Rapid population increase of the threatened Australian amphibian Litoria aurea in response to wetlands constructed as a refuge from chytrid-induced disease and introduced fish.

Amphibians have declined due to multiple impacts including invasive fish and the disease chytridiomycosis caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd). Wetland restoration can be used to increase amphibian populations. However the design of created wetlands must account for threats such as Bd and introduced fish. There have been no attempts on a landscape level to manage these threats with habitat design. Here we monitored the green and golden bell frog (Litoria aurea) in 2.6 ha of constructed wetlands designed to enhance breeding and increase survival through passive mitigation of Bd and exotic fish. We compared the fecundity, adult population sizes, introduced fish occupancy, Bd prevalence and survival rates of frogs in created wetlands (CW) to three control sites to determine if and why the habitat design was successful. Monitoring involved weekly capture-recapture during the austral spring and summer for three L. aurea breeding seasons. We hypothesised that (1) if the CWs were successful in passively limiting fish colonisation, a larger number of breeding events would be detected compared to control sites which are known to be widely colonised by introduced fish. (2) If the wetlands were successful in passively mitigating Bd, then we would observe an equal or greater survival rate and equal to or lower Bd prevalence compared to control wetlands. We observed a 3.3-fold increase in adult population size in CW from season 1 to 2, and the population increased further in season 3.We found strong support for hypothesis (1) and weak support for (2). Based on these results, we conclude that this design was beneficial shortly after their formation primarily due to fish exclusion, but further study is required to determine if these benefits extend long-term. Future amphibian restoration studies are needed to improve the design of wetlands to enhance suppression of Bd.

The remarkable convergence of skull shape in crocodilians and toothed whales.

The striking resemblance of long-snouted aquatic mammals and reptiles has long been considered an example of morphological convergence, yet the true cause of this similarity remains untested. We addressed this deficit through three-dimensional morphometric analysis of the full diversity of crocodilian and toothed whale (Odontoceti) skull shapes. Our focus on biomechanically important aspects of shape allowed us to overcome difficulties involved in comparing mammals and reptiles, which have fundamental differences in the number and position of skull bones. We examined whether diet, habitat and prey size correlated with skull shape using phylogenetically informed statistical procedures. Crocodilians and toothed whales have a similar range of skull shapes, varying from extremely short and broad to extremely elongate. This spectrum of shapes represented more of the total variation in our dataset than between phylogenetic groups. The most elongate species (river dolphins and gharials) are extremely convergent in skull shape, clustering outside of the range of the other taxa. Our results suggest the remarkable convergence between long-snouted river dolphins and gharials is driven by diet rather than physical factors intrinsic to riverine environments. Despite diverging approximately 288 million years ago, crocodilians and odontocetes have evolved a remarkably similar morphological solution to feeding on similar prey.

Chronic effects of an invasive species on an animal community.

Invasive species can trigger trophic cascades in animal communities, but published cases involving their removal of top predators are extremely rare. An exception is the invasive cane toad (Rhinella marina) in Australia, which has caused severe population declines in monitor lizards, triggering trophic cascades that facilitated dramatic and sometimes unexpected increases in several prey of the predators, including smaller lizards, snakes, turtles, crocodiles, and birds. Persistence of isolated populations of these predators with a decades-long sympatry with toads suggests the possibility of recovery, but alternative explanations are possible. Confirming predator recovery requires longer-term study of populations with both baseline and immediate post-invasion densities. Previously, we quantified short-term impacts of invasive cane toads on animal communities over seven years at two sites in tropical Australia. Herein, we test the hypothesis that predators have begun to recover by repeating the study 12 yr after the initial toad invasion. The three predatory lizards that experienced 71-97% declines in the short-term study showed no sign of recovery, and indeed a worse fate: two of the three species were no longer detectable in 630 km of river surveys, suggesting local extirpation. Two mesopredators that had increased markedly in the short term due to these predator losses showed diverse responses in the medium term; a small lizard species increased by ~500%, while populations of a snake species showed little change. Our results indicate a system still in ecological turmoil, having not yet reached a "new equilibrium" more than a decade after the initial invasion; predator losses due to this toxic invasive species, and thus downstream effects, were not transient. Given that cane toads have proven too prolific to eradicate or control, we suggest that recovery of impacted predators must occur unassisted by evolutionary means: dispersal into extinction sites from surviving populations with alleles for toxin resistance or toad avoidance. Evolution and subsequent dispersal may be the only solution for a number of species or communities affected by invasive species for which control is either prohibitively expensive, or not possible.

Invasive toads shift predator-prey densities in animal communities by removing top predators.

Although invasive species can have substantial impacts on animal communities, cases of invasive species facilitating native species by removing their predators have rarely been demonstrated across vertebrate trophic linkages. The predictable spread of the invasive cane toad (Rhinella marina), however, offered a unique opportunity to quantify cascading effects. In northern Australia, three species of predatory monitor lizards suffered severe population declines due to toad-induced lethal toxic ingestion (yellow-spotted monitor (Varanus panoptes), Mertens' water monitor (V. mertensi), Mitchell's water monitor (V. mitchelli). We, thus, predicted subsequent increases in the abundance and recruitment of prey species due to the reduction of those predators. Toad-induced population-level declines in the water monitor species approached 50% over a five-year period spanning the toad invasion, apparently causing fledging success of the Crimson Finch (Neochmia.phaeton) to increase from 55% to 81%. The consensus of our original and published long-term data is that invasive cane toads are causing predators to lose a foothold on top-down regulation of their prey, triggering shifts in the relative densities of predator and prey in the Australian tropical savannah ecosystem.

It's not easy being green: Comparing typical skin colouration among amphibians with colour abnormalities associated with chromatophore deficits.

Amphibians can obtain their colour from a combination of several different pigment and light reflecting cell types called chromatophores, with defects in one or several of the cells leading to colour abnormalities. There is a need for better recording of colour abnormalities within wild amphibian populations, as this may provide baseline data that can be used to determine changes in environmental conditions and population dynamics, such as inbreeding. In this study, we provide records of several types of chromatophore deficiencies, including those involving iridophores, xanthophores and melanophores, among two Australian tree frog species; the green and golden bell frog, Litoria aurea, and the eastern dwarf tree frog, L. fallax. We explore these colour abnormalities in terms of the chromatophores that have likely been affected and associated with their expression, in combination with typical colour phenotypes, colour variations and colour changes for these species. We intend for our photographs to be used as a visual guide that addresses the need for more accessible information regarding the physical manifestation of different chromatophore defects among amphibians.

A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus (Megalania) priscus.

The predatory ecology of Varanus komodoensis (Komodo Dragon) has been a subject of long-standing interest and considerable conjecture. Here, we investigate the roles and potential interplay between cranial mechanics, toxic bacteria, and venom. Our analyses point to the presence of a sophisticated combined-arsenal killing apparatus. We find that the lightweight skull is relatively poorly adapted to generate high bite forces but better adapted to resist high pulling loads. We reject the popular notion regarding toxic bacteria utilization. Instead, we demonstrate that the effects of deep wounds inflicted are potentiated through venom with toxic activities including anticoagulation and shock induction. Anatomical comparisons of V. komodoensis with V. (Megalania) priscus fossils suggest that the closely related extinct giant was the largest venomous animal to have ever lived.

The craniomandibular mechanics of being human.

Diminished bite force has been considered a defining feature of modern Homo sapiens, an interpretation inferred from the application of two-dimensional lever mechanics and the relative gracility of the human masticatory musculature and skull. This conclusion has various implications with regard to the evolution of human feeding behaviour. However, human dental anatomy suggests a capacity to withstand high loads and two-dimensional lever models greatly simplify muscle architecture, yielding less accurate results than three-dimensional modelling using multiple lines of action. Here, to our knowledge, in the most comprehensive three-dimensional finite element analysis performed to date for any taxon, we ask whether the traditional view that the bite of H. sapiens is weak and the skull too gracile to sustain high bite forces is supported. We further introduce a new method for reconstructing incomplete fossil material. Our findings show that the human masticatory apparatus is highly efficient, capable of producing a relatively powerful bite using low muscle forces. Thus, relative to other members of the superfamily Hominoidea, humans can achieve relatively high bite forces, while overall stresses are reduced. Our findings resolve apparently discordant lines of evidence, i.e. the presence of teeth well adapted to sustain high loads within a lightweight cranium and mandible.

Novel habitat causes a shift to diurnal activity in a nocturnal species.

Plastic responses may allow individuals to survive and reproduce in novel environments, and can facilitate the establishment of viable populations. But can novel environments reveal plasticity by causing a shift in a behavior as fundamental and conspicuous as daily activity? We studied daily activity times near the invasion front of the cane toad (Rhinella marina), an invasive species that has colonized much of northern Australia. Cane toads in Australia are nocturnal, probably because diurnal activity would subject them to intolerably hot and dry conditions in the tropical savannah during the dry season. Our study can demonstrate, however, that upon reaching novel environments some toad populations became diurnal. Sandstone gorges offered cane toads novel, deeply shaded habitat. Gorges with an east-west axis (day-long northern shadow), narrow gorges and narrow sections of gorges contained toads that were primarily diurnal, while gorges with a north-south axis, wide gorges and wide sections of gorges contained mainly nocturnal toads. For example, remote camera data (1314 observations of toad activity times over 789 trap days) revealed strictly nocturnal activity at four 'exposed' sites (99% of 144 observations over 179 days), compared to mostly diurnal activity at a 'shaded' site (78% of 254 observations). Visual encounter surveys confirmed that diurnal activity occurred exclusively at shaded sites, while most nocturnal activity occurred at exposed sites. The close proximity of diurnal and nocturnal toads (4-7 km) provided compelling evidence for the abovementioned physical factors as the proximate cause of the behavioral dichotomy, and for a novel (deeply shaded gorges) environment causing the shift to diurnal activity.

Cranial performance in the Komodo dragon (Varanus komodoensis) as revealed by high-resolution 3-D finite element analysis.

The Komodo dragon (Varanus komodoensis) displays a unique hold and pull-feeding technique. Its delicate 'space-frame' skull morphology differs greatly from that apparent in most living large prey specialists and is suggestive of a high degree of optimization, wherein use of materials is minimized. Here, using high-resolution finite element modelling based on dissection and in vivo bite and pull data, we present results detailing the mechanical performance of the giant lizard's skull. Unlike most modern predators, V. komodoensis applies minimal input from the jaw muscles when butchering prey. Instead it uses series of actions controlled by postcranial muscles. A particularly interesting feature of the performance of the skull is that it reveals considerably lower overall stress when these additional extrinsic forces are added to those of the jaw adductors. This remarkable reduction in stress in response to additional force is facilitated by both internal and external bone anatomy. Functional correlations obtained from these analyses also provide a solid basis for the interpretation of feeding ecology in extinct species, including dinosaurs and sabre-tooth cats, with which V. komodoensis shares various cranial and dental characteristics.

The vector of jaw muscle force as determined by computer-generated three dimensional simulation: a test of Greaves' model.

We present results from a detailed three-dimensional finite element analysis of the cranium and mandible of the Australian dingo (Canis lupus dingo) during a range of feeding activities and compare results with predictions based on two-dimensional methodology [Greaves, W.S., 2000. Location of the vector of jaw muscle force in mammals. Journal of Morphology 243, 293-299]. Greaves showed that the resultant muscle vector intersects the mandible line slightly posterior to the lower third molar (m3). Our work demonstrates that this is qualitatively correct, although the actual point is closer to the jaw joint. We show that it is theoretically possible for the biting side of the mandible to dislocate during unilateral biting; however, the bite point needs to be posterior to m3. Simulations show that reduced muscle activation on the non-biting side can considerably diminish the likelihood of dislocation with only a minor decrease in bite force during unilateral biting. By modulating muscle recruitment the animal may be able to maximise bite force whilst minimising the risk of dislocation.

Claw morphometrics in monitor lizards: Variable substrate and habitat use correlate to shape diversity within a predator guild.

Numerous studies investigate morphology in the context of habitat, and lizards have received particular attention. Substrate usage is often reflected in the morphology of characters associated with locomotion, and, as a result, claws have become well-studied ecomorphological traits linking the two. The Kimberley predator guild of Western Australia consists of 10 sympatric varanid species. The purpose of this study was to quantify claw size and shape in the guild using geometric morphometrics, and determine whether these features correlated with substrate use and habitat. Each species was assigned a Habitat/substrate group based on the substrate their claws interact with in their respective habitat. Claw morphometrics were derived for both wild caught and preserved specimens from museum collections, using a 2D semilandmark analysis. Claw shape significantly separated based on Habitat/substrate group. Varanus gouldii and Varanus panoptes claws were associated with sprinting and extensive digging. Varanus mertensi claws were for shallow excavation. The remaining species' claws reflected specialization for some form of climbing, and differed based on substrate compliance. Varanus glauerti was best adapted for climbing rough sandstone, whereas Varanus scalaris and Varanus tristis had claws ideal for puncturing wood. Phylogenetic signal also significantly influenced claw shape, with Habitat/substrate group limited to certain clades. Positive size allometry allowed for claws to cope with mass increases, and shape allometry reflected a potential size limit on climbing. Claw morphology may facilitate niche separation within this trophic guild, especially when considered with body size. As these varanids are generalist predators, morphological traits associated with locomotion may be more reliable candidates for detecting niche partitioning than those associated directly with diet.

Computer simulation of feeding behaviour in the thylacine and dingo as a novel test for convergence and niche overlap.

The extinct marsupial thylacine (Thylacinus cynocephalus) and placental grey wolf (Canis lupus) are commonly presented as an iconic example of convergence. However, various analyses suggest distinctly different behaviours and specialization towards either relatively small or large prey in the thylacine, bringing the degree of apparent convergence into question. Here we apply a powerful engineering tool, three-dimensional finite element analysis incorporating multiple material properties for bone, to examine mechanical similarity and niche overlap in the thylacine and the wolf subspecies implicated in its extinction from mainland Australia, Canis lupus dingo. Comparisons of stress distributions not only reveal considerable similarity, but also informative differences. The thylacine's mandible performs relatively poorly where only the actions of the jaw muscles are considered, although this must be considered in the light of relatively high bite forces. Stresses are high in the posterior of the thylacine's cranium under loads that simulate struggling prey. We conclude that relative prey size may have been comparable where both species acted as solitary predators, but that the dingo is better adapted to withstand the high extrinsic loads likely to accompany social hunting of relatively large prey. It is probable that there was considerable ecological overlap. As a large mammalian hypercarnivore adapted to taking small-medium sized prey, the thylacine may have been particularly vulnerable to disturbance.

Biomechanics of the rostrum in crocodilians: a comparative analysis using finite-element modeling.

This article reports the use of simple beam and finite-element models to investigate the relationship between rostral shape and biomechanical performance in living crocodilians under a range of loading conditions. Load cases corresponded to simple biting, lateral head shaking, and twist feeding behaviors. The six specimens were chosen to reflect, as far as possible, the full range of rostral shape in living crocodilians: a juvenile Caiman crocodilus, subadult Alligator mississippiensis and Crocodylus johnstoni, and adult Caiman crocodilus, Melanosuchus niger, and Paleosuchus palpebrosus. The simple beam models were generated using morphometric landmarks from each specimen. Three of the finite-element models, the A. mississippiensis, juvenile Caiman crocodilus, and the Crocodylus johnstoni, were based on CT scan data from respective specimens, but these data were not available for the other models and so these--the adult Caiman crocodilus, M. niger, and P. palpebrosus--were generated by morphing the juvenile Caiman crocodilus mesh with reference to three-dimensional linear distance measured from specimens. Comparison of the mechanical performance of the six finite-element models essentially matched results of the simple beam models: relatively tall skulls performed best under vertical loading and tall and wide skulls performed best under torsional loading. The widely held assumption that the platyrostral (dorsoventrally flattened) crocodilian skull is optimized for torsional loading was not supported by either simple beam theory models or finite-element modeling. Rather than being purely optimized against loads encountered while subduing and processing food, the shape of the crocodilian rostrum may be significantly affected by the hydrodynamic constraints of catching agile aquatic prey. This observation has important implications for our understanding of biomechanics in crocodilians and other aquatic reptiles.

Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa.

We provide the first predictions of bite force (BS) in a wide sample of living and fossil mammalian predators. To compare between taxa, we calculated an estimated bite force quotient (BFQ) as the residual of BS regressed on body mass. Estimated BS adjusted for body mass was higher for marsupials than placentals and the Tasmanian devil (Sarcophilus harrisii) had the highest relative BS among extant taxa. The highest overall BS was in two extinct marsupial lions. BFQ in hyaenas were similar to those of related, non-osteophagous taxa challenging the common assumption that osteophagy necessitates extreme jaw muscle forces. High BFQ in living carnivores was associated with greater maximal prey size and hypercarnivory. For fossil taxa anatomically similar to living relatives, BFQ can be directly compared, and high values in the dire wolf (Canis dirus) and thylacine (Thylacinus cynocephalus) suggest that they took relatively large prey. Direct inference may not be appropriate where morphologies depart widely from biomechanical models evident in living predators and must be considered together with evidence from other morphological indicators. Relatively low BFQ values in two extinct carnivores with morphologies not represented among extant species, the sabrecat, Smilodon fatalis, and marsupial sabretooth, Thylacosmilus atrox, support arguments that their killing techniques also differed from extant species and are consistent with 'canine-shear bite' and 'stabbing' models, respectively. Extremely high BFQ in the marsupial lion, Thylacoleo carnifex, indicates that it filled a large-prey hunting niche.

The sensitivity of biological finite element models to the resolution of surface geometry: a case study of crocodilian crania.

The reliability of finite element analysis (FEA) in biomechanical investigations depends upon understanding the influence of model assumptions. In producing finite element models, surface mesh resolution is influenced by the resolution of input geometry, and influences the resolution of the ensuing solid mesh used for numerical analysis. Despite a large number of studies incorporating sensitivity studies of the effects of solid mesh resolution there has not yet been any investigation into the effect of surface mesh resolution upon results in a comparative context. Here we use a dataset of crocodile crania to examine the effects of surface resolution on FEA results in a comparative context. Seven high-resolution surface meshes were each down-sampled to varying degrees while keeping the resulting number of solid elements constant. These models were then subjected to bite and shake load cases using finite element analysis. The results show that incremental decreases in surface resolution can result in fluctuations in strain magnitudes, but that it is possible to obtain stable results using lower resolution surface in a comparative FEA study. As surface mesh resolution links input geometry with the resulting solid mesh, the implication of these results is that low resolution input geometry and solid meshes may provide valid results in a comparative context.

The relationship between cranial structure, biomechanical performance and ecological diversity in varanoid lizards.

Skull structure is intimately associated with feeding ability in vertebrates, both in terms of specific performance measures and general ecological characteristics. This study quantitatively assessed variation in the shape of the cranium and mandible in varanoid lizards, and its relationship to structural performance (von Mises strain) and interspecific differences in feeding ecology. Geometric morphometric and linear morphometric analyses were used to evaluate morphological differences, and finite element analysis was used to quantify variation in structural performance (strain during simulated biting, shaking and pulling). This data was then integrated with ecological classes compiled from relevant scientific literature on each species in order to establish structure-function relationships. Finite element modelling results showed that variation in cranial morphology resulted in large differences in the magnitudes and locations of strain in biting, shaking and pulling load cases. Gracile species such as Varanus salvadorii displayed high strain levels during shaking, especially in the areas between the orbits. All models exhibit less strain during pull back loading compared to shake loading, even though a larger force was applied (pull =30N, shake = 20N). Relationships were identified between the morphology, performance, and ecology. Species that did not feed on hard prey clustered in the gracile region of cranial morphospace and exhibited significantly higher levels of strain during biting (P = 0.0106). Species that fed on large prey clustered in the elongate area of mandible morphospace. This relationship differs from those that have been identified in other taxonomic groups such as crocodiles and mammals. This difference may be due to a combination of the open 'space-frame' structure of the varanoid lizard skull, and the 'pull back' behaviour that some species use for processing large prey.

Oldest pathology in a tetrapod bone illuminates the origin of terrestrial vertebrates.

The origin of terrestrial tetrapods was a key event in vertebrate evolution, yet how and when it occurred remains obscure, due to scarce fossil evidence. Here, we show that the study of palaeopathologies, such as broken and healed bones, can help elucidate poorly understood behavioural transitions such as this. Using high-resolution finite element analysis, we demonstrate that the oldest known broken tetrapod bone, a radius of the primitive stem tetrapod Ossinodus pueri from the mid-Viséan (333 million years ago) of Australia, fractured under a high-force, impact-type loading scenario. The nature of the fracture suggests that it most plausibly occurred during a fall on land. Augmenting this are new osteological observations, including a preferred directionality to the trabecular architecture of cancellous bone. Together, these results suggest that Ossinodus, one of the first large (>2m length) tetrapods, spent a significant proportion of its life on land. Our findings have important implications for understanding the temporal, biogeographical and physiological contexts under which terrestriality in vertebrates evolved. They push the date for the origin of terrestrial tetrapods further back into the Carboniferous by at least two million years. Moreover, they raise the possibility that terrestriality in vertebrates first evolved in large tetrapods in Gondwana rather than in small European forms, warranting a re-evaluation of this important evolutionary event.

The Dry Season Shuffle: Gorges Provide Refugia for Animal Communities in Tropical Savannah Ecosystems.

In the wet-dry tropics, animal species face the major challenges of acquiring food, water or shelter during an extended dry season. Although large and conspicuous animals such as ungulates and waterfowl migrate to wetter areas during this time, little is known of how smaller and more cryptic animal species with less mobility meet these challenges. We fenced off the entire entrance of a gorge in the Australian tropical savanna, offering the unique opportunity to determine the composition and seasonal movement patterns of the small vertebrate community. The 1.7 km-long fence was converted to a trapline that was deployed for 18-21 days during the early dry season in each of two years, and paired traps on both sides of the fence allowed us to detect the direction of animal movements. We predicted that semi-aquatic species (e.g., frogs and turtles) would move upstream into the wetter gorge during the dry season, while more terrestrial species (e.g., lizards, snakes, mammals) would not. The trapline captured 1590 individual vertebrates comprising 60 species. There was a significant bias for captures on the outside of the fence compared to the inside for all species combined (outside/inside = 5.2, CI = 3.7-7.2), for all vertebrate classes, and for specific taxonomic groups. The opposite bias (inside/outside = 7.3, N= 25) for turtles during the early wet season suggested return migration heading into the wet season. Our study revealed that the small vertebrate community uses the gorge as a dry season refuge. The generality of this unreplicated finding could be tested by extending this type of survey to tropical savannahs worldwide. A better understanding of how small animals use the landscape is needed to reveal the size of buffer zones around wetlands required to protect both semi-aquatic and terrestrial fauna in gorges in tropical savannah woodland, and thus in ecosystems in general.

An interactive three dimensional approach to anatomical description-the jaw musculature of the Australian laughing kookaburra (Dacelo novaeguineae).

The investigation of form-function relationships requires a detailed understanding of anatomical systems. Here we document the 3-dimensional morphology of the cranial musculoskeletal anatomy in the Australian Laughing Kookaburra Dacelo novaeguineae, with a focus upon the geometry and attachments of the jaw muscles in this species. The head of a deceased specimen was CT scanned, and an accurate 3D representation of the skull and jaw muscles was generated through manual segmentation of the CT scan images, and augmented by dissection of the specimen. We identified 14 major jaw muscles: 6 in the temporal group (M. adductor mandibulae and M. pseudotemporalis), 7 in the pterygoid group (M. pterygoideus dorsalis and M. pterygoideus ventralis), and the single jaw abductor M. depressor mandibulae. Previous descriptions of avian jaw musculature are hindered by limited visual representation and inconsistency in the nomenclature. To address these issues, we: (1) present the 3D model produced from the segmentation process as a digital, fully interactive model in the form of an embedded 3D image, which can be viewed from any angle, and within which major components can be set as opaque, transparent, or hidden, allowing the anatomy to be visualised as required to provide a detailed understanding of the jaw anatomy; (2) provide a summary of the nomenclature used throughout the avian jaw muscle literature. The approach presented here provides considerable advantages for the documentation and communication of detailed anatomical structures in a wide range of taxa.