Small vertebrates running on uneven terrain: a biomechanical study of two differently specialised lacertid lizards.

While running, small animals frequently encounter large terrain variations relative to their body size, therefore, terrain variations impose important functional demands on small animals. Nonetheless, we have previously observed in lizards that running specialists can maintain a surprisingly good running performance on very uneven terrains. The relatively large terrain variations are offset by their capacity for leg adjustability that ensures a 'smooth ride' of the centre of mass (CoM). The question as to how the effect of an uneven terrain on running performance and locomotor costs differs between species exhibiting diverse body build and locomotor specializations remains. We hypothesise that specialized runners with long hind limbs can cross uneven terrain more efficiently than specialized climbers with a dorso-ventrally flattened body and equally short fore and hind limbs. This study reports 3D kinematics using high-speed videos (325 Hz) to investigate leg adjustability and CoM movements in two lacertid lizards (Acanthodactylus boskianus, running specialist; Podarcis muralis, climbing specialist). We investigated these parameters while the animals were running on a level surface and over a custom-made uneven terrain. We analysed the CoM dynamics, we evaluated the fluctuations of the positive and negative mechanical energy, and we estimated the overall cost of transport. Firstly, the results reveal that the climbers ran at lower speeds on flat level terrain but had the same cost of transport as the runners. Secondly, contrary to the running specialists, the speed was lower and the energy expenditure higher in the climbing specialists while running on uneven terrain. While leg movements adjust to the substrates' variations and enhance the stability of the CoM in the running specialist, this is not the case in the climbing specialist. Although their legs are kept more extended, the amplitude of movement does not change, resulting in an increase of the movement of the CoM and a decrease in locomotor efficiency. These results are discussed in light of the respective (micro-)habitat of these species and suggest that energy economy can also be an important factor for small vertebrates.

Habitat shapes the thermoregulation of Mediterranean lizards introduced to replicate experimental islets.

Both environmental temperatures and spatial heterogeneity can profoundly affect the biology of ectotherms. In lizards, thermoregulation may show high plasticity and may respond to environmental shifts. In the context of global climate change, lizards showing plastic thermoregulatory responses may be favored. In this study, we designed an experiment to evaluate the extent to which lizard thermoregulation responds to introduction to a new environment in a snapshot of time. In 2014, we captured individuals of the Aegean Wall lizard (Podarcis erhardii) from Naxos Island (429.8 km2) and released them onto two small, lizard-free islets, Galiatsos (0.0073 km2) and Kampana (0.004 km2) (Aegean Sea, Greece). In 2017, we returned to the islets and estimated the effectiveness (E), accuracy and precision of thermoregulation measuring operative, preferred (Tpref) and body temperatures. We hypothesized that the three habitats would differ in thermal quality and investigated the extent to which lizards from Naxos demonstrate plasticity when introduced to the novel, islet habitats. Thermal parameters did not differ between Galiatsos and Naxos and this was reflected in the similar E and Tpref. However, lizards from Kampana deviated in all focal traits from Naxos, resulting in higher E and a preference for higher Tpref. In sum, Naxos lizards shifted their thermoregulatory profile due to the idiosyncratic features of their new islet habitat. Our results advocate a high plasticity in lizard thermoregulation and suggest that there is room for effective responses to environmental changes, at least for Podarcis lizards in insular habitats.

Habitat use and vestibular system's dimensions in lacertid lizards.

The vestibular system is crucial for movement control during locomotion. As the dimensions of the vestibular system determine the fluid dynamics of the endolymph and, as such, the system's function, we investigate the interaction between vestibular system size, head size and microhabitat use in lizards. We grouped 24 lacertid species in three microhabitat types, we acquired three-dimensional models of the bony vestibular systems using micro-computer tomography scanning, and we performed linear and surface measurements. All vestibular measurements scale with a negative allometry with head size, suggesting that smaller heads house disproportionally large ears. As the sensitivity of the vestibular system is positively related to size, a sufficiently large vestibular system in small-headed animals may meet the sensitivity demands during challenged locomotion. We also found that the microhabitat affects the locomotor dynamics: lizards inhabiting open microhabitats run at higher dimensionless speeds. On the other hand, no statistical relationship exists between dimensionless speed and the vestibular system dimensions. Hence, if the vestibular size would differ between microhabitats, this would be a direct effect (i.e. imposed, for instance, by requirements for manoeuvring, balance control, etc.), rather than depending on the lizards' intrinsic running speed. However, we found no effect of the microhabitat on the allometric relationship between head and vestibular system size. The finding that microhabitat is not reflected in the vestibular system size (hence sensitivity) of the lacertids in this study is possibly due to spatial constraints of the skull.

Compliant legs enable lizards to maintain high running speeds on complex terrains.

Substrate variations are likely to constrain animal performance in natural environments, as running over complex terrains challenges the dynamic stability of the body differently in each step. Yet, being able to negotiate complex terrains at top speed is a strong advantage for animals that have to deal with predators and evasive prey. Little is known on how animals negotiate such terrain variability at high speed. We investigated this in fast-running Acanthodactylus boskianus lizards, by measuring their 3D kinematics using four synchronised high-speed video cameras (325 Hz) on an adaptable racetrack. This racetrack was covered with four different substrates, representing increasing levels of terrain complexity. We found that the lizards deal with this complexity gradient by gradually adopting more erect parasagittal leg postures. Legs in a more-erect position are more compliant and are therefore highly adjustable on complex terrains. Additionally, the lizards stabilise their head, which facilitates vestibular and visual perception. Together, compliant legs and head stabilisation enable the lizards to minimise movements of the body centre of mass, even when running on highly irregular terrains. This suggests that the head and the centre of mass are the priority targets for running on uneven terrains. As a result, running performance (mean forward speed) decreases only slightly, and only on the most challenging substrate under investigation.

Enhanced contrast in X-ray microtomographic images of the membranous labyrinth using different X-ray sources and scanning modes.

The vestibular system, located in the inner ear, plays a crucial role in balance and gaze stabilisation by sensing head movements. The interconnected tubes with membranous walls of the vestibular system are located in the skull bone (the 'membranous labyrinth'). Unfortunately, these membranes are very hard to visualise using three-dimensional (3D) X-ray imaging techniques. This difficulty arises due to the embedment of the membranes in the dense skull bone, the thinness of the membranes, and the small difference in X-ray absorption between the membranes and the surrounding fluid. In this study, we compared the visualisation of very small specimens (lizard heads with vestibular systems smaller than 3 mm) by X-ray computed micro-tomography (µCT) based on synchrotron radiation and conventional sources. A visualisation protocol using conventional X-ray µCT would be very useful thanks to the ease of access and lower cost. Careful optimisation of the acquisition parameters enables detection of the membranes by using µCT scanners based on conventional microfocus sources, but in some cases a low contrast-to-noise ratio (CNR) prevents fast and reliable segmentation of the membranes. Synchrotron radiation µCT proved to be preferable for the visualisation of the small samples with very thin membranes, because of their high demands for spatial and contrast resolution. The best contrast was obtained by using synchrotron radiation µCT working in phase-contrast mode, leading to up to twice as high CNRs than the best conventional µCT results. The CNR of the synchrotron radiation µCT scans was sufficiently high enough to enable the construction of a 3D model by the means of semi-automatic segmentation of the membranous labyrinth. Membrane thickness was found to range between 2.7 and 36.3 µm. Hence, the minimal membrane thickness was found to be much smaller than described previously in the literature (between 10 and 50 µm).

Author Correction: Evolutionary morphology of the lizard chemosensory system.

A correction to this article has been published and is linked from the HTML version of this paper. The error has not been fixed in the paper.

Evolutionary morphology of the lizard chemosensory system.

Foraging mode plays a pivotal role in traditional reconstructions of squamate evolution. Transitions between modes are said to spark concerted changes in the morphology, physiology, behaviour, and life history of lizards. With respect to their sensory systems, species that adopt a sit-and-wait strategy are thought to rely on visual cues primarily, while actively hunting species would predominantly use chemical information. The morphology of the tongue and the vomeronasal-organs is believed to mirror this dichotomy. Still, support for this idea of concerted evolution of the morphology of the lizard sensory system merely originates from studies comparing only a few, distantly related taxa that differ in many aspects of their biology besides foraging mode. Hence, we compared vomeronasal-lingual morphology among closely related lizard species (Lacertidae). Our findings show considerable interspecific variation indicating that the chemosensory system of lacertids has undergone substantial change over a short evolutionary time. Although our results imply independent evolution of tongue and vomeronasal-organ form, we find evidence for co-variation between sampler and sensor, hinting towards an 'optimization' for efficient chemoreception. Furthermore, our findings suggest species' degree of investment in chemical signalling, and not foraging behaviour, as a leading factor driving the diversity in vomeronasal-lingual morphology among lacertid species.

Jumping performance in the highly aquatic frog, Xenopus tropicalis: sex-specific relationships between morphology and performance.

Frogs are characterized by a morphology that has been suggested to be related to their unique jumping specialization. Yet, the functional demands associated with jumping and swimming may not be that different as suggested by studies with semi-aquatic frogs. Here, we explore whether features previously identified as indicative of good burst swimming performance also predict jumping performance in a highly aquatic frog, Xenopus tropicalis. Moreover, we test whether the morphological determinants of jumping performance are similar in the two sexes and whether jumping performance differs in the two sexes. Finally we test whether jumping capacity is positively associated with burst swimming and terrestrial endurance capacity in both sexes. Our results show sex-specific differences in jumping performance when correcting for differences in body size. Moreover, the features determining jumping performance are different in the two sexes. Finally, the relationships between different performance traits are sex-dependent as well with females, but not males, showing a trade-off between peak jumping force and the time jumped to exhaustion. This suggests that different selective pressures operate on the two sexes, with females being subjected to constraints on locomotion due to their greater body mass and investment in reproductive capacity. In contrast, males appear to invest more in locomotor capacity giving them higher performance for a given body size compared to females.