Built to bite: cranial design and function in the wrinkle‐faced bat

One of the major goals of evolutionary biology is to explain phenotypic diversity and understand the limits imposed by those phenotypes. The cranial morphology of the wrinkle-faced bat Centurio senex (Family Phyllostomidae) is bizarre and enigmatic. Its extremely short and wide skull consistently emerges as an outlier in morphological studies and many researchers have speculated about its function. Here, we investigate the hypothesis that the unique skull morphology of Centurio is associated with the ability to generate high bite forces and/or high bite forces at wide gapes. We accomplish this by comparing bite force data gathered in the field and estimates of gape limitations gathered from museum specimens. We also examine the possibility that Centurio uses unique feeding behaviors that may impose unique loading regimes on the facial skeleton. We found that relative to head size, Centurio generates the strongest bites known for any fruit-eating phyllostomid bat, but that its ability to generate high bite forces at wide gape angles is likely limited. We also propose that its exceptionally strong bite indicates the ability to consume hard food items when other resources are limited, and that these ‘resource bottlenecks’ may have imposed strong selective pressure on its skull morphology. Behavioral data indicate that Centurio exhibits a unique reliance on unilateral biting (loading) during feeding. Based on data summarizing bite force, estimates of gape ability and feeding behavior, we suggest that Centurio’s exceptionally short and wide skull reflects adaptations for high bite forces and repeated unilateral loading of the facial skeleton during feeding.

[1]  R. Sokal,et al.  Biometry: The Principles and Practice of Statistics in Biological Research (2nd ed.). , 1982 .

[2]  Anthony Herrel,et al.  Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analyses , 1999 .

[3]  A. Herrel,et al.  Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource , 2008, Proceedings of the National Academy of Sciences.

[4]  N. Seavy,et al.  A Comparison of the Phyllostomid Bat Assemblages in Undisturbed Neotropical Forest and in Forest Fragments of a Slash‐and‐Burn Farming Mosaic in Petén, Guatemala 1 , 2000 .

[5]  Anthony Herrel,et al.  The effects of gape angle and bite point on bite force in bats , 2003, Journal of Experimental Biology.

[6]  Patricia W. Freeman,et al.  Ecomorphology of Bats: Comparative and Experimental Approaches Relating Structural Design to Ecology , 2003 .

[7]  S. Herring,et al.  The Superficial Masseter and Gape in Mammals , 1974, The American Naturalist.

[8]  A. Greenhall,et al.  A review of the bats of Trinidad and Tobago : descriptions, rabies infection, and ecology. Bulletin of the AMNH ; v. 122, article 3 , 1961 .

[9]  M. Fenton,et al.  Phyllostomid Bats (Chiroptera - Phyllostomidae) as Indicators of Habitat Disruption in the Neotropics , 1992 .

[10]  W. Greaves The relative positions of the jaw joint and the tooth row in mammals , 1998 .

[11]  E. Kalko,et al.  CHAPTER 16 – Organization, Diversity, and Long-Term Dynamics of a Neotropical Bat Community , 1996 .

[12]  A. Herrel,et al.  The implications of food hardness for diet in bats , 2003 .

[13]  Ian R Grosse,et al.  Finite-element analysis of biting behavior and bone stress in the facial skeletons of bats. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[14]  J. Paradiso A REVIEW OF THE WRINKLE-FACED BATS (CENTURIO SENEX GRAY), WITH DESCRIPTION OF A NEW SUBSPECIES , 1967 .

[15]  T. Schoener,et al.  Predator-induced behaviour shifts and natural selection in field-experimental lizard populations , 2004, Nature.

[16]  E. Kalko,et al.  Relation of fig fruit characteristics to fruit‐eating bats in the New and Old World tropics , 1996 .

[17]  G. Storch Funktionsmorphologische Untersuchungen an der Kaumuskulatur - und an korrelierten Schädelstrukturen der Chiropteren , 1968 .

[18]  Patricia W. Freeman Canine teeth of bats (Microchiroptera): size, shape and role in crack propagation , 1992 .

[19]  F. Bonaccorso,et al.  FEEDING BEHAVIOUR AND FORAGING STRATEGIES OF CAPTIVE PHYLLOSTOMID FRUIT BATS: AN EXPERIMENTAL STUDY , 1987 .

[20]  E. Dumont Feeding mechanisms in bats: variation within the constraints of flight. , 2007, Integrative and comparative biology.

[21]  R. Medellín,et al.  Vegetation complexity and bat‐plant dispersal in Calakmul, Mexico , 2009 .

[22]  E. Dumont,et al.  Connecting behaviour and performance: the evolution of biting behaviour and bite performance in bats , 2009, Journal of evolutionary biology.

[23]  R. Nowak Walker's bats of the world , 1994 .

[24]  A. Estrada,et al.  Bat species richness and abundance in tropical rain forest fragments and in agricultural habitats at Los Tuxtlas, Mexico , 1993 .

[25]  Patricia W. Freeman Frugivorous and animalivorous bats (Microchiroptera): dental and cranial adaptations , 1988 .

[26]  M A Spencer,et al.  Constraints on masticatory system evolution in anthropoid primates. , 1999, American journal of physical anthropology.

[27]  L. Rome,et al.  Mechanical and Metabolic Design of the Muscular System in Vertebrates , 2011 .

[28]  Peter Aerts,et al.  Morphological and mechanical determinants of bite force in bats: do muscles matter? , 2008, Journal of Experimental Biology.

[29]  L. Sternberg,et al.  Trophic relationships in a neotropical bat community: a preliminary study using carbon and nitrogen isotopic signatures , 1998 .

[30]  A. Herrel,et al.  Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[31]  John G. Fleagle,et al.  Neotropical rainforest mammals: A field guide , 1991 .

[32]  K. Stoner Differential habitat use and reproductive patterns of frugivorous bats in tropical dry forest of northwestern Costa Rica , 2001 .

[33]  N. Seavy,et al.  A Comparison of the Phyllostomid Bat Assemblages in Undisturbed Neotropical Forest and in Forest Fragments of a Slash-and-Burn Farming Mosaic in Petén, Guatemala1 , 2000 .

[34]  R. Stevens Functional morphology meets macroecology: size and shape distributions of New World bats , 2005 .

[35]  M. Rockman,et al.  PHYLOGENY OF PHYLLOSTOMID BATS (MAMMALIA: CHIROPTERA): DATA FROM DIVERSE MORPHOLOGICAL SYSTEMS, SEX CHROMOSOMES, AND RESTRICTION SITES , 2000 .

[36]  Miguel Equihua,et al.  Bat Diversity and Abundance as Indicators of Disturbance in Neotropical Rainforests , 2000, Conservation biology : the journal of the Society for Conservation Biology.

[37]  A. Peracchi,et al.  FIG-SEED PREDATION BY 2 SPECIES OF CHIRODERMA: DISCOVERY OF A NEW FEEDING STRATEGY IN BATS , 2003 .

[38]  G. F. Meenaghan,et al.  Biology of bats of the New World family Phyllostomatidae , 1976 .

[39]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[40]  A. Herrel,et al.  Functional Consequences of Extreme Morphologies in the Craniate Trophic System , 2008, Physiological and Biochemical Zoology.

[41]  B. Kirkpatrick,et al.  Wildlife of the Tibetan Steppes , 2000 .

[42]  Richard Shine,et al.  An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia , 2006, Proceedings of the Royal Society B: Biological Sciences.

[43]  R L Lieber,et al.  Sarcomere length operating range of vertebrate muscles during movement. , 2001, The Journal of experimental biology.

[44]  A. Peracchi,et al.  Ecomorphological analysis of the masticatory apparatus in the seed-eating bats, genus Chiroderma (Chiroptera: Phyllostomidae) , 2005 .

[45]  E. Kalko,et al.  Trophic structure in a large assemblage of phyllostomid bats in Panama , 2004 .

[46]  W. López-Forment,et al.  Additonal Records of Some Mexican Bats , 1979 .

[47]  E. Dumont The effect of food hardness on feeding behaviour in frugivorous bats (Phyllostomidae): an experimental study , 1999 .

[48]  E. Dumont,et al.  Food Hardness and Feeding Behavior in Old World Fruit Bats (Pteropodidae) , 2004 .