The biomechanical consequences of longirostry in crocodilians and odontocetes
Introduction
Living crocodilians and odontocetes (toothed whales) have evolved a similar range of variation in rostral shape, varying from longirostrine with an elongate and narrow rostrum, to brevirostrine with a short and broad rostrum (Brochu, 2001, McHenry et al., 2006, Walmsley et al., 2013b). Elongation of the rostrum is also associated with a relatively longer mandibular symphysis in the most longirostrine taxa (e.g. river dolphins or gharials) (Walmsley et al., 2013b). Within crocodilians longirostry is also associated with a loss of pseudoheterodonty (differences in tooth size) and a loss of undulation in the jaw margins (Cleuren and De Vree, 2000). Busbey (1995) classified longirostrine crocodilians as those with rostral length/condylobasal length values over 0.7, mesorostrine crocodilians as those with values between 0.55 and 0.7, and brevirostrine crocodilians as any with values under 0.55. The morphology of the skull within this spectrum (brevirostrine-longirostrine) has been hypothesised to relate to the functional and ecological limitations of the species (McHenry, 2009, McHenry et al., 2006, Walmsley et al., 2013b). Specifically, it has been suggested that brevirostrine morphotypes are able to handle higher loads during feeding, an adaptation that would allow them to feed on larger or harder prey (Busbey, 1995, McHenry et al., 2006, Walmsley et al., 2013b). Extensive analyses have been undertaken on the load bearing and force producing capabilities of crocodilian cranial systems (Busbey, 1989, Busbey, 1995, Erickson et al., 2012, Cleuren and De Vree, 2000, Erickson et al., 2003, McHenry et al., 2006, Pierce et al., 2008, Porro et al., 2011, Rayfield et al., 2007, Reed et al., 2011, van Drongelen and Dullemeijer, 1982, Walmsley et al., 2013b) but no studies have directly compared their functional abilities to odontocetes to understand exactly why these different groups have evolved such a similar range of morphologies.
Crocodilians and odontocetes are often used as extant morphological and ecological analogues for extinct marine tetrapods such as archaeocetes, ichthyosaurs, thallatosuchians and pliosaurs because of their similarities in body form, limb shape and rostral proportions (Massare, 1987, Massare, 1988, Walmsley et al., 2013b, Young et al., 2012). While crocodilians, odontocetes and these extinct marine reptile groups qualitatively appear to have a similar range of cranial variation, varying in rostral dimensions from short and broad through to elongate and slender (Walmsley et al., 2013b), we still do not know whether these similarities in morphology translate to performance characteristics. Identifying similar form/function relationships between aquatic reptiles and mammals is a necessary step before using living odontocetes or crocodilians to predict the biomechanical and ecological characteristics of extinct taxa.
Furthermore, while odontocetes and crocodilians occupy similar aquatic environments and feed using similar “raptorial feeding” tactics, they vary considerably in other aspects of sensory biology and feeding behaviour. These differences in sensory biology and feeding behaviour are reflected in the anatomy of the skull (Fig. 1). Odontocetes have the ability to produce suction to aid in feeding, although the use of this tactic varies considerably between species, with some species only using suction for intra-oral transport (Bloodworth and Marshall, 2005, Werth, 2000, Werth, 2006a, Werth, 2006b). Within the skull this influences the shape of the mandible as well as the palate morphology, with suction feeding specialists having blunter mandibles and more highly vaulted palates (Werth, 2006a). Crocodilians also engage in some prey processing behaviours not undertaken by odontocetes, including twisting off pieces of prey using a “death roll” (Fish et al., 2007). In terms of sensory ability, odontocetes have the ability to echolocate prey using specialised sound production and reception organs such as the melon and phonic lips (Nachtigall, 1980). The odontocete mandible also plays a role in echolocation by allowing sound to be received by the ear through an extremely thin section of bone in the posterior of the mandible called the pan bone (Norris, 1968) (Fig. 1). In crocodilians this posterior region of the mandible acts to withstand biting forces generated by the jaw muscles (Walmsley et al., 2013b). Crocodilians also possess pterygoid flanges (Fig. 1) that act to prevent medial bending of the mandible during loading (Porro et al., 2011). It is unclear to what extent these morphological differences might alter the fundamental form/function relationships that could be expected in a range of brevirostrine-longirostrine morphologies.
Predictions of the mechanical response of brevirostrine - longirostrine forms can be generated using principles such as beam theory (Bauchau and Craig, 2009, Metzger et al., 2005, Walmsley et al., 2013b), but applying beam theory to capture the morphological differences between phylogenetically disparate taxa is very difficult. Testing how well form/function relationships match basic predictions requires an approach that can account for complex differences in morphology. Finite element analysis is a modelling technique that can predict the response of complex structures to applied load using numerical methods. Previous studies using this technique have shown that the cranial morphology of a species often relates to its preferences in feeding (Dumont et al., 2005, McCurry et al., 2015b, McHenry et al., 2007, Moreno et al., 2008, Soons et al., 2010). Here we aim to use finite element analysis to:
- (1)
Determine whether longirostry has similar effects on structural performance during biting, shaking and twisting in crocodilians and odontocetes.
- (2)
Examine the effects of differences in anatomy between crocodilians and odontocetes on the location and magnitude of strain.
We hypothesise that more longirostrine morphotypes will exhibit higher levels of strain than more brevirostrine morphotypes during all loading scenarios (biting, shaking and twisting at any tooth position). This is expected to occur in a relative sense (e.g. patterns within each group) rather than in an absolute sense.
Section snippets
Specimen selection and mesh generation
Specimens were accessed from the Field Museum of Natural History (FMNH), The Australian Museum Mammalogy and Herpetology collections (AMM and AMR), Museum Victoria Vertebrate Zoology collections (NMVC), The National Museum of Natural History Vertebrate Zoology collections (USNM) and Texas Memorial Museum Vertebrate Paleontology Laboratory (TMM). The cranium and mandible of four species of crocodilian (Osteolaemus tetraspis – FMNH 98936, Crocodylus novaeguineae – AMR 24446, Mecistops
Bite force scaled bite loads
During bite force scaled bite loading scenarios at the anterior teeth the two most brevirostrine odontocetes experienced less strain than the most longirostrine odontocetes (Fig. 3A–H and Fig. 4). In all taxa bite loading resulted in high strain in the posterior of the palate. Within the odontocete models high levels of strain primarily occurred in the thin pan bone at the posterior of the mandible, the lateral margin of the maxilla and the dorsal surface of the rostrum (Norris, 1968). Strain
The biomechanical consequences of longirostry
Here we set out with the goal of understanding how convergent similarities in cranial morphology in crocodilians and odontocetes manifested in similar biomechanical performance. When we loaded the models at the anterior tooth positions our results supported the hypothesis that longirostrine morphotypes of both crocodilians and odontocetes exhibit higher levels of strain. This trend held true in biting, shaking and twisting scenarios at the anterior dentition. However, when loaded at the
Conflict of interest
We have no competing interests.
Authors’ contributions
All authors were involved in the study and preparation of the manuscript. The material within has not been and will not be submitted for publication elsewhere.
Acknowledgments
The authors acknowledge Matthew Colbert and Jesse Maisano (Digital Morphology, University of Texas) and Chris Brochu (University of Iowa) for access to CT data. We thank Eleanor Cunningham (Newcastle Mater hospital), Mason Meers (University of Tampa), Janine Hinton (National Museum of Natural History) and Bruno Frohlich (National Museum of Natural History) for scanning of specimens. Ross Sadlier and Cecilie Beatson (Australian Museum), as well as Katie Date and Karen Roberts (Museum Victoria)
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