' S and 67 ° 6' W) are both upland sites near black-water tributaries of the Juruh and Jutai rivers, respectively. Jaraqui and Riozinho are in many ways similar to Lago da Fortuna. These sites had been hunted at least since the expansion of the

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Carlos A. Peres

rubber trade to the Jurufi river, their current human density is less than 0-1 inhabitant km-2, and they have similar faunas. Villagers from Carauari, a town on the west bank of the Jurufi, hunted sporadically in these sites, taking ungulates (i.e. tapirs, peccaries and brocket-deer) mostly for commercial purposes and smaller game including primates during hunting trips. These sites had been recently abandoned by rubber tappers practising local subsistence hunting because the rubber price had crashed. The fourth hunted site, Silo Domingos, is located near Sena Madureira, on the border of Acre and Amazonas (8 ° 55' S and 68 ° 20' W) and along the unpaved extension of the Transamazon highway (BR-364). Prior to the surveys, several families had been resettled along the road as part of a largescale programme of land colonization. Densities of humans in this area were thus far greater than that allowed by the local carrying capacity of an upland Amazonian forest (Gross, 1975; Fearnside, 1986). Mammalian game species consisted primarily of caviomorph rodents, collared peccaries and primates (e.g. howler monkeys). I compiled data from four additional Amazonian sites which had been subject to consistent hunting pressure (Ponta da Castanha, Tef6, Brazil: Johns, 1986; Tahuayo, Iquitos, Peru: Bodmer et al., in press) or never hunted (Cosha Cashu, Manu National Park, Peru: Terborgh, 1983; A~aituba, Tef6, Brazil: Johns, 1986). All primate-rich, non-hunted sites in western Amazonia from which primate density estimates are available are covered by this study. I restrict this analysis to communities rich in primate species because they provide hunters with the largest number of potential targets. A minimum of 10 species of primates occur, or recently occurred, in Silo Domingos, the least rich community. The maximum of 14 species in Lago da Fortuna and Riozinho is richer than that reported for forest primate communities anywhere in the world (Peres, in press).

Population surveys Estimates of primate density and biomass were obtained by walking a measured transect several times and noting all encounters with primate groups or individuals. Upon sighting, group size and composition were determined during a standardized period of 10-15 min or until the group was no longer visible. Only accurate counts were considered. Distance between the first animal sighted and the observer, perpendicular distance to the transect and distance along the transect from starting point were noted. One transect of 4-5-6 km was walked at each site between 0630 and 1130 h during 10 consecutive mornings without rain. At the upper Urucu drilling site this procedure was replicated two additional times. Sightings on returns were not considered because animals were less active, or less detectable, after

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1130 h. I censused all transects individually at speeds of 1-1"5 km h - 1, with stops every 100m for about 20s. In three of the seven surveyed sites, I walked abandoned seismic transects through a single general habitat type: undisturbed, continuous primary forest on smoothly dissected terrain. Surveys were thus unbiased towards habitat specialists, and selection of transects was not a critical consideration. Seismic transects had all been previously marked at every 50 m with small wooden blocks, and marks were visible for at least one year after transects were abandoned. In other survey sites new transects were established and marked every 50 m with coloured surveyor's tape. This provided reference points for sighting events, and aided mapping and exclusion of individual groups detected more than once. Rubber-tapping trails were used at Lago Fortuna. This was possible because these trails had been abandoned by tappers prior to surveys, and human disturbance on natural rubber stands was restricted to hunting during the tapping season.

Data analysis An expanded Fourier series programme (Burnham et al., 1980) was used to process each species' sightings per site when sample sizes were sufficiently large. In the case of rare species (those sighted less than 10 times in any given site), I used Emlen's (1971) 'most effective sighting distance' to estimate survey strip width. This method is most appropriate for relatively small data sets and produces density estimates which are comparable to those of other primate surveys recently conducted in Brazilian Amazonia (e.g. Ayres, 1986; Johns, 1986; Peres, 1989). Crude biomass was calculated for each species using B W , D (kg km-21, where B W and D are, respectively, the average adult body weight and population density of a species. Weights were obtained from carcasses provided by hunters (Peres, unpublished data), or from other studies (Ayres, 1986; Johns, 1986; J. M. Ayres, pers. comm.) (Table 1). Metabolic biomass is a relevant measure in size-graded communities because it takes into account that energy allocation increases allometrically with body weight to the power 0.75 (Peters, 1983). Metabolic biomass was then calculated as B W °'75 * D (kg °'75 k m - 2). RESULTS

Hunting selectivity Large-bodied, prehensile-tailed primate genera, such as woolly monkeys L a g o t h r i x lagotricha, spider monkeys and howlers, were prime targets in

hunted sites. Woollies and spider monkeys were extremely rare, if not locally

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extinct, probably because of hunting at Lago da Fortuna, Jaraqui, and Riozinho. Spider monkeys met the same fate at S~o Domingos. Interviews with rubber tappers indicated that several small-bodied primates (less than 3 kg) were ignored by hunters irrespective of their local abundance. Using expensive ammunition on these targets was simply uneconomic. At Lago da Fortuna, for instance, shotgun shells are purchased at US$1.5 each, a price much higher than that paid for 1 kg of the most commercial species of fish, pirarucu Arapaima gigas. On the other hand, hunters during the day often used trails as far as 9 km away from their huts to shoot primates weighing 5 kg or more. Given the opportunity, these species were shot even when hunters hoped for largerbodied ungulates, The additional carcass load and excess meat was often not a problem because (1) up to 45 kg of game, which excluded tapirs only, could be carried by a single man; (2) solitary hunters could always fetch help from others in uncohesive hunting parties before the carcass deteriorated; (3) permanent creeks, particularly during the wet season (when hunting becomes the most important source of meat) permitted canoe access to most of their hunting range; and (4) the boundary between subsistence and commercial hunting in many rubber-tapping communities was very narrow: whatever meat could not be consumed by the community was salted and sold in a village. The potential impact of even a few hunters was therefore very clear. For example, one isolated, extended family of rubber tappers, consisting of 3 hunters, women and children, who had exclusive use of the Riozinho site between early 1985 and late 1986, was responsible for killing over 200 woolly monkeys, over 100 spider monkeys and over 80 howlers. A few sakis Pithecia irrorata and brown capuchins Cebus apella were the only other monkeys hunted. At this site, woollies were locally extinct, spider monkeys nearly extinct and howlers drastically reduced. Few feeding taboos were recorded for primates. In Lago da Fortuna and Riozinho, white uacaris Cacajao calvus novaesi (mean weight = 3.2 kg: Ayres, 1986) were never shot because of their 'human-like' physical appearance. The large, 'demoniac' black spider monkey Ateles paniscus chamek in the same site was known to aggravate infectious diseases and cause digestive disruptions if consumed by pregnant women, but only 'at certain times of the year'. Such taboos may reflect the locally high protein availability from aquatic fauna. For instance, no taboos were respected in S~o Domingos, where animal protein was considerably scarcer.

The primate communities Using population densities, I calculated the total density, crude biomass and metabolic biomass of 18 diurnal primate species in 11 genera censused at

Amazonian primates and hunting

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each site (Table 1). The only nocturnal monkey Aotus sp., was excluded from this analysis because night surveys were conducted in only 3 sites. Hunted sites (n = 6) had a mean total density of 168 diurnal monkeys km -2 (SD = 65), comprising a mean crude biomass of 233 kg k m - 2 (SD = 122) and a mean metabolic biomass of 198kg °Ts km -2 (SD = 97). U n h u n t e d sites (n = 5) had a mean density of 132 monkeys km -2 (SD = 76), comprising 4 1 3 k g k m -2 ( S D = 1 5 4 ) and 2 8 7 k g ° ~ S k m -z ( S D - 1 2 0 ) . The average diurnal monkey in non-hunted sites thus weighed 3-131 kg, over twice as heavy as that of hunted sites (1-387 kg). Hunted sites did not differ from unhunted sites in their total primate densities (Kruskal-Wallis one-way A N O V A , H = 0"83, 10 d.f., p = 0"36) and total metabolic biomass (H = 1.2, 10 d.f., p = 0.27). Total crude biomass, however, was significantly greater in unhunted sites (H = 4-0, 10 d.f., p = 0.045), and when differences in expected site productivity were considered as indicated by overall densities, both crude and metabolic biomasses were greater in unhunted sites (~2= 7.5, HUNTED SITES

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10 d.f., p = 0"006). I also examined differences in the contribution of largebodied, most-hunted species (i.e. Alouatta, Ateles, and Lagothrix) to the crude biomass of their communities (Table 1): monkeys greater than 4 kg contributed 16-2% to the biomass of hunted communities (n = 6, SD = 12"6) and 64-1%0 (n = 5, SD = 11.1) to unhunted communities (t-test, t = 6-7, 9 d.f., p < 0.001). Meanwhile, the variance in the biomass of small-bodied primates was not affected by hunting (ANOVA, F 1,9 = 0-34, p = 0.57), presumably because they are unattractive to hunters. All sites considered, primate body mass explained only 16.8% of the variation in population biomass ( r = 0"41, F1,11z = 22"7, p < 0-001). This correlation, however, was highly positive for unhunted sites (r=0"76, F1,47 = 65"4, p <<0"001), but not for hunted sites (r = - 0 " 0 3 , n.s.) (Fig. 2). Body mass at all sites explained only 7-7% of the variation in population density (r = 0"28, F~.~ 12 = 9"3, p = 0"0028). This correlation was not significant in unhunted sites (r = 0"19), but significantly negative in hunted sites (r =--0"55, F1,63 = 28.1, p <<0"001). The same results were repeated when logarithmic transformations of each species' body mass, density and population biomass were computed. Logged body mass was a good direct predictor of logged biomass in unhunted sites (r=0"75, F 1 , 4 7 = 62"4, p << 0"001), and a good inverse predictor of density in hunted sites (r = - 0"53, F l , 6 3 = 21"8, p << 0"001).

DISCUSSION H u m a n predation on Amazonian primates was initially documented by early naturalists. According to Bates (1863), one small tribal group accounted for some 200 woolly monkeys each year. Large Neotropical primates are extremely rare and shy of humans wherever they have been hunted in the past (Hernandez-Camacho & Cooper, 1976; Robinson & Ramirez, 1982; this study). Other studies of hunting in Amazonia (Smith, 1976; Johns, 1986; Peres, 1987; Redford & Robinson, 1987; Ayres e l aL, in press) also indicate that large mammals (e.g. ungulates, Atelinae primates) and large birds (e.g. cracids) are the main targets. These species share a large proportion of fruits available in the canopy (Terborgh, 1983) or on the forest floor (Smythe, 1986) and are generally abundant if not subjected to hunting. Arboreal vertebrates offer hunters a much narrower range of body mass than ground-living species, because arboreality imposes higher physical and metabolic constraints on the upper threshold of body size (Peters, 1983). There are few species of Neotropical arboreal vertebrates heavier than 5 kg. These species make preferred targets and hunting pressure is potentially very high. The choice for hunters of large ground-living species is relatively

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57

greater, and harvests tend to be more evenly distributed. Primates such as the large Atelinae (e.g. Ateles, Lagothrix) and Alouatta are then more likely to absorb much of the hunting pressure targeted at all vertebrates harvesting fruits before they fall from the canopy. Taxonomic differences in reproductive rates, abundance, and population dispersion drastically affect a game species' ability to co-exist with, and recover from, hunting pressure. Large primates have low reproductive rates, single infants are separated by relatively long inter-birth periods, and not all mature females are reproductively active at any one time because of complex patterns of group structure. Such characteristics make continued harvest of primates unsustainable compared to ungulates, which tend to maintain a comparable biomass in both unhunted and moderately hunted forests (Bodmer et al., in press). Hunting may also affect the sex ratio of primates, influencing their potential rate of population growth. Breeding females are preferred targets in many species because the infants they carry may be captured alive and sold as pets (e.g. Lagothrix). Differences between primate communities in hunted and non-hunted sites are due to hunting depressing the density and crude biomass of large-bodied species. The apparent density compensation suggested by greater densities of some small-sized species such as Saguinus (Fig. 2) need not be the case. Small and large Neotropical primates tend to use different resources, and hunting activity is sometimes correlated with other patterns of habitat disturbance which may increase the densities of small-sized primates through different mechanisms (Johns & Skorupa, 1987). Differences between group and individual densities may also be affected by interactions between body size, group size, and hunting. For example, large-bodies primates such as woolly monkeys, which live in large groups, occur in relatively low group density, and are severely affected by hunting because single encounters between one or more hunters and a group can destroy a large proportion of the local population (Peres, unpublished data), The same is true for the ungulate most susceptible to hunting in the Neotropics, the white-lipped peccary Tayassu pecari. Woollies and whitelipped peccaries were also the first game species to become extinct in many western Amazonian sites I have visited. On the other hand, small-sized species living in small groups (e.g. Saguinus, Callicebus, Aotus) often occur in relatively high group densities, but suffer little from hunting. Despite their higher gross metabolic requirements, larger animals may be less vulnerable to environmentally unstable conditions because their food resources are subject to less fluctuation. For instance, the smallest representatives of polytypic mammalian genera tend to drop out in unfavourable habitats (Eisenberg, 1979; Emmons, 1984). In addition, a large body size is probably an advantage to an animal in seasonal environments

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Carlos A. Peres

because it permits long fasts (Lindstedt & Boyce, 1985). Smaller species, however, could be better than larger ones at coping with extended periods of arthropod and fruit scarcity by shifting to an alternative high-energy diet (e.g. nectar) and adjusting their time budgets accordingly (Terborgh, 1983). Thus, the implications of body size in the differential resilience of primate species to local disturbance may be considerable. Further work is, however, necessary to establish a predictive theory on how shifts in primate community organization are affected by body size alone.

ACKNOWLEDGEMENTS This study was financed by World Wildlife F u n d - U S project 6199 coordinated by Dr R. Mittermeier and Rod Mast. Access to such remote survey sites would not have been possible without helicopter transportation offered by Petrobras, the Brazilian oil company. I am most grateful to Eng. Dr Amaro Apoluceno and geologist Guy Siegl for allowing me to take full advantage of the support offered by drilling rigs and seismic surveys conducted in the Urucu and Jurufi river basins. Paul Honess and Jay Malcolm helped me conduct one survey, and Dr R. Bodmer made his unpublished data available. Dr E. Duffey and Dr D. J. Chivers reviewed an earlier draft of this manuscript. My studies at Cambridge University are supported by an Overseas Graduate Fellowship from the Brazilian Council of Science and Technology--CNPq.

REFERENCES Ayres, J. M. (1986). Uakaries and Amazonian flooded forest. PhD thesis, University of Cambridge. Ayres, J. M., Lima, D. M., Martins, E. S. & Leme, J. L. (in press). On the track of the road: changes in subsistence hunting in a Brazilian Amazonian village. In Wildlijb Uses in the Neotropics, ed. J. G. Robinson & K. Redford. Chicago University Press, Chicago. Bates, H. W. (1863). The Naturalist on the River Amazons. John Murray, London. Bodmer, R. E., Fang, T. G. & Ibanez, L. M. (in press). Primates and ungulates: a comparison in susceptibility to hunting. Primate Conserv. Burnham, K. P., Anderson, D. R. & Laake, J. L. (1980). Estimation of density from line transect sampling of biological populations. Wildl. Monogr., 72, 1-202. Eisenberg, J. F. (1979). Habitat, economy, and society: some correlations and hypothesis for the neotropical primates. In Primate Ecology and Human Origins, ed. I. S. Bernstein & E. O. Smith. Garland STMP Press, New York, pp. 215-62 Emlen, J. T. (1971). Population studies of birds derived from transect counts. Auk, 88, 323~42.

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Emmons, L. H. (1984). Geographic variation in densities and diversities of nonflying mammals in Amazonia. Biotropica, 16, 210-22. Fearnside, P. M. (1986). Human Carrying CapaciO' o[" the Brazilian Rain/orest. Columbia University Press, New York. Gross, D. R. (1975). Protein capture and cultural development in the Amazon basin. Am. Anthropol., 77, 52649. Hernandez-Camacho, J. & Cooper, R. W. (1976). The non-human primates of Colombia. In Neotropical Primates: Field Studies and Conservation, ed. R. W. Thorington, Jr & P. G. Heltne. National Academy of Sciences, Washington, DC, pp. 35--69. Johns, A. D. (1986). Effects of habitat disturbance on rain forest wildlife in Brazilian Amazonia. Report to the World Wildlife Fund--US, Washington DC (unpublished). Johns, A. D. & Skorupa, J. P. (1987). Responses of rain-forest-primates to habitat disturbance: a review. Int. J. Primatol., 8, 157-91. Lindstedt, S. & Boyce, M. (1985). Seasonality, fasting endurance, and body size in mammals. Am. Nat., 125, 873-8. MacArthur, R. H. (1972). Geographical Ecology. Harper & Row, New York. Mittermeier, R. A. (1987). Effects of hunting on rain forest primates. In Primate Conservation in the Tropical Rain Forest, ed. C. Marsh & R. A. Mittermeier. Alan R. Liss, New York, pp. 11)9-46. Peres, C. A. (1987). Conservation of primates in western Brazilian Amazonia. Report to the World Wildlife Fund--US, Washington DC (unpublished). Peres, C. A. (1989). A survey of a gallery forest primate community, Marajo Island, Para, Brazil. Vida Silvestre Neotropical, 2, 32 7. Peres, C. A. (in press). Primate community structure in western Amazonia. Primate Conserl~.

Peters, R. H. (1983). The Ecological bnplications of Body Size. Cambridge University Press, Cambridge. Redford, K. & Robinson, J. G. (1987). A game of choice: patterns of indian and colonist hunting in the Neotropics. Am. Anthropol., 89, 650-67. Robinson, J. G. & Ramirez, C. J. (1982). Conservation biology of neotropical primates. In Mammalian Biology, ed. M. H. Mares & H. M. Genoways. Spec, Publs, Pymatuning Laboratory of Ecology, University of Pittsburgh, Linesville, Pa, No. 6, 329 44. Smith, N. J. H. (1976). Utilization of game along Brazil's Transamazon highway. Aeta Amazonica, 6, 455-66. Smythe, N. (1986). Competition and resource partitioning in the guild of Neotropical terrestrial frugivorous mammals. Ann. Rev. Ecol. Syst., 17, 169 88. Terborgh, J. (1983). Five New World Primates: A Study in Comparative Ecology. Princeton University Press, Princeton.