Insights into the Ecology and Evolutionary Success of Crocodilians Revealed through Bite-Force and Tooth-Pressure Experimentation

BackgroundCrocodilians have dominated predatory niches at the water-land interface for over 85 million years. Like their ancestors, living species show substantial variation in their jaw proportions, dental form and body size. These differences are often assumed to reflect anatomical specialization related to feeding and niche occupation, but quantified data are scant. How these factors relate to biomechanical performance during feeding and their relevance to crocodilian evolutionary success are not known.Methodology/Principal FindingsWe measured adult bite forces and tooth pressures in all 23 extant crocodilian species and analyzed the results in ecological and phylogenetic contexts. We demonstrate that these reptiles generate the highest bite forces and tooth pressures known for any living animals. Bite forces strongly correlate with body size, and size changes are a major mechanism of feeding evolution in this group. Jaw shape demonstrates surprisingly little correlation to bite force and pressures. Bite forces can now be predicted in fossil crocodilians using the regression equations generated in this research.Conclusions/SignificanceCritical to crocodilian long-term success was the evolution of a high bite-force generating musculo-skeletal architecture. Once achieved, the relative force capacities of this system went essentially unmodified throughout subsequent diversification. Rampant changes in body size and concurrent changes in bite force served as a mechanism to allow access to differing prey types and sizes. Further access to the diversity of near-shore prey was gained primarily through changes in tooth pressure via the evolution of dental form and distributions of the teeth within the jaws. Rostral proportions changed substantially throughout crocodilian evolution, but not in correspondence with bite forces. The biomechanical and ecological ramifications of such changes need further examination

Dental measurements and pressure generation for extant Crocodylia.

<p><b>N</b> = Number of Specimens.</p><p><b>CCA</b> = Taxon Representative Caniniform Contact Area @1 mm depth (mm²).</p><p><b>RCCA</b> = Range of Caniniform Contact Areas @ 1 mm depth (mm²).</p><p><b>CP</b> = Taxon Representative Caniniform Pressure (MPa).</p><p><b>RCP</b> = Range of Caniniform Pressures (MPa).</p><p><b>MCA</b> = Taxon Representative Molariform Contact Area @ 1 mm depth (mm²).</p><p><b>RMCA</b> = Range of Molariform Contact Areas @ 1 mm depth (mm²).</p><p><b>MP</b> = Taxon Representative Molariform Pressure (MPa).</p><p><b>RMP</b> = Range of Molariform Pressures (MPa).</p

Linear regressions of residual caniniform tooth pressures, and residual molariform tooth pressures versus rostral proportion phylogenetic independent contrasts.

<p>The (<i>A</i>) residual caniniform, and (<i>B</i>) residual molariform regressions show the low correlation between these parameters after accounting for body mass and phylogenetic relatedness.</p

Phylogenetic hypothesis for extant Crocodylia showing variation in rostral proportions.

<p>The cladogram is based on reanalysis (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031781#s4" target="_blank">Materials and Methods</a>) of molecular data from Gatesy and colleagues <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031781#pone.0031781-Gatesy1" target="_blank">[2]</a> using maximum likelihood and non-parametric rate-smoothing with branch lengths proportional to time. Lineages shown in blue represent caiman (a–e) and alligators (f,g) ( = Alligatoridae), and those in green crocodiles (h–t) and gharials (u,v) ( = Crocodylidae+Gavialidae). The Yacare caiman, <i>Caiman yacare</i> is not shown for it was not utilized in the Gatesy et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031781#pone.0031781-Gatesy1" target="_blank">[2]</a> analysis. Dorsal views of heads are modified from Wermuth and Fuchs <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031781#pone.0031781-Wermuth1" target="_blank">[53]</a> and standardized to the same length to show relative differences in rostral form. Bracketed numbers following taxon names are the mean rostral proportions or RP ( = mid-rostral width/snout length) for each taxon from our study. Phylogenetic Independent Contrasts were performed on these 22 species; however, bite force, tooth pressure, and morphometric measurements and subsequent TIPs analyses were performed for all 23 extant taxa, including <i>Caiman yacare</i>.</p

Skull and jaws of a wild adult American alligator (<i>Alligator mississippiensis</i>) showing the prominent teeth used for initially seizing and crushing prey.

<p>The most prominent caniniform and molariform teeth of the upper jaw that are associated with the convexities in the maxilla are highlighted. Because of their greater length relative to the adjacent teeth, and the propensity of crocodilians to bite unilaterally, the crowns of these teeth typically initiate contact with prey during biting. This specimen demonstrates the natural <i>in situ</i> condition of the teeth, which often fall out during skeletonization and must be reattached. As such the natural prominence of the teeth is sometimes not represented in prepared specimens. The caniniform teeth in crocodilians are longer, more slender, and generally have rounder cross-sectional shapes than the molariform teeth. In <i>A. mississippiensis</i> the apices of the caniniforms are fairly dull, whereas in more piscivorous species they are sharp and needle-like. Besides being utilized for seizing prey, caniniform teeth are also used in fighting, defense, aggression, and display. Crocodilian molariforms, on the other hand, are shorter and are typically blunter-tipped than the caniniform teeth. They range interspecifically from having a rounded bulbous morphology to being laterally compressed and blade-like. The intermediate condition seen here is characteristic of <i>A. mississippiensis</i>. Molariform teeth are primarily used for crushing and gripping prey in preparation for swallowing, but are also utilized for display and seizing prey.</p

Taxon representative adult bite forces for extant Crocodylia with respect to mean body mass and the relationship between rostral proportion and force generation.

<p>(<i>A</i>) Members of the Alligatoridae are shown in blue, and members of the Crocodylidae+Gavialidae in green. The OLS regression equation describes the strong correspondence between body mass and bite force. Extant alligators and caiman (Alligatoridae), and crocodiles (Crocodylidae) show comparable relative bite-force capacities. Note that only <i>Gavialis gangeticus</i> is a statistical (i.e. outside the 95% confidence interval) low-force outlier. (<i>B</i>) Linear regression of the size-standardized residual bite force versus rostral proportion phylogenetic independent contrasts showing the low correlation between these after accounting for phylogeny and body mass.</p

Caniniform pressure values for extant Crocodylia, their phylogenetic distribution, and inferred ancestral character states.

<p>(<i>A</i>) Members of the Alligatoridae are shown in blue, and members of the Crocodylidae+Gavialidae in green. The OLS regression equation describes the weak relationship between body mass and caniniform pressure. Note that slender-snouted piscivorous to semi-piscivorous ecomorphs (<i>Gavialis gangeticus and Crocodylus intermedius</i>, respectively) show exceptionally high-pressure values (outside the 95% confidence interval), and <i>Crocodylus johnsoni</i> shows pressures expected of animals nearly a magnitude in size larger. Other ecomorphs show much lower and similar relative values. The arrow indicates the typical ultimate shear strength of bone. (<i>B</i>) Ancestral character-state reconstruction using squared-change parsimony of size-standardized caniniform pressures. Residual caniniform pressure values are color coded to MPa (squared-change parsimony; squared length = 19.491). Vertical scale is in relative time, with the outgroup/ingroup root arbitrarily set to 1.0. High relative pressures were achieved independently in <i>Crocodylus intermedius</i>, <i>Gavialis gangeticus</i>, and <i>Crocodylus johnsoni</i>. Uncolored branches represent taxa for which the caniniform teeth were shed or broken, and so pressure estimation was not possible.</p

Molariform pressure values for extant Crocodylia, their phylogenetic distribution, and inferred ancestral character states.

<p>(<i>A</i>) Members of the Alligatoridae are shown in blue, and members of the Crocodylidae+Gavialidae in green. The OLS regression equation describes the relationship between body size and molariform pressure. Note that the range of values shows similar interspecific correspondence to the caniniform pressure data shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031781#pone-0031781-g004" target="_blank">Figure 4A</a>. The arrow indicates the typical ultimate shear strength of bone. (<i>B</i>) Ancestral-state reconstruction using squared-change parsimony of size-standardized molariform pressures. Pressures are color coded to MPa. Vertical scale is in relative time, with the outgroup/ingroup root arbitrarily set to 1.0. The notable similarities between unrelated taxa and differences between related taxa illustrate the large amount of convergence for this trait among crocodilians.</p