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Form, Function, and Evolution in Skulls and Teeth of Bats University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers in Natural Resources Natural Resources, School of May 1998 Form, Function, and Evolution in Skulls and Teeth of Bats Patricia W. Freeman University of Nebraska-Lincoln, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/natrespapers Part of the Natural Resources and Conservation Commons Freeman, Patricia W., "Form, Function, and Evolution in Skulls and Teeth of Bats" (1998). Papers in Natural Resources. 9. https://digitalcommons.unl.edu/natrespapers/9 This Article is brought to you for free and open access by the Natural Resources, School of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Natural Resources by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. 9 Form, Function, and Evolution in Skulls and Teeth of Bats PATRICIA W FREEMAN Bats provide a model system for tracking change from the stylar shelves and elongated skulls with larger brain vol- primitive mammalian tooth pattern to patterns indicating umes and external ears than their insectivorous relatives. As the more-derived food habits of carnivory, nectarivory, in terrestrial mammals, however, there is no clear distinc- frugivory, and sanguinivory. Whereas microchiropteran tion between insectivorous and carnivorous species (Savage bats show all these transitions, megachiropterans illustrate 1977; Freeman 1984). Microchiropteran nectarivores are an alternative pattern concerned only with frugivory and also on a continuum with insectivores but are characteris- nectarivory. In rnicrochiropterans, it is likely that carnivory tically long-snouted with large canines and diminutive post- nectarivory, frugivory, and sanguinivory are all derived canine teeth (Freeman 1995). Finally among microchirop- from a dilambdodont insectivorous tooth pattern. Mega- terans, frugivores differ from insectivore 1carnivores and chiropterans are troublesome because they appear as nec- insectivore/nectarivores by having a substantially different tarivores or frugivores without a clear relationship to ances- cusp pattern on the molars. The paracone and metacone tral taxa. are pushed labially or buccally to become a simple, raised The nature of the food item and how teeth respond to but sharpened ridge at the perimeter of the dental arcade that item evolutionarily is an issue I have addressed pre- (Freeman 1988, 1995). viously diet by diet (Freeman 1979, 1981a, 1981b, 1984, First I examine function of dfferently shaped skulls and 1988, 1995). With the insectivorous family Molossidae, palates of bats in different dietary groups. Among Megachi- and among insectivorous microchiropteran bats in general, roptera, frugivores are on a continuum with nectarivores, consumers of hard-bodied prey can be dstinguished from but there are characteristics of robustness that appear to be consumers of soh-bodied prey by their more robust mandi- good indicators of det that distinguish the two (Freeman bles and crania, larger but fewer teeth, longer canines, and 199.5). Megachiropterans have several convergent charac- abbreviated third upper molars (M3; Freeman 1979, 1981 a, teristics in common with microchiropteran nectarivores. I 1981b; Strait 1993a, 1993b). Carnivorous microchiropterans believe this convergence is not only the key to explaining have distinctive large upper molars with lengthened meta- cranial and palatal shape and jaw function in bats but also is Bat Teeth and Skulls 141 critical to understanding the evolution of nectarivory and canine length, zygomatic breadth, and temporal height; fiugivory in chiropterans. Associated with the shape of the Freeman 1984, 1988, 1992, 1995). palate is the way that allocation and emphasis of tooth ma- Experimental work examining form and function in bat terial on the toothrow shift between suborders. The relative canine teeth involved finite-element modeling and photo- area that each kind of tooth occupies on the toothrow is elastic analysis. Shapes of cross sections in canine teeth can quantified and serves as the basis for my interpretations. be edged and nonedged (Freeman 1992), and experiments A second goal is to examine function in bat teeth. Here I with models of teeth puncturing a substance can show how synthesize my past work on tooth function, particularly these two different types of cross sections initiate different with regard to canines and molars, and introduce a novel patterns of stress or toothmarks in a substance ("food; way to examine function in canines. Function in more com- Freeman and Weins, unpublished data). Finite-elementmod- plex teeth involves a review of the principal cusps on the eling is a mathematical description of dimensional or geo- upper and lower molars and how cusp patterns have evolved metric change in a structure when a force is applied to de- relative to different diets. Specifically, I contrast carnivory in form the structure to reveal where the most intense stresses terrestrial mammals and bats, insectivory in insectivorous should occur (Zienkiewicz and Taylor 1989; Rensberger and nectarivorous species, and fiugivory in mega- and mi- 1995). crochiropterans. Finally, I suggest that the evolution of di- Two-dmensional models were constructed to show lambdonty can be correlated with packaging and digest- stresses occurring in the "food when penetrated by teeth ibility of the food item. with 30°, 60°, and 90" angles at their edges and a circular or nonedged tooth. In three dimensions, actual stress analysis Study Methods tests were performed with a metal cone and a pyramid with an edge of go0, simulating oversized replicas of teeth This study is based on 103 species representing 78 genera, (Caputo and Standlee 1987). These oversized "teeth were 10 families, and two suborders of the order Chiroptera. loaded into plastic ("food) that had been heated to the Among microchiropterans there are 40 insectivorous, 7 car- point of being liquid and allowed to cool around the loaded nivorous, 18 nectarivorous, 14 frugivorous, and 2 sangui- forms (called stress-fieezing). Cooling freezes the stress- nivorous species. Megachiropteran fiugivores and nectar- induced patterns permanently in the plastic. The plastic is ivores are represented by 11 species each (Appendix 9.1). photoelastic, which means that the birefringent (refiactive Each species was usually represented by a single adult male in two hrections) patterns of stress caused by the deforma- skull in perfect or near-perfect condition (i.e., no broken or tion of the plastic by the different shapes can be observed missing parts), although a perfect adult female skull was under polarized light. The visual results of that experiment preferable to an imperfect male skull. There are no missing are presented here. Photoelasticity has been used in den- data except for naturally missing teeth in the toothrow, tistry for several years (Guard et al. 1958; Fisher et al. 1975), which are treated as missing data and not as zero; including but only to examine what stresses are being placed on the the latter would substantially affect the average of those tooth and not how the tooth is stressing the food. bats with the tooth present. Homologies for tooth number are from Andersen (1912). Areal measurements, recalculated for this study, are fiom Results camera lucida drawings that were scanned into a Macintosh Cranial and Palatal Form computer and taken automatically inside (teeth) or outside (palate) high-contrast occlusal outlines. Areas include upper Shapes of bat skulls, represented by zygomatic breadth &- incisors (I); upper canines (C); nonrnolariform upper pre- vided by condylocanine length, vary between being as wide molars (other PMs); fourth upper premolars (PM4); and as they are long to being only a third of the skull length. first, second, and third upper molars (MI, M2, and M3), However, skull width of most species is one-half to three- where found; the area of the raised stylar shelf (including quarters the length of the skull (Figure 9.1A). Extremes are PM4); and the area of the palate (as modified in Freeman represented by the microchiropteran family Phyllostomi- 1988, 1995). Linear measurements are the same as those in dae, with Centurio and other stenodermatines on the wide Freeman (1995; but see also Freeman 1984,1988). end and Musonycteris and other glossophagines on the nar- This chapter is concerned with large-scale patterns. De- row end. Four wide-faced insectivorous species, mentioned tails on variation among species can be found in earlier in earlier studes (Freeman 1984), group together at 0.8 papers. The size character is the same as that used in pre- above the majority of species. On the other hand, shapes of vious papers (SIZE = sum of the natural logs of condylo- palates of bats (breadth across the molars divided by length ZBICCL = 0.447 + 0.022 . log, SIZE; R' = 0.041 INSECTIVORE + CARNIVORE A NECTARIVORE FRUGNORE x SANGUINIVORE 0 MEGA-frug A MEGA-nect L 6.5 7 7.5 8 8.5 9 9.5 10 10.5 11 11.5 SlZE M-MIMTR = 1.388 - 0.052 . log, SIZE; R' = 0.035 B 2.2 INSECTIVORE CARNIVORE NECTARNORE FRUGIWE SANGUINIVORE MEGA-frug MEGA-nect .2 Figure 9.1. Cranial and palatal features that are (A) 6.5 7 7.5 8 8.5 9 9.5 10 10.5 11 11.5 important in chiropterans. Zygomatic SlZE breadth (ZB) divided by condylocanine length (CCL) regressed against SIZE (see Methods). (B) Breadth across upper molars (M-M)divided by length of maxillary toothrow (MTR) TTAIPAL = 0.253 + 7.095e-~. log, SIZE; R2= 2.772e-3 regressed against SIZE. (C) Total tooth area C .6 (TTA) divided by palatal area (PAL) regressed against SIZE. Open symbols denote megachrop- terans; all other symbols denote microchirop- INSECTIVORE terans. Megachiropterans have heads that are CARNNORE relatively as wide as most other chropterans' heads (A) but have narrower palates (B). Mega- NECTARIVORE chiropterans (both frugivores and nectarivores, FRUGNORE MEGA-frug and MEGA-nect) and microchrop- SANGUINIVORE teran nectarivores have small teeth on large MEGA-frug palates, whereas microchropteran insectivores, MEGA-nect carnivores, and frugivores have large teeth on small palates (C).
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