The ontogenetic scaling of bite force and head size in loggerhead sea turtles (Caretta caretta): implications for durophagy in neritic, benthic habitats

Ontogenetic studies of vertebrate feeding performance can help address questions relevant to foraging ecology. Feeding morphology and performance can either limit access to food resources or open up new trophic niches in both aquatic and terrestrial systems. Loggerhead sea turtles are long-lived vertebrates with complex life histories that are marked by an ontogenetic shift from an oceanic habitat to a coastal neritic habitat, and a transition from soft oceanic prey to hard, benthic prey. Although considered durophagous and strong biters, bite performance has not been measured in loggerheads, nor has the ontogeny of bite performance been characterized. In the present study, we collected measurements of bite force in loggerhead turtles from hatchlings to adults. When subadults reach the body size at which the ontogenetic shift occurs, their crushing capability is great enough for them to consume numerous species of hard benthic prey of small sizes. As loggerheads mature and bite performance increases, larger and harder benthic prey become accessible. Loggerhead bite performance eventually surpasses the crushing capability of other durophagous carnivores, thereby potentially reducing competition for hard benthic prey. The increasing bite performance and accompanying changes in morphology of the head and jaws are likely an effective mechanism for resource partitioning and decreasing trophic competition. Simultaneous measurements of body and head size and the use of non-linear reduced major axis regression show that bite force increases with significant positive allometry relative to body size (straight carapace length, straight carapace width and mass) and head size (head width, height and length). Simple correlation showed that all recorded morphometrics were good predictors of measured bite performance, but an AICc-based weighted regression showed that body size (straight carapace width followed by straight carapace length and mass, respectively) were more likely predictors of bite force than head size morphometrics (head width and head length)

Increasing Dietary Breadth Through Allometry: Bite Forces in Sympatric Australian Skinks

Ecomechanical measures of performance such as bite force may function as an indirect measure of niche. This study proposes that allometric changes in performance may contribute to niche separation, especially in a group where the specific mechanism(s) remains unclear. We surveyed the bite force and morphology of 5 wild caught, sympatric skink species in the Kimberley region of Western Australia. Skinks were collected from trapline fences, weighed, photographed, and maximum bite force was measured with a piezoresistive force sensor. Morphological metrics were derived from photographs of the dorsum. Normalized morphological traits indicate interspecific variability in form, particularly in forelimb length, which may be a result of habitat separation. Bite force showed strong, significantly positive, allometric scaling against most morphological traits. Tail length was the only morphological trait that scaled isometrically. Allometric changes in bite force may increase dietary breadth, allowing larger skinks to supplement their diet with larger, more durable prey. This study reveals that ecologically relevant traits may be explained by allometric differences coupled with size variation. Future work should focus on (1) an increase in sample size, (2) long-term measurement of diet selection, and (3) accessibility of prey items to our focal animals

Sexual dimorphism in bite performance drives morphological variation in chameleons

Phenotypic performance in different environments is central to understanding the evolutionary and ecological processes that drive adaptive divergence and, ultimately, speciation. Because habitat structure can affect an animal's foraging behaviour, anti-predator defences, and communication behaviour, it can influence both natural and sexual selection pressures. These selective pressures, in turn, act upon morphological traits to maximize an animal's performance. For performance traits involved in both social and ecological activities, such as bite force, natural and sexual selection often interact in complex ways, providing an opportunity to understand the adaptive significance of morphological variation with respect to habitat. Dwarf chameleons within the Bradypodion melanocephalum-Bradypodion thamnobates species complex have multiple phenotypic forms, each with a specific head morphology that could reflect its use of either open-or closed-canopy habitats. To determine whether these morphological differences represent adaptations to their habitats, we tested for differences in both absolute and relative bite performance. Only absolute differences were found between forms, with the closed-canopy forms biting harder than their open-canopy counterparts. In contrast, sexual dimorphism was found for both absolute and relative bite force, but the relative differences were limited to the closed-canopy forms. These results indicate that both natural and sexual selection are acting within both habitat types, but to varying degrees. Sexual selection seems to be the predominant force within the closed-canopy habitats, which are more protected from aerial predators, enabling chameleons to invest more in ornamentation for communication. In contrast, natural selection is likely to be the predominant force in the open-canopy habitats, inhibiting the development of conspicuous secondary sexual characteristics and, ultimately, enforcing their overall diminutive body size and constraining performance

Bite force in the horned frog (Ceratophrys cranwelli) with implications for extinct giant frogs

Of the nearly 6,800 extant frog species, most have weak jaws that play only a minor role in prey capture. South American horned frogs (Ceratophrys) are a notable exception. Aggressive and able to consume vertebrates their own size, these "hopping heads" use a vice-like grip of their jaws to restrain and immobilize prey. Using a longitudinal experimental design, we quantified the ontogenetic profile of bite-force performance in post-metamorphic Ceratophrys cranwelli. Regression slopes indicate positive allometric scaling of bite force with reference to head and body size, results that concur with scaling patterns across a diversity of taxa, including fish and amniotes (lizards, tuatara, turtles, crocodylians, rodents). Our recovered scaling relationship suggests that exceptionally large individuals of a congener (C. aurita) and extinct giant frogs (Beelzebufo ampinga, Late Cretaceous of Madagascar) probably could bite with forces of 500 to 2200 N, comparable to medium to large-sized mammalian carnivores.A. Kristopher Lappin, Sean C. Wilcox, David J. Moriarty, Stephanie A.R. Stoeppler, Susan E. Evans, Marc E.H. Jone

Ontogenetic allometry underlies trophic diversity in sea turtles (Chelonioidea)

Despite only comprising seven species, extant sea turtles (Cheloniidae and Dermochelyidae) display great ecological diversity, with most species inhabiting a unique dietary niche as adults. This adult diversity is remarkable given that all species share the same dietary niche as juveniles. These ontogenetic shifts in diet, as well as a dramatic increase in body size, make sea turtles an excellent group to examine how morphological diversity arises by allometric processes and life habit specialisation. Using three-dimensional geometric morphometrics, we characterise ontogenetic allometry in the skulls of all seven species and evaluate variation in the context of phylogenetic history and diet. Among the sample, the olive ridley (Lepidochelys olivacea) has a seemingly average sea turtle skull shape and generalised diet, whereas the green (Chelonia mydas) and hawksbill (Eretmochelys imbricata) show different extremes of snout shape associated with their modes of food gathering (grazing vs. grasping, respectively). Our ontogenetic findings corroborate previous suggestions that the skull of the leatherback (Dermochelys coriacea) is paedomorphic, having similar skull proportions to hatchlings of other sea turtle species and retaining a hatchling-like diet of relatively soft bodied organisms. The flatback sea turtle (Natator depressus) shows a similar but less extreme pattern. By contrast, the loggerhead sea turtle (Caretta caretta) shows a peramorphic signal associated with increased jaw muscle volumes that allow predation on hard shelled prey. The Kemp’s ridley (Lepidochelys kempii) has a peramorphic skull shape compared to its sister species the olive ridley, and a diet that includes harder prey items such as crabs. We suggest that diet may be a significant factor in driving skull shape differences among species. Although the small number of species limits statistical power, differences among skull shape, size, and diet are consistent with the hypothesis that shifts in allometric trajectory facilitated diversification in skull shape as observed in an increasing number of vertebrate groups

Clade-wide variation in bite-force performance is determined primarily by size, not ecology

Performance traits are tightly linked to the fitness of organisms. However, because studies of variation in performance traits generally focus on just one or several closely related species, we are unable to draw broader conclusions about how and why these traits vary across clades. One important performance trait related to many aspects of an animal's life history is bite-force. Here, we use a clade-wide phylogenetic comparative approach to investigate relationships between size, head dimensions and bite-force among lizards and tuatara (lepidosaurs), using the largest bite-force dataset collated to date for any taxonomic group. We test four predictions: that bite-force will be greater in larger species, and for a given body size, bite-force will be greatest in species with acrodont tooth attachment, herbivorous diets, and non-burrowing habits. We show that bite-force is strongly related to body and head size across lepidosaurs and, as predicted, larger species have the greatest bite-forces. Contrary to our other predictions, tooth attachment, diet and habit have little predictive power when accounting for size. Herbivores bite more forcefully simply because they are larger. Our results also highlight priorities for future sampling to further enhance our understanding of broader evolutionary patterns

Bite performance and feeding kinematics in loggerhead turtles (Caretta caretta) within the context of longline fishery interactions

Feeding biomechanics and foraging behavior are likely contributors to loggerhead sea turtle (Caretta caretta) bycatch in the pelagic longline fishery. To investigate these contributions, loggerhead bite performance was measured in several size classes of captive-reared juveniles, captive sub-adults and adults, as well as wild loggerheads. A kinematic study was conducted to investigate loggerhead interactions with modified longline hooks. Kinematic and behavioral variables were assessed in relation to five longline hooks to determine if loggerhead feeding behavior is modulated relative to hook type, size, and offset. The bite force study demonstrated that mean maximum post-hatchling bite force was 2.5N and mass was the best predictor of post-hatchling bite force. Mean maximum bite force of juveniles with mean straight carapace length (SCL) of 12, 31, 44, and 65 cm were 27, 152, 343, and 374 N, respectively. Sub-adult and adult mean maximum bite force was 575 N. Maximum bite force had a positive linear relationship with all head and body morphometrics (P<0.001). Carapace width was the best predictor of bite force throughout ontogeny. The kinematic study demonstrated no differences between hook treatments in all kinematic variables analyzed. The results of this study suggest loggerhead feeding behavior may be stereotypical. Only 33% of all interactions resulted in “hooking” events. “Hooking” was lowest in 16 gage circle hooks with no offset and the 18 gage circle hooks with 10°offset which may be indicative of a lower possibility of the turtle drowning. “Hooking” was highest in the 16 gage circle hooks with 10°offset. The proportion of turtles “hooked” in the mouth was significantly greater than those “hooked” in the throat (P=0.001). Sixteen gage circle hooks with 10° offset had the highest percentage of throat “hooking”, and the 18 gage circle hooks without offset resulted in the lowest percentage of throat hooking. When interacting with J hooks with a 25° offset (9 gage), turtles mostly oriented their head away from the hook offset; however, when interacting with the 16 and 18 gage circle hooks with 10° offset, turtles mostly oriented their heads toward the hook offset. These data suggest that turtles may distinguish between small and large offsets, and may modulate their feeding behavior accordingly. Alternatively, turtles may be detecting hook size or hook shape. A more thorough characterization of loggerhead bite performance and feeding kinematics will be useful when developing or modifying longline fishery gear aimed at reducing loggerhead bycatch