AMERICAN JOURNAL OF PHYSICAL. ANTHROPOLOGY 88515-524 (1992) Atelinae Adaptations: Behavioral Strategies and Ecological Constraints KAREN B. STRIER Department of Anthropology, University of Wisconsin-Madison, Madison, Wisconsin 53706 KEY WORDS ality Atelin, Alouatta, Diet, Ranging behavior, Season- ABSTRACT Comparisons between the four genera that make up the Atelinae reveal two distinct behavioral patterns, one in which energy expenditure is minimized (Alouatta) and one in which energy intake is maximized (Lagothrix,Ateles, and Brachyteles). Among the atelins, Lagothrix and Ateles devote over 75% of their annual feeding time to fruit, while Brachyteles devotes between 50% and 67% of their feeding time to leaves. Pronounced seasonality in the Atlantic coastal forest inhabited by Brachyteles may be responsible for its more folivorous diet. Alouatta falls in the body size range of Lagothrix and is much smaller than Ateles and Brachyteles. Nonetheless, Alouatta is more folivorous than sympatric atelins. The atelins also share a rapid, suspensory mode of locomotion that appears to enable them to minimize travel time between widely dispersed fruit sources. Alouatta, by contrast, employs a slower, but more energetically efficient, quadrupedal locomotion. Ranging patterns among the Atelinae are consistent with both diet and locomotor abilities: Atelins travel daily distances up to 5,000 m; Alouatta ranges are much shorter. Further distinctions are evident in Atelinae grouping patterns. Alouatta remains in small cohesive groups that occupy home ranges less than 60 ha in size. Both Lagothrix and Ateles have large groups that fission to reduce the costs of intragroup feeding competition when preferred fruits occur in small patches within much larger community ranges. While greater reliance on low-energy foods such as leaves may release Brachyteles from similar competitive constraints, their tendency toward fluid grouping associations is consistent with the pursuit of a frugivorous diet. o 1992 WiIey-Liss, Inc. The Atelinae are the largest and most ern Amazon, Alouatta occurs with Ateles. In widely distributed New World primates. the western Amazon, Alouatta overlaps with Four genera make up the subfamily: Lago- both Ateles and Lagothrix. In the Atlantic thrix, or woolly monkeys, with two species; coastal forest of southeastern Brazil, AlAteles, or spider monkeys, with four species; ouatta is sympatric with Brachyteles, the Brachyteles, or muriquis, a monotypic ge- only other Atelinae whose range extends so nus; and Alouatta, or howler monkeys, the far from the equator (Wolfheim, 1983). Morphological and behavioral analyses of most diverse with seven species (Table 1). Alouatta has the most extensive geo- ateline phylogenetic relationships reveal graphic distribution, ranging from southern two distinct patterns that distinguish AlMexico through northern Argentina and ouatta from the other three genera, collecthroughout the Amazon basin. It is sympat- tively referred to as the atelins (Fig. 1).Alric with a t least one other Atelinae except in the most extreme parts of its ranges. Received July l l, 1990; accepted September 12,1991 Throughout Central America and the east0 1992 WILEY-LISS, INC 516 K.B. STRIER species tend to be more folivorous than smaller ones. Their absolutely greater nutriGenus Species tional requirements necessitate the incluLagothriz Zagotricha sion of abundantly available foods, such a s flavicauda leaves, in their diet, while their relatively Ateles geof f r oyi lower basal metabolic rates permit them to fusciceps belzebuth rely on these lower quality foods, which repaniscus quire longer passage times to extract energy Brachyteles arachnoides and nutrients (Gaulin, 1979). Alouatta belzebul Nonetheless, the relationship between fusca seniculus body size and diet among the Atelinae is not palliata clearcut. Body weights among female coibensis Atelinae average from 4.5 kg for Alouatta pigra caravo. fusca to 9.5 kg for Brachyteles (Fig. 2). There is substantial variation within each genus From Mittermeier et al.. 1988. as well as overlap between Alouatta and Lagothrix and between Ateles and Brachyouatta appears to follow a strategy that teles. Although recent weight data from freeminimizes energy expenditure, while the ranging Brachyteles indicate that it is only atelins appear to maximize energy intake slightly larger than Ateles (Lemos de Sa and (Rosenberger and Strier, 1989). These strat- Glander, in preparation), it is much more egies have been associated with folivory in folivorous (Fig. 3). Alouatta and Lagothrix Alouatta (Milton, 1980) and frugivory in Ate- are the smallest genera, but Alouatta is les (Klein and Klein, 1977; van Roosmalen, more folivorous than Lagothrix and Ateles 1980; Symington, 1988a) and more recently and in some cases Brachyteles. Brachyteles Lagothrix (Defler, 1987; Soini, 1987). In falls within the range of folivory observed in Brachyteles, however, this dichotomy is con- Alouatta; although it is much larger, it is not founded; although Brachyteles resembles proportionately more folivorous. One explanation for these unexpected Alouatta in its folivorous diet, it resembles the other atelins in its ranging and grouping findings is that dietary representations patterns. While these latter resemblances based on annual averages obscure the imsupport the generally accepted phylogenetic portance of seasonal variability. When seaseparation between Alouatta on the one sonal variation in diet is examined in the hand and Ateles, Brachyteles, and Lagothrix three genera (Ateles, Brachyteles, and Alon the other, the strong craniodental and ouatta) for which published data exist (Tadietary similarities between Brachyteles ble 21, it is clear that categorizations such as and Alouatta (Zingeser, 1973) suggest at “frugivorous” and “folivorous” are misleadleast a functional convergence between ing. For example, the Ateles groups devoted an average of 75-78% of their feeding time them. This paper reviews field data on ateline to fruit, but in one study where rainfall was diets, ranging parameters, and grouping highly seasonal (Chapman, 19871, fruit conpatterns from a comparative perspective. sumption dropped and leaf consumption The effects of body size, locomotor abilities, rose dramatically during certain months and seasonality are considered because of (see also van Roosmalen, 1980). Both their significance in understanding the be- Brachyteles study populations fall within the range of Alouatta in the proportion of havioral strategies of the Atelinae. feeding time devoted to fruit and leaves. In BODY SIZE AND DIET fact, the variation between these genera is Body size is a n important predictor of diet less profound than that between different among closely related species (Kay, 1984). Alouatta populations. The importance of seasonality to diet is Although all primates greater than 1 kg in body weight consume both fruit and leaves evident from comparisons between the six (Hladik, 1978, 1981; Richard, 19851, larger Alouatta studies in which annual diet and T A B L E 1. Recognized Atelinae species 517 ATELINAE ADAFTATIONS Lagothrix Alouatta Brachyteles Ateles I; Fig. 1. Phylogenetic relationships of Atelinae (From Rosenberger, 1981). 12.0 11.5 h 9 g.-Eul v ~ 8 m 2 ,f! Q 3 11.0 10.5 9.0 9.5 - -I 8.58.0 7.5 7.0 - /achnoides belzebufh -- geoffroyi 6.5- 5.0 454.0 6.0 5.5 3.5 Alouatta Lagothrix Ateles Brachyteles Genus Fig. 2. Variation in adult female body weights. Points represent mean values for each species; bars indicate range of variation for each genus. Mean values and ranges taken from Ford and Davis (this issue); four adult female weights for Brachyteles uruchnoides from Lemos de Sa and Glander (in preparation) are included. rainfall have been reported (Fig. 4).The average proportion of leaves included in the diet was inversely related to rainfall (Spearman rank correlation, rs = 0.89, n = 6 , P < 0.051, supporting the suggestion that interspecific differences in Alouatta diets are smaller than habitat differences within species (Crockett and Eisenberg, 1987). A similar trend appears to occur within the atelins (Fig. 41, although the relationship between rainfall and folivory in Ateles and Brachyteles is not significant (rs = -0.80, n = 4,P > 0.05). One way to distinguish further between the effects of seasonality on dietary strategies is to examine data obtained on sympat- K.B. STRIER 518 folivory in Brachyteles and the fact that Alouatta fusca is more folivorous, on average, than more equatorial Alouatta species indiBrachyteles cate the importance of seasonal food availability in the Atlantic forest where these species live. Alouatta caraya, studied in northern Argentina, where annual rainfall averaged 1,200 mm, exceeded all other Atelinae by devoting an average of 76% of their annual feeding time to leaves (Table 2; Zunino and Rumiz, 1986). Suggesting that Brachyteles employs a strategy of maximizing energy intake by exploiting fruit when it is available does not minimize the importance of leaves in its Ateles diet. As was indicated above, all Brachyteles populations studied to date consume substantial quantities of leaves, as expected from body size energetics and reflected in their craniodental morphology (Zingeser, 1973).Nonetheless, Brachyteles differs from k I I 8I I 9I I 1I 0 1 1I 1 ’ iI 2 Alouatta in its digestive strategy. Alouatta is characterized by slow passage rates, Mean Female Body Weight(kg) which allow for the efficient absorption of plant nutrients, while Brachyteles, by conFig. 3. Proportion of feeding time devoted to leaves by mean female body weight. Bars represent range of trast, exhibits a surprisingly rapid passage rate that resembles that of both Ateles and annual averages reported for each genus, as indicated in Table 2. Lugothrix diet was estimated from Soini (1987). Lagothrix (Milton, 1984b). Although fast passage time in Brachyteles has been attributed to a strategy emphasizing rapid turnric taxa studied under similar ecological con- over of low-quality foods (Milton, 1984b), a ditions. Figure 5 shows the diets of three more parsimonious explanation may be that sets of sympatric Atelinae: Ateles and Al- it is a shared characteristic retained from a ouatta at two sites and Brachyteles and Al- frugivorous atelin ancestor. ouatta at one site. As indicated previously, Ateles is the most frugivorous, and Brachy- LOCOMOTION AND RANGING BEHAVIOR Intergeneric comparisons of locomotor teles falls within the range of both Alouatta palliata populations. However, Brachyteles patterns support the distinction between Alis nearly 50% more frugivorous than sym- ouatta and the other atelins, including patric Alouatta fusca studied during the Brachyteles. Brachyteles resembles the same time period a t Fazenda Montes Claros. other atelins in its mode of suspensory locoAlthough the absolute proportion of feeding motion, which permits more rapid long distime these species devote to fruit is lower, tance travel than does the quadrupedal locothe difference between these species’diets is motion employed by Alouatta. Cant (1986) proportionate to that between Ateles and Al- discussed the importance of rapid travel beouatta palliata a t the two sites represented. tween widely dispersed fruit sources for AteThese comparisons reveal a fundamental les and suggested that the high energy exdifference between the feeding strategies of pended per unit time in suspensory travel Brachyteles and Alouatta. Even under con- (Parsons and Taylor, 1977) is compensated ditions of similar food availability, Alouatta for both by the energy-rich fruits that can be is more folivorous than Brachyteles, whose exploited and by the actual time saved in annual diet includes a greater proportion of travel. Suspensory locomotion may confer a leaves than the diets of other atelins. Both similar advantage in Brachyteles, permit- I > 519 ATELINAE ADAPTATIONS TABLE 2. Seasonality in Atelinae diets (ranges are compiled or estimated from variation reported by authors)' Rainfall (mm) Species Ateles belzebuth (Klein and Klein, 1977) Ateles geoffroyi (Chapman, 1987, 1988a,b) Ateles paniscus (van Roosmalen, 1980) (Symington 1987, 1988a) Brachyteles arachnoides (Milton, 1984a) (Strier, 1986, 1991a) Alouatta caraya (Zuni0 and Rumiz, 1986) Alouatta fusca (Mendes, 1989) Alouatta palliata (Glander, 1978) (Milton, 1980) (Estrada, 1984) (Chapman,l987) Alouatta seniculus (Gaulin and Gaulin, 1982) Percent fruit Mean Range Percent leaves Mean Range ? 83 78-100 7 3-22 900-2,400 78 0-100 12 0--80 2,000-2,400 1,971 83 75 58-96 55-99 8 16 1-23 <I-38 1,263 1,186 21 32 4-59 13-66 67 51 41-93 28-78 1,200 24 ? 76 ? 1,186 16 -I--30 71 -64--78 1,431 2,730 4,500 900-2,400 13 42 51 29 -9--15 10--65 0-80 0-55 64 48 49 49 -59--67 -25-44 20-100 0-95 1,942 42 ? 53 ? 'For duration of studies, see Rosenberger and Strier (1989). 6 -1 5- 0 Y E 0 LT Alouatta 0 Atelins 0 4- 3- 0 0 0 0 0 0 21 - 0 0 0 4 5 0 0 1 2 3 Rank Rainfall 6 Fig. 4. Rank rainfall and degree of folivory in Alouatta and two atelins, Brachyteles and Ateles. Rainfall and annual averages for each species are taken from sources in Table 2 when reported annual rainfall variation was 1500 mm. ting it to include a larger proportion of fruit Roosmalen, 1980), although average daily in its diet than sympatric, quadrupedal Al- ranges are generally lower. Alouatta travels substantially less each day and utilizes ouatta. Table 3 shows data on ranging parame- smaller home ranges. Brachyteles is interters compiled from a subset of longterm mediate, exhibiting a high degree of instudies on Atelinae. The two most frugivo- traspecific variation. Both day range and rous genera, Ateles and Lagothrix, have the home range were greater at the site where longest average day ranges and the largest Brachyteles was more frugivorous. Furtherhome ranges; Ateles have been reported to more, Brachyteles at Fazenda Montes Claros travel daily distances of up to 5,000 m (van exploited a home range over twice as large, K.B. STRIER 520 80 60 2 .-9 0 2 40 LL 3? 20 0 BCI, Panama Milton (1981) Santa Rosa, CR Chapman (1987) FMC, Brazil Strier (1986) 2,730 mm 900-2,400 rnrn 1156 rnm Fig. 5. Dietary comparisons between sympatric atelins (Ateles and Brachyteles) and Alouatta. Site, source, and annual rainfall are given below each comparison. TABLE 3. Rangingparameters and group size Species Lagothriz lagothricha (Defler, 1987) (Nishimura, 1990) Ateles paniscus (Symington, 1988a,b) Brachyteles arachnoides (Miton, 1984a) (Strier, 198713, 1991a) Alouatta fusca (Mendes, 1989) Alouatta palliata (Milton, 1980) (Estrada, 1984) Alouatta seniculus (Gaulin and Gaulin, 1982) Day range (m) Home range (ha) Group size Percent fruit 3,000 ? 740 450/350 20-23 45/13 ? ? 1,977 1531231 40/37 75 630 1,283 70 168+ 7 26 21 32 523 8 7 16 443 123 31 60 17 9 42 51 706 22 9 42 and traveled on average over twice as far daily as sympatricAlouatta. Thus it appears that both the locomotor and the ranging patterns among the Atelinae support a division between Alouatta and the atelins that is consistent with their dietary strategies. Differences in group size may confound both intra- and interspecific comparisons. Across primates with similar diets, larger, heavier groups generally require larger food supply areas (Milton and May, 1976; Clutton-Brock and Harvey, 19771, but how large the area is is also determined by food density. For example, in Symington’s (1988b) study of two Ateles groups of roughly similar size, home ranges differed by nearly 50% depending on habitat quality. GROUPING PATTERNS Grouping patterns among the Atelinae show considerable variability. Alouatta groups are typically smaller than atelin groups (Table 3), although group fissioning in atelins may result in feeding parties that are quite similar in size to those ofAlouatta. On a continuum with fluid groups at one extreme and cohesive groups at the other, Ateles and Lagothrix fall at one end, while Alouatta falls at the other. Fluid atelin groups are believed to reflect the patchy na- ATELINAE ADAPTATIONS Minimizers ENERGY 521 Maximizers Bracbytetes, Ateles, Lagotbrix Alouatta 3 folivory '-4 Diet -b frugivory short -4 Day Range -b long small -4 Home Range -b large -4 Grouping -b fluid cohesive Fig. 6. Schematic representation of behavioral divergence in Atelinae. ture of their fruit resources. Atelin groups typical of this genus than previous observafission to avoid feeding competiton at small tions a t Montes Claros have suggested. It is possible that Brachyteles can remain fruit patches and reunite a t larger patches where a greater number of individuals can in more cohesive groups than other atelins feed together. A number of studies have because their ability to include greater proshown a strong positive relationship be- portions of leaves in their diet mediates the tween food patch size and subgroup, or constraints of feeding competition at patchy party, size in Ateles (Klein and Klein, 1977; resources. This proposition, however, is unSymington, 1988a; Chapman, 1988a). Be- likely for two reasons. First, other atelins cause Alouatta includes a greater proportion retain their fluid grouping patterns while of more evenly distributed leaves in its diet, relying heavily on leaves when fruits are it does not face comparable levels of intra- seasonally scarce (see above). Second, longigroup feeding competition, and groups can tudinal data indicate that Brachyteles may remain cohesive. The physical constraints of maintain more fluid associations when patch size may still, however, be important large fruit patches are unavailable or when in determining feeding associations in oth- groups become too large to feed together in erwise cohesive groups (see, e.g., Leighton fruit patches (Strier, 1989; Strier et al., 1992). and Leighton, 1982; Strier, 1989). Despite their intraspecific variability, Brachyteles appear to resemble the atelins DISCUSSION in their fluid grouping patterns. At Fazenda Despite a high degree of intrageneric variBarreiro Rico, one Brachyteles group comprising seven individuals had fluid associa- ation, Lagothrix and Ateles are clearly distions (Milton, 1984a). Groups of 14 tinct from Alouatta in their feeding, rangBrachyteles at Fazenda Esmeralda (Lemos ing, and grouping patterns (Fig. 6). The de Sa, 1988) and 26 a t Fazenda Montes atelins are more frugivorous, have longer Claros (Strier, 1987a,b)traveled as cohesive day ranges and larger home ranges, and units. However, a s the size and biomass of have more fluid grouping associations than the Montes Claros group have increased Alouatta. These differences persist in comover the last 8 years, the group has begun to parisons between sympatric species, sugshow increased tendencies toward fission- gesting that these genera pursue divergent ing (Strier, 1989, 1991b; Strier et al., 1992). strategies that are consistent with their food It may be that the fluid groups observed by passage rates, divergent modes of locomoMilton (1984a) at Barreiro Rico are more tion, and evolutionary history. 522 K.B. STRIER Brachyteles is more folivorous than the other atelins, but, in sympatric comparisons with Alouatta, it is more frugivorous than would be expected from its large body size, just as Ateles is more frugivorous than sympatric Alouatta in less seasonal habitats. The ranging behavior of Brachyteles reflects the rapid bursts of long-distance travel associated with suspensory locomotion between high-quality dispersed fruit resources; its fluid grouping patterns resemble those of other atelin groups, which fission to avoid feeding competition a t fruit patches. Folivory in Brachyteles may be regarded as a secondary adaptation imposed on an otherwise atelin strategy involving maximizing energy intake (see Rosenberger and Strier, 1989). This reasoning follows Rosenberger and Kinzey’s (1976) “critical function” hypothesis, which posits that what an animal must be able to do during periods of food shortage is more important to understanding its functional morphology than its overall annual diet. From this perspective, the morphological and behavioral adaptations for folivory in Brachyteles are critical during seasonal fruit shortages. They are not, however, necessarily representative of a folivorous strategy in which energetic expenditure is restricted by an energy-poor diet (but see Milton, 1984a). Seasonality in food availability may also account for the high variation in folivory across Alouatta. It does not, however, obscure the divergence between Alouatta and atelin behavior. All Atelinae are more folivorous in more seasonal habitats, but Alouatta is even more so. The fact that Alouatta is sympatric with a t least one other atelin throughout most of its range suggests that niche divergence between these genera is an important feature of their evolutionary relationships. Comparative approaches are essential to elucidate behavioral ecological relationships (Clutton-Brock and Harvey, 1984). They also provide a basis for evaluating phylogenetic relationships reconstructed from morphological traits (Rosenberger and Strier, 1989). It is difficult, for example, to interpret the significance of folivory in Brachyteles without comparative data on other Atelinae in diverse habitats. Sympatric comparisons between closely related species are particularly important in providing a basis to distinguish between diet and overall behavioral strategies. ACKNOWLEDGMENTS I am grateful to the Brazilian government and CNPq for permission to conduct research in Brazil and to Dr. Celio Valle for his sponsorship and support. E. Veado, F.D. Mendes, and J. Rimoli contributed to the longitudinal data collection in the field; L. Johnson and M. Steele assisted in the preparation of the illustrations. The field research was supported by NSF grants BNS 8305322, BNS 8619442, and BNS 8958298; the Fulbright Foundation; grant 213 from the Joseph Henry Fund of NAS, Sigma Xi, the World Wildlife Fund, and the L.S.B. Leakey Foundation. A version of this paper was presented at the 58th Annual Meeting of the American Association of Physical Anthropologists. I thank P. Garber and W. Kinzey for inviting me to participate in their symposium and P. Garber, S. Ford, and the anonymous reviewers for their comments on the manuscript. R.M. Lemos de Sa and K.E. Glander generously permitted me to cite their recent (and as yet unpublished) weight data for Brachyteles. LITERATURE CITED Cant JGH (1986) Locomotion and feeding postures of spider and howling monkeys: Field study and evolutionary interpretation. Folia Primatol. 46t1-14. Chapman C (1987) Flexibility in the diets of three species of Costa Rican primates. Folia Primatol. 49:90105. Chapman C (1988a) Patterns of foraging and range use by three species of Neotropical primates. Primates 29: 177-194. Chapman C (1988b) Patch use and patch depletion by the spider and howling monkeys of Santa Rosa National Park, Costa Rica. Behaviour 10.599-116. Clutton-Brock TH, and Harvey PH (1977) Species differences in feeding and ranging behavior in primates. In TH Clutton-Brock (ed.): Primate Ecology. London: Academic Press, pp. 557-584. Clutton-Brock TH, and Harvey PH (1984) Comparative approaches to investigating adaptation. In J R Krebs and NB Davies (eds.):Behavioural Ecology. Sunderland, MA: Sinauer, pp. 7-29. Crockett CM, and Eisenberg JF (1!%37) Howlers: variations in group size and demography. In BB Smuts, DL Cheney, RM Seyfarth, RW Wrangham, and TT Struhsaker (eds.): Primate Societies. Chicago: Unviersity of Chicago Press, pp. 54-68. ATELINAE ADAPTATIONS Defler TR (1987) Ranging and the use of space in a group of woolly monkeys (Lagothrix lagothricha) in the NW Amazon of Columbia. Int. J . Primatol. 8t420. Estrada A (1984) Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas, Veracruz, Mexico. Int. J. Primatol. 5t105-131. Ford SM, and Davis LC (1992) Systematics and body size: Implications for feeding adaptations in New World monkeys. Am. J. Phys. Anthropol. (this issue). Gaulin SJC (1979)A JarmanBell model of primate feeding niches. Hum. Ecol. 7tl-20. Gaulin SJC, and Gaulin CK (1982)Behavioral ecology of Alouatta seniculus in Andean cloud forest. Int. J. Primatol. 3t1-32. Glander KE (1978) Howling monkey feeding behavior and plant secondary compounds: a study of strategies. In GG Montgomery (ed.):The Ecology of Arboreal Folivores. Washington, DC: Smithsonian Institution Press, pp. 561-574. Hladik CM (1978) Adaptive strategies of primates in relation to leaf-eating. In GG Montgomery (ed.): The Ecology of Arboreal Folivores. Washington, DC: Smithsonian Institution Press, pp. 373-396. Hladik CM (1981) Diet and the evolution of feeding strategies among forest primates. In RSO Harding and G Teleki (eds.): Omnivorous Primates: Gathering and Hunting in Human Evolution. New York: Columbia University Press, pp. 215-254. Kay RF (1984)On the use of anatomical features to infer foraging behavior in extinct primates. In PS Rodman and JGH Cant (eds.): Adaptations for Foraging in Nonhuman Primates. New York: Columbia University Press, pp. 21-53. Klein LL, and Klein DJ (1977) Feeding behavior of the Columbian spider monkey. In TH Clutton-Brock (ed.): Primate Ecology. London: Academic Press, pp. 1 5 6 181. Leighton M, and Leighton DR (1982) The relationships of size of feeding aggregate to size of food patch: Howler monkeys (Alouatta paZliata) feeding in Trichilia cipo fruit trees on Barro Colorado Island. Biotropica 14:81-90. Lemos de Sa RM (1988) Situaqao de uma Populaqao de Mono-Carroeiro, Brachyteles arachnoides, em fragmento de mata Atlantica (M.G.) e Implicagoes para sua Conservaqao.MA Thesis, Universidade de Brasilia. Mendes SL (1989) Estudo ecologico de Alouatta fusca (Primates: Cebidae) na Estaqao Biologica de Caratinga, MG. Rev. Nordestina Biol. 6r71-104. Milton K (1980) The Foraging Strategy of Howler Monkeys. New York: Columbia University Press. Milton K (1981) Food choice and digestive strategies of two sympatric primate species. Am. Nat. 117:496505. Milton K (1984a) Habitat, diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1806). Int. J. Primatol. 5t491-514. Milton K (1984b) The role of food processing factors in primate food choice. In P Rodman and JGH Cant (eds.): Adaptations for Foraging in Nonhuman Primates. New York: Columbia University Press, pp. 249-279. 523 Milton K, and May ML (1976) Body weight, diet and home range area in primates. Nature 259:459-462. Mittermeier RA, Rylands AB, and Coimbra-Filho AF (1988) Systematics: species and subspecies-an update. In RA Mittermeier, AB Rylands, AF CoimbraFilho, and GAB Fonseca (eds.): Ecology and Behavior of Neotropical Primates, Vol. 2. Contegem, Minas Gerais: Editora Littera Maciel Ltd., pp. 13-75. Nishimura A (1990)A sociological and behavioral study of woolly monkeys, Lagothrix lagotricha, in the Upper Amazon. Sci. Eng. Rev. Doshisha University 31r87121. Parsons PE, and Taylor CR (1977) Energetics of brachiation versus walking: A comparison of a suspended and an inverted pendulum mechanism. Physiol. Zool. 50:182-188. Richard A (1985) Primates in Nature. New York: WH Freeman. Rosenberger AL (1981) Systematics: the higher taxa. In AF Coimbra-Filho and RA Mittermeier (eds.):Ecology and Behavior of Neotropical Primates vol. 1. Rio de Janeiro: Academia Brasileira de Ciencias, pp. 9-26. Rosenberger AL, and Kinzey WG (1976) Functional patterns of molar occlusion in platyrrhine primates. Am. J. Phys. Anthropol. 45:281-298. Rosenberger AL, and Strier KB (1989) Adaptive radiation of the ateline primates. J. Hum. Evol. 18~717750. Soini P (1987) Ecology of Lagothrix lagothrzcha on the Rio Pacaya, northeastern Peru. Int. J. Primatol. 8:421. Strier KB (1986) The behavior and ecology of the woolly spider monkey, or muriqui (Brachyteles arachnoides E. Geoffroy 1806).PhD Dissertation, Harvard University. Strier KB (1987aj Demographic patterns in one group of free-ranging woolly spider monkeys. Primate Conserv. 8:73-74. Strier KB (1987b) Ranging behavior of woolly spider monkeys. Int. J. Primatol. 8:575-591. Strier KB (1989) Effects of patch size on feeding associations in muriquis. Folia Primatol. 52r70-77. Strier KB (1991a) Diet in one group of woolly spider monkeys, or muriquis (Bruchyteles aruchnoides). Am. J. Primatol. 23r113-126. Strier KB (1991b) Demography and conservation of a n endangered primate, Brachyteles aruchnoides. Conserv. Biol. 5.214-218. Strier KB, Mendes FDC, Rimoli J, and Rimoli A 0 (1992) Demography and social structure of one group of muriquis (Brachyteles arachnoides). Int. J . Primatol. (in press) Symington MM (1987) Ecological and social correlates of party size in the black spider monkey, Ateles paniscus chamek. PhD Dissertation, Princeton University. Symington MM (1988a) Food compositon and foraging party size in the black spider monkey (Atelespaniscus chamek). Behaviour 105:117-134. Symington MM (1988b) Demography, ranging patterns, and activity budgets of black spider monkeys (Ateles paniscus chamek) in the Manu National Park, Peru. Am. J. Primatol. 15:45-67. 524 K.B. STRIER van Roosmalen MGM (1980) Habitat preferences, diet, feeding behavior, and social organization of the black spider monkey, Ateles paniscus panzscus in Surinam. PhD Dissertation, University of Wageningen, The Netherlands. Wolfheim J H (1983) Primates of the World. Seattle: University of Washington Press. Zingeser MR (1973) Dentition of Brachyteles arachnoides with reference to Alouattine and Atelinine affinities. Folia Primatol. 20:351-390. Zunino GE, and Rurniz DI (1986)Observaciones sobre el comportamiento territorial del mono aullador negro (Alouatta caraya). Bol. Primatol. Argentino 4:3652.