2 - Morphology and evolution of the spider monkey, genus Ateles  pp. 19-49

Morphology and evolution of the spider monkey, genus <i>Ateles</i>

By Alfred L. Rosenberger, Lauren Halenar, Siobhán B. Cooke and Walter C. Hartwig

Image View Previous Chapter Next Chapter



Introduction

Spider monkeys cast a distinct morphological silhouette – long scrawny arms and a snaky prehensile tail arching from a narrow pot-belly torso, topped by a small round head and blunt face. The commitment of this relatively large-bodied platyrrhine to a large-tree, upper canopy milieu and to ripe fruit foraging is seen throughout its skeletal and craniodental morphology. Spider monkeys are the signature New World suspensory-postured brachiators. Bodily, they are the closest thing to a gibbon that has evolved anywhere else within the Order Primates. Less obvious may be the fact that they are also gibbonesque craniodentally. But in the context of the adaptive array of Latin America's four ateline genera, Alouatta, Lagothrix, Brachyteles and Ateles, spider monkeys are not simply the polar end of an adaptive morphocline, standing opposite howlers or even opposite Lagothrix if we draw our comparison more narrowly, to encompass only atelins. Spider monkeys are different by far. For example, as close as Brachyteles is to the visage of a spider monkey with its ungainly limbs and shortness of face, it does not match Ateles in the high-energy lifestyle that goes along with eating quickly metabolized fruit and little else. Nor can Brachyteles deftly fly and lope through the trees as if gravity and substrate did not matter and hands, feet and tail were octopus tentacles. How ironic that Geoffroy Saint-Hilaire was so impressed with the spider monkey's lone anatomical “deficiency,” its missing thumb, that in 1806 he named the genus Ateles, meaning imperfect.

Anapol, F. and Lee, S. (1994). Morphological adaptation to diet in platyrrhine primates. Am. J. Phys. Anthropol., 94, 239–261.
Ankel, F. (1972). Vertebral morphology of fossil and extant primates. In Functional and Evolutionary Biology of the Primates, ed. R. Tuttle, Chicago: Aldine and Atherton, pp. 223–240.
Anthony, M. R. L. and Kay, R. F. (1993). Tooth form and diet in ateline and alouattine primates: reflections on the comparative method. Am. J. Sci., 293A, 356–382.
Armstrong, E. and Shea, M. A. (1997). Brains of New World and Old World monkeys. In New World Primates: Ecology, Evolution, and Behavior, ed. W. G. Kinzey, New York: Aldine de Gruyter, pp. 25–44.
Ashton, E. H. and Oxnard, C. E. (1963). The musculature of the primate shoulder. Trans. Zool. Soc. Lond., 29, 553–650.
Ashton, E. H. and Oxnard, C. E. (1964). Functional adaptations in the primate shoulder girdle. Proc. Zool. Soc. Lond., 142, 49–66.
Campbell, B. (1937). The shoulder musculature of the Platyrrhine monkeys. J. Mammal., 18(1), 66–71.
Campbell, K. E., Frailey, C. D. and Romero-Pittman, L. (2006). The Pan-Amazonian Ucayali Peneplain, late Neogene sedimentation in Amazonia, and the birth of the modern Amazon River system. Palaeogeog., Palaeoclimat., Palaeoecol., 239, 166–219.
Canavez, F. C., Moreira, M. A. M., Ladoski, J. L., et al. (1999). Molecular phylogenetics of New World primates (Platyrrhine) based on b2-Microglobulin DNA sequences. Mol. Phylogen. Evol., 12, 74–82.
Cant, J. G. H., Youlatos, D. and Rose, M. D. (2001). Locomotor behavior of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park, Ecuador: general patterns and non-suspensory modes. J. Hum. Evol., 41, 141–166.
Cartelle, C. and Hartwig, W. C. (1996). A new extinct primate among the Pleistocene megafauna of Bahia, Brazil. Proc. Natl. Acad. Sci., 93, 6405–6409.
Cartmill, M. (1974). Pads and claws in arboreal locomotion. In Primate Locomotion, ed. F. A. Jenkins, New York: Academic Press, pp. 45–83.
Chapman, C. A. and Chapman, L. J. (1990). Reproductive biology of free-ranging spider monkeys. Zoo Biol., 9, 1–9.
Collins, A. C. (2004). Atelinae phylogenetic relationships: the trichotomy revived? Am. J. Phys. Anthropol., 124, 285–296.
Corner, B. D. and Richtsmeier, J. T. (1993). Cranial growth and growth dimorphism in Ateles geoffroyi. Am. J. Phys. Anthropol., 92, 371–394.
Defler, T. R. (1999). Locomotion and posture in Lagothrix lagotricha. Folia Primatol., 70, 313–327.
Delson, E. and Rosenberger, A. L. (1984). Are there any anthropoid primate “living fossils”? In Living Fossils, ed. N. Eldredge and S. Stanley, New York: Fischer, pp. 50–61.
Di Fiore, A. and Campbell, C. J. (2007). The atelines: variation in ecology, behavior, and social organization. In Primates in Perspective, ed. C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger and S. K. Beader, New York: Oxford University Press, pp. 155–185.
Erickson, G. E. (1963). Brachiation in New World monkeys and in Anthropoid apes. Symp. Zool. Soc. Lond., 10, 135–164.
Fajardo, R. J. and Müller, R. (2001). Three-dimensional analysis of nonhuman primate trabecular architecture using micro-computed tomography. Am. J. Phys. Anthropol., 115, 327–336.
Fontaine, R. (1990). Positional behavior in Saimiri boliviensis and Ateles geoffroyi. Am. J. Phys. Anthropol., 82, 485–508.
Ford, S. E. (1994). Evolution of sexual dimorphism in body weight in platyrrhines. Am. J. Primatol., 34, 221–244.
Ford, S. E. and Davis, L. (1992). Systematics and body size: implications for feeding adaptations in New World monkeys. Am. J. Phys. Anthropol., 88, 415–468.
Gebo, D. L. (1996). Climbing, brachiation, and terrestrial quadrupedalism: historical precursors of hominid bipedalism. Am. J. Phys. Anthropol., 101, 55–92.
German, R. (1982). Functional morphology of caudal vertebrae in new world monkeys. Am. J. Phys. Anthropol., 58, 453–459.
Harada, M. L., Schneider, H., Schneider, M. P. C., et al. (1995). DNA evidence on the phylogenetic systematics of New World monkeys: support for the sister-grouping of Cebus and Saimiri from two unlinked nuclear genes. Mol. Phylogen. Evol., 4, 331–349.
Hartwig, W. C. (1993). Comparative Morphology, Ontogeny and Phylogenetic Analysis of the Platyrrhine Cranium. Ann Arbor: University Microfilms International.
Hartwig, W. C. (1996). Perinatal life history traits in New World monkeys. Am. J. Primatol., 40, 99–130.
Hartwig, W. C. (2005). Implications of molecular and morphological data for understanding ateline phylogeny. Int. J. Primatol., 26, 999–1015.
Hartwig, W. C. and Cartelle, C. (1996). A complete skeleton of the giant South American primate Protopithecus. Nature 381, 307–311.
Harvey, P., Kavanagh, M. and Clutton-Brock, T. H. (1978). Sexual dimorphism in primate teeth. J. Zool. (Lond.), 186, 475–485.
Hershkovitz, P. (1970). Cerebral fissural patterns in platyrrhine monkeys. Folia Primatol., 13, 213–240.
Hershkovitz, P. (1977). Living New World Primates (Platyrrhini), Vol. 1. Chicago: University of Chicago Press.
Horovitz, I., Zaradoya, R. and Meyer, A. (1998). Platyrrhine systematics: a simultaneous analysis of molecular and morphological data. Am. J. Phys. Anthropol., 106, 261–281.
Hylander, W. L. (1979). Functional significance of primate mandibular form. J. Morphol., 160, 223–239.
Inman, V. T., Saunders, M. and Abbott, L. C. (1944). Observations on the function of the shoulder joint. J. Bone Joint Surg., 26, 1–30.
Jenkins, F. A. (1981). Wrist rotation in primates: a critical adaptation for brachiators. Symp. Zool. Soc. Lond., 48, 429–451.
Jenkins, F. A., Dombrowski, P. J. and Gordon, E. P. (1978). Analysis of the shoulder in brachiating spider monkeys. Am. J. Phys. Anthropol., 48, 65–76.
Johnson, S. E. and Shapiro, L. J. (1998). Positional and vertebral morphology in atelines and cebines. Am. J. Phys. Anthropol., 105, 333–354.
Jones, A. (2004). The evolution of brachiation in atelines: a phylogenetic comparative study. Unpublished Ph.D. thesis. University of California, Davis.
Jouffroy, F. K. and Lessertisseur, J. (1977). Processus de réduction des doigts (main et pied) chez les primates. Modalités, implications génétiques. Colloques internationaux C.N.R.S. No. 266 Méchanisme de la Rudimentation de Organes chez les Embryons de Vertébrés, pp. 381–389.
Jouffroy, F. K., Godinot, M. and Nakano, Y. (1991). Biometrical characteristics of primate hands. Hum. Evol., 6, 269–306.
Jungers, W. L. (1985). Allometry of primate limb proportions. In Size and Scaling in Primate Biology, ed. W. L. Jungers, New York: Plenum Press, pp. 345–381.
Jungers, W. L. and Stern, J. T. (1984). Kinesiological aspects of brachiation in lar gibbons. In The Lesser Apes, ed. H. Preuschoft, D. J. Chivers, W. Y. Brockelman and N. Creel. Edinburgh: Edinburgh University Press, pp. 119–134.
Kay, R. F. (1975). The functional adaptations of primate molar teeth. Am. J. Phys. Anthropol., 43, 195–216.
Kay, R. F. (1987). Analysis of primate dental microwear using image processing techniques. Scanning Microscopy, 1, 657–662.
Kay, R. F. (1990). The phyletic relationships of extant and fossil Pitheciinae (Platyrrhini, Anthropoidea). J. Hum. Evol., 19, 175–208.
Kay, R. F. and Cozzuol, M. A. (2006). New platyrrhine monkeys from the Solimões Formation (late Miocene, Acre State, Brazil). J. Hum. Evol., 50, 673–686.
Kay, R. F. and Hiiemae, K. M. (1974). Jaw movement and tooth use in recent and fossil primates. Am. J. Phys. Anthropol., 40, 227–256.
Kay, R. F., Plavcan, J. M., Glander, K. E. and Wright, P. C. (1988). Sexual selection and canine dimorphism in New World monkeys. Am. J. Phys. Anthropol., 77, 385–397.
Kinzey, W. G. (1970). Basic rectangle of the mandible. Nature, 228, 289–290.
Konstant, W., Stern, J. T., Fleagle, J. G. and Jungers, W. L. (1982). Function of the subclavius muscle in a nonhuman primate, the spider monkey (Ateles). Folia Primatol., 38, 170–182.
Larson, S. G. (1995). New characters for the functional interpretation of primate scapulae and proximal humeri. Am. J. Phys. Anthropol., 98, 13–35.
Larson, S. G. (1998). Unique aspects of quadrupedal locomotion in nonhuman primates. In Primate Locomotion: Recent Advances, ed. E. Strasser, J. Fleagle, A. Rosenberger and H. McHenry, New York: Plenum Press, pp. 157–173.
Larson, S. G. and Stern, J. T. (1986). EMG of scapulohumeral muscles in the chimpanzee during reaching and “arboreal” locomotion. Am. J. Anat., 176, 171–190.
Lemelin, P. (1995). Comparative and functional myology of the prehensile tail in New World monkeys. J. Morphol., 224, 351–368.
Lemelin, P. and Schmitt, D. (1998). The relation between hand morphology and quadrupedalism in primates. Am. J. Phys. Anthropol., 105, 185–197.
Lewis, O. J. (1971). Brachiation and the early evolution of the Hominoidea. Nature, 230, 577–578.
Lewis, O. J. (1972). Osteological features characterizing the wrists of monkeys and apes, with a reconsideration of this region in Dryopithecus (Proconsul) africanus. Am. J. Phys. Anthropol., 36, 45–58.
MacPhee, R. D. E. and Meldrum, D. J. (2006). Postcranial remains of the extinct monkeys of the greater Antilles, with evidence of semiterrestriality in Paralouatta. Am. Mus. Novitates, 3516, 1–65.
Masterson, T. J. and Hartwig, W. C. (1998). Degrees of sexual dimorphism in Cebus and other New World monkeys. Am. J. Phys. Anthropol., 107, 243–256.
Matthews, L. and Rosenberger, A. (in press). An object lesson for primate systematics: parsimony analysis (PAUP*) and the taxonomy of the yellow-tailed woolly monkey, Lagothrix flavicauda. Am. J. Phys. Anthropol.
Meireles, C. M., Czelusniak, J., Schneider, M. P. C., et al. (1999). Molecular phylogeny of ateline New World monkeys (Platyrrhini, Atelinae) based on g-Globin gene sequences: evidence that Brachyteles is the sister group of Lagothrix. Mol. Phylogen. Evol., 12, 10–30.
Meldrum, D. J. (1993). Postcranial adaptations and positional behavior in fossil platyrrhines. In Postcranial Adaptation in Nonhuman Primates, ed. D. L. Gebo, DeKalb: Northern Illinois University Press, pp. 235–251.
Mittermeier, R. A. (1978). Locomotion and posture in Ateles geoffroy and Ateles paniscus. Folia Primatol., 30, 161–193.
Napier, J. R. (1961). Prehensility and opposability in the hands of primates. Symp. Zool. Soc. Lond., 5, 115–132.
Norconk, M. A., Rosenberger, A. L. and Garber, P. A., eds. (1996). Adaptive Radiations of Neotropical Primates. New York: Plenum Press.
Orlosky, F. (1973). Comparative Dental Morphology of Extant and Extinct Cebidae. Ann Arbor: University Microfilms.
Oxnard, C. E. (1963). Locomotor adaptations in the primate forelimb. Proc. Zool. Soc. Lond., 10, 165–182.
Oxnard, C. E. (1967). The functional morphology of the primate shoulder as revealed by comparative anatomical, osteometric and discriminant function techniques. Am. J. Phys. Anthropol., 26, 219–240.
Oxnard, C. E. (1968). A note on the Olduvia clavicular fragment. Am. J. Phys. Anthropol., 29, 429–432.
Plavcan, J. M. and Kay, R. F. (1988). Sexual dimorphism and dental variability in platyrrhine primates. Int. J. Primatol., 9, 169–178.
Plavcan, J. M. and van Schaik, C. (1997). Intrasexual competition and body weight dimorphism in anthropoid primates. Am. J. Phys. Anthropol., 103, 37–68.
Rafferty, K. L. (1998). Structural design of the femoral neck in primates. J. Hum. Evol., 34, 361–384.
Rose, M. D. (1975). Functional proportions of primate lumbar vertebral bodies. J. Hum. Evol., 4, 21–38.
Rose, M. D. (1988). Another look at the anthropoid elbow. J. Hum. Evol., 15, 333–367.
Rosenberger, A. L. (1983) Tail of tails: parallelism and prehensility. Am. J. Phys. Anthropol., 60, 103–107.
Rosenberger, A. L. (1992). Evolution of feeding niches in New World monkeys. Am. J. Phys. Anthropol., 88, 525–562.
Rosenberger, A. L. and Strier, K. (1989). Adaptive radiation of the ateline primates. J. Hum. Evol., 18, 717–750.
Rosenberger, A. L., Setoguchi, T. and Shigerhara, N. (1990). The fossil record of callitrichine primates. J. Hum. Evol., 19, 209–236.
Rosenberger, A. L., Tejedor, M., Cooke, S. B., Pekar, S. (in press). Platyrrhine ecophylogenetics in space and time. In South American Primates: Comparative Perspectives in the Study of Behavior, Ecology and Conservation, ed. P. Garber, New York: Springer.
Schneider, H., Sampaio, I., Harada, M. L., et al. (1996). Molecular phylogeny of the New World monkeys (Platyrrhini, Primates) based on two unlinked nuclear genes: IRBP intron 1 and ε-globin sequences. Am. J. Phys. Anthropol., 100, 153–179.
Schneider, H., Schneider, M. P. C., Sampaio, M. I. C., et al. (1993). Molecular phylogeny of the New World monkeys (Platyrrhini, Primates). Mol. Phylogen. Evol., 2, 225–242.
Schultz, A. H. (1960). Age changes and variability in the skull and teeth of the Central American monkeys Alouatta, Cebus and Ateles. Proc. Zool. Soc. Lond., 133, 337–390.
Schultz, A. H. (1961). Vertebral column and thorax. Primatologia, 4, 1–66.
Setoguchi, T. and Rosenberger, A. L. (1987). A fossil owl monkey from La Venta, Colombia. Nature, 326, 692–694.
Smith, R. J. (1978). Mandibular biomechanics and temporomandibular joint function in primates. Am. J. Phys. Anthropol., 49, 341–349.
Smith, R. J. and Jungers, W. L. (1997). Body mass in comparative primatology. J. Hum. Evol., 32, 523–559.
Stern, J. T. (1971). Functional Myology of the Hip and Thigh of Cebid Monkeys and its Implications for the Evolution of Erect Posture (Bibilotheca primatologica). Chicago: S. Karger.
Stern, J. T. and Larson, S. G. (1993). EMG of the supinator and pronators in the gibbon and chimpanzee. Am. J. Phys. Anthropol., Suppl., 16, 187–188.
Strier, K. B. (1992). Atelinae adaptations: behavioral strategies and ecological constraints. Am. J. Phys. Anthropol., 88, 515–524.
Swartz, S. M. (1990). Curvature of the forelimb bones of anthropoid primates: overall allometric patterns and specializations in suspensory species. Am. J. Phys. Anthropol., 83, 477–498.
Tague, R. G. (1997). Variability of a vestigial structure: first metacarpal in Colobus guereza and Ateles geoffroyi. Evolution, 51, 595–605.
Takahashi, L. K. (1990). Morphological basis of arm-swinging: multivariate analyses of the forelimbs of Hylobates and Ateles. Folia Primatol., 54, 70–85.
Turnquist, J. E. (1983). Forelimb musculature and ligaments in Ateles, the spider monkey. Am. J. Phys. Anthropol., 62, 209–226.
Turnquist, J. E., Schmitt, D., Rose, M. D. and Cant, J. G. H. (1999). Pendular motion in the brachiation of captive Lagothrix and Ateles. Am. J. Primatol., 48, 263–281.
Voisin, J. (2006). Clavicle, a neglected bone: morphology and relation to arm movements and shoulder architecture in primates. Anat. Rec. A, 288A, 944–953.
von Dornum, M. and Ruvolo, M. (1999). Phylogenetic relationships of the New World monkeys (Primates, Platyrrhini) based on nuclear G6PD DNA sequences. Mol. Phylogen. Evol., 11, 459–476.
Wall, C. E. (1999). A model of temporomandibular joint function in anthropoid primates based on condylar movements during mastication. Am. J. Phys. Anthropol., 109, 67–88.
Youlatos, D. (2000). Functional anatomy of forelimb muscles in Guianan atelines (Platyrrhini: Primates). Annales des Sciences Naturelles-Zoologie et Biologie Animale, 21, 137–151.
Youlatos, D. (2002). Positional behavior of black spider monkeys (Ateles paniscus) in French Guiana. Int. J. Primatol., 23, 1071–1094.
Young, N. M. (2003). A reassessment of living hominoid postcranial variability: implications for ape evolution. J. Hum. Evol., 45, 441–464.
Zingeser, M. R. (1973). Dentition of Brachyteles arachnoides with reference to alouattine and atelinine affinities. Folia Primatol., 20, 351–390.