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Can phenology explain the scarcity of folivory in New World primates.

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American Journal of Primatology 55:171–175 (2001)
Can Phenology Explain the Scarcity of Folivory in New
World Primates?
Abteilung Verhaltensforschung und Ökologie, Deutsches Primatenzentrum, Göttingen,
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
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 [1987] 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:
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 [1987] with data on the phenology of neotropical sites
compiled from the primatological literature.
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.
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.
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 [1987]. 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 [1997] 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 [1984] 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
San Jacinto
(Colombia; 9°30′N 75°21′W)
Embalse de Guri
(Venzuela; 7°45′N 62°53′W)
(Surinam; 4°41′N 56°10′W)
Estación Biológica Caparú
(Colombia; 1°5.55′S 69°30.8′W)
Lago Teiú
(Brasil; 2°58′S 64°55′W)
Estación Biológica Quebrada Blanco
(Peru; 4°21′S 73°09′W)
(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
Cuervo Diaz et al. [1986]
Homburg [1998]
van Roosmalen [1985]
mf–yl, Terraza forest
mf–yl, Igapó forest
mf–yl, Colina forest
Ayres [1986]
Tirado and Heymann
unpublished data
Peres [1984]
Heiduck [1997]
Galetti et al. [1994]
Terborgh and van Schaik [1987]
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.
The correlation provided by Heiduck [1997] is based on 26 phenological sample points (2 per mo).
Defler and Defler [1996]
Phenology and Platyrrhine Folivory / 173
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
[2001], 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.
I thank Wolfgang Dittus, Karen B. Strier, Dietmar P. Zinner, and an anonymous referee for very helpful comments on an earlier version of the manuscript,
and Karen B. Strier for additional discussion.
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