Translator Disclaimer
1 June 2004 Patterns of Diversity in Cranial Shape Among Plant-Visiting Bats
Author Affiliations +
Abstract

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.

LITERATURE CITED

  1. K. K. Acharya , R. Anubba , and A. Krishna . 1998. Relative role of olfactory cues and certain non-olfactory factors in foraging of fruiteating bats. Behavioural Processes, 44: 59–64. Google Scholar

  2. L. F. Aguirre , 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. Google Scholar

  3. L. F. Aguirre , A. Herrel , R. Van Damme , and E. Matthysen . 2003. The implications of food hardness for diet in bats. Functional Ecology, 17: 201–212. Google Scholar

  4. J. N. Darroch , and J. E. Mosimann . 1985. Canonical and principal components of shape. Biometrics, 72: 241–252. Google Scholar

  5. E. R. Dumont 1997. Cranial shape in fruit, nectar, and exudate feeders: Implications for interpreting the fossil record. American Journal of Physical Anthropology, 102: 187–202. Google Scholar

  6. E. R. Dumont 1999. The effect of food hardness on feeding behaviour in frugivorous bats (Phyllostomidae): an experimental study. Journal of Zoology (London), 248: 219–229. Google Scholar

  7. E. R. Dumont 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. Google Scholar

  8. E. R. Dumont 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. Google Scholar

  9. E. R. Dumont , and A. Herrel . 2003. The effects of gape angle and bite point on bite force in bats. Journal of Experimental Biology, 206: 2117–2123. Google Scholar

  10. E. R. Dumont , 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. Google Scholar

  11. P. Eby 1998. An analysis of diet specialization in frugivorous Pteropus poliocephalus (Megachiroptera) in Australian subtropical rainforest. Australian Journal of Ecology, 23: 443–456. Google Scholar

  12. A. B. Falsetti , 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. Google Scholar

  13. H. Ferrarezzi , 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. Google Scholar

  14. T. H. Fleming 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. Google Scholar

  15. T. H. Fleming 1986. Opportunism versus specialization: The evolution of feeding strategies in frugivorous bats. Pp. 105–118, in Frugivores and seed dispersal ( A. Estrada and T. H. Fleming , eds.). Dr W. Junk Publishers, Dordrecht, 398 pp. Google Scholar

  16. T. H. Fleming 1993. Plant-visiting bats. American Scientist, 81: 460–467. Google Scholar

  17. T. H. Fleming 2004. Community assembly rules for nectar- and fruit-eating vertebrates. Bat Research News, 44: 138. Google Scholar

  18. T. H. Fleming , R. Brietwisch , and G. H. Whitesides . 1987. Patterns of tropical frugivore diversity. Annual Review of Ecology and Systematics, 18: 91–109. Google Scholar

  19. P. W. Freeman 1981. Correspondence of food habits and morphology in insectivorous bats. Journal of Mammalogy, 62: 166–173. Google Scholar

  20. P. W. Freeman 1984. Functional cranial analysis of large animalivorous bats (Microchiroptera). Biological Journal of the Linnean Society, 21: 387–408. Google Scholar

  21. P. W. Freeman 1988. Frugivorous and animalivorous bats (Microchiroptera) — dental and cranial adaptations. Biological Journal of the Linnean Society, 33: 249–272. Google Scholar

  22. P. W. Freeman 1995. Nectarivorous feeding mechanisms in bats. Biological Journal of the Linnean Society, 56: 439–463. Google Scholar

  23. P. W. Freeman 2000. Macroevolution in Microchiroptera: recoupling morphology and ecology with phylogeny. Evolutionary Ecology Research, 2: 317–335. Google Scholar

  24. A. Goudy-Trainor , and P. W. Freeman . 2002. Call parameters and facial features in bats: a surprising failure of form following function. Acta Chiropterologica, 4: 1–16. Google Scholar

  25. A. Herrel , E. De Grauw , and J. A. Lemos-Espinal . 2001. Head shape and bite performance in xenosaurid lizards. Journal of Experimental Zoology, 290: 101–107. Google Scholar

  26. J. E. Hill , and J. D. Smith . 1984. Bats: A natural history. Henry Ling Ltd., Dorchester, 243 pp. Google Scholar

  27. D. A. N. Hoyte 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. Google Scholar

  28. J. M. Hutcheon , 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. Google Scholar

  29. J. M. Hutcheon , 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. Google Scholar

  30. W. L. Hylander , 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. Google Scholar

  31. W. L. Jungers , A. B. Falsetti , and C. E. Wall . 1995. Shape, relative size, and size-adjustments in morphometrics. American Journal of Physical Anthropology, 38: 137–161. Google Scholar

  32. E. K. V. Kalko , and M. A. Condon . 1998. Echolocation, olfaction and fruit display: how bats find fruit of flagellichorous cucurbits. Functional Ecology, 12: 364–372. Google Scholar

  33. K. F. Koopman 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. Google Scholar

  34. A. Larson , 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. Google Scholar

  35. M. Laska 1990. Olfactory discrimination ability in short-tailed fruit bat, Carollia perspicillata (Chiroptera, Phyllostomatidae). Journal of Chemical Ecology, 16: 3291–3299. Google Scholar

  36. S. Luft , E. Curio , and B. Tacud . 2003. The use of olfaction in the foraging behaviour of the goldenmantled flying fox, Pteropus pumilus, and the greater musky fruit bat, Ptenochirus jagori (Megachiroptera: Pteropodidae). Naturwissenschaften, 90: 84–87. Google Scholar

  37. A. L. Mack 1993. The sizes of vertebrate-dispersed fruits: a neotropical-paleotropical comparison. American Naturalist, 142: 840–856. Google Scholar

  38. S. P. Mickleburgh , 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. Google Scholar

  39. G. S. Miller Jr . 1907. The families and genera of bats. Bulletin of the United States National Museum, 57: 1–282. Google Scholar

  40. G. Neuweiler 2000. The biology of bats. Oxford University Press, Oxford, 310 pp. Google Scholar

  41. C. W. Nicolay 2001. Ecological morphology and nectar-feeding performance in flower-visiting bats. Ph.D. Thesis, Kent State University, Ohio, 268 pp. Google Scholar

  42. C. W. Nicolay , and E. R. Dumont . 2000. An experimental analysis of feeding performance in Syconycteris australis (Megachiroptera, Pteropodidae). Mammalia, 64: 155–161. Google Scholar

  43. V. E. Noble , 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. Google Scholar

  44. R. M. Nowak 1994. Walker's bats of the world. Johns Hopkins University Press, Baltimore, 287 pp. Google Scholar

  45. S. C. Pedersen 1993. Cephalometric correlates of echolocation in the chiroptera. Journal of Morphology, 218: 85–98. Google Scholar

  46. S. C. Pedersen 1998. Morphometric analysis of the chiropteran skull with regard to mode of echolocation. Journal of Mammalogy, 79: 91–103. Google Scholar

  47. S. C. Pedersen 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. Google Scholar

  48. C. J. Phillips 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. Google Scholar

  49. M. J. Ravosa , K. R. Johnson , and W. L. Hylander . 2000. Strain in the galago facial skull. Journal of Morphology, 245: 51–66. Google Scholar

  50. R. L. Reep , 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. Google Scholar

  51. J. F. Rieger , and E. M. Jakob . 1988. The use of olfaction in food location by frugivorous bats. Biotropica, 20: 161–164. Google Scholar

  52. C. F. Ross 2001. In vivo function of the craniofacial haft: The interorbital ‘pillar’. American Journal of Physical Anthropology, 116: 108–139. Google Scholar

  53. N. B. Simmons , 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. Google Scholar

  54. R. R. Sokal , and F. J. Rohlf . 1995. Biometry: the principles and practice of statistics in biological research. W. H. Freeman and Company, New York, 887 pp. Google Scholar

  55. S. G. Strait , and D. J. Overdorff . 1996. Physical properties of fruits eaten by Malagasy primates. American Journal of Physical Anthropology, 22: 244A. Google Scholar

  56. P. Swanepoel , and H. H. Genoways . 1983. Brachyphylla cavernarum. Mammalian Species, 205: 1–6. Google Scholar

  57. B. G. Tabachnick , and L. S. Fidell . 1996. Using multivariate statistics. HarperCollins, New York, 880 pp. Google Scholar

  58. E. C. Teeling , 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. Google Scholar

  59. E. C. Teeling , 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. Google Scholar

  60. W. Thies , 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. Google Scholar

  61. P. S. Ungar 1995. Fruit preferences of 4 sympatric primate species at Ketambe, northern Sumatra, Indonesia. International Journal of Primatology, 16: 221–245. Google Scholar

  62. R. C. B. Utzurrum 1995. Feeding ecology of Philippine fruit bats: Patterns of resource use and seed dispersal. Symposium of the Zoological Society of London, 67: 63–77. Google Scholar

  63. V. Van Cakenberghe , 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. Google Scholar

  64. R. A. Van Den Bussche , 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. Google Scholar

  65. A. L. Wetterer , 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. Google Scholar

  66. M. R. Willig , 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. Google Scholar

  67. Y. Winter , and O. Von Helverson . 2003. Operational tongue length in phyllostomid nectar-feeding bats. Journal of Mammalogy, 84: 886–896. Google Scholar

© Museum and Institute of Zoology PAS
Elizabeth R. Dumont "Patterns of Diversity in Cranial Shape Among Plant-Visiting Bats," Acta Chiropterologica 6(1), 59-74, (1 June 2004). https://doi.org/10.3161/001.006.0105
Received: 3 November 2003; Accepted: 1 January 2004; Published: 1 June 2004
JOURNAL ARTICLE
16 PAGES


SHARE
ARTICLE IMPACT
Back to Top