Nonconvergence in the evolution of primate life history and socio-ecology

Biological Journal of the Linnean Society (1996), 59: 297–326. With 8 figures

Nonconvergence in the evolution of primate life history and socio-ecology PETER M. KAPPELER AND ECKHARD W. HEYMANN ¨ AG Verhaltensforschung/Okologie, Deutsches Primatenzentrum, Kellnerweg 4, 37077 G¨ottingen, Germany Received 5 July 1995, accepted for publication 11 December 1995

The goal of this study was to investigate the extent of convergence in four basic life history and socioecological traits among the primates of Africa, Asia, South America and Madagascar. The convergence hypothesis predicts that similar abiotic conditions should result in similar adaptations in independent taxa. Because primates offer a unique opportunity among mammals to examine adaptations of independent groups to tropical environments, we collected information on body mass, activity pattern, diet and group size from all genera for quantitative tests of this hypothesis. We revealed a number of qualitative and quantitative differences among the four primate groups, indicating a lack of convergence in these basic aspects of life history and socio-ecology. Our analyses demonstrated that New World primates are on average significantly smaller than primates in other regions and characterized by a lack of species larger than about 10 kg. Madagascar harbours significantly more nocturnal species than the other regions and is home to all but one of the primates with irregular bursts of activity. Asia is the only region with strictly faunivorous primates, but lacks primarily gummivorous ones. The Neotropics are characterized by the absence of primarily folivorous primates. Solitary species are not represented in the New World, whereas solitary and pair-living species make up the majority of Malagasy primates. Lemurs live in significantly smaller groups than other primates, even after controlling for differences in body size. The lack of convergence among the major primate groups is neither primarily due to phylogenetic constraints as a result of founder effects, nor can it be sufficiently explained as a passive consequence of body size differences. However, because the role of adaptive forces, such as interspecific competition, predation or phenology in shaping the observed differences is largely unexplored, we conclude that it is premature to discard the convergence hypothesis without further tests. ©1996 The Linnean Society of London

ADDITIONAL KEY WORDS: — convergence – life history – ecology – behaviour – evolution – phylogeny – biogeography – primates. CONTENTS Introduction . . . . . . . . Material and methods . . . . . Results . . . . . . . . . . Discussion . . . . . . . . . Assumptions of the convergence Interactions among variables . Phylogeny . . . . . . . Adaptation to biotic factors .

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Correspondence to P.M. Kappeler e-mail: [email protected] 0024–4066/96/011297 + 30 $25.00/0

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INTRODUCTION

Convergence is a concept in evolutionary biology that is implicated whenever similar adaptations to comparable environmental factors have arisen independently (Futuyma, 1986). Convergences have been documented on several levels of organization, i.e. from physiology and morphology to social behavior and community structure (e.g. Rensch, 1959; Walter, 1984; Lee & Cockburn 1985; Randall, 1994). However, most recent quantitative comparisons of birds or mammals revealed many unexpected differences among regions or communities, thereby generating interest in evolutionary mechanisms and constraints responsible for these patterns (Mares, 1976; Pearson, 1977; Karr, 1980; Cristoffer, 1987; Terborgh & van Schaik, 1987; Terborgh, 1992; Mack, 1993; Randall, 1994). Primates are an excellent group for the study of convergence for at least four reasons. First, compared to other mammals, primates are characterized by a remarkable diversity in life history strategies, social systems and ecological specializations (Smuts et al., 1987) that is rare among mammals (cf. Lee & Cockburn, 1985; Gittleman, 1989). Thus, the evolution of convergences is not principally constrained by primate-specific traits, and there is sufficient variation in these traits for natural selection to act upon. Second, the geographical distribution of living primates is confined to tropical and subtropical regions with broadly similar climates (Richard, 1985). Only a few species have ranges largely or completely outside the tropics, e.g. Macaca mulatta, M. arctoides, M. sylvanus, M. fuscata, Semnopithecus entellus, Pygathrix roxellanae, P. bieti and P. brelichi. Primate habitats in tropical forests around the world have also been assumed to be structurally similar because they have similar productivity, leaf size and shape, canopy height, degree of stratification and tree density (Leigh, 1975; Emmons & Gentry, 1983; Brown & Lugo 1984; but see Gentry 1993). Moreover, they are dominated by the same few plant families: except for Southeast Asia, where the Dipterocarpaceae are the dominant group, most trees growing in tropical forests belong to the Leguminosae, Rubiaceae, Moraceae, Annonaceae, Euphorbiaceae, Lauraceae and Sapotaceae (Terborgh & van Schaik, 1987; Gentry, 1988; Terborgh, 1992; Mack, 1993). Thus, the majority of the more than 200 primate species has evolved in climatically and structurally similar environments. Third, in contrast to other mammalian orders with a primarily tropical distribution, only primates have colonized all tropical regions (except Australia) and developed a relatively high taxonomic diversity in all of them (Table 1). Fourth, primates are among the most thoroughly studied vertebrates and more information from behavioral and ecological field studies is available for primates than for any other large mammal group. In addition, the colonization of Africa, Asia, Madagascar and the Neotropics by primates can be considered as partly independent evolutionary experiments, resulting in taxa that have evolved in isolation from each other for millions of years and generations. The adaptive radiation of Malagasy lemurs is the result of a single colonization event by African or Asian strepsirhines in the Eocene (Martin, 1990;

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TABLE 1. Taxonomic and regional diversity of mammals with primarily tropical distribution. The number of living genera (G) and species (S) of 11 mammalian orders in five regions. Only orders in which the majority of species has a (primarily) tropical or subtropical distribution are considered. Data for non-primates from Grzimek, 1988 Asia

Africa

America

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Australia

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S

G

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G

S

G

S

Primates Dermoptera Scandentia Pholidota Proboscidea Hyracoidea Tubulidentata Macroscelidea Xenarthra Marsupialia Monotremata

12 1 5 1 1 — — — — — —

62 2 17 3 1 — — — — — —

18 — — 1 1 3 1 4 — — —

64 — — 4 1 11 1 15 — — —

16 — — — — — — — 13 9 —

77 — — — — — — — 29 17 —

14 — — — — — — — — — —

32 — — — — — — — — — —

— — — — — — — — — 60 3

— — — — — — — — — 128 3

Yoder, 1994). Similarly, the radiation of neotropical primates dates back to a single colonization; probably by African haplorhines in the Oligocene (Martin, 1990). Interestingly, these two groups represent natural experiments, where either a strepsirhine or haplorhine radiation took place in the absence of representatives of the other suborder. The living primates of Africa and Asia are heterogeneous groups of haplorhines and strepsirhines, with a likely common origin in Africa (Martin, 1990). Today, however, these two groups have only one genus in common: the Barbary macaque (Macaca sylvanus) is the only African representative of an otherwise exclusively Asian genus. Thus, even though these four geographically defined groups are members of the same order and two of the faunas are clades, they can be considered as independent groups for the purpose of broad comparisons, although it must be kept in mind that the possible factors affecting diversity are confounded statistically. In this report we test the prediction of the convergence hypothesis that the primates of Africa, Asia, South America and Madagascar have evolved similar diversities in body size, activity, diet and group size. Because of these aspects of their evolutionary history, primates provide a unique opportunity among mammals to examine convergent adaptations to tropical habitats. Even in this case, however, a formal test of the convergence hypothesis is not straightforward. First, the predictions of the convergence hypothesis do not differ from the null-hypothesis. Second, the evolution of convergences may be hampered or counteracted by several internal and external factors, such as founder effects, different intensities of interspecific competition and predation, or variation in the spatiotemporal distribution of resources. Thus, (small?) deviations from the null hypotheses are to be expected, but their direction and magnitude are difficult to predict, thereby increasing the probability of rejecting a true null hypothesis. This problem will be discussed in more detail below (see also Schluter, 1986; Medel, 1995). Several traits of some primate groups have already been examined for convergences (Bourliere, 1985; Robinson & Janson, 1987; Reed & Fleagle, 1995). Most notably, Terborgh & van Schaik (1987) identified a number of differences, such as the lack of large folivores in the Neotropics and the lower biomass and alphadiversity of Asian primates. Their comparisons were preliminary, however, because

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they were largely qualitative, did not include Malagasy lemurs, and were based on data from only a few (primarily rain forest) sites in the other regions. In this paper, we extend their pioneering comparisons to quantitative analyses of differences in body size, activity, diet and group size among all primate genera. We chose these four variables because they represent basic life history traits or because they reflect major ecological and social adaptations. Body size is probably the most fundamental life history trait and is related to many aspects of an organism’s physiology and ecology (Calder, 1984; Schmidt-Nielsen, 1984). Whether a species is active at day or at night also has important consequences for basic aspects of its ecology and behaviour (Eisenberg, 1981). An animal’s behaviour is a target of natural selection where convergences are expected, because behaviour mediates the interactions between the organism and its environment. Since feeding animals interact most directly with structural aspects of their habitats, the ecological diversity of a group of species can be indexed by characterizing the feeding behaviour of each species (Pearson, 1977). Finally, the behaviour of individuals towards conspecifics is also thought to be largely shaped by ecological factors, such as the distribution of resources or the risk of predation (Dunbar, 1988). Individuals decide at the behavioral level whether they lead a solitary life or form permanent groups, and which group size is optimal under a given set of ecological conditions (Terborgh & Janson, 1986).

MATERIAL AND METHODS

We collected information on primate body size, activity, diet and group size from an intensive survey of the literature. To circumvent problems posed by varying degrees of sexual dimorphism among species, we chose body mass of adult nonpregnant females as the most meaningful measure of body size. Data from wild populations were given priority over weights of captive animals. Whenever data for several subspecies were available, the sample with the largest size was chosen to represent the respective species. Values in the Appendix present means of the weights of several females in the majority of species. In some cases, midpoints of reported ranges were accepted for these broad comparisons. Empirically estimated weights of subfossil Malagasy lemurs were included in the analysis of body size diversity, because they were part of the modern fauna and went extinct only a few centuries ago (Dewar, 1984; Richard & Dewar, 1991). The activity of each species was classified as strictly diurnal, strictly nocturnal or as cathemeral. Cathemeral activity is defined by irregular bursts of activity around the 24 h cycle (Tattersall, 1987). The classification of the diet of each species was based on qualitative and quantitative data from field studies. A species was classified as predominantly frugivorous, folivorous, gummivorous, faunivorous, or as belonging to one of the possible combinations of these categories, whenever the majority of feeding items throughout the year were from the respective category(ies). While this classification is necessarily crude and ignores potential regional and seasonal variation, it is the only meaningful way of comparing all available information among the four groups. Information on mean group size was obtained by calculating the arithmetic mean of the number of adult and subadult animals counted in individual groups of a species, as reported in the primary literature. Solitary species were assigned a group

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size value of 1, even though females are (temporarily) associated with their offspring, at least until weaning (see van Schaik & Kappeler 1993). Data for some Old World species were taken from the secondary literature because their grouping patterns have been thoroughly reviewed recently (Smuts et al., 1987, Gauthier-Hion et al., 1988; Davies & Oates, 1994). An important question in comparative studies concerns the taxonomic level of analysis. Dependence among species due to common descent poses statistical problems in quantitative analysis (Felsenstein, 1985). Techniques for dealing with this problem include empirical determination of the appropriate level of analysis and implementation of phylogenetic controls (Harvey & Pagel, 1991). Because we were interested in comparing diversity among radiations, we explicitly chose species as the most meaningful taxonomic level for comparisons because they represent the fundamental biological unit. Moreover, appropriate phylogenetic methods are not yet available to tackle all of the questions dealt with in this paper. Nevertheless, where appropriate, analyses were repeated with generic means to provide a statistically more conservative examination of particular trends. A second problem related to taxonomic diversity had also to be addressed before our analysis. Because of phylogenetic inertia as a result of niche conservatism, phylogenetic time lags or similar adaptive responses, one expects less diversity among species within genera than among genera within families, etc. (Harvey & Pagel, 1991). It is therefore possible that potential differences among the four primate groups are partly due to differences in their taxonomic diversity. To investigate this possibility, we obtained a measure of taxonomic diversity at different levels for each group by counting the number of subspecies, species, genera and families (Table 2). Because the number of families and genera, where most phylogenetic inertia is located, is remarkably similar among the four groups, and the proportion of (living) families, genera and species does not differ significantly among the four regions (χ2-test of independence: χ2 = 8.57, df = 6, n.s.), it is unlikely that our analyses were biased by taxonomic artefacts. Including subfossil lemurs does not change this conclusion (χ2 = 11.79, df = 6, n.s.). We collated similarities and differences in body size and group size of African, Asian, South American and Malagasy primates by comparing pairs of frequency distributions with a Kolmogorov-Smirnov two-sample test (Siegel & Castellan, 1988). TABLE 2. Taxonomic diversity of primates. For each region, the number of living families, genera, species and subspecies of nonhuman primates is presented. Monotypic species are included in the subspecies count. Numbers for described subfossil Malagasy taxa are provided in parentheses and provide minimum estimates as new taxa are still being discovered. Note that Africa and Asia share a genus and a family. See Appendix for additional details Number of Families Africa Asia America Madagascar Total

4 5 2 5 (+3) 15

Genera 18 12 16 14 (+8) 59

Species

Subspecies

64 62 77 32 (+16) 235

180 182 165 51 (+16) 578

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We chose this procedure because only it is sensitive to any kind of difference between two samples and because we had no a priori predictions about the type of potential differences (e.g. in central tendency or skewness). Because samples from each region were included in more than one test, the alpha-level was set at 0.01 to reduce the probability of commiting a type I error (Sokal & Rohlf, 1981). Differences in body mass were further examined by comparing the means of log-transformed variates among regions with ANOVA, followed by post hoc comparisons using Fisher’s protected least significant difference (PLSD). We compared the proportion of species with different activity patterns across the four regions with a χ2-test of independence (Sokal & Rohlf, 1981). Because of small expected values for cathemeral species, they were omitted from one analysis and lumped with nocturnal species in another. The evolution of primate activity patterns was reconstructed using the parsimonious algorithm of MacClade (Maddison & Maddison, 1992). A comparison of the proportion of species with different feeding adaptations across the four regions was not possible due to too many small expected values. Because combination of the already crude categories seemed unadvisable, we restrict our analysis of dietary differences across groups to qualitative comparisons. Differences in mean group size among the four groups were examined with and without controlling for differences in body size after log-transformation of generic means. All computations were performed in Statview 4.02. Our data base includes information on all four variables for 155 species (66%), representing 58 or 59 extant primate genera. For the majority of the remaining species, data for at least two variables were available, so that our sample is representative of the existing variation among primates in these traits. Biases in favor of certain taxonomic groups or gregarious diurnal species are not evident (see Appendix).

RESULTS

Our first comparison revealed several qualitative and quantitative differences in body size among the four groups (Fig. 1). All body mass frequency distributions were significantly different from each other, except for the Africa-Madagascar comparison (Table 3). These general differences were partly due to differences in central tendency among the four size distributions (ANOVA: F3,203 = 7.87, P < 0.0001). Post hoc comparisons revealed that the Neotropics, which lacks species with more than about 10 kg, harbours primates that are on average smaller than those in all other regions (Fisher’s PLSD: Africa-South America: 0.447, P = 0.0003; Asia-South America: 0.558, P < 0.0001; Madagascar-South America: 0.414, P = 0.0016), whereas no differences among the other regions were detected. Across all primates, diurnality is the most common activity pattern (Fig. 2), but there is significant variation among the four regions in the proportions of diurnal and nocturnal species (χ2 = 50.0, df = 3, P < 0.0001; cathemeral and nocturnal species lumped: χ2 = 68.9, df = 3, P < 0.0001). This heterogeneity is caused by the large proportion of nocturnal species in Madagascar because the proportion of species with different activity pattern does not differ among Africa, Asia and America (χ2 = 2.86, df = 2, n.s.; cathemeral and nocturnal species lumped: χ2 = 2.31, df = 2, n.s.). Madagascar is also home to all but one of the cathemeral primates: Aotus azar, the owl monkey of Paraguay, is the only cathemeral species outside

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Madagascar (Wright, 1985, 1989). The other South American Owl monkeys (Aotus spec.) became secondarily nocturnal from diurnal ancestors (Fig. 3). The phylogenetic reconstruction also revealed that nocturnal activity is the ancestral state for primates and that diurnality evolved independently at least three times; twice among Malagasy lemurs and once in a common ancestor of the New and Old World anthropoids (Fig. 3). Our comparison of feeding strategies revealed several qualitative differences and indicated a number of quantitative dissimilarities among regions (Fig. 4). The Asian genus Tarsius contains the only exclusively faunivorous primates, whereas primarily gummivorous species are found in all regions but Asia. The most notable qualitative difference concerns the lack of primarily folivorous primates in the New World. It is also striking that Africa lacks one clearly dominating category, whereas folivorousfrugivorous species in Asia (44.4%), folivorous species in Madagascar (50.0%) and

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Figure 1. Primate body size. The number of species in 10 size classes, ranging from < 100 g to > 50 kg, is depicted for Africa (n = 56, median: 3618, inter-quartile range {iqr}: 6375, min.: 69, max.: 93 000), Asia (n = 45, median: 5900, iqr: 4150, min.: 110, max.: 37 000), America (n = 56, median: 860, iqr: 2202, min.: 122, max.: 8800) and Madagascar (n = 44, median: 2597, iqr: 12 290, min.: 31, max.: 197 500). Subfossil Malagasy species are indicated by lighter shading. All descriptive statistics are in gramms. New World primates are on average smaller than primates in each of the other regions (see text for details).

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TABLE 3. Comparison of primate body and group sizes. Dstatistics (Kolmogorov-Smirnov two-sample test) are provided for all pairwise comparisons between African (AFR), Asian (ASI), Neotropical (SA) and Malagasy (MAD) species. See Figs 1 and 5 for sample sizes Body mass

AFR-ASI AFR-SA AFR-MAD ASI-SA ASI-MAD SA-MAD

Group size

D

P

D

P

0.336 0.506 0.255 0.651 0.391 0.364

.007 <.0001 ns <.0001 0.002 0.002

0.203 0.312 0.596 0.242 0.504 0.652

ns ns 0.004 ns 0.013 0.002

frugivorous-faunivorous species in South America (53.7%) clearly form the largest guilds in their respective regions. The primates of the four regions also differ in their diversity of group sizes (Fig. 5). At the qualitative level, Africa is the region with the greatest diversity in group sizes. Asia lacks species that form very large groups, i.e. those with more than 50 or so members, even though some species may form large aggregations, consisting of several hundred individuals from several groups (Newton & Dunbar, 1994). The average size of lemur groups is even more reduced; species with more than 15–20 animals per group are lacking entirely in Madagascar. However, a much larger proportion of lemurs is solitary or pair-living, compared to all other regions. South America lacks solitary species and species that form very large groups are rare in the New World. All pairwise comparisons revealed that group sizes of Malagasy primates differ significantly from those in all other regions (Table 3). 80

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Figure 2. Primate activity. The number of ( ) diurnal, ( ) cathemeral and ( ) nocturnal species of African (n = 64), Asian (n = 62), Malagasy (n = 32) and Neotropical (n = 77) primates. The proportion of diurnal and nocturnal species differs significantly across regions due to the large proportion of nocturnal lemurs (see text).

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Mean group size differed significantly across regions (ANOVA of generic means: F3,55 = 3.82, P = 0.015) because lemurs form smaller groups than African and Neotropical primates (Fisher’s PLSD: Africa-Madagascar: 0.505, P = 0.012; Madagascar-South America: 0.633, P < 0.002; all other post hoc comparisons: n.s.). Primate genera in different continents also differed in mean group size after controlling for differences in body size (ANCOVA of generic means: F3,54 = 4.88, P = 0.004; Fig. 6). Relative mean generic group size of New World primates was significantly larger than in their Asian and Malagasy relatives (Fig. 7). Because these comparisons of mean group size may be biased by the lack of solitary species in the New World, we repeated the previous analyses after excluding all solitary genera. Again, regions differed significantly in mean generic group size (F3,40 = 6.15, P = 0.001), due to significant differences between (1) Africa and all other regions and (2) between Madagascar and South America. Finally, because the assumptions of ANCOVA were violated, we compared residual generic group size after leastsquares regression on generic body mass and found significant heterogeneity among regions (F3,40 = 4.42, P = 0.009; Fig. 8), due to significant differences between

Figure 3. Phylogenetic reconstruction of primate activity. The activity pattern of various primate taxa is used to reconstruct character states of common ancestors and to identify instances of evolutionary change. The ancestor of all primates was nocturnal (black). Diurnal (white) and cathemeral (grey) activity evolved several times independently. Equivocal character states are represented by striped branches. Phylogeny is based primarily on patterns of chromosomal evolution (Rumpler & Dutrillaux, 1986).

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Figure 4. Primate diets. The number of primates with predominantly folivorous, folivorous-frugivorous, frugivorous, frugivorous-faunivorous, faunivorous or gummivorous diets in Africa (n = 43), Asia (n = 45), Madagascar (n = 32) and America (n = 54). Small expected values preclude statistical comparison of categories across regions.

Madagascar and America (Fisher’s PLSD: 0.388, P = 0.013), Madagascar and Africa (Fisher’s PLSD: 0.527, P = 0.002) and Asia and Africa (Fisher’s PLSD: 0.366, P = 023).

DISCUSSION

Our intercontinental comparison of independent primate radiations, in which we demonstrated qualitative, as well as quantitative differences in four basic life history and socio-ecological traits, revealed little evidence for convergent evolution. Several explanations for these deviations are possible: either important assumptions of the convergence hypothesis were violated or interactions among our variables, phylogenetic effects or adaptations to other forces prevented or hampered convergent evolution. Assumptions of the convergence hypothesis The convergence hypothesis is based on the assumption that the environments under consideration are highly similar in aspects relevant to the investigated traits. There are some indications that parts of this assumption may be violated in the present case. First, climate and floristic diversity are similar in the habitats of most, but not all primates. While the majority of species inhabits tropical rain forests,

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primates are by no means restricted to this type of habitat (Richard, 1985). However, less humid and more open habitats used by primates exist in all regions. Furthermore, the number of species adapted to ‘untypical’ habitats, such as savannahs, deserts or high mountains, is so small that it is unlikely to affect our broad comparisons. Second, even structurally and climatically similar habitats, such as rain forests, may differ in other characteristics important to the animals. Terborgh & van Schaik (1987), for example, suggested that the lack of strictly folivorous New World monkeys is due to phenological peculiarities of neotropical forests. Based on phenological data from four sites in the Old and New World, they proposed that rhythms of fruiting and flushing are synchronized in the Neotropics, whereas they alternate in African and Asian rainforests. As a result, leaves are not available during periods of fruit scarcity in the New World, making it impossible for primates to specialize on this resource because of metabolic size constraints imposed by the available food. While their general point is well taken, it must be noted that their hypothesis rests solely on phenological data from Barro Colorado Island, Panama, a site not representative of

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Figure 5. Primate group size. The number of species in 7 classes, ranging from solitary animals to groups with more than 100 members, is depicted for Africa (n = 51, median: 14, iqr: 23.5 min.: 1, max.: 115), Asia (n = 49, median: 8, iqr: 16.8, min.: 1, max.: 50), America (n = 57, median: 7.2, iqr: 11.6, min.: 2.7, max.: 60) and Madagascar (n = 32, median: 2.5, iqr: 3.6, min.: 1, max.: 15.3).

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Figure 6. Body and group size of primates. The mean group size of African (s), Asian (n), Malagasy (G) and Neotropical primates (h) belonging to the same genus is plotted against their mean body size. Ignoring likely additional phylogenetic effects, body mass accounts for 32.8% of the variation in group size (F1,57 = 27.8, P < 0.0001, r = 0.57, n = 59) across all primates at this level. Note: means for Macaca based on Asian species only; Macaca sylvanus was omitted.

other Neotropical areas (cf. Roosmalen, 1985; Peres, 1994a). A similar argument has been advanced to explain the paucity of frugivores on Madagascar (S. Goodman, personal communication). Third, in a comparison of African and Neotropical floras, Gentry (1993) found that Africa has overall fewer plant species than South America, but that they usually have larger ranges than South American species. This difference may have

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Figure 7. Group size variation among primate genera. The least squares means ( ± SE) of relative group size of Malagasy (n = 14), Asian (n = 12), African (n = 17) and American (n = 16) genera. Differences between Madagascar and America (t = 3.33, P = 0.002) and between Asia and America (t = 3.02, P = 0.004) are significant.

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Figure 8. Group size variation among non-solitary primate genera. Mean residual group size ( ± SE) of Malagasy (n = 8), Asian (n = 9), African (n = 11) and American (n = 16) genera of group-living species. See text for post hoc comparisons.

consequences for niche separation of sympatric plant consumers. In Africa, with a typically smaller number of different food species available, dietary overlap should be high and separation should occur with respect to the plant parts eaten, whereas sympatric Neotropical consumers may feed on the same plant parts, but from different species. This floristic difference between regions may contribute to the observed differences in feeding strategies between African and Neotropical primates, and similar mechanisms may contribute to the divergence among the other groups. Fourth, a comparison of fruit size between the Old World and New World tropics revealed that fruits were larger in the Paleotropics, apparently an adaptation to the size of frugivorous seed dispersers (Mack, 1993). There is indeed a trend towards larger frugivorous vertebrates in the Old World (Fleming, Breitwisch & Whitesides, 1987), but the causes of this pattern are unclear. One possibility is that aspects of vegetation structure account for this divergence between frugivores. For example, trees are linked by many lianas in Africa, compared to an intermediate number in South America and very few in tropical Asia (Emmons & Gentry, 1983). These structural differences seem to affect locomotor styles of arboreal vertebrates, but, because the size distributions of African and Asian primates are similar to each other and both differ from South America, this aspect of vegetation structure cannot explain the observed size differences among primates. Tree size and density may therefore be more relevant. Gentry (1993) also described a greater prevalence of very large trees in Africa and a higher density of smaller trees in South America. If larger trees can support larger animals, this difference may account for the divergence of primate size distributions between Africa and South America. However, more long-term data on tree phenology, forest structure and other abiotic factors from different regions (cf. van Schaik, Terborgh & Wright, 1993) are clearly necessary to further evaluate these particular hypotheses, as well as the general assumptions concerning abiotic similarities of primate habitats.

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Finally, there may be inherent differences in testing convergence because of difficulties in formulating realistic predictions. Because the exact starting points and conditions of different taxa are not known, we cannot reconstruct evolutionary trajectories, which are necessary for a deep understanding of adaptation (Harvey & Pagel, 1991), even though incorporating information about fossils may partly resolve this problem. Thus, we cannot exclude the possibility that some groups are still on their way towards convergence with other groups. On the other hand, how should we measure or test anything less than total convergence? Similar studies of taxa with longer separate evolutionary histories may reveal how general or fundamental this problem is. Interactions among variables By comparing single variables between primates of the four geographical regions we did not consider known or potential interactions and relationships among variables, making our tests both rigorous and naive. An examination of all pairwise relationships among variables revealed, however, that our main conclusions are not affected by existing inter-dependencies among variables. As expected, body size (mass) is most closely associated with the other variables, such as diet (Clutton-Brock & Harvey, 1977). For example, it is well established that body size sets a lower limit for folivory and an upper limit for insectivory in primates (Kay, 1984) and other mammals (McNab, 1986). It has therefore been argued that the Neotropics lack folivorous primates because there are no large primates there (Terborgh & van Schaik 1987). This does not explain the absence of large species, however. It should be noted in passing that several, yet untested hypotheses on this issue have been proposed (Peres, 1994b), and some recent evidence indicates that at least one primate larger than 15 kg existed in the New World (Hartwig, 1995). Furthermore, the other primate radiations do not vary significantly in body size, yet they exhibit differences in dietary adaptations. Thus, body size can only explain part of the variation in feeding adaptations among the four primate radiations. Similarly, there is a well known positive correlation between body size and group size across primates (Clutton-Brock & Harvey, 1977; Terborgh & Janson, 1986). However, this size effect can explain neither the qualitative peculiarity of Neotropical primates, nor the quantitative differences in group size between lemurs and other radiations. First, the lack of solitary species in South America is puzzling because they are on average smaller than other primates. Activity obviously exerts a more important effect on group size than body size because group-living offers benefits to small diurnal species in terms of reduced predation risk (van Schaik, 1983). The only solitary diurnal primate (the orang-utan, Pongo pygmaeus) is probably largely immune from predation because of its large size (Cheney & Wrangham, 1987; Rodman & Mitani, 1987). Thus, we should ask more precisely why there are no nocturnal solitary platyrrhines. Phylogenetic, anatomical and size constraints cannot be invoked in answering this question because nocturnal activity has evolved secondarily in a small New World primate (genus Aotus). Interspecific competition with non-primate species (see below) may provide one explanation, which is difficult to test, however. Alternatively, life history inertia related to infant development and parental care may make a change from a non-solitary to a solitary lifestyle impossible (van Schaik & Kappeler, 1993).

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Second, the small group size of Malagasy primates is also not a result of their small body size, because differences in mean group size between lemurs and most other primates persist after statistically controlling for the effects of size. In addition, Madagascar harbours proportionally more solitary species than the other continents. This idiosyncracy of lemur social organization may be related to other unusual social traits of this radiation, such as even adult sex ratios, lack of sexual dimorphism, female dominance and intolerance among relatives (Richard, 1987; Kappeler, 1990; Richard & Dewar, 1991; Kappeler, 1993a,b; Pereira, 1993; van Schaik & Kappeler, 1993). Ultimately, lemur group size may be constrained by ecological factors, such as strong seasonality of food availability (Richard & Dewar, 1991) or the size of feeding patches. Crown diameters of primate feeding trees, for example, are much smaller in Madagascar than in Peru (Terborgh, 1983; Ganzhorn, 1988; see also Gentry 1993), but the currently possible comparisons are confounded by important differences between sites, such as altitude. In conclusion, body size can clearly not account for the most striking difference in group size among the four primate radiations. The relationship between size and activity is less clear-cut. Size constraints seem to influence activity, as evidenced by the observation that all but one nocturnal species (Daubentonia madagascariensis) weigh less than about 1.5 kg, but some subfossil nocturnal lemurs may have been even larger than the extant aye-aye (Kay, 1984; Martin, 1990; Simons, 1994) and most neotropical primates weighing less than 1 kg are diurnal. Differences in the proportion of species with different activity patterns among the four radiations are therefore also not caused by size differences. In summary, the effects of body size on variation in activity, diet and group size are not pervasive enough to account for the observed patterns of nonconvergence because qualitative and quantitative differences in these traits exist among these four radiations independent of body size. Furthermore, at least one other evolutionary force must be invoked to explain the observed size differences among radiations, so that body size alone cannot explain the observed pattern. The relationship between the other pairs of variables is so loose that potential interactions among them are unlikely causes of nonconvergence. For example, at least one species can be found to represent almost every possible combination of the character states of the discrete variables activity and diet. Similarly, for each dietary category, there is at least one example from solitary, pair-living, and group-living species, suggesting that there are no interactions among these traits, either. Only activity seems to affect group size; the formation of groups larger than family units is apparently hampered by nocturnal activity (van Schaik, 1983). The possible effects of other basic life history traits on primate social systems have recently been discussed elsewhere (van Schaik & Kappeler, 1993; Dunbar 1995). In summary, then, it is unlikely that differences among the four primate radiations in these traits are due to size constraints or tight inter-dependencies among the other traits under investigation. Phylogeny Phylogenetic inertia (Wilson, 1975), either as a result of traits specific to suborders or of founder effects, may be responsible for the lack of convergence (Clutton-Brock & Harvey, 1977). However, body size is not principally constrained by such forces.

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The basic Bauplan of strepsirhine and haplorhine primates allows for the same degree of variability. Even though haplorhines are on average larger than strepsirhines, both the smallest and the largest known primates are strepsirhines (Tattersall, 1993; Schmid & Kappeler, 1994). Similarly, even though most strepsirhines are nocturnal and the majority of haplorhines are diurnal, activity is not fixed within the two primate suborders. In Malagasy lemurs, diurnal activity evolved several times independently, and in South America, nocturnal activity evolved secondarily in Aotus from a diurnal ancestor. Furthermore, despite some clear dietary specializations at the family level (e.g. Bearder, 1987; Goldizen, 1987; Davies & Oates, 1994), there is no basic difference in feeding adaptations between the two suborders. Finally, group size is also not principally determined by phylogenetic factors because solitary, pair- and groupliving species are found in both suborders. At best, haplorhines could be characterized as non-solitary animals, since there is only one exception, the orangutan (Pongo pygmaeus). Thus, even though the four primate groups differ in their taxonomic composition, phylogenetic inertia associated with the divergence between strepsirhine and haplorhine primates is not responsible for the observed patterns of nonconvergence because both subgroups display the full diversity of variation in all traits. Furthermore, qualitative idiosyncracies of the Malagasy and Neotropical primate radiations can not be explained as the result of founder effects for the same reasons. Adaptation to biotic factors Even if the majority of primate habitats were characterized by similar abiotic features, they may differ in aspects of community structure that affect primate adaptations. Competition with other taxa and differences in predation pressure, in particular, may influence the availability of particular niches for primates. The possible role of stochastic ecological processes is difficult to evaluate, because the associated hypotheses are difficult to falsify (Kappeler & Ganzhorn, 1994). Competition with arboreal mammals is one likely mechanism influencing primate diversity (Bourliere, 1985). For example, it has been suggested that marsupials occupied the nocturnal mammal niches in the Neotropics before the arrival of primates, thereby hampering the evolution of nocturnal primates there (Fleming et al., 1987). On the other hand, the biomass of primates frequently equals or exceeds that of all other aboreal mammals combined (Emmons, Gauther-Hion & Dubost, 1981; Terborgh, 1983; Terborgh & van Schaik, 1987), suggesting that primates can successfully compete with other mammals. Frugivorous primates are primarily affected by competition with birds (Fleming et al., 1987) and possibly bats. Similarly, folivory in New World primates may be limited by competition with sloths (Bourliere, 1985) and possibly leaf-cutting ants (Rockwood & Glander, 1979), and an analogous explanation may exist for the lack of gummivorous primates in Asia. Crude predictions of this competition hypothesis could be tested by comparing populations of potentially competing taxa in different habitats, ideally including areas in which either primates or their potential competitors are lacking. Vulnerability to predators depends on size, activity, habitat choice and the presence and/or diversity of predators. The risk of predation in a given environment may be minimal at several adaptive peaks, defined by particular combinations of the

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above-mentioned variables and certain behavioral strategies, such as crypsis or gregariousness (Clutton-Brock & Harvey, 1977; van Schaik, 1983). Because the presence or absence of certain predators can have relative short-term effects on activity and grouping patterns of primates (van Schaik & Kappeler, 1993; Goodman, 1994; van Schaik & H¨orstermann, 1994), broad differences among primate radiations in these traits may reflect adaptive responses to different types and intensities of predation pressure. This hypothesis can be tested by comparing intraand interspecific variation in the crucial variables in the presence and (induced) absence of certain predators (cf. Isbell & Young, 1993; Alcover & McMinn, 1994; van Schaik & H¨orstermann, 1994). Finally, the level of our comparison may have been too coarse. Convergences in some variables, such as feeding strategies, may be more pronounced among sympatric sets of species, because most habitats seem to include a limited number of primate niches, e.g. for one small and one large frugivore, etc. (Terborgh, 1983; Robinson & Janson, 1987; Gauthier-Hion, 1988a; Ganzhorn, 1989; Bennett & Davies, 1994). Comparisons among individual sites may therefore reveal that the 5–10 primate species co-occurring in most localities may occupy similar niches at a given site and differ less in aspects of life history and socioecology than all members of the different radiations. Differences in continental and local diversity may therefore partly reflect inter-continental differences in primate habitat availability and or use (cf. Reed & Fleagle, 1995). Developing suitable criteria and methods (see Schluter, 1986; Medel, 1995) for comparing local primate diversity across continents should therefore be an important goal for future studies of primate evolutionary ecology.

Conclusions The four geographically independent primate groups exhibit qualitative and quantitative differences in fundamental aspects of life history and socio-ecology. Our analyses indicate that these examples of nonconvergence are neither the result of founder effects, nor of associated phylogenetic or allometric constraints or interdependencies among these particular variables, but fully phylogenetic analyses might modify some of these conclusions, once appropriate methods become available. Rather than rejecting the convergence hypothesis based on this evidence, we identify adaptive hypotheses concerning ecological mechanisms that may have contributed to the observed pattern of inter-specific variation across continents and propose several testable hypotheses. They could provide a Darwinian explanation for nonconvergence and contribute to a more comprehensive understanding of primate evolution.

ACKNOWLEDGEMENTS

We thank John Fleagle, J¨org Ganzhorn, Barbara K¨onig, Hans-J¨urg Kuhn, Andy Purvis, Carel van Schaik and an anonymous reviewer for helpful comments on this manuscript and for many stimulating discussions.

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APPENDIX

Primate data base. This table summarizes published information on primate body mass (BM), group size (GS), activity, diet, taxonomy (Genus, Species, Subspecies [#SSP]) and distribution (REG). Within regions, genera and species are ordered alphabetically. BM refers to the mean body mass of adult non-pregnant females in the vast majority of species. Midpoints of ranges or other reliable estimates were accepted to increase sample size; see references for details. Recently extinct subfossil Malagasy lemurs are included and identified by *. GS refers to counts or precise estimates of all individuals in at least one group. Activity is either diurnal (D), nocturnal (N) or cathemeral (C). If possible, species were classified as being primarily frugivorous (Fr), folivorous (Fo), faunivorous (Fa), gummivorous (G) or as belonging to one of the possible combinations of these classes. #SSP denotes the number of recognized subspecies within a species, following recent taxonomic reviews (e.g. Gauthier-Hion et al., 1988; Davies & Oates 1994); monotypic species were scored as 0. Whenever two references are given, the first refers to BM and the second one to GS. Whenever BM or GS were calculated from several sources, only the most recent reference is provided, but a complete list is available from the authors upon request. Additional information was taken primarily from Kappeler & Ganzhorn (1993, 1994), Harcourt & Thornback (1990), Gauthier-Hion et al. (1988), Smuts et al. (1987), Davies & Oates (1994) and references therein. Genus

Species

BM

GS ACT DIET #SSP REG

Allenopithecus Arctocebus

nigroviridis calabarensis

3250 298

40 1

Cercocebus

albigena

5350 16.6 D

aterrimus atys galeritus torquatus

5638 D 6200 35 D 5662 18.3 D 5500 26.8 D

aethiops

2980 28.9 D Fr/Fo

albogularis ascanius campbelli cephus diana dryas erythrogaster erythrotis hamlyni l’hoesti mitis mona neglectus nictitans petaurista pogonias preussi pygerythrus sabaeus salongo solatus tantalus wolfi angolensis guereza polykomos

D 12 2790 26.3 D Fr/Fo 5 2700 14 D 2 2900 11 D Fr 2 3900 23 D Fr/Fa 2 2250 D 0 D 0 D 3 3361 D 2 3500 17.4 D Fr/Fo 0 3830 16.3 D Fr/Fo 8 2500 D Fr/Fo 0 3550 5 D Fr/Fo 0 3650 16 D Fr/Fo 3 2900 14 D 2 3030 15 D Fr 3 5 D 2 3000 D 14 D 0 D 0 10 D 0 3585 D 3 2760 D 4 6300 10.9 D Fr/Fo 8 9200 8.3 D Fr/Fo 8 8300 10.2 D Fo 2

satanas

9500 15.5 D

vellerosus

6900

Cercopithecus

Colobus

16

D N Fr/Fa

0 2

Fr

2

Fr Fr

2 0 3 2

Fr

D Fr/Fo

4

0 0

References

AFR Colyn, 1994; Gauthier-Hion, 1988a AFR Kappeler, 1991; Charles-Dominique, 1977 AFR Gevaerts, 1992; Melnick & Pearl, 1987 AFR Colyn, 1994 AFR Oates et al., 1990 AFR Colyn, 1994; Melnick & Pearl, 1987 AFR Harvey, Martin & Clutton-Brock, 1987; Melnick & Pearl, 1987 AFR Turner, Anapol & Jolly, 1994; Fedigan & Fedigan, 1988 AFR AFR Gevaerts, 1992; Cords, 1987 AFR Oates et al., 1990 AFR Gauthier-Hion, 1988b; Cords, 1987 AFR Oates et al., 1990; Cords, 1987 AFR Colyn, 1994 AFR AFR AFR Colyn, 1994 AFR Gevaerts, 1992; Cords, 1987 AFR Gevaerts, 1992; Cords, 1987 AFR Harvey et al., 1987 AFR Gevaerts, 1992; Cords, 1987 AFR Gevaerts, 1992; Cords, 1987 AFR Oates et al., 1990 AFR Gauthier-Hion, 1988b; Cords, 1987 AFR Gauthier-Hion, 1988a AFR Harvey et al., 1987 AFR AFR AFR Gauthier-Hion, 1988a AFR Colyn, 1994 AFR Gevaerts, 1992 AFR Gevaerts, 1992; Oates, 1994 AFR Oates et al., 1990 AFR Oates et al., 1990; van Schaik & Hörstermann, 1994 AFR Oates et al., 1990; van Schaik & Hörstermann, 1994 AFR Oates et al., 1990

322

P. M. KAPPELER AND E. W. HEYMANN APPENDIX. Continued

Genus

Species

BM

GS ACT DIET #SSP REG

Erythrocebus Euoticus Galago

patas elegantulus gallarum matschiei moholi

6000 293 210 155

28 1 1 1 1

D N N N N

4 2 0 0 0

AFR AFR AFR AFR AFR

senegalensis alleni

206 300

1 1

N Fr/Fa/G 5 N Fr/Fa 0

AFR AFR

demidovii

69

1

N Fr/Fa

4

AFR

Gorilla

thomasi zanzibaricus gorilla

100 136 93000

1 1 7

N Fr/Fa N Fr/Fa D Fo

0 2 3

AFR AFR AFR

Macaca

sylvanus

10000 18.3 D Fr/Fo

0

AFR

Miopithecus

talapoin

1120 115

D Fr/Fa

0

AFR

Otolemur

crassicaudatus garnettii

1242 1028

N Fr/Fa/G 4 N Fr/Fa 4

AFR AFR

Pan

paniscus

32880 85

D Fr/Fo

0

AFR

troglodytes

31000 60

D Fr/Fo

3

AFR

anubis

12000 40

D

0

AFR

cynocephalus

15000 55.4 D Fr/Fo

2

AFR

hamadryas leucophaeus papio sphinx ursinus

9400 10000 13000 11500 16800

0 2 0 0 0

AFR AFR AFR AFR AFR

3

AFR

Galagoides

Papio

1 1

7.3 17

D D D 13.9 D 57.1 D

Fo Fr

Perodicticus

potto

989

Procolobus

badius verus

8200 34 4200 6.3

D Fr/Fo 14 D Fo 0

AFR AFR

Theropithecus Hylobates

gelada agilis concolor gabriellae hoolock klossii lar leucogenys moloch muelleri pileatus syndactylus tardigradus

13600 10 5700 4.4 5800 4

D D D D D D D D D D D D N

AFR ASI ASI ASI ASI ASI ASI ASI ASI ASI ASI ASI ASI

arctoides assamensis brunnescens cyclopis

8000 6700

Loris Macaca

1

Fr/Fa G/Fa Fr/Fa Fr/Fa Fr/Fa/G

6500 3.6 5900 3.6 5300 3.9 5700 3.3 3.4 3.5 10600 3.6 193 1

N Fr/Fa

D D D 20.2 D 21

Fr Fr/Fo Fr/Fo Fr/Fo Fr/Fo Fr/Fo Fr/Fo Fr/Fo Fr/Fo Fr/Fo Fr/Fa

0 3 6 0 2 0 5 2 0 3 0 2 6 2 2 0 0

References Butynski, 1988; Cords, 1987 Charles-Dominique, 1977 Nash, Bearder & Olsson, 1989 Nash et al., 1989 Kappeler, 1991; Bearder & Doyle, 1974 Nash et al., 1989 Kappeler, 1991; Charles-Dominique, 1977 Kappeler, 1991; Charles-Dominique, 1977 Nash et al., 1989 Harcourt & Nash, 1986 Harvey et al., 1987; Stewart & Harcourt, 1987 Harvey et al., 1987; Melnick & Pearl, 1987 Gauthier-Hion, 1988b; Melnick & Pearl, 1987 Kappeler, 1991; Clark, 1985 Kappeler, 1991; Nash & Harcourt, 1986 Plavcan & van Schaik, 1992; Nishida & Haraiwa-Hasegawa, 1987 Harvey et al., 1987; Nishida & Haraiwa-Hasegawa, 1987 Harvey et al., 1987; Melnick & Pearl, 1987 Harvey et al., 1987 Melnick & Pearl, 1987 Harvey et al., 1987; Stammbach, 1987 Harvey et al., 1987; Stammbach, 1987 Harvey et al., 1987 Harvey et al., Stammbach, 1987 Harvey et al., 1987; Melnick & Pearl, 1987 Kappeler, 1991; Charles-Dominique, 1977 Oates et al., 1990; Oates, 1994 Oates et al., 1990; van Schaik & Hörstermann, 1994 Harvey et al., 1987; Stammbach, 1987 Harvey et al., Cowlishaw, 1992 Harvey et al., Cowlishaw, 1992 Harvey et al., 1987; Cowlishaw, 1992 Harvey et al., 1987; Cowlishaw, 1992 Harvey et al., 1987; Cowlishaw 1992

Harvey et al., 1987; Cowlishaw, 1992 Cowlishaw, 1992 Cowlishaw, 1992 Harvey et al., 1987; Cowlishaw, 1992 Kappeler, 1991; Petter & Hladik, 1970 ASI Harvey et al., 1987 ASI Fooden 1986, 1988 ASI ASI Kawamura, Norikoshi & Azuma, 1991

NONCONVERGENCE IN PRIMATE EVOLUTION

323

APPENDIX. Continued Genus

Nasalis Nycticebus Pongo Presbytis Presbytis

Species

BM

GS ACT DIET #SSP REG

fascicularis

4100

27

D

fuscata

9100

45

D Fr/Fo

2

hecki maura mulatta

5100 3000

36

D D D

Fr

0 0 3

nemestrina

7800 18.3 D

Fr

3

nigra nigrescens ochreata radiata silenus

6600

D Fr/Fo D D 3850 24.9 D Fr 5000 26.5 D Fr/Fa

0 0 0 2 0

sinica thibetana tonkeana larvatus

3170 21.6 D Fr 10100 21 D Fr D 10000 10.5 D Fr/Fo

2 0 0 0

coucang pygmaeus pygmaeus

1195 376 37000

N Fr/Fa N Fr/Fa D Fr/Fo

4 0 2

D D D

2 0 3

Fr

35

1 1 1 6.5

19

comata frontata hosei

5700

melalophos

5800 11.6 D Fr/Fo 17

potenziani

6400 3.7

D Fr/Fo

2

rubicunda

5700 6.5

D Fr/Fo

5

thomasi avunculus bieti

6000

8

9000

50

D D D

Fo

3 0 0

brelichi nemaeus

6.1 4100 9.3

D D

Fo Fo

0 2

Semnopithecus

roxellana entellus

11600` 12000 25

Simias

concolor

7100 4.5

D

Fo

0

Tarsius

bancanus

127

1

N

Fa

2

dianae pumilis spectrum syrichta

110

1 1 2.5 1

N N N N

Fa Fa Fa Fa

0 0 0 0

auratus cristatus

11 D 5700 22.8 D

Fo Fo

0 7

francoisi geei

D 9500 12.5 D

Fo

6 0

Pygathrix

Trachypithecus

195 117

7

D Fr/Fo 0 D Fr/Fo 15

References

ASI Harvey et al., 1987; Melnick & Pearl, 1987 ASI Harvey et al., 1987; Melnick & Pearl, 1987 ASI ASI Harvey et al., 1987 ASI Harvey et al., 1987; Melnick & Pearl, 1987 ASI Harvey et al., 1987; Melnick & Pearl, 1987 ASI Harvey et al., 1987; Groves, 1980 ASI ASI ASI Fooden, 1986, 1988 ASI Harvey et al., 1987; Kurup & Kumar, 1993 ASI Fooden, 1986, 1988 ASI Fooden, 1986, 1988 ASI ASI Oates, Davies & Delson, 1994; Bennett & Davies, 1994 ASI Kappeler, 1991; Bearder, 1987 ASI Kappeler, 1991; Bearder, 1987 ASI Harvey et al., 1987; Rodman & Mitani, 1987 ASI Bennett & Davies, 1994 ASI ASI Davies, 1994; Newton & Dunbar, 1994 ASI Oates et al., 1994; Bennett & Davies, 1994 ASI Oates et al., 1994; Bennett & Davies, 1994 ASI Oates et al., 1994; Newton & Dunbar, 1994 ASI Davies, 1994; Newton & Dunbar, 1994 ASI ASI Oates et al., 1994; Newton & Dunbar, 1994 ASI Newton & Dunbar, 1994 ASI Chivers, 1994; Newton & Dunbar, 1994 ASI Jablonski & Ruliang, 1995 ASI Oates et al., 1994; Newton & Dunbar, 1994 ASI Oates et al., 1994; Bennett & Davies, 1994 ASI Kappeler, 1991; Crompton & Andau, 1987 ASI Tremble, Muskita & Supriatna, 1993 ASI Musser & Dagosto, 1987 ASI Mackinnon & Mackinnon, 1980 ASI Kappeler, 1991; Haring & Wright, 1989 ASI Bennett & Davies, 1994 ASI Oates et al., 1994; Bennett & Davies, 1994 ASI ASI Oates et al., 1994; Bennett & Davies, 1994

324

P. M. KAPPELER AND E. W. HEYMANN APPENDIX. Continued

Genus

Species

BM

GS ACT DIET #SSP REG

johnii

10900 14.8 D

obscurus

6600

phayrei

6900 12.9 D

Fo

3

pileatus

10000 8.5

D

Fo

5

vetulus

5900 8.8

D Fr/Fo

4

85 1 197500 24500 13900 1316 2.5

N Fr/Fa

0

Avahi

trichotis fontoynonti* edwardsi* majori* laniger

N

Fo

0

occidentalis radofilai* major

875 2.5 16200 443 1

N

Fo

0

Babakotia Cheirogaleus

medius madagascariensis robusta* coronatus fulvus macaco mongoz rubriventer

282 2516 13500 1687 2397 2487 1658 2139

Hadropithecus Hapalemur

stenognathus* aureus

16700 1500

Indri

griseus simus indri

892 2.6 1300 8 6250 3.1

Allocebus Archaeoindris Archaeolemur

Daubentonia Eulemur

17

Fo

D Fr/Fo

7

N Fr/Fa

2

N Fr/Fa N Fr/Fa

0 0

8.4 9.2 8.4 3.5 3.2

C C C C C

Fr/Fo Fr/Fo Fr/Fo Fr/Fo Fr/Fo

0 6 2 0 0

3

C

Fo

0

C C D

Fo Fo Fo

3 0 0

1 1

catta 2678 15.3 D Fr dorsalis 1 N Fo edwardsi 1 N Fo leucopus 544 1 N Fo microdon 1 N Fo mustelinus 594 1 N Fo ruficaudatus 845 1 N Fo septentrionalis 1 N Fo Megaladapis edwardsi* 75400 grandidieri* madagascariensis* 38000 Mesopropithecus dolichobrachion* 10600 globiceps* 9400 pithecoides* 9700 Microcebus murinus 57 1 N Fr/Fa myoxinus 31 1 N Fr/Fa rufus 49 1 N Fr/Fa Mirza coquereli 263 1 N Fr/Fa Pachylemur insignis* 10000 jullyi* 12800 Palaeopropithecus ingens* 39500 maximus* 52600 Phaner furcifer 328 2.5 N G Lemur Lepilemur

0

0 0 0 0 0 0 0 0

0 0 0 0

4

References

ASI Oates et al., 1994; Bennett & Davies, 1994 ASI Oates et al., 1994; Bennett & Davies, 1994 ASI Oates et al., 1994; Bennett & Davies, 1994 ASI Oates et al., 1994; Bennett & Davies, 1994 ASI Oates et al., 1994; Newton & Dunbar, 1994 MAD Meier & Albignac, 1991 MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Glander et al., 1992; Ganzhorn, Abraham & RazanahoeraRakotomalala, 1985 MAD Kappeler, 1991; Albignac, 1981a MAD Godfrey et al., 1995 MAD Kappeler, 1991; Petter, Albignac & Rumpler, 1977 MAD Kappeler, 1991; Petter, 1988 MAD Glander, 1994; Sterling, 1993 MAD Godfrey et al., 1995 MAD Kappeler, 1991; Wilson et al., 1989 MAD Kappeler, 1991; Sussman, 1974 MAD Kappeler, 1991; Andrews, 1990 MAD Kappeler, 1991; Tattersall, 1976 MAD Kappeler, 1991; Dague & Petter, 1988 MAD Godfrey et al., 1995 MAD Glander et al., 1992; Wright et al., 1986 MAD Kappeler, 1991; Pollock, 1986 MAD Meier et al., 1987; Wright et al., 1986 MAD Stephan & Bauchot, 1965; Pollock, 1975 MAD Kappeler, 1991; Sussman, 1991 MAD Petter et al., 1977 MAD Albignac, 1981b MAD Russell, 1977 MAD Petter et al., 1977 MAD Ratsirarson & Rumpler, 1988 MAD Kappeler, 1991 MAD Ratsirarson & Rumpler, 1988 MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Schmid & Kappeler, 1994 MAD Schmid & Kappeler, 1994 MAD Harcourt, 1987 MAD Kappeler, unpubl. data MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Godfrey et al., 1995 MAD Kappeler unpubl. data; CharlesDominique & Petter, 1980

NONCONVERGENCE IN PRIMATE EVOLUTION

325

APPENDIX. Continued Genus

Species

BM

Propithecus

diadema

5895 5.1

D

Fo

tattersalli verreauxi

3167 4.1 3696 6.0

D D

Fo Fo

variegata belzebul caraya

3512 5.3 5525 7.4 4605 8.9

D Fr D D Fr/Fo

coibensis fusca palliata

5.2 D 4550 6.8 D Fr/Fo 4020 13.7 D Fr/Fo

pigra

6434 5.4

D

seniculus

5300 8.0

D Fr/Fo

azarae brumbacki infulatus lemurinus miconax nancymae nigriceps trivirgatus vociferans

780 455

Ateles

belzebuth

8466 22.0 D Fr/Fo

Brachyteles

fusciceps geoffroyi paniscus arachnoides

8800 D 6700 42.0 D Fr/Fo 8590 38.5 D Fr/Fo 8375 19.2 D Fr/Fo

calvus melanocephalus brunneus caligatus cupreus

2880 30.0 D Fr 2740 30.0 D Fr 805 4.0 D Fr/Fo D 1119 3.1 D Fr/Fo

Varecia Alouatta Alouatta

Aotus

Cacajao Callicebus

859 780 930

GS ACT DIET #SSP REG

4.1 N/C Fr/Fo N N N N 4.0 N 3.3 N Fr/Fa N 3.3 N

donacophilus modestus moloch oenanthe olallae personatus

1285 3.7

D D D D D D Fr/Fo

torquatus

1265 4.0

D Fr/Fa

Callimico Callithrix

goeldii argentata

582 360

7.7 9.5

D Fr/Fa D Fr/Fa

429

6.0 9.8

Cebuella Cebus

aurita flaviceps geoffroyi humeralifer jacchus kuhli penicillata pygmaea albifrons

Fr/Fa G/Fa Fr/Fa Fr/Fa G/Fa Fr/Fa G/Fa G/Fa Fr/Fa

860

D D 190 D 380 11.5 D 236 8.4 D 375 D 182 7.3 D 122 5.7 D 1814 16.8 D

4

References

MAD Glander et al., 1992; Meyers & Wright, 1993 0 MAD Kappeler, 1991; Meyers, 1993 4 MAD Kappeler, 1991; Richard, Rakotomanga & Schwartz, 1991 2 MAD Kappeler, 1991; Morland, 1991 4 SA Peres, 1994a; Bonvicino, 1989 0 SA Peres, 1994a Thoringron, Ruiz & Eisenberg, 1984 2 SA Milton & Mittermeier, 1977 2 SA Peres, 1994a; Mendes, 1989 3 SA Glander et al., 1991; Fedigan, Fedigan & Chapman, 1985 0 SA Peres, 1994a; Horwich & Gebhard, 1983 0 SA Peres, 1994a; Crockett & Eisenberg, 1987 2 SA Ford & Davis, 1992; Wright, 1985 0 SA Hernandez-Camacho & Defler, 1985 0 SA 2 SA Hernandez-Camacho & Defler, 1985 0 SA 0 SA Aquino & Encarnacion, 1986 0 SA Wright, 1978 0 SA Ayres, 1986 0 SA Aquino, Puertes & Encarnacion, 1990 3 SA Rosenberger & Strier, 1989; Robinson & Janson, 1987 2 SA Ford & Davis, 1992 9 SA Fedigan et al., 1988; Chapman, 1990 2 SA Ayres, 1986; Symington, 1987 0 SA Lemos de Sa & Glander, 1993; Strier et al., 1993 4 SA Ayres, 1986 2 SA Ayres, 1986; Cunha & Barrett, 1989 0 SA Ford & Davis, 1992; Wright, 1985 0 SA 3 SA Ford & Davis, 1992; Robinson, Wright & Kinzey, 1987 0 SA 0 SA 0 SA Ford & Davis, 1992 0 SA 0 SA 3 SA Ford & Davis, 1992; Kinzey & Becker, 1983 3 SA Hernandez-Camacho & Defler, 1985; Defler, 1983 0 SA Ross, 1991; Buchanan-Smith, 1990a 3 SA Ayres, 1986; Stallings & Mittermeier, 1983 0 SA Muskin, 1984 0 SA Ferrari & Lopez-Ferrari, 1989 0 SA Ford & Davis, 1992 3 SA Ayres, 1986; Rylands, 1982 0 SA Ford & Davis, 1992; König, 1992 0 SA Ford & Davis, 1992 0 SA Ford & Davis, 1992; Faria, 1986 0 SA Soini, 1988; Soini & Soini, 1990a 13 SA Ford & Davis, 1992; Soini, 1986

326

P. M. KAPPELER AND E. W. HEYMANN APPENDIX. Continued

Genus

Species

BM

Chiropotes

apella capucinus olivaceus albinasus satanas flavicauda lagotricha

2450 2283 2395 2520 2660

11.1 21.0 17.1 22.5 9.7 9.1 5750 16.7

D D D D D D D

Fr/Fa Fr/Fa Fr/Fa Fr Fr Fr/Fo Fr/Fo

5 0 0 0 3 0 4

SA SA SA SA SA SA SA

caissara chrysomelas chrysopygus

572 535 615

6.7 3.6

D D Fr/Fa D Fr/Fa

0 0 0

SA SA SA

rosalia

598

7.2

D Fr/Fa

0

SA

aequatorialis albicans irrorata

4.6 1875 4.4

D D Fr/Fo D

0 0 2

SA SA SA

monachus pithecia bicolor fuscicollis geoffroyi imperator inustus labiatus

2170 1590 430 348 507 450 803 515

D D D D D D D D

Fr/Fo 2 Fr/Fo 2 Fr/Fa 3 Fr/Fa 13 Fr/Fa 0 Fr/Fa 2 0 Fr/Fa 2

SA SA SA SA SA SA SA SA

leucopus midas mystax nigricollis oedipus tripartitus boliviensis oerstedi sciureus ustus vanzolinii

490 520 530 460 430

0 2 3 3 0 0 5 2 4 0 0

SA SA SA SA SA SA SA SA SA SA SA

Lagothrix Leontopithecus

Pithecia

Saguinus

Saimiri

GS ACT DIET #SSP REG

4.0 2.7 6.7 5.1 6.9 6.0 6.3

D D D D D D 751 60.0 D 600 50.0 D 810 35.0 D 795 D 650 40 D 6.4 5.5 6.3 7.2

Fr/Fa Fr/Fa Fr/Fa Fr/Fa Fr/Fa Fr/Fa Fr/Fa Fr/Fa Fr/Fa

References Ayres, 1986; Soini, 1986 Glander et al., 1991; Mitchell, 1989 Ford & Davis, 1992; Robinson, 1988 Ayres, 1981 Ayres, 1981, 1986 Robinson & Janson, 1987 Ford & Davis, 1992; Stevenson, Quinones & Ahumada, 1994 Lorini & Persson, 1990 Ford & Davis, 1992; Rylands, 1982 Ford & Davis, 1992; Carvalho & Carvalho, 1989 Dietz, Baker & Miglioretti, 1994; Kleinman et al., 1986 Peres, 1993 Ford & Davis, 1992; BuchananSmith, 1990b Ayres, 1986; Soini, 1988 Oliveira et al., 1985 Ford & Davis, 1992; Egler, 1986 Soini, 1990; Goldizen et al., 1996 Dawson, 1977 Ford & Davis, 1992; Terborgh, 1983 Hernandez-Camacho & Defler, 1985 Snowdon & Soini, 1988; BuchananSmith, 1990a Hernandez-Camacho & Defler, 1985 Ayres, 1986; Saxton & Evans, 1984 Soini & Soini, 1982, 1990b Ayres, 1986; Izawa, 1978 Neyman, 1977 Mitchell, Boinski & van Schaik, 1991 Boinski, 1989; Mitchell et al., 1991 Ayres, 1986; Soini, 1986 Ford & Davis, 1992 Ayres, 1985