Christofer J. Clemente

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.

Pushing versus pulling: division of labour between tarsal attachment pads in cockroaches

Adhesive organs on the legs of arthropods and vertebrates are strongly direction dependent, making contact only when pulled towards the body but detaching when pushed away from it. Here we show that the two types of attachment pads found in cockroaches (Nauphoeta cinerea), tarsal euplantulae and pretarsal arolium, serve fundamentally different functions. Video recordings of vertical climbing revealed that euplantulae are almost exclusively engaged with the substrate when legs are pushing, whereas arolia make contact when pulling. Thus, upward-climbing cockroaches used front leg arolia and hind leg euplantulae, whereas hind leg arolia and front leg euplantulae were engaged during downward climbing. Single-leg friction force measurements showed that the arolium and euplantulae have an opposite direction dependence. Euplantulae achieved maximum friction when pushed distally, whereas arolium forces were maximal during proximal pulls. This direction dependence was not explained by the variation of shear stress but by different contact areas during pushing or pulling. The changes in contact area result from the arrangement of the flexible tarsal chain, tending to detach the arolium when pushing and to peel off euplantulae when in tension. Our results suggest that the euplantulae in cockroaches are not adhesive organs but ‘friction pads’, mainly providing the necessary traction during locomotion.

Insect tricks: two-phasic foot pad secretion prevents slipping

Many insects cling to vertical and inverted surfaces with pads that adhere by nanometre-thin films of liquid secretion. This fluid is an emulsion, consisting of watery droplets in an oily continuous phase. The detailed function of its two-phasic nature has remained unclear. Here we show that the pad emulsion provides a mechanism that prevents insects from slipping on smooth substrates. We discovered that it is possible to manipulate the adhesive secretion in vivo using smooth polyimide substrates that selectively absorb its watery component. While thick layers of polyimide spin-coated onto glass removed all visible hydrophilic droplets, thin coatings left the emulsion in its typical form. Force measurements of stick insect pads sliding on these substrates demonstrated that the reduction of the watery phase resulted in a significant decrease in friction forces. Artificial control pads made of polydimethylsiloxane showed no difference when tested on the same substrates, confirming that the effect is caused by the insects’ fluid-based adhesive system. Our findings suggest that insect adhesive pads use emulsions with non-Newtonian properties, which may have been optimized by natural selection. Emulsions as adhesive secretions combine the benefits of ‘wet’ adhesion and resistance against shear forces.

Friction ridges in cockroach climbing pads: anisotropy of shear stress measured on transparent, microstructured substrates

The contact of adhesive structures to rough surfaces has been difficult to investigate as rough surfaces are usually irregular and opaque. Here we use transparent, microstructured surfaces to investigate the performance of tarsal euplantulae in cockroaches (Nauphoeta cinerea). These pads are mainly used for generating pushing forces away from the body. Despite this biological function, shear stress (force per unit area) measurements in immobilized pads showed no significant difference between pushing and pulling on smooth surfaces and on 1-μm high microstructured substrates, where pads made full contact. In contrast, on 4-μm high microstructured substrates, where pads made contact only to the top of the microstructures, shear stress was maximal during a push. This specific direction dependence is explained by the interlocking of the microstructures with nanometre-sized “friction ridges” on the euplantulae. Scanning electron microscopy and atomic force microscopy revealed that these ridges are anisotropic, with steep slopes facing distally and shallow slopes proximally. The absence of a significant direction dependence on smooth and 1-μm high microstructured surfaces suggests the effect of interlocking is masked by the stronger influence of adhesion on friction, which acts equally in both directions. Our findings show that cockroach euplantulae generate friction using both interlocking and adhesion.

Is body shape of varanid lizards linked with retreat choice

In our earlier analysis ofVaranusbody shape, size was a dominating factor with some qualitative phylogenetic patterns and grouping of species into ecological categories. With a phylogeny and an improved capacity to account for the effects of size, we have reanalysed our morphometric data for male Australian goannas (Varanus spp.) using an increased numberofspecimensandspeciestoexaminewhethervariationsinbodyshapecanbeaccountedforbyretreatchoice,asitcan for Western Australian Ctenophorus dragon lizards. After accounting for body size in the current analysis, four ecotypes basedonretreatchoice(i.e.thosethatretreattoobliquecrevicesbetweenlargerocksorrockfaces,thosethatretreattoburrows dug into the ground, those that retreat to spaces under rocks or in tree hollows, and those that retreat to trees but not tree hollows)accountedformuchofthevariationinbodyshape.Thereisaphylogeneticpatterntotheecotypes,butaccountingfor phylogeneticeffectsdidnotweakenthelinkbetweenbodyshapeandecotypebasedonretreatchoice.Thissuggeststhatthere are large differences in body shape among ecotypes, and shape is relatively independent of phylogeny. The strong link between shape and choice of retreat site in Varanus spp. is consistent with that for Ctenophorus spp. We speculate on why there might be a strong link between retreat choice and body shape for both Varanus and Ctenophorus.

Extreme positive allometry of animal adhesive pads and the size limits of adhesion-based climbing

Significance How adhesive forces can be scaled up from microscopic to macroscopic levels is a central problem for biological and bio-inspired adhesives. Here, we elucidate how animals with sticky footpads cope with large body sizes. We find an extreme positive allometry of footpad area across all 225 species studied, implying a 200-fold increase of relative pad area from mites to geckos. Within groups, however, pads were almost isometric, but their adhesive strength increased with size, inconsistent with existing models. Extrapolating the observed scaling, we show that to support a human’s body weight, an unrealistic 40% of the body surface would have to be covered with adhesive pads, suggesting that anatomical constraints may prohibit the evolution of adhesion-based climbers larger than geckos. Organismal functions are size-dependent whenever body surfaces supply body volumes. Larger organisms can develop strongly folded internal surfaces for enhanced diffusion, but in many cases areas cannot be folded so that their enlargement is constrained by anatomy, presenting a problem for larger animals. Here, we study the allometry of adhesive pad area in 225 climbing animal species, covering more than seven orders of magnitude in weight. Across all taxa, adhesive pad area showed extreme positive allometry and scaled with weight, implying a 200-fold increase of relative pad area from mites to geckos. However, allometric scaling coefficients for pad area systematically decreased with taxonomic level and were close to isometry when evolutionary history was accounted for, indicating that the substantial anatomical changes required to achieve this increase in relative pad area are limited by phylogenetic constraints. Using a comparative phylogenetic approach, we found that the departure from isometry is almost exclusively caused by large differences in size-corrected pad area between arthropods and vertebrates. To mitigate the expected decrease of weight-specific adhesion within closely related taxa where pad area scaled close to isometry, data for several taxa suggest that the pads’ adhesive strength increased for larger animals. The combination of adjustments in relative pad area for distantly related taxa and changes in adhesive strength for closely related groups helps explain how climbing with adhesive pads has evolved in animals varying over seven orders of magnitude in body weight. Our results illustrate the size limits of adhesion-based climbing, with profound implications for large-scale bio-inspired adhesives.

Running faster causes disaster: trade-offs between speed, manoeuvrability and motor control when running around corners in northern quolls (Dasyurus hallucatus)

Movement speed is fundamental to all animal behaviour, yet no general framework exists for understanding why animals move at the speeds they do. Even during fitness-defining behaviours like running away from predators, an animal should select a speed that balances the benefits of high speed against the increased probability of mistakes. In this study, we explored this idea by quantifying trade-offs between speed, manoeuvrability and motor control in wild northern quolls (Dasyurus hallucatus) – a medium-sized carnivorous marsupial native to northern Australia. First, we quantified how running speed affected the probability of crashes when rounding corners of 45, 90 and 135 deg. We found that the faster an individual approached a turn, the higher the probability that they would crash, and these risks were greater when negotiating tighter turns. To avoid crashes, quolls modulated their running speed when they moved through turns of varying angles. Average speed for quolls when sprinting along a straight path was around 4.5 m s−1 but this decreased linearly to speeds of around 1.5 m s−1 when running through 135 deg turns. Finally, we explored how an individuals morphology affects their manoeuvrability. We found that individuals with larger relative foot sizes were more manoeuvrable than individuals with smaller relative foot sizes. Thus, movement speed, even during extreme situations like escaping predation, should be based on a compromise between high speed, manoeuvrability and motor control. We advocate that optimal – rather than maximal – performance capabilities underlie fitness-defining behaviours such as escaping predators and capturing prey.

Form follows function: morphological diversification and alternative trapping strategies in carnivorous Nepenthes pitcher plants

Carnivorous plants of the genus Nepenthes have evolved a striking diversity of pitcher traps that rely on specialized slippery surfaces for prey capture. With a comparative study of trap morphology, we show that Nepenthes pitcher plants have evolved specific adaptations for the use of either one of two distinct trapping mechanisms: slippery wax crystals on the inner pitcher wall and ‘insect aquaplaning’ on the wet upper rim (peristome). Species without wax crystals had wider peristomes with a longer inward slope. Ancestral state reconstructions identified wax crystal layers and narrow, symmetrical peristomes as ancestral, indicating that wax crystals have been reduced or lost multiple times independently. Our results complement recent reports of nutrient source specializations in Nepenthes and suggest that these specializations may have driven speciation and rapid diversification in this genus.

A bio-robotic platform for integrating internal and external mechanics during muscle-powered swimming

To explore the interplay between muscle function and propulsor shape in swimming animals, we built a robotic foot to mimic the morphology and hind limb kinematics of Xenopus laevis frogs. Four foot shapes ranging from low aspect ratio (AR = 0.74) to high (AR = 5) were compared to test whether low-AR feet produce higher propulsive drag force resulting in faster swimming. Using feedback loops, two complementary control modes were used to rotate the foot: force was transmitted to the foot either from (1) a living plantaris longus (PL) muscle stimulated in vitro or (2) an in silico mathematical model of the PL. To mimic forward swimming, foot translation was calculated in real time from fluid force measured at the foot. Therefore, bio-robot swimming emerged from muscle-fluid interactions via the feedback loop. Among in vitro-robotic trials, muscle impulse ranged from 0.12 ± 0.002 to 0.18 ± 0.007 N s and swimming velocities from 0.41 ± 0.01 to 0.43 ± 0.00 m s(-1), similar to in vivo values from prior studies. Trends in in silico-robotic data mirrored in vitro-robotic observations. Increasing AR caused a small (∼10%) increase in peak bio-robot swimming velocity. In contrast, muscle force-velocity effects were strongly dependent on foot shape. Between low- and high-AR feet, muscle impulse increased ∼50%, while peak shortening velocity decreased ∼50% resulting in a ∼20% increase in net work. However, muscle-propulsion efficiency (body center of mass work/muscle work) remained independent of AR. Thus, we demonstrate how our experimental technique is useful for quantifying the complex interplay among limb morphology, muscle mechanics and hydrodynamics.

Lizard tricks: overcoming conflicting requirements of speed versus climbing ability by altering biomechanics of the lizard stride

SUMMARY Adaptations promoting greater performance in one habitat are thought to reduce performance in others. However, there are many examples of animals in which, despite habitat differences, such predicted differences in performance do not occur. One such example is the relationship between locomotory performance to habitat for varanid lizards. To explain the lack of difference in locomotor performance we examined detailed observations of the kinematics of each lizards stride. Differences in kinematics were greatest between climbing and non-climbing species. For terrestrial lizards, the kinematics indicated that increased femur adduction, femur rotation and ankle angle all contributed positively to changes in stride length, but they were constrained for climbing species, probably because of biomechanical restrictions on the centre of mass height (to increase stability on vertical surfaces). Despite climbing species having restricted stride length, no differences have been previously reported in sprint speed between climbing and non-climbing varanids. This is best explained by climbing varanids using an alternative speed modulation strategy of varying stride frequency to avoid the potential trade-off of speed versus stability on vertical surfaces. Thus, by measuring the relevant biomechanics for lizard strides, we have shown how kinematic differences among species can mask performance differences typically associated with habitat variation.