Ecomorphological analysis of the masticatory apparatus in the seed-eating bats, genus Chiroderma (Chiroptera: Phyllostomidae)
Marcelo R. Nogueira,
Leandro R. Monteiro,
Adriano L. Peracchi,
Alexandre F. B. de Araújo,
Corresponding Author
Marcelo R. Nogueira
Laboratório de Mastozoologia–IB, Universidade Federal Rural do Rio de Janeiro, 23890-000, Seropédica, RJ, Brazil
*M. R. Nogueira. E-mail: [email protected]Search for more papers by this authorLeandro R. Monteiro
Laboratório de Ciências Ambientais–CBB, Universidade Estadual do Norte Fluminense, 28013-600, Campos dos Goytacazes, RJ, Brazil
Search for more papers by this authorAdriano L. Peracchi
Laboratório de Mastozoologia–IB, Universidade Federal Rural do Rio de Janeiro, 23890-000, Seropédica, RJ, Brazil
Search for more papers by this authorAlexandre F. B. de Araújo
Laboratório de Ecologia de Vertebrados, IB, Universidade Federal Rural do Rio de Janeiro, Brazil
Search for more papers by this author
Marcelo R. Nogueira,
Leandro R. Monteiro,
Adriano L. Peracchi,
Alexandre F. B. de Araújo,
Corresponding Author
Marcelo R. Nogueira
Laboratório de Mastozoologia–IB, Universidade Federal Rural do Rio de Janeiro, 23890-000, Seropédica, RJ, Brazil
*M. R. Nogueira. E-mail: [email protected]Search for more papers by this authorLeandro R. Monteiro
Laboratório de Ciências Ambientais–CBB, Universidade Estadual do Norte Fluminense, 28013-600, Campos dos Goytacazes, RJ, Brazil
Search for more papers by this authorAdriano L. Peracchi
Laboratório de Mastozoologia–IB, Universidade Federal Rural do Rio de Janeiro, 23890-000, Seropédica, RJ, Brazil
Search for more papers by this authorAlexandre F. B. de Araújo
Laboratório de Ecologia de Vertebrados, IB, Universidade Federal Rural do Rio de Janeiro, Brazil
Search for more papers by this authorAbstract
Recent data have shown that owing to their seed-predator capacity Chiroderma doriae and Chiroderma villosum trophically depart from all previously studied species within the canopy fruit-bat ensemble. In this paper, the hypothesis that morphological adaptations related to granivory have evolved in these bats is investigated and discussed. A canonical variate analysis was used to search for possible divergent trends between the masticatory apparatus of Chiroderma and other stenodermatines currently recognized in the same ensemble. A total of 142 specimens representative of eight species was included in the analysis. Species of Chiroderma can be discriminated from all other species in the sample based on the increased development of masseter-related variables (height of the anterior zygomatic arch, masseter moment arm, and masseter volume), which, in conjunction with other morphological characteristics (dentition and gape angle) discussed herein, corroborates the evolution of durophagy in this group. A complementary analysis based on a Mantel test revealed that the pattern of morphological differentiation that emerged from the canonical variate analysis does not agree with the one expected based solely on the phylogenetic relationships adopted for the canopy fruit-bats studied here. This result is consistent with the hypothesis that morphological adaptations related to granivory have evolved in Chiroderma.
REFERENCES
- Aguirre, L. F., Herrel, A., Van Damme, R. & Matthysen, E. (2002). Ecomorphological analysis of trophic niche partitioning in a tropical savanna bat community. Proc. R. Soc. Lond. B Biol. Sci. 269: 1271–1278.
- Aguirre, L. F., Herrel, A., Van Damme, R. & Mathyssen, E. (2003). The implications of food hardness for diet in bats. Funct. Ecol. 17: 201–212.
- Anapol, F. & Lee, S. (1994). Morphological adaptation to diet in platyrrhine primates. Am. J. Phys. Anthropol. 94: 239–261.
- Baker, R. J., Hoofer, S. R., Porter, C. A. & Van Den Bussche, R. A. (2003). Diversification among New World leaf-nosed bats: an evolutionary hypothesis and classification inferred from digenomic congruence of DNA sequence. Occas. Pap. Mus. Tex. Tech Univ. 230: 1–32.
- Barlow, K. E., Jones, G. & Barratt, E. M. (1997). Can skull morphology be used to predict ecological relationships between bat species? A test using two cryptic species of pipistrelle. Proc. R. Soc. Lond. B Biol. Sci. 264: 1695–1700.
- Barquez, R. M., Mares, M. A. & Braun, J. K. (1999). The bats of Argentina. Spec. Publ. Mus. Tex. Tech Univ. 42: 1–257.
- Biknevicius, A. R. & Ruff, C. B. (1992). The structure of the mandibular corpus and its relationship to feeding behaviours in extant carnivorans. J. Zool. (Lond.) 228: 479–507.
- Bolnick, D. I., Svanbäck, R., Fordyce, J. A., Yang, L. H., Davis, J. M., Hulsey, C. D. & Forister, M. L. (2003). The ecology of individuals: incidence and implications of individual specialization. Am. Nat. 161: 1–28.
- Bonaccorso, F. J. (1979). Foraging and reproductive ecology in a Panamanian bat community. Bull. Fla State Mus. Biol. Sci. 24: 359–408.
- Bouvier, M. & Hylander, W. L. (1981). Effect of bone strain on cortical bone structure in macaques (Macaca mulatta). J. Morphol. 167: 1–12.
- Cavalcanti, M. J. (2001). Test for association between two symmetric distance matrices with permutation iterations. Version 1.14. Rio de Janeiro : Museu Nacional do Rio de Janeiro.
- De Gueldre, G. & de Vree, F (1988). Quantitative electromyography of the masticatory muscles of Pteropus giganteus (Megachiroptera). J. Morphol. 196: 73–106.
- De Gueldre, G. & de Vree, F. (1990). Biomechanics of the masticatory apparatus of Pteropus giganteus (Megachiroptera). J. Zool. (Lond.) 220: 311–332.
10.1111/j.1469-7998.1990.tb04310.x Google Scholar
- Dobson, G. E. (1878). Catalogue of the Chiroptera in the collection of the British Museum. London : British Museum.
- Dumont, E. R. (1997). Cranial shape in fruit, nectar and exudates feeders: implications for interpreting the fossil record. Am. J. Phys. Anthropol. 102: 187–202.
10.1002/(SICI)1096-8644(199702)102:2<187::AID-AJPA4>3.0.CO;2-W CASPubMedWeb of Science®Google Scholar
- Dumont, E. R. (1999). The effect of food hardness on feeding behaviour in frugivorous bats (Family Phyllostomidae): an experimental study. J. Zool. (Lond.) 248: 219–229.
- Dumont, E. R. (2003). Bats and fruit: an ecomorphological approach. In Bat ecology: 398–429. T. H. Kunz & M. B. Fenton (Eds). Chicago : University of Chicago Press.
- Dumont, E. R. & Herrel, A. (2003). The effects of gape angle and bite point on bite force in bats. J. exp. Biol. 206: 2117–2123.
- Dumont, E. R. & O'Neal, R. (2004). Food hardness and feeding behaviour in old world fruit-bats (Pteropodidae). J. Mammal. 85: 8–14.
- Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125: 1–15.
- Figueiredo, R. A. (1999). A comparison of the quality of dispersion of Ficus eximia Schott (Moraceae) by birds and bats in southeastern Brazil. Leandra 14: 37–42.
- Figueiredo, R. A. & Perin, E. (1995). Germination ecology of Ficus luschnathiana drupelets after bird and bat ingestion. Acta Oecol. 16: 71–75.
- Fleming, T. H. (1988). The short-tailed fruit bat: a study in plant-animal interactions. Chicago : University of Chicago Press.
- Freeman, P. W. (1979). Specialized insectivory: beetle-eating and moth-eating molossid bats. J. Mammal. 60: 467–479.
- Freeman, P. W. (1981). Correspondence of food habits and morphology in insectivorous bats. J. Mammal. 62: 166–173.
- Freeman, P. W. (1988). Frugivorous and animalivorous bats (Microchiroptera): dental and cranial adaptations. Biol. J. Linn. Soc. 33: 249–272.
- Freeman, P. W. (1995). Nectarivorous feeding mechanisms in bats. Biol. J. Linn. Soc. 56: 439–463.
- Freeman, P. W. (1998). Form, function, and evolution in skulls and teeth of bats. In Bat biology and conservation: 140–156. T. H. Kunz & P. A. Racey (Eds). Washington , DC : Smithsonian Institution Press.
- Freeman, P. W. (2000). Macroevolution in Microchiroptera: recoupling morphology and ecology with phylogeny. Evol. Ecol. Res. 2: 317–335.
- Garland, T., Jr, Midford, P. E. & Ives, A. R. (1999). An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Am. Zool. 39: 374–388.
- Giannini, N. P. & Kalko, E. K. V. (2004). Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105: 209–220.
- Handley, C. O., Jr, Gardner, A. L. & Wilson, D. E. (1991). Food habits. In Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panama. Smithsonian Contributions to Zoology No. 511: 141–146. C. O. Handley, D. E. Wilson & A. L. Gardner (Eds). Washington , DC : Smithsonian Institution Press.
- Herring, S. W. & Herring, S. E. (1974). The superficial masseter and gape in mammals. Am. Nat. 108: 561–576.
- Hylander, W. L. & Johnson, K. R. (1997). In vivo bone strain patterns in the zygomatic arch of macaques and the significance of these patterns for functional interpretations of craniofacial form. Am. J. Phys. Anthropol 102: 203–232.
10.1002/(SICI)1096-8644(199702)102:2<203::AID-AJPA5>3.0.CO;2-Z CASPubMedWeb of Science®Google Scholar
- Jacobs, D. S. (1996). Morphological divergence in an insular bat, Lasiurus cinereus semotus. Funct. Ecol. 10: 622–630.
- James, F. C. & McCulloch, C. E. (1990). Multivariate analysis in ecology and systematics: panacea or Pandora's box Annu. Rev. Ecol. Syst. 21: 129–166.
- Jones, G. & Rydell, J. (2003). Attack and defense: interactions between echolocating bats and their insect prey. In Bat ecology: 301–345. T. H. Kunz & M. B. Fenton (Eds). Chicago : University of Chicago Press.
- Kalko, E. K. V. & Handley, C. O., Jr (2001). Neotropical bats in the canopy: diversity, community structure, and implications for conservation. Plant Ecol. 153: 319–333.
- Kalko, E. K. V., Herre, E. A. & Handley, C. O., Jr (1996). Relation of fig fruit characteristics to fruit-eating bats in the New and Old World tropics. J. Biogeogr. 23: 565–576.
- Koopman, K. F. (1994). Chiroptera: Systematics. Handbook of Zoology, VIII, Mammalia Part 60. New York : Walter de Gruyter.
- Kunz, T. H. & Ingalls, A. (1994). Folivory in bats: an adaptation derived from frugivory. Funct. Ecol. 8: 665–668.
- Lim, B. K., Pedro, W. A. & Passos, F. C. (2003). Differentiation and species status of the Neotropical yellow-eared bats Vampyressa pusilla and V. thyone (Phyllostomidae) with a molecular phylogeny and review of the genus. Acta Chiropt. 5: 15–29.
- Lucas, P. W. & Luke, D. A. (1984). Chewing it over: basic principles of food breakdown. In Food acquisition and processing in primates: 283–301. D. J. Chivers, B. A. Wood & A. Bilsborough (Eds). New York : Plenum Press.
10.1007/978-1-4757-5244-1_12 Google Scholar
- Maynard-Smith, J. & Savage, R. J. G. (1959). The mechanics of mammalian jaws. Sch. Sci. Rev. 40: 289–301.
- Mickleburgh, S. P., Hutson, A. M. & Racey, P. A. (1992). Old World fruit bats: an action plan for their conservation. Gland , Switzerland : International Union for Conservation of Nature and Natural Resources.
- Miller, G. S. Jr (1907). The families and genera of bats. Bull. U.S. Natl. Mus. 57: 1–282.
- Monteiro, L. R., Duarte, L. C. & Reis, S. F. (2003). Environmental correlates of geographical variation in skull and mandible shape of the punaré rat Thrichomys apereoides (Rodentia: Echimyidae). J. Zool. (Lond.) 261: 47–57.
- Monteiro, L. R. & Reis, S. F. (1999). Principios de morfometria geometrica. Ribeirão Preto : Editora Holos.
- Muchhala, N. & Jarrín-V., P. (2002). Flower visitation by bats in cloud forests of Western Ecuador. Biotropica 34: 387–395.
- Nogueira, M. R. & Peracchi, A. L. (2002). The feeding specialization in Chiroderma doriae with comments on its conservational implications. Chir. Neotrop. 8: 143–148.
- Nogueira, M. R. & Peracchi, A. L. (2003). Fig-seed predation by two species of Chiroderma: discovery of a new feeding strategy in bats. J. Mammal. 84: 225–233.
- Page, R. D. M. (2001). TREEVIEW: An application to display phylogenetic trees on personal computers. Comput. Applic. Biosci. 12: 357–358.
- Patterson, B. D., Willig, M. R. & Stevens, R. D. (2003). Trophic strategies, niche partitioning, and patterns of ecological organization. In Bat ecology: 536–579. T. H. Kunz & M. B. Fenton (Eds). Chicago : University of Chicago Press.
- Pérez-Barbería, F. J. & Gordon, I. J. (1999). The functional relationship between feeding type and jaw and cranial morphology in ungulates. Oecologia (Berl.) 118: 157–165.
- Peterson, R. L. (1968). A new bat of the genus Vampyressa from Guyana, South America. R. Ont. Mus. Life Sci. Contrib. 73: 1–17.
- Phillips, C. J. (2000). A theoretical consideration of dental morphology, ontogeny, and evolution in bats. In Ontogeny, functional ecology, and evolution of bats: 247–274. R. A. Adams & S. C. Pedersen (Eds). Cambridge : Cambridge University Press.
10.1017/CBO9780511541872.008 Google Scholar
- Porter, C. A. & Baker, R. J. (2004). Systematics of Vampyressa and related genera of phyllostomid bats as determined by cytochrome-b sequences. J. Mammal. 85: 126–132.
- Radinsky, L. (1985). Patterns in the evolution of ungulate jaw shape. Am. Zool. 25: 303–314.
- Simmons, N. B. & Conway, T. M. (2003). Evolution of ecological diversity in bats. In Bat ecology: 493–535. T. H. Kunz & M. B. Fenton (Eds). Chicago : University of Chicago Press.
- Slaughter, B. H. (1970). Evolutionary trends of chiropteran dentitions. In About bats: 51–83. B. H. Slaughter & D. W. Walton (Eds). Dallas : Southern Methodist University Press.
- Sokal, R. R. & Rohlf, F. J. (1995). Biometry: the principles and practice of statistics in biological research. New York : W. H. Freeman.
- SPSS (1996). SPSS for Windows. Release 7.5. Chicago : SPSS.
- StatSoft (1995). STATISTICA for Windows [Computer program manual]. Tulsa , OK : StatSoft.
- Strait, S. G. (1993). Molar morphology and food texture among small-bodied insectivorous mammals. J. Mammal. 74: 391–402.
- Swartz, S. M., Freeman, P. W. & Stockwell, E. F. (2003). Ecomorphology of bats: comparative and experimental approaches relating structural design to ecology. In Bat ecology: 580–621. T. H. Kunz & M. B. Fenton (Eds). Chicago : University of Chicago Press.
- Taddei, V. A. (1979). Phyllostomidae (Chiroptera) do Norte-Ocidental do Estado de São Paulo. III – Stenodermatinae. Cie. Cult. 31: 900–914.
- Van Cakenberghe, V., Herrel, A. & Aguirre, L. F. (2002). Evolutionary relationships between cranial shape and diet in bats (Mammalia: Chiroptera). In Topics in functional and ecological vertebrate morphology: 205–236. P. Aerts, K. D'aout, A. Herrel & R. Damme (Eds). Maastricht : Shaker.
- Vaughan, T. A. (1972). Mammalogy. Philadelphia : W. B. Saunders.
- Von Helversen, O. & Winter, Y. (2003). Glossophagine bats and their flowers: costs and benefits for plants and pollinators. In Bat ecology: 346–397. T. H. Kunz & M. B. Fenton (Eds). Chicago : University of Chicago Press.
- Wetterer, A. L., Rockman, M. V. & Simmons, N. B. (2000). Phylogeny of phyllostomid bats (Mammalia, Chiroptera): data from diverse morphological systems, sex chromosomes, and restriction sites. Bull. Am. Mus. Nat. Hist. 248: 1–200.
10.1206/0003-0090(2000)248<0001:POPBMC>2.0.CO;2 Google Scholar
- Willis, K. B., Willig, M. R. & Jones, J. K. Jr (1990). Vampyrodes caraccioli. Mammal. Spec. 359: 1–4.
10.2307/3504287 Google Scholar
