AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 88411413 11992)
Feeding Adaptations in New World Primates: An Evolutionary Perspective: Introduction PAUL A. GARBER AND WARREN G . KINZEY Department of Anthropology, Uniuersity of Illinois, Urbana Illinois 61801 (P.A.G.);Department of Anthropology, City College of New York, New York, New York 10031 (W.G.K.)
Research conducted over the past decade has dramatically increased our knowledge of the evolutionary biology, behavior, and ecology of New World primates. Extensive field data have been collected for species from virtually all of the 16 extant genera. During this same period, the discovery of a large number of platyrrhine fossils from the Oligocene of Argentina and Bolivia, and the Miocene of Colombia, has led to a major reevaluation of the evolution and systematics of this primate group (Fleagle and Rosenberger, 1990). These specimens provide a more complete sequence from which to identify phylogenetic relationships between fossil and living forms. There is now serious doubt concerning the simple and longstanding dichotomy of New World primates into “clawed and “nonclawed taxa, and researchers have constructed a new framework for assessing the adaptive trends which characterize this important primate radiation. The papers presented in this issue of the American Journal of Physical Anthropology were originally presented on April 7, 1989, a t the 58th Annual Meeting of the American Association of Physical Anthropologists in San Diego, California. The purpose of the symposium was to examine in detail the evolution of feeding adapations in each of the four subfamilies of living New World primates-Callitrichinae, Cebinae, Pitheciinae, and Atelinae. Within each paper, special attention is given to relationships between body size, diet, dental morphology, locomotor anatomy, and foraging behavior. Comparisons are made between extinct and extant taxa, as well as interspecific comparisons within subfamilies. These provide a basis for understanding the origin and function of dietary adaptations in Platyrrhini. 0 1992 WILEY-LISS, INC
The lead paper by Ford and Davis outlines the major issues and lines of evidence that have been used to construct the phylogenetic history of New World primates. Beginning with the argument that the traditional CallitrichidaeICebidae classification can no longer be supported, these authors review several recently proposed schemes of platyrrhine systematics. Although these schemes are in general agreement regarding the taxonomic grouping within the Callitrichinae (the marmosets and tamarins; termed Callitrichidae by some authors), and the close evolutionary relationship between the Atelinae and the saki-uakari group, the positions ofdotus, Callicebus, Saimiri, and Cebus continue to be debated. Ford and Davis also address a series of questions regarding the influence of body size (weight) on Neotropical primate foraging strategies. These authors argue that the evolutionary history of many platyrrhine lineages has been characterized by major increases andor decreases in body size. Comparisons of feeding adaptations in extant species, therefore, must consider “patterns of body size change through time,” and whether particular taxa have attained similar size through common or independent evolutionary pathways. Ford and Davis provide four alternative cladograms t o account for the direction and magnitude of body weight changes in living New World monkeys and use these reconstructions to identify significant dietary, behavioral, locomotor, and ecological issues in
Received for publication July 11, 1990; revision received February 20,1992. Address correspondence to Warren G . Kinzey, Department of Anthropology, City College of New York, Covent Avenue and 138th Street, New York, NY 10031.
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platyrrhine evolution. Many of these issues are addressed directly by other authors in the symposium. Garber examines relationships between body size and foraging adaptations in callitrichine primates. All tamarins and marmosets possess clawlike nails which enable them to cling to large vertical trunks while exploiting resources such as insects and plant exudates. These resources are rarely utilized by other platyrrhine taxa. There is evidence of at least 4 distinct large-branch foraging patterns within the subfamily. Many of these patterns are associated with derived features of the dentition, digestive tract, and locomotor skeleton. In terms of their anatomy and feeding ecology, the marmosets, pygmy marmoset, and lion marmosets are the most specialized of the callitrichine genera, whereas many Saguinus species may be regarded as ecologically more generalized. He suggests that the widespread availability of trunk-foraging niches in the Neotropics may have enabled ancestral callitrichines to broaden a preexisting small-branch, undercanopy foraging pattern to include the exploitation of trunksurface and bark-refuging resources. Kinzey examines the evidence for a relationship between the traditionally recognized saki-uakaris and Aotus and Callicebus. No one questions the close relationship among Pithecia, Chiropotes, and Cacajao, but Ford and Davis (this volume) point out wide divergences in opinion regarding the relationship of the former two taxa. All saki-uakaris are seed predators with each genus occupying a separate niche: Cacajao in flooded forests of the Amazon basin, Chiropotes in the upper canopy of non-flooded high forest, and Pithecia, frequently sympatric with Chiropotes, in the mid to lower canopy of the same forests and also in disturbed forests. Callicebus represents the best living example of what Kinzey envisions the last common ancestor of the saki-uakaris to have been--an incipient seed predator, feeding in small groups in emergent trees on small quantities of unripe fruit, before sufficient fruit is available for a larger biomass of frugivores. Kinzey suggests that extant members of the Pitheciini are adapted for sclerocarpic foraging. This is a two stage process of seed pre-
dation involving (a) specialized features of the incisors and canine capable of removing a hard pericarp which protects a seed or seeds, followed by (b) mastication by the posterior dentition having low cusp relief to triturate seeds with a relatively soft and uniform consistency. The platyrrhine fossils, Soriacebus and Cebupithecia, demonstrate that robusticity and flaring of the canine preceded development of low cusp relief on molars in the evolution of morphological features associated with sclerocarpic foraging. The Janson and Boinski paper examines both morphological and behavioral adaptations in cebine foraging. Although these authors document relationships among body size, jaw morphology, and feeding patterns in these primates, they argue that “probably the most striking ecological specialization of the Cebinae is their lack of obvious physical specializations.’’ Behavioral flexibility and enhanced manual prehension allow both Cebus and Saimiri to exploit and manipulate an extreme variety of foraging substrates and food types. Cebus is regarded as a large bodied faunivore that uses its strength to break open dead branches and attack wasp nests to extract concealed and protected invertebrate prey. In addition, Cebus consumes vertebrates such as young birds during certain times of the year, and can open hard-shelled nuts and seeds. Saimiri, in contrast, searches the surface of branches and leaves to capture relatively mobile insects and manipulates leaf curls t o extract hidden prey. Janson and Boinski argue that expansion of the neural system in Sairniri and especially in Cebus may favor the development of complex foraging behaviors enabling these primates to locate and harvest scarce energy-rich food sources efficiently. These authors conclude that although morphology “is very useful in predicting species differences in gross diet among cebines. . . it is [also] necessary to know about how food types are presented in the environment” and the range of behavioral flexibility of the species. In her article on ateline adaptations, Strier argues that this successful radiation of large-bodied, prehensile-tailed New World monkeys is characterized by 2 contrasting patterns of foraging and resource
FEEDING ADAPTATIONS IN NEW WORLD PRIMATES
exploitation. The atelins, which include the genera Ateles, Lagothrix, and Brachyteles, are described as energy maximizers in terms of their frugivorous dietary habitat, suspensory mode of locomotion, large day range, and extremely fluid social grouping pattern. In contrast, Alouatta, despite its smaller body size, appears t o minimize daily energy expenditure by its slow mode of quadrupedal travel, long daily rest periods, limited day range, slow rate of food passage, and folivorous diet. Within the atelins, body size is a good predictor of dietary pattern. The largest species, Brachyteles arachnoides, includes the highest proportion of leaves in its diet. A comparison of feeding patterns in sympatric populations of Alouatta and Brachyteles indicates, however, that despite being 3 times lighter, the brown howler (A.fusca)is more folivorous than the woolly spider monkey. Strier proposes that leaf-eating is a “secondary adaptation” in Brachyteles and enables this largest New World primate to exploit this alternative and relatively abundant food source “when preferred fruit resources are seasonally scarce.” In the final paper, Rosenberger examines evidence for adaptive shifts and diversity of feeding niches in both living and fossil New World primates. He argues that platyrrhines represent 2 monophyletic taxa. One is a Frugivore-Insectivore guild, the Family Cebidae (Cebus, Saimiri, and the callitrichines), and the second is a Frugivore-Folivore guild assigned to the Family Atelidae. Within each clade, however, changes in body size, behavior, morphology, and related for-
413
aging adaptations have resulted in an array of novel patterns of habitat exploitation and dietary patterns. In particular, Rosenberger discusses functional relationships between the physical and chemical properties of different foods and the ability of primate consumers to harvest, masticate, and digest them. In this regard he discusses the concept of “critical function” suggesting that “the physical properties of even those food items eaten rarely present biomechanical challenges that would select for form. . . and the requisite functional capacities.” Rosenberger provides an analysis of dental adaptations in platyrrhines indicating important differences in puncture, crushing, shearing functions. Comparisons between genera and higher taxa are included as are relationships between dental form and feeding adaptations in fossil platyrrhines. A major question posed in this paper is how to classify primate diets. Using the pithecines as an example, Rosenberger proposes that frugivory in general contributes little in identifying form-function relationships in diet and dentition. Occlusal function in platyrrhines appears t o be related to selective pressures imposed by other food types such as leaves, insects, hard fruits, and seeds. He concludes with a discussion of how factors such as seasonality, resource scarcity, body size, predation, and niche vacancy have contributed to feeding adaptations in New World primates. LITERATURE CITED Fleagle JG; and Rosenberger AL (eds.) (1990) The Platyrrhine Fossil Record. London: Academic Press.
Feeding Adaptations in New World Primates: An Evolutionary Perspective: Introduction PAUL A. GARBER AND WARREN G . KINZEY Department of Anthropology, Uniuersity of Illinois, Urbana Illinois 61801 (P.A.G.);Department of Anthropology, City College of New York, New York, New York 10031 (W.G.K.)
Research conducted over the past decade has dramatically increased our knowledge of the evolutionary biology, behavior, and ecology of New World primates. Extensive field data have been collected for species from virtually all of the 16 extant genera. During this same period, the discovery of a large number of platyrrhine fossils from the Oligocene of Argentina and Bolivia, and the Miocene of Colombia, has led to a major reevaluation of the evolution and systematics of this primate group (Fleagle and Rosenberger, 1990). These specimens provide a more complete sequence from which to identify phylogenetic relationships between fossil and living forms. There is now serious doubt concerning the simple and longstanding dichotomy of New World primates into “clawed and “nonclawed taxa, and researchers have constructed a new framework for assessing the adaptive trends which characterize this important primate radiation. The papers presented in this issue of the American Journal of Physical Anthropology were originally presented on April 7, 1989, a t the 58th Annual Meeting of the American Association of Physical Anthropologists in San Diego, California. The purpose of the symposium was to examine in detail the evolution of feeding adapations in each of the four subfamilies of living New World primates-Callitrichinae, Cebinae, Pitheciinae, and Atelinae. Within each paper, special attention is given to relationships between body size, diet, dental morphology, locomotor anatomy, and foraging behavior. Comparisons are made between extinct and extant taxa, as well as interspecific comparisons within subfamilies. These provide a basis for understanding the origin and function of dietary adaptations in Platyrrhini. 0 1992 WILEY-LISS, INC
The lead paper by Ford and Davis outlines the major issues and lines of evidence that have been used to construct the phylogenetic history of New World primates. Beginning with the argument that the traditional CallitrichidaeICebidae classification can no longer be supported, these authors review several recently proposed schemes of platyrrhine systematics. Although these schemes are in general agreement regarding the taxonomic grouping within the Callitrichinae (the marmosets and tamarins; termed Callitrichidae by some authors), and the close evolutionary relationship between the Atelinae and the saki-uakari group, the positions ofdotus, Callicebus, Saimiri, and Cebus continue to be debated. Ford and Davis also address a series of questions regarding the influence of body size (weight) on Neotropical primate foraging strategies. These authors argue that the evolutionary history of many platyrrhine lineages has been characterized by major increases andor decreases in body size. Comparisons of feeding adaptations in extant species, therefore, must consider “patterns of body size change through time,” and whether particular taxa have attained similar size through common or independent evolutionary pathways. Ford and Davis provide four alternative cladograms t o account for the direction and magnitude of body weight changes in living New World monkeys and use these reconstructions to identify significant dietary, behavioral, locomotor, and ecological issues in
Received for publication July 11, 1990; revision received February 20,1992. Address correspondence to Warren G . Kinzey, Department of Anthropology, City College of New York, Covent Avenue and 138th Street, New York, NY 10031.
412
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platyrrhine evolution. Many of these issues are addressed directly by other authors in the symposium. Garber examines relationships between body size and foraging adaptations in callitrichine primates. All tamarins and marmosets possess clawlike nails which enable them to cling to large vertical trunks while exploiting resources such as insects and plant exudates. These resources are rarely utilized by other platyrrhine taxa. There is evidence of at least 4 distinct large-branch foraging patterns within the subfamily. Many of these patterns are associated with derived features of the dentition, digestive tract, and locomotor skeleton. In terms of their anatomy and feeding ecology, the marmosets, pygmy marmoset, and lion marmosets are the most specialized of the callitrichine genera, whereas many Saguinus species may be regarded as ecologically more generalized. He suggests that the widespread availability of trunk-foraging niches in the Neotropics may have enabled ancestral callitrichines to broaden a preexisting small-branch, undercanopy foraging pattern to include the exploitation of trunksurface and bark-refuging resources. Kinzey examines the evidence for a relationship between the traditionally recognized saki-uakaris and Aotus and Callicebus. No one questions the close relationship among Pithecia, Chiropotes, and Cacajao, but Ford and Davis (this volume) point out wide divergences in opinion regarding the relationship of the former two taxa. All saki-uakaris are seed predators with each genus occupying a separate niche: Cacajao in flooded forests of the Amazon basin, Chiropotes in the upper canopy of non-flooded high forest, and Pithecia, frequently sympatric with Chiropotes, in the mid to lower canopy of the same forests and also in disturbed forests. Callicebus represents the best living example of what Kinzey envisions the last common ancestor of the saki-uakaris to have been--an incipient seed predator, feeding in small groups in emergent trees on small quantities of unripe fruit, before sufficient fruit is available for a larger biomass of frugivores. Kinzey suggests that extant members of the Pitheciini are adapted for sclerocarpic foraging. This is a two stage process of seed pre-
dation involving (a) specialized features of the incisors and canine capable of removing a hard pericarp which protects a seed or seeds, followed by (b) mastication by the posterior dentition having low cusp relief to triturate seeds with a relatively soft and uniform consistency. The platyrrhine fossils, Soriacebus and Cebupithecia, demonstrate that robusticity and flaring of the canine preceded development of low cusp relief on molars in the evolution of morphological features associated with sclerocarpic foraging. The Janson and Boinski paper examines both morphological and behavioral adaptations in cebine foraging. Although these authors document relationships among body size, jaw morphology, and feeding patterns in these primates, they argue that “probably the most striking ecological specialization of the Cebinae is their lack of obvious physical specializations.’’ Behavioral flexibility and enhanced manual prehension allow both Cebus and Saimiri to exploit and manipulate an extreme variety of foraging substrates and food types. Cebus is regarded as a large bodied faunivore that uses its strength to break open dead branches and attack wasp nests to extract concealed and protected invertebrate prey. In addition, Cebus consumes vertebrates such as young birds during certain times of the year, and can open hard-shelled nuts and seeds. Saimiri, in contrast, searches the surface of branches and leaves to capture relatively mobile insects and manipulates leaf curls t o extract hidden prey. Janson and Boinski argue that expansion of the neural system in Sairniri and especially in Cebus may favor the development of complex foraging behaviors enabling these primates to locate and harvest scarce energy-rich food sources efficiently. These authors conclude that although morphology “is very useful in predicting species differences in gross diet among cebines. . . it is [also] necessary to know about how food types are presented in the environment” and the range of behavioral flexibility of the species. In her article on ateline adaptations, Strier argues that this successful radiation of large-bodied, prehensile-tailed New World monkeys is characterized by 2 contrasting patterns of foraging and resource
FEEDING ADAPTATIONS IN NEW WORLD PRIMATES
exploitation. The atelins, which include the genera Ateles, Lagothrix, and Brachyteles, are described as energy maximizers in terms of their frugivorous dietary habitat, suspensory mode of locomotion, large day range, and extremely fluid social grouping pattern. In contrast, Alouatta, despite its smaller body size, appears t o minimize daily energy expenditure by its slow mode of quadrupedal travel, long daily rest periods, limited day range, slow rate of food passage, and folivorous diet. Within the atelins, body size is a good predictor of dietary pattern. The largest species, Brachyteles arachnoides, includes the highest proportion of leaves in its diet. A comparison of feeding patterns in sympatric populations of Alouatta and Brachyteles indicates, however, that despite being 3 times lighter, the brown howler (A.fusca)is more folivorous than the woolly spider monkey. Strier proposes that leaf-eating is a “secondary adaptation” in Brachyteles and enables this largest New World primate to exploit this alternative and relatively abundant food source “when preferred fruit resources are seasonally scarce.” In the final paper, Rosenberger examines evidence for adaptive shifts and diversity of feeding niches in both living and fossil New World primates. He argues that platyrrhines represent 2 monophyletic taxa. One is a Frugivore-Insectivore guild, the Family Cebidae (Cebus, Saimiri, and the callitrichines), and the second is a Frugivore-Folivore guild assigned to the Family Atelidae. Within each clade, however, changes in body size, behavior, morphology, and related for-
413
aging adaptations have resulted in an array of novel patterns of habitat exploitation and dietary patterns. In particular, Rosenberger discusses functional relationships between the physical and chemical properties of different foods and the ability of primate consumers to harvest, masticate, and digest them. In this regard he discusses the concept of “critical function” suggesting that “the physical properties of even those food items eaten rarely present biomechanical challenges that would select for form. . . and the requisite functional capacities.” Rosenberger provides an analysis of dental adaptations in platyrrhines indicating important differences in puncture, crushing, shearing functions. Comparisons between genera and higher taxa are included as are relationships between dental form and feeding adaptations in fossil platyrrhines. A major question posed in this paper is how to classify primate diets. Using the pithecines as an example, Rosenberger proposes that frugivory in general contributes little in identifying form-function relationships in diet and dentition. Occlusal function in platyrrhines appears t o be related to selective pressures imposed by other food types such as leaves, insects, hard fruits, and seeds. He concludes with a discussion of how factors such as seasonality, resource scarcity, body size, predation, and niche vacancy have contributed to feeding adaptations in New World primates. LITERATURE CITED Fleagle JG; and Rosenberger AL (eds.) (1990) The Platyrrhine Fossil Record. London: Academic Press.
