Patterns of diversity in cranial shape among plant-visiting bats

• Autorzy: Dumont E.R.
• Języki publikacji: EN

Abstrakty

EN

Adaptations to a plant-based diet have evolved in bats on two occasions — once in the Old World family Pteropodidae and again within the New World family Phyllostomidae. Although the skulls of all plant-visiting bats exhibit adaptations for relatively large eyes, enlarged brains, and reduced molar complexity, the skulls of bats from the two families look very different. The goals of this study are to pinpoint the fundamental differences in the cranial shape between pteropodids and plant-visiting phyllostomids and to investigate patterns of diversity in cranial shape within each lineage. Analyses are based on 19 size adjusted, linear variables collected from 335 specimens that represent 71% of pteropodid and 45% of plant-visiting phyllostomid genera. Results of a stepwise discriminant function analysis indicate that differences in cranial shape between pteropodids and plant-visiting phyllostomids involve general aspects of relative braincase width, palate width and coronoid process height. Pteropodids have relatively narrow skulls and palates, and dentaries with tall coronoid processes, while the opposite is true of phyllostomids. Principal components analysis and an investigation of coefficients of variation reveal a high level of variation among the skulls of plant-visiting phyllostomids while cranial architecture among pteropodids is more conservative. This study documents patterns of morphological diversity in the skulls of plant-visiting bats. Several potential ecological and biomechanical mechanisms underlying these patterns are discussed.

• Wydawca: -
• Czasopismo: Acta Chiropterologica
• Rocznik: 2004
• Tom: 06
• Numer: 1
• Opis fizyczny: p.59-74,fig.,ref.

Twórcy

autor

Dumont E.R.

• Department of Biology, Morrill Science Center, University of Massachusetts, 611 North Pleasant Street, Amherst, MA 01003, USA

Bibliografia

• Acharya, K. K., R. Anubba, and A. Krishna. 1998. Relative role of olfactory cues and certain non-olfactory factors in foraging of fruit-eating bats. Behavioural Processes, 44: 59-64.
• Aguirre, L. F., A. Herrel, R. Van Damme, and E. Matthysen. 2002. Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community. Proceedings of the Royal Society of London, Series B — Biological Sciences, 269: 1271-1278.
• Aguirre, L. F., A. Herrel, R. Van Damme, and E. Matthysen. 2003. The implications of food hardness for diet in bats. Functional Ecology, 17: 201-212.
• Darroch, J. N., and J. E. Mosimann. 1985. Canonical and principal components of shape. Biometrics, 72: 241-252.
• Dumont, E. R. 1997. Cranial shape in fruit, nectar, and exudate feeders: Implications for interpreting the fossil record. American Journal of Physical Anthropology, 102: 187-202.
• Dumont, E. R. 1999. The effect of food hardness on feeding behaviour in frugivorous bats (Phyllostomidae): an experimental study. Journal of Zoology (London), 248: 219-229.
• Dumont, E. R. 2000. Cranial morphology and diet in gliding marsupials and flying lemurs. Pp. 249-273, in Biology of gliding mammals (R. L. Goldingay and J. S. Scheibe, eds.). Filander Press, Fürth, 271 pp.
• Dumont, E. R. 2003. Bats and fruit: an ecomorphological approach. Pp. 398-429, in Bat ecology (T. H. Kunz and M. B. Fenton, eds.). University of Chicago Press, Chicago, 779 pp.
• Dumont, E. R., and A. Herrel. 2003. The effects of gape angle and bite point on bite force in bats. Journal of Experimental Biology, 206: 2117-2123.
• Dumont, E. R., and R. O’Neal. 2004. Fruit hardness, feeding behavior, and resource partitioning in Old World fruit bats (Family Pteropodidae). Journal of Mammalogy, 85: 8-14.
• Eby, P. 1998. An analysis of diet specialization in frugivorous Pteropus poliocephalus (Megachiroptera) in Australian subtropical rainforest. Australian Journal of Ecology, 23: 443-456.
• Falsetti, A. B., W. L. Jungers, and T. M. Cole. 1993. Morphometrics of the callitrichid forelimb — a case study in size and shape. International Journal of Primatology, 14: 551-572.
• Ferrarezzi, H., and E. D. A. Gimenez. 1996. Systematic patterns and the evolution of feeding habits in Chiroptera (Archonta: Mammalia). Journal of Computational Biology, 1: 75-94.
• Fleming, T. H. 1982. Foraging strategies of plant-visiting bats. Pp. 287-325, in Ecology of bats (T. H. Kunz, ed.). Plenum Publishing Co., New York, 425 pp.
• Fleming, T. H. 1986. Opportunism versus specialization: The evolution of feeding strategies in fru- givorous bats. Pp. 105-118, in Frugivores and seed dispersal (A. Estrada and T. H. Fleming, eds.). Dr W. Junk Publishers, Dordrecht, 398 pp.
• Fleming, T. H. 1993. Plant-visiting bats. American Scientist, 81: 460-467.
• Fleming, T. H. 2004. Community assembly rules for nectar- and fruit-eating vertebrates. Bat Research News, 44: 138.
• Fleming, T. H., R. Brietwisch, and G. H. Whitesides. 1987. Patterns of tropical frugivore diversity. Annual Review of Ecology and Systematics, 18: 91-109.
• Freeman, P. W. 1981. Correspondence of food habits and morphology in insectivorous bats. Journal of Mammalogy, 62: 166-173.
• Freeman, P. W. 1984. Functional cranial analysis of large animalivorous bats (Microchiroptera). Biological Journal of the Linnean Society, 21: 387-408.
• Freeman, P. W. 1988. Frugivorous and animalivorous bats (Microchiroptera) — dental and cranial adaptations. Biological Journal of the Linnean Society, 33: 249-272.
• Freeman, P. W. 1995. Nectarivorous feeding mechanisms in bats. Biological Journal of the Linnean Society, 56: 439—163.
• Freeman, P. W. 2000. Macroevolution in Microchiroptera: recoupling morphology and ecology with phylogeny. Evolutionary Ecology Research, 2: 317-335.
• Goudy-Trainor, A., and P. W. Freeman. 2002. Call parameters and facial features in bats: a surprising failure of form following function. Acta Chiropterologica, 4: 1-16.
• Herrel, A., E. De Grauw, and J. A. Lemos-Espinal. 2001. Head shape and bite performance in xenosaurid lizards. Journal of Experimental Zoology, 290: 101-107.
• Hill, J. E., and J. D. Smith. 1984. Bats: A natural history. Henry Ling Ltd., Dorchester, 243 pp.
• Hoyte, D. A. N. 1987. Muscles and cranial form. Pp. 123-144, in Mammalia depicta: morphogenesis of the mammalian skull (H. Kuhn and U. Zeller, eds.). Verlag Paul Parley, Hamburg, 200 pp.
• Hutcheon, J. M., J. A. W. Kirsch, and J. D. Pettigrew. 1998. Base-compositional biases and the bat problem. III. The question of microchiropteran monophyly. Philosophical Transactions of the Royal Society of London Series B. Biological Sciences, 353: 607-617.
• Hutcheon, J. M., J. W. Kirsch, and T. Garland. 2002. A comparative analysis of brain size in relation to foraging ecology and phylogeny in the Chiroptera. Brain Behavior and Evolution, 60: 165-180.
• Hylander, W. L., P. G. Picq, and K. R. Johnson. 1991. Masticatory stress hypotheses and the supraorbital region of primates. American Journal of Physical Anthropology, 86: 1-36.
• Jungers, W. L., A. B. Falsetti, and C. E. Wall. 1995. Shape, relative size, and size-adjustments in morphometrics. American Journal of Physical Anthropology, 38: 137-161.
• Kalko, E. K. V., and M. A. Condon. 1998. Echolocation, olfaction and fruit display: how bats find fruit of flagellichorous cucurbits. Functional Ecology, 12: 364-372.
• Koopman, K. F. 1993. Order Chiroptera. Pp. 137-241, in Mammal species of the world: a taxonomic and geographic reference (D. E. Wilson and D. M. Reeder, eds.). Smithsonian Institution Press, Washington D.C., 1206 pp.
• Larson, A., and J. B. Losos. 1996. Phylogenetic systematics of adaptation. Pp. 187-220, in Adaptation (M. R. Rose and G. V. Lauder, eds.). Academic Press, San Diego, 511 pp.
• Laska, M. 1990. Olfactory discrimination ability in short-tailed fruit bat, Carollia perspicillata (Chiroptera, Phyllostomatidae). Journal of Chemical Ecology, 16: 3291-3299.
• Luft, S., E. Curio, and B. Tacud. 2003. The use of olfaction in the foraging behaviour of the golden- mantled flying fox, Pteropus pumilus, and the greater musky fruit bat, Ptenochirus jagori (Megachiroptera: Pteropodidae). Naturwissenschaften, 90: 84-87.
• Mack, A. L. 1993. The sizes of vertebrate-dispersed fruits: a neotropical-paleotropical comparison. American Naturalist, 142: 840-856.
• Mickleburgh, S. P., A. M. Hutson, and P. A. Racey. 1992. Old World fruit bats: An action plan for their conservation. International Union for Conservation of Nature and Natural Resources, Gland, 252 pp.
• Miller, G. S., Jr. 1907. The families and genera of bats. Bulletin of the United States National Museum, 57: 1-282.
• Neuweiler, G. 2000. The biology of bats. Oxford University Press, Oxford, 310 pp.
• Nicolay, C. W. 2001. Ecological morphology and nectar-feeding performance in flower-visiting bats. Ph.D. Thesis, Kent State University, Ohio, 268 pp.
• Nicolay, C. W., and E. R. Dumont. 2000. An experimental analysis of feeding performance in Syconycteris australis (Megachiroptera, Pteropodidae). Mammalia, 64: 155-161.
• Noble, V. E., E. M. Kowalski, and M. J. Ravosa. 2000. Orbit orientation and the function of the mammalian postorbital bar. Journal of Zoology (London), 250: 405-418.
• Nowak, R. M. 1994. Walker’s bats of the world. Johns Hopkins University Press, Baltimore, 287 pp.
• Pedersen, S. C. 1993. Cephalometric correlates of echolocation in the chiroptera. Journal of Morphology, 218: 85-98.
• Pedersen, S. C. 1998. Morphometric analysis of the chiropteran skull with regard to mode of echolocation. Journal of Mammalogy, 79: 91-103.
• Pedersen, S. C. 2003. Skull growth and the acoustical axis of the head. Pp. 174-213, in Ontogeny, functional ecology, and evolution of bats (R. A. Adams and S. C. Pedersen, eds.). Cambridge University Press, Cambridge, 398 pp.
• Phillips, C. J. 2003. A theoretical consideration of dental morphology, ontogeny, and evolution in bats. Pp. 247-274, in Ontogeny, functional ecology, and evolution of bats (R. A. Adams and S. C. Pedersen, eds.). Cambridge University press, Cambridge, 398 pp.
• Ravosa, M. J., K. R. Johnson, and W. L. Hylander. 2000. Strain in the galago facial skull. Journal of Morphology, 245: 51-66.
• Reep, R. L., and K. P. Bhatnagar. 2003. Brain ontogeny and ecomorphology in bats. Pp. 93-136, in Ontogeny, functional ecology, and evolution of bats (R. A. Adams and S. C. Pedersen, eds.). Cambridge University Press, Cambridge, 398 pp.
• Rieger, J. F., and E. M. Jakob. 1988. The use of olfaction in food location by frugivorous bats. Biotropica, 20: 161-164.
• Ross, C. F. 2001. In vivo function of the craniofacial haft: The interorbital ‘pillar’. American Journal of Physical Anthropology, 116: 108-139.
• Simmons, N. B., and J. H. Geisler. 1998. Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bulletin of the American Museum of Natural History, 235: 4-182.
• Sokal, R. R., and F. J. Rohlf. 1995. Biometry: the principles and practice of statistics in biological research. W. H. Freeman and Company, New York, 887 pp.
• Strait, S. G., and D. J. Overdorff. 1996. Physical properties of fruits eaten by Malagasy primates. American Journal of Physical Anthropology, 22: 244A.
• Swanepoel, P., and H. H. Genoways. 1983. Brachyphylla cavernarum. Mammalian Species, 205: 1-6.
• Tabachnick, B. G., and L. S. Fidell. 1996. Using multivariate statistics. HarperCollins, New York, 880 pp.
• Teeling, E. C., M. Scally, D. J. Kao, M. L. Romagnoli, M. S. Springer, and M. J. Stanhope. 2000. Molecular evidence regarding the origin of echolocation and flight in bats. Nature, 403: 188-192.
• Teeling, E. C., O. Madsen, R. A. Van Den Bussche, W. W. De Jong, M. J. Stanhope, and M. S. Springer. 2002. Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats. Proceedings of the National Academy of Sciences of the United States of America, 99: 1431-1436.
• Thies, W., E. K. V. Kalko, and H.-U. Schnitzler. 1998. The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behavioral Ecology and Sociobiology, 42: 397-409.
• Ungar, P. S. 1995. Fruit preferences of 4 sympatric primate species at Ketambe, northern Sumatra, Indonesia. International Journal of Primatology, 16: 221-245.
• Utzurrum, R. C. B. 1995. Feeding ecology of Philippine fruit bats: Patterns of resource use and seed dispersal. Symposium of the Zoological Society of London, 67: 63-77.
• Van Cakenberghe, V., A. Herrel, and L. F. Aguirre. 2002. Evolutionary relationships between cranial shape and diet in bats (Mammalia: Chiroptera). Pp. 205-236, in Topics in functional and ecological vertebrate morphology (P. Aerts, K. D’Aout, A. Herrel, and R. Van Damme, eds.). Shaker Publishing, Maastricht, 359 pp.
• Van Den Bussche, R. A., S. R. Hoofer, and E. W. Hansen. 2002. Characterization and phylogenetic utility of the mammalian protamine P1 gene. Molecular Phylogenetics and Evolution, 22: 333-341.
• Wetterer, A. L., M. V. Rockman, and N. B. Simmons. 2000. Phylogeny of phyllostomid bats (Mammalia: Chiroptera): data from diverse morphological systems, sex chromosomes, and restriction sites. Bulletin of the American Museum of Natural History, 248: 4-200.
• Willig, M. R., G. R. Camilo, and S. J. Noble. 1993. Dietary overlap in frugivorous and insectivorous bats from edaphic cerrado habitats of Brazil. Journal of Mammalogy, 74: 117-128.
• Winter, Y., and O. von Helverson. 2003. Operational tongue length in phyllostomid nectar-feeding bats. Journal of Mammalogy, 84: 886-896.