American Journal of Primatology 55:171–175 (2001) BRIEF REPORTS Can Phenology Explain the Scarcity of Folivory in New World Primates? ECKHARD W. HEYMANN* Abteilung Verhaltensforschung und Ökologie, Deutsches Primatenzentrum, Göttingen, Germany I evaluated the hypothesis that the scarcity of folivorous neotropical primate taxa is due to fruiting and leafing occurring in phase in the New World. I compiled phenological information from different primatological studies, and correlated patterns of fruiting and leafing. Contrary to the prediction of the hypothesis, at most sites there was no synchronization of fruiting and leafing. Thus, the scarcity of folivorous platyrrhine taxa can not be attributed to specific phenological patterns of the neotropics. Some potential alternative hypotheses are suggested. Am. J. Primatol. 55:171–175, 2001. © 2001 Wiley-Liss, Inc. Key words: phenology; folivory; Alouatta; Brachyteles; Platyrrhini INTRODUCTION A striking difference between neotropical and paleotropical primate communities is the scarcity of folivorous taxa in the New World [Terborgh & van Schaik, 1987; Fleagle & Reed, 1996]. Amongst New World primates, only howler monkeys (Alouatta sp.) and muriquis (Brachyteles sp.) are consistently folivorous [Milton, 1980, 1984; Mendes, 1989; Strier, 1992; Chiarello, 1994; Julliot & Sabatier, 1994; de Moraes et al., 1998]. This scarcity has been interpreted as a result of fruiting and leafing occurring in phase in the neotropics, and out of phase in the paleotropics [Terborgh & van Schaik, 1987]. When fruiting and leafing are in phase, young leaves, which are usually preferred over mature leaves [Milton, 1980; Strier, 1991; Julliot & Sabatier, 1994], cannot provide an alternative resource during periods of reduced fruit availability, and the evolution of folivorous primates would be constrained. In contrast, when fruiting and leafing are out of phase, leaves become available as an alternative resource during periods of fruit scarcity. In line with their hypothesis, Terborgh and van Schaik  showed asynchronous production of fruits and leaves for several paleotropical sites, and synchronized fruiting and leafing for one neotropical site (Barro Colorado Island, Panama). Given the peripheral position of Barro Colorado within the neotropics, it can be asked whether this phenology pattern is typical for the major part of the neotropics, i.e., Amazonia and adjacent regions, where most neotropical pri- *Correspondence to: Dr. Eckhard W. Heymann, Abteilung Verhaltensforschung und Ökologie, Deutsches Primatenzentrum, Kellnerweg 4, D-37077 Göttingen, Germany. E-mail: firstname.lastname@example.org Received 10 April 2001; revision accepted 30 July 2001 © 2001 Wiley-Liss, Inc. 172 / Heymann mate diversity is located [Rylands et al., 1995]. Here I evaluate the hypothesis of Terborgh and van Schaik  with data on the phenology of neotropical sites compiled from the primatological literature. METHODS I screened the neotropical primate literature for information on the phenology of fruiting and leafing. I used the correlation coefficient between fruiting and leaving provided in the respective papers, or read monthly indices of fruiting and leafing from figures in these papers. I correlated the monthly indices with Spearman’s rank correlation using the nonparametrics module of Statistica 5.1. The use of nonparametric correlations eliminates any bias that might result from inaccuracy in reading absolute values from figures, since the relative height (rank) of each data point is relevant in these statistics, not its absolute value. Papers that provided only seasonal values (wet vs. dry season) for fruiting and leaving indices [e.g., Rimoli & Ades, 1997] or semiquantitative information [e.g., Milton, 1984] were not considered for the quantitative analysis, but are included in the discussion. RESULTS Table I shows the correlation coefficients between fruiting and leafing for nine sites located in different parts of South America, and for Barro Colorado Island. At two sites located in Amazonia, a significant negative correlation between fruiting and leafing exists. At the other sites from Amazonia or adjacent biogeographic regions, there is no consistent relation between fruiting and leafing, but there is a trend towards negative correlations. At only two sites, from the Atlantic rain forests of eastern Brazil (Santa Genebra Reserve and Lemos Maia), a significant positive correlation is found. DISCUSSION The result of the analysis indicates that there is no general synchrony of fruiting and leafing in neotropical forests. This result is inconsistent with the original prediction of the hypothesis of Terborgh and van Schaik . Therefore, contrary to this hypothesis, the scarcity of folivorous primate taxa in the neotropics cannot be explained simply by generally deviating phenological patterns in neotropical forests. While the two Atlantic forest sites for which the relation between fruiting and leafing could be examined quantitatively showed an asynchrony of these phenological activities, there is evidence for intersite variation within this region. Rimoli and Ades  observed an increase in leafing and a decrease in fruiting in the dry season and the reverse in the wet season at the Estação Biológica de Caratinga (19°50′S 41°50′W). Milton  noted at Barreiro Rico (22°40′S 48°11′W) that fruit production started when leafing began to taper off. These observations indicate that fruiting and leafing may be asynchronous in Atlantic forest sites, too, and support the objection against the Terborgh-van Schaik hypothesis. What Are Potential Alternative Explanations? Constraints imposed by body size. The generally smaller body size of platyrrhines in comparison to Old World primates [Terborgh, 1992; Fleagle & Reed, 1996; Kappeler & Heymann, 1996] could have reduced the opportunity for TABLE I. Correlation Between Fruiting and Leafing at Different Neotropical Forest Sites Comparisona San Jacinto (Colombia; 9°30′N 75°21′W) Embalse de Guri (Venzuela; 7°45′N 62°53′W) Raleighvalen-Voltzberg (Surinam; 4°41′N 56°10′W) Estación Biológica Caparú (Colombia; 1°5.55′S 69°30.8′W) fr–yl? –0.84 mf–yl Lago Teiú (Brasil; 2°58′S 64°55′W) Estación Biológica Quebrada Blanco (Peru; 4°21′S 73°09′W) Urucu (Brasil; 4°50′52′′S 65°16′05′′W) Lemos Maia, Una (Brasil; 15°20′S 39°05′W) Santa Genebra Reserve (Brasil; 22°49′S 47°07′W) Barro Colorado Island a nb Reference <0.001 12 Cuervo Diaz et al.  –0.51 0.04 17 Homburg  mf–yl –0.46 0.13 12 van Roosmalen  mf–yl, Terraza forest mf–yl, Igapó forest mf–yl, Colina forest fr–yl –0.79 –0.28 0.03 –0.52 <0.01 0.38 0.92 0.08 12 Ayres  mf–yl uf–yl mf–yl uf–yl mf–yl –0.37 –0.33 –0.15 –0.50 0.43 0.10 0.15 0.58 0.07 <0.05 21 21 14 14 13d Tirado and Heymann unpublished data Peres  Heiduck  fr–yl 0.92 <0.001 12 Galetti et al.  0.63 <0.03 12 Terborgh and van Schaik  rs P mf, mature fruits; uf, unripe fruits; yl, young leaves; fr, fruits (mature+immature). Number of mo. Fruit phenology based on 52 mo, leafing phenology on 36 mo. d The correlation provided by Heiduck  is based on 26 phenological sample points (2 per mo). b c c Defler and Defler  c c Phenology and Platyrrhine Folivory / 173 Site 174 / Heymann the evolution of folivory. For allometric reasons, larger animals are better able to subsist on a leafy diet [Demment & van Soest, 1985]. It will be interesting to examine which dietary strategy had been employed by the large fossil platyrrhines discovered from the Pleistocene of southeastern Brazil [Cartelle & Hartwig, 1996; Hartwig & Cartelle, 1996]. However, it is also conceivable that a reduced ability to exploit leaves (for whatever reason) has limited the evolution of largebodied folivores. Sensory constraints. If trichromatic color vision has been selected primarily as an adaptation to folivory, as recently suggested by Dominy and Lucas , the lack of routine trichromacy in platyrrhines except Alouatta may constrain the degree of folivory. Information on the chromatic system of other platyrrhines that regularly include leaves in their diet, particularly Brachyteles, is needed to test this hypothesis. Competition with other folivores. Folivory in platyrrhines could be limited by competition with sloths and leaf-cutting ants [Bourlière, 1985; Rockwood & Glander, 1979]. Both taxa account for a high proportion of the folivore biomass in neotropical forests. In the paleotropics, no comparative competitors exist, except perhaps for tree hyraxes in Africa [Bourlière, 1985]. Outcompetition of other folivorous primates by Alouatta. In terms of geographic distribution and diversity of habitat use, howler monkeys are the most successful platyrrhines [Peres, 1997]. Occupation of the folivorous niche by Alouatta may have constrained the evolution of folivory in other platyrrhines. Comparison of diet overlap and population densities between howler monkeys and other atelines, particularly Brachyteles, in areas of sympatry would be instrumental. This list of hypotheses does not imply a rank order of importance and is not exhaustive; additional hypotheses (e.g., related to soil fertility and plant chemistry) are conceivable. In summary, examination of phenological patterns has not provided evidence for a role of synchronized fruiting and leafing in the scarcity of folivorous platyrrhine taxa. Alternative hypotheses are needed, but only with the emergence of more ecological and physiological data (e.g., feeding ecology, sensory capacities, and plant chemistry) will comparative analyses be possible which could enhance the understanding of the factors determining the scarcity of folivory amongst neotropical primates. 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