Is a blunt sword pointless? Tooth wear impacts puncture performance in Tasmanian devil canines.

As teeth wear, their shapes change and functional features can be dulled or lost, presumably making them less effective for feeding. However, we do not know the magnitude and effect of this wear. Using Tasmanian devil canines as a case study, we investigated the impact of wear on puncture in pointed teeth. We measured aspects of shape impacted by wear (tip sharpness, height and volume) in teeth of varying wear followed by 3D printing of real and theoretical forms to carry out physical puncture tests. Tooth wear acts in two ways: by blunting tooth tips, and decreasing height and volume, both of which impact performance. Sharper tips in unworn teeth decrease the force and energy required to puncture compared with blunter worn teeth, while taller unworn teeth provide the continuous energy necessary to propagate fracture relative to shorter worn teeth. These wear-modulated changes in shape necessitate more than twice the force to drive worn teeth into ductile food and decrease the likelihood of puncture success.

Intrinsic and extrinsic drivers of shape variation in the albatross compound bill.

Albatross are the largest seabirds on Earth and have a suite of adaptations for their pelagic lifestyle. Rather than having a bill made of a single piece of keratin, Procellariiformes have a compound rhamphotheca, made of several joined plates. Drivers of the shape of the albatross bill have not been explored. Here we use three-dimensional scans of 61 upper bills from 12 species of albatross to understand whether intrinsic (species assignment & size) or extrinsic (diet) factors predict bill shape. Diet is a significant predictor of bill shape with coarse dietary categories providing higher R2 values than dietary proportion data. We also find that of the intrinsic factors, species assignment accounts for ten times more of the variation than size (72% versus 6.8%) and that there is a common allometric vector of shape change between all species. When considering species averages in a phylogenetic framework, there are significant Blomberg's K results for both shape and size (K = 0.29 & 1.10) with the first axis of variation having a much higher K value (K = 1.9), reflecting the split in shape at the root of the tree. The influence of size on bill shape is limited, with species assignment and diet predicting far more of the variation. The results show that both intrinsic and extrinsic factors are needed to understand morphological evolution.

Taking a stab at modelling canine tooth biomechanics in mammalian carnivores with beam theory and finite-element analysis.

Canine teeth are vital to carnivore feeding ecology, facilitating behaviours related to prey capture and consumption. Forms vary with specific feeding ecologies; however, the biomechanics that drive these relationships have not been comprehensively investigated. Using a combination of beam theory analysis (BTA) and finite-element analysis (FEA) we assessed how aspects of canine shape impact tooth stress, relating this to feeding ecology. The degree of tooth lateral compression influenced tolerance of multidirectional loads, whereby canines with more circular cross-sections experienced similar maximum stresses under pulling and shaking loads, while more ellipsoid canines experienced higher stresses under shaking loads. Robusticity impacted a tooth's ability to tolerate stress and appears to be related to prey materials. Robust canines experience lower stresses and are found in carnivores regularly encountering hard foods. Slender canines experience higher stresses and are associated with carnivores biting into muscle and flesh. Curvature did not correlate with tooth stress; however, it did impact bending during biting. Our simulations help identify scenarios where canine forms are likely to break and pinpoint areas where this breakage may occur. These patterns demonstrate how canine shape relates to tolerating the stresses experienced when killing and feeding, revealing some of the form-function relationships that underpin mammalian carnivore ecologies.

Fang shape varies with ontogeny and sex in the venomous elapid snake Pseudonaja affinis.

A predator's preferred prey often changes over the course of its life as it grows from an inexperienced juvenile through to a sexually mature adult. For species with highly specialised feeding strategies, this may require its anatomy to change over the course of its life. The dugite (Pseudonaja affinis, Günther 1872) is a venomous snake from Australia that displays such a diet shift, with juveniles feeding on small reptiles, while adults mainly target mammals. We examined the morphology of fangs across both sexes and throughout ontogeny using geometric morphometrics and cross-sectional sharpness measurements of key functional regions on these teeth. This highlighted key differences in shape that likely relate to the varied properties of their adult and juvenile diet. We found that juveniles display a more robust and blunter fang, which likely relates to feeding on scaly lizard prey, whereas adults have slender fangs with sharper tips, which reflects their diet of softer mammalian prey. There were also differences between males and females, with male snakes having significantly more slender fangs than females, which might be an indication of niche partitioning between the sexes. Using snout-vent length as a proxy for age, we found that the ontogenetic shift in fang shape occurs when P. affinis is around 60 cm long, corresponding with previous studies that found this size to be the moment where these snakes switch from their juvenile to adult diet.

Sharp and fully loaded: 3D tissue reconstruction reveals how snake fangs stay deadly during fang replacement.

Snake venom is produced, transported and delivered by the sophisticated venom delivery system (VDS). When snakes bite, the venom travels from the venom gland through the venom duct into needle-like fangs that inject it into their prey. To counteract breakages, fangs are continuously replaced throughout life. Currently, the anatomy of the connection between the duct and the fang has not been described, and the mechanism by which the duct is reconnected to the replacement fang has not been identified. We examined the VDS in 3D in representative species from two families and one subfamily (Elapidae, Viperidae, Atractaspidinae) using contrast-enhanced microCT (diceCT), followed by dissection and histology. We observed that the venom duct bifurcates immediately anterior to the fangs so that both the original and replacement fangs are separately connected and functional in delivering venom. When a fang is absent, the canal leading to the empty position is temporarily closed. We found that elapid snakes have a crescent-shaped venom reservoir where venom likely pools before it enters the fang. These findings form the final piece of the puzzle of VDS anatomy in front-fanged venomous snakes. Additionally, they provide further evidence for independent evolution of the VDS in these three snake taxa.

Wearing the devil down: Rate of tooth wear varies between wild and captive Tasmanian devils.

Mammalian carnivores rely on their sharp teeth to effectively kill and consume prey. However, over time this causes wear and breakage that alters tooth shape, reducing their effectiveness. Extreme tooth wear and damage is especially prevalent in species that scavenge carcasses, like the Tasmanian devil (Sarcophilus harrisii), which are well known for their voracious appetites and ability to consume almost all of a carcass, including bone. In this study, we comprehensively describe tooth wear in captive and wild devils to look for differences in the patterns and rate of wear between these environments. To do this we surveyed tooth condition in skulls from 182 wild and 114 captive devils for which age was estimated using canine over-eruption. We found the types of tooth wear documented were the same in captive and wild devils, but captive animals have less severe wear than wild devils of the same estimated age. There was no difference in the proportion of captive or wild individuals with broken canine or molar teeth; however, breakage occurred at a younger age in wild devils. Although not considered anomalous or harmful, this indicates a difference in the way teeth are being used and/or the foods consumed between captive and wild devils. We hypothesize how these results relate to differences in diet or behavior that may stem from their various feeding environments, for example, higher quality food (fresh, whole, and yet to be scavenged carcasses) provided to captive devils likely causes less wear. Further, we support management options that closely replicate wild diet items and behaviors suitable for a long-term insurance population.

Convergent evolution of forelimb-propelled swimming in seals.

Modern pinnipeds (true and eared seals) employ two radically different swimming styles, with true seals (phocids) propelling themselves primarily with their hindlimbs, whereas eared seals (otariids) rely on their wing-like foreflippers.1,2 Current explanations of this functional dichotomy invoke either pinniped diphyly3-5 or independent colonizations of the ocean by related but still largely terrestrial ancestors.6-8 Here, we show that pinniped swimming styles form an anatomical, functional, and behavioral continuum, within which adaptations for forelimb swimming can arise directly from a hindlimb-propelled bauplan. Within phocids, southern seals (monachines) show a convergent trend toward wing-like, hydrodynamically efficient forelimbs used for propulsion during slow swimming, turning, bursts of speed, or when initiating movement. This condition is most evident in leopard seals, which have well-integrated foreflippers with little digit mobility, reduced claws, and hydrodynamic characteristics comparable to those of forelimb-propelled otariids. Using monachines as a model, we suggest that the last common ancestor of modern seals may have been hindlimb-propelled and aquatically adapted, thus resolving the apparent contradiction at the root of pinniped evolution.

Fang evolution in venomous snakes: Adaptation of 3D tooth shape to the biomechanical properties of their prey.

Venomous snakes are among the world's most specialized predators. During feeding, they use fangs to penetrate the body tissues of their prey, but the success of this penetration depends on the shape of these highly specialized teeth. Here, we examined the evolution of fang shape in a wide range of snakes using 3D geometric morphometrics (3DGM) and cross-sectional tooth sharpness measurements. We investigated the relationship of these variables with six diet categories based on the prey's biomechanical properties, and tested for evolutionary convergence using two methods. Our results show that slender elongate fangs with sharp tips are used by snakes that target soft-skinned prey (e.g., mammals), whereas fangs become more robust and blunter as the target's skin becomes scaly (e.g., fish and reptiles) and eventually hard-shelled (e.g., crustaceans), both with and without correction for evolutionary allometry. Convergence in fang shape is present, indicating that fangs of snakes with the same diet are more similar than those of closely related species with different diets. Establishing the relationship between fang morphology and diet helps to explain how snakes became adapted to different lifestyles, while also providing a proxy to infer diet in lesser known species or extinct snakes from the fossil record.

A universal power law for modelling the growth and form of teeth, claws, horns, thorns, beaks, and shells.

BACKGROUND: A major goal of evolutionary developmental biology is to discover general models and mechanisms that create the phenotypes of organisms. However, universal models of such fundamental growth and form are rare, presumably due to the limited number of physical laws and biological processes that influence growth. One such model is the logarithmic spiral, which has been purported to explain the growth of biological structures such as teeth, claws, horns, and beaks. However, the logarithmic spiral only describes the path of the structure through space, and cannot generate these shapes. RESULTS: Here we show a new universal model based on a power law between the radius of the structure and its length, which generates a shape called a 'power cone'. We describe the underlying 'power cascade' model that explains the extreme diversity of tooth shapes in vertebrates, including humans, mammoths, sabre-toothed cats, tyrannosaurs and giant megalodon sharks. This model can be used to predict the age of mammals with ever-growing teeth, including elephants and rodents. We view this as the third general model of tooth development, along with the patterning cascade model for cusp number and spacing, and the inhibitory cascade model that predicts relative tooth size. Beyond the dentition, this new model also describes the growth of claws, horns, antlers and beaks of vertebrates, as well as the fangs and shells of invertebrates, and thorns and prickles of plants. CONCLUSIONS: The power cone is generated when the radial power growth rate is unequal to the length power growth rate. The power cascade model operates independently of the logarithmic spiral and is present throughout diverse biological systems. The power cascade provides a mechanistic basis for the generation of these pointed structures across the tree of life.

Low elbow mobility indicates unique forelimb posture and function in a giant extinct marsupial.

Joint mobility is a key factor in determining the functional capacity of tetrapod limbs, and is important in palaeobiological reconstructions of extinct animals. Recent advances have been made in quantifying osteological joint mobility using virtual computational methods; however, these approaches generally focus on the proximal limb joints and have seldom been applied to fossil mammals. Palorchestes azael is an enigmatic, extinct ~1000 kg marsupial with no close living relatives, whose functional ecology within Australian Pleistocene environments is poorly understood. Most intriguing is its flattened elbow morphology, which has long been assumed to indicate very low mobility at this important joint. Here, we tested elbow mobility via virtual range of motion (ROM) mapping and helical axis analysis, to quantitatively explore the limits of Palorchestes' elbow movement and compare this with their living and extinct relatives, as well as extant mammals that may represent functional analogues. We find that Palorchestes had the lowest elbow mobility among mammals sampled, even when afforded joint translations in addition to rotational degrees of freedom. This indicates that Palorchestes was limited to crouched forelimb postures, something highly unusual for mammals of this size. Coupled flexion and abduction created a skewed primary axis of movement at the elbow, suggesting an abducted forelimb posture and humeral rotation gait that is not found among marsupials and unlike that seen in any large mammals alive today. This work introduces new quantitative methods and demonstrates the utility of comparative ROM mapping approaches, highlighting that Palorchestes' forelimb function was unlike its contemporaneous relatives and appears to lack clear functional analogues among living mammals.

A new large-bodied Pliocene seal with unusual cutting teeth.

Today, monachine seals display the largest body sizes in pinnipeds. However, the evolution of larger body sizes has been difficult to assess due to the murky taxonomic status of fossil seals, including fossils referred to Callophoca obscura, a species thought to be present on both sides of the North Atlantic during the Neogene. Several studies have recently called into question the taxonomic validity of these fossils, especially those from the USA, as the fragmentary lectotype specimen from Belgium is of dubious diagnostic value. We find that the lectotype isolated humerus of C. obscura is too uninformative; thus, we designate C. obscura as a nomen dubium. More complete cranial and postcranial specimens from the Pliocene Yorktown Formation are described as a new taxon, Sarcodectes magnus. The cranial specimens display adaptations towards an enhanced ability to cut or chew prey that are unique within Phocidae, and estimates indicate S. magnus to be around 2.83 m in length. A parsimony phylogenetic analysis found S. magnus is a crown monachine. An ancestral state estimation of body length indicates that monachines did not have a remarkable size increase until the evolution of the lobodontins and miroungins.

Using accelerometers to develop time-energy budgets of wild fur seals from captive surrogates.

BACKGROUND: Accurate time-energy budgets summarise an animal's energy expenditure in a given environment, and are potentially a sensitive indicator of how an animal responds to changing resources. Deriving accurate time-energy budgets requires an estimate of time spent in different activities and of the energetic cost of that activity. Bio-loggers (e.g., accelerometers) may provide a solution for monitoring animals such as fur seals that make long-duration foraging trips. Using low resolution to record behaviour may aid in the transmission of data, negating the need to recover the device. METHODS: This study used controlled captive experiments and previous energetic research to derive time-energy budgets of juvenile Australian fur seals (Arctocephalus pusillus) equipped with tri-axial accelerometers. First, captive fur seals and sea lions were equipped with accelerometers recording at high (20 Hz) and low (1 Hz) resolutions, and their behaviour recorded. Using this data, machine learning models were trained to recognise four states-foraging, grooming, travelling and resting. Next, the energetic cost of each behaviour, as a function of location (land or water), season and digestive state (pre- or post-prandial) was estimated. Then, diving and movement data were collected from nine wild juvenile fur seals wearing accelerometers recording at high- and low- resolutions. Models developed from captive seals were applied to accelerometry data from wild juvenile Australian fur seals and, finally, their time-energy budgets were reconstructed. RESULTS: Behaviour classification models built with low resolution (1 Hz) data correctly classified captive seal behaviours with very high accuracy (up to 90%) and recorded without interruption. Therefore, time-energy budgets of wild fur seals were constructed with these data. The reconstructed time-energy budgets revealed that juvenile fur seals expended the same amount of energy as adults of similar species. No significant differences in daily energy expenditure (DEE) were found across sex or season (winter or summer), but fur seals rested more when their energy expenditure was expected to be higher. Juvenile fur seals used behavioural compensatory techniques to conserve energy during activities that were expected to have high energetic outputs (such as diving). DISCUSSION: As low resolution accelerometry (1 Hz) was able to classify behaviour with very high accuracy, future studies may be able to transmit more data at a lower rate, reducing the need for tag recovery. Reconstructed time-energy budgets demonstrated that juvenile fur seals appear to expend the same amount of energy as their adult counterparts. Through pairing estimates of energy expenditure with behaviour this study demonstrates the potential to understand how fur seals expend energy, and where and how behavioural compensations are made to retain constant energy expenditure over a short (dive) and long (season) period.

Clawed forelimbs allow northern seals to eat like their ancient ancestors.

Streamlined flippers are often considered the defining feature of seals and sea lions, whose very name 'pinniped' comes from the Latin pinna and pedis, meaning 'fin-footed'. Yet not all pinniped limbs are alike. Whereas otariids (fur seals and sea lions) possess stiff streamlined forelimb flippers, phocine seals (northern true seals) have retained a webbed yet mobile paw bearing sharp claws. Here, we show that captive and wild phocines routinely use these claws to secure prey during processing, enabling seals to tear large fish by stretching them between their teeth and forelimbs. 'Hold and tear' processing relies on the primitive forelimb anatomy displayed by phocines, which is also found in the early fossil pinniped Enaliarctos. Phocine forelimb anatomy and behaviour therefore provide a glimpse into how the earliest seals likely fed, and indicate what behaviours may have assisted pinnipeds along their journey from terrestrial to aquatic feeding.

Ancient whales did not filter feed with their teeth.

The origin of baleen whales (Mysticeti), the largest animals on Earth, is closely tied to their signature filter-feeding strategy. Unlike their modern relatives, archaic whales possessed a well-developed, heterodont adult dentition. How these teeth were used, and what role their function and subsequent loss played in the emergence of filter feeding, is an enduring mystery. In particular, it has been suggested that elaborate tooth crowns may have enabled stem mysticetes to filter with their postcanine teeth in a manner analogous to living crabeater and leopard seals, thereby facilitating the transition to baleen-assisted filtering. Here we show that the teeth of archaic mysticetes are as sharp as those of terrestrial carnivorans, raptorial pinnipeds and archaeocetes, and thus were capable of capturing and processing prey. By contrast, the postcanine teeth of leopard and crabeater seals are markedly blunter, and clearly unsuited to raptorial feeding. Our results suggest that mysticetes never passed through a tooth-based filtration phase, and that the use of teeth and baleen in early whales was not functionally connected. Continued selection for tooth sharpness in archaic mysticetes is best explained by a feeding strategy that included both biting and suction, similar to that of most living pinnipeds and, probably, early toothed whales (Odontoceti).

A behavioural framework for the evolution of feeding in predatory aquatic mammals.

Extant aquatic mammals are a key component of aquatic ecosystems. Their morphology, ecological role and behaviour are, to a large extent, shaped by their feeding ecology. Nevertheless, the nature of this crucial aspect of their biology is often oversimplified and, consequently, misinterpreted. Here, we introduce a new framework that categorizes the feeding cycle of predatory aquatic mammals into four distinct functional stages (prey capture, manipulation and processing, water removal and swallowing), and details the feeding behaviours that can be employed at each stage. Based on this comprehensive scheme, we propose that the feeding strategies of living aquatic mammals form an evolutionary sequence that recalls the land-to-water transition of their ancestors. Our new conception helps to explain and predict the origin of particular feeding styles, such as baleen-assisted filter feeding in whales and raptorial 'pierce' feeding in pinnipeds, and informs the structure of present and past ecosystems.

Seeing It All: Evaluating Supervised Machine Learning Methods for the Classification of Diverse Otariid Behaviours.

Constructing activity budgets for marine animals when they are at sea and cannot be directly observed is challenging, but recent advances in bio-logging technology offer solutions to this problem. Accelerometers can potentially identify a wide range of behaviours for animals based on unique patterns of acceleration. However, when analysing data derived from accelerometers, there are many statistical techniques available which when applied to different data sets produce different classification accuracies. We investigated a selection of supervised machine learning methods for interpreting behavioural data from captive otariids (fur seals and sea lions). We conducted controlled experiments with 12 seals, where their behaviours were filmed while they were wearing 3-axis accelerometers. From video we identified 26 behaviours that could be grouped into one of four categories (foraging, resting, travelling and grooming) representing key behaviour states for wild seals. We used data from 10 seals to train four predictive classification models: stochastic gradient boosting (GBM), random forests, support vector machine using four different kernels and a baseline model: penalised logistic regression. We then took the best parameters from each model and cross-validated the results on the two seals unseen so far. We also investigated the influence of feature statistics (describing some characteristic of the seal), testing the models both with and without these. Cross-validation accuracies were lower than training accuracy, but the SVM with a polynomial kernel was still able to classify seal behaviour with high accuracy (>70%). Adding feature statistics improved accuracies across all models tested. Most categories of behaviour -resting, grooming and feeding-were all predicted with reasonable accuracy (52-81%) by the SVM while travelling was poorly categorised (31-41%). These results show that model selection is important when classifying behaviour and that by using animal characteristics we can strengthen the overall accuracy.

Foraging-Based Enrichment Promotes More Varied Behaviour in Captive Australian Fur Seals (Arctocephalus pusillus doriferus).

During wild foraging, Australian fur seals (Arctocephalus pusillus doriferus) encounter many different types of prey in a wide range of scenarios, yet in captive environments they are typically provided with a narrower range of opportunities to display their full repertoire of behaviours. This study aimed to quantitatively explore the effect of foraging-based enrichment on the behaviour and activity patterns displayed by two captive Australian fur seals at Melbourne Zoo, Australia. Food was presented as a scatter in open water, in a free-floating ball device, or in a static box device, with each treatment separated by control trials with no enrichment. Both subjects spent more time interacting with the ball and static box devices than the scatter feed. The total time spent pattern swimming was reduced in the enrichment treatments compared to the controls, while the time spent performing random swimming behaviours increased. There was also a significant increase in the total number of bouts of behaviour performed in all three enrichment treatments compared to controls. Each enrichment method also promoted a different suit of foraging behaviours. Hence, rather than choosing one method, the most effective way to increase the diversity of foraging behaviours, while also increasing variation in general activity patterns, is to provide seals with a wide range of foraging scenarios where food is encountered in different ways.

Australian fur seals (Arctocephalus pusillus doriferus) use raptorial biting and suction feeding when targeting prey in different foraging scenarios.

Foraging behaviours used by two female Australian fur seals (Arctocephalus pusillus doriferus) were documented during controlled feeding trials. During these trials the seals were presented with prey either free-floating in open water or concealed within a mobile ball or a static box feeding device. When targeting free-floating prey both subjects primarily used raptorial biting in combination with suction, which was used to draw prey to within range of the teeth. When targeting prey concealed within either the mobile or static feeding device, the seals were able to use suction to draw out prey items that could not be reached by biting. Suction was followed by lateral water expulsion, where water drawn into the mouth along with the prey item was purged via the sides of the mouth. Vibrissae were used to explore the surface of the feeding devices, especially when locating the openings in which the prey items had been hidden. The mobile ball device was also manipulated by pushing it with the muzzle to knock out concealed prey, which was not possible when using the static feeding device. To knock prey out of this static device one seal used targeted bubble blowing, where a focused stream of bubbles was blown out of the nose into the openings in the device. Once captured in the jaws, prey items were manipulated and re-oriented using further mouth movements or chews so that they could be swallowed head first. While most items were swallowed whole underwater, some were instead taken to the surface and held in the teeth, while being vigorously shaken to break them into smaller pieces before swallowing. The behavioural flexibility displayed by Australian fur seals likely assists in capturing and consuming the extremely wide range of prey types that are targeted in the wild, during both benthic and epipelagic foraging.