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Biomedical subjects

Anthony Herrel

Publications and source records attributed to Anthony Herrel.

At least 19 recordsLinked to original sources

No trade-off between biting and suction feeding performance in clariid catfishes.

It is generally assumed that biting performance trades off with suction performance in fish because both feeding types may place conflicting demands on the cranial musculo-skeletal system. However, the functional consequences of morphological adaptations enhancing biting on the mechanics and performance of suction feeding in fish remain obscure. In this study, suction feeding performance was compared between three clariid catfish species differing considerably in their biting capacity, by measuring the velocity of a standardized prey being sucked into the buccal cavity using high-speed cineradiography. In addition, buccal volume changes during prey capture were quantified by ellipse modelling. As all species were able to accelerate the prey to similar peak velocities, our results demonstrate the possibility for catfishes to increase bite performance considerably without compromising suction performance. The amount of buccal expansion in the ventral direction is approximately equal for all species. Consequently, the system generating expansion through ventral rotation of the lower jaw, hyoid and pectoral girdle is apparently not constrained (mechanically or architectonically) by the hypertrophy of the jaw adductors. As the effect of a reduced magnitude of lateral expansion (suspensorium abduction) on suction performance in Clariidae appears to be negligible (for example in Gymnallabes typus), these data demonstrate the dominant role of ventral expansion for producing suction in these fish.

Animals↗

Rotational feeding in caecilians: putting a spin on the evolution of cranial design.

Caecilians are a poorly known group of amphibians with a highly derived skull and cranial musculature that has evolved in response to their specialized head-first burrowing lifestyle. They possess a unique jaw-closing system, which is shown to be capable of generating considerable bite forces for its head width (1.09+/-0.34 and 0.62+/-0.31 N for Schistometopum thomense and Boulengerula taitanus, respectively). However, comprehensive dietary studies indicate that there is no need for large bite forces, since most caecilians appear to be generalist predators of subterranean macrofauna. Here, we demonstrate, based on in vivo external and X-ray video recordings of animals feeding, that long-axis body rotations are used independent of prey size by these two species of caeciliid caecilians when feeding underground. Further, we show that individuals are capable of generating a substantial spinning force, which is greater than their bite force (1.35+/-0.26 and 1.02+/-0.18 N, respectively). These observations shed light on the functional and the evolutionary significance of several unique features of the cranial design in derived caecilians; spinning may allow the individuals to judge prey size and subsequently reduce oversized prey within gape limits.

Amphibians↗

Microhabitat use, diet, and performance data on the Hispaniolan twig anole, Anolis sheplani: pushing the boundaries of morphospace.

Caribbean Anolis lizards are often cited as a textbook example of adaptive radiation. Similar morphologies (ecomorphs) have originated in similar ecological settings on different large islands in the West Indies. However, relatively little is known about one of the morphologically most specialized and divergent ecomorphs: the twig anoles. Here, we investigate aspects of morphology, dewlap size, locomotor and bite performance, structural habitat and diet of the poorly known twig anole, Anolis sheplani from Hispaniola. Few observations have previously been made of this species in its natural habitat, and few quantitative data on its natural history are available. A. sheplani is an extreme twig anole with respect to its morphology, performance capacities, and ecological niche. Males and females of this species do not differ from each other in body dimensions, performance or habitat use, but males do have a bigger dewlap than females. We present data for 25 individuals and compare them with data for other Greater Antillean anoles. It becomes apparent that twig anoles constitute a large component of the morphological, functional, and ecological diversity of Anolis lizards. Small twig anoles such as A. sheplani appear to be pushing the boundaries of morphospace and are thus crucial in our understanding of the evolution of phenotypic diversity.

Animals↗

Whole-organism studies of adhesion in pad-bearing lizards: creative evolutionary solutions to functional problems.

Understanding the evolution of complex functional traits is a challenge for evolutionary physiology. Here we investigate the evolution of subdigital toepads in lizards, which have arisen independently at least three times, although with subtle anatomical differences. Some designs (anole, gecko) appear functionally equivalent, whereas other designs (skink) are inferior. The functional equivalence of geckos and anoles highlights the creative aspect of the evolutionary process in that these two groups have arrived at the same functional endpoint along very different trajectories. However, this functional equivalence does not result in equivalence for performance at whole-organism tasks (e.g., running uphill), as the evolution of behavior (e.g., toe-furling) has enabled geckos to be superior climbers than anoles. We also show that adaptive increases in the toepad size within a closely related lizard genus (Anolis) has resulted in concomitant evolution of enhanced clinging ability and increased perch heights. A third insight is that pad-bearing geckos are capable of carrying tremendous loads (up to 250% of body weight) up smooth surfaces, and that the toepad itself does not appear limiting. This comparative and whole-organism approach to lizard toepads underscores how organisms can evolve multiple solutions to evolutionary problems.

Adaptation, Physiological↗

Hydrodynamic modelling of aquatic suction performance and intra-oral pressures: limitations for comparative studies.

The magnitude of sub-ambient pressure inside the bucco-pharyngeal cavity of aquatic animals is generally considered a valuable metric of suction feeding performance. However, these pressures do not provide a direct indication of the effect of the suction act on the movement of the prey item. Especially when comparing suction performance of animals with differences in the shape of the expanding bucco-pharyngeal cavity, the link between speed of expansion, water velocity, force exerted on the prey and intra-oral pressure remains obscure. By using mathematical models of the heads of catfishes, a morphologically diverse group of aquatic suction feeders, these relationships were tested. The kinematics of these models were fine-tuned to transport a given prey towards the mouth in the same way. Next, the calculated pressures inside these models were compared. The results show that no simple relationship exists between the amount of generated sub-ambient pressure and the force exerted on the prey during suction feeding, unless animals of the same species are compared. Therefore, for evaluating suction performance in aquatic animals in future studies, the focus should be on the flow velocities in front of the mouth, for which a direct relationship exists with the hydrodynamic force exerted on prey.

Animals↗

Modulation and variability of prey capture kinematics in clariid catfishes.

Species with narrow or limited diets (trophic specialists) are expected to be less flexible in their feeding repertoire compared to species feeding on a wide range of different prey (trophic generalists). The ability to modulate prey capture kinematics in response to different prey types and prey position, as well as the overall variability in prey capture kinematics, is evaluated in four clariid species ranging from trophic generalist (Clarias gariepinus) to species with morphological specializations and a narrow diet (Channallabes apus and Gymnallabes typus). High-speed video recordings were made of prey captures on two prey that differ in shape, attachment strength and hardness. While the observed amount of strike-to-strike variability in prey capture kinematics is similar for all species and not influenced by prey type, only the two less specialized species showed the ability to modulate their prey capture kinematics in function of the presented prey types. All species did, however, show positional modulation during the strike by adjusting the magnitude of neurocranial elevation. These results indicate that the narrow dietary breadth of trophic specialists is indeed indicative of functional stereotypy in this group of fishes. Although most studies focussing on prey processing found a similar result, the present study is one of the few that was able to demonstrate this relationship when focussing on prey capture mechanics. Possibly, this relationship is less frequently observed for prey capture compared to prey processing because, regardless of prey type, the initial capture of prey requires a higher amount of variability.

Animals↗

Evolution: a catfish that can strike its prey on land.

An important step towards understanding the evolution of terrestriality in vertebrates is to identify how the aquatic ancestors of tetrapods were able to access ground-based prey. We have discovered that the 'eel catfish' Channallabes apus, an inhabitant of the muddy swamps of tropical Africa, has a remarkable ability to forage and capture prey on land. The animal's capacity to bend its head down towards the ground while feeding seems to be an essential feature that may have enabled fish to make the transition from an aquatic to a terrestrial mode.

Africa↗

Out on a limb: The differential effect of substrate diameter on acceleration capacity in Anolis lizards.

We investigated how substrate diameter affects acceleration performance in three Anolis lizard species (A. sagrei, A. carolinensis and A. valencienni), representing three different ecomorphs (trunk-ground, trunk-crown, and twig, respectively). We did so by measuring maximal acceleration capacity of the three species on a broad and narrow dowel. In addition to acceleration capacity, we quantified maximal sprint speed on both dowels. Both acceleration capacity and sprint speed are affected by substrate diameter, but the way in which they are, differs among species. Acceleration capacity in the trunk-ground anole, A. sagrei, was least affected by dowel diameter, whereas it was greatly reduced on the narrow dowel in the twig anole, A. valencienni. Sprint speed on the narrow dowel, however, was reduced to the greatest extent in the fastest running species, A. sagrei, whereas sprint speed was hardly affected by dowel diameter in the slow A. valencienni. The differential effect of dowel diameter on maximal acceleration capacity cannot be explained by differences in the timing of reaching maximal acceleration, but may be due to interspecific differences in the relative positioning of the limbs on the different dowels. The differential effect of dowel diameter on sprint speed, on the other hand, may be based on interspecific differences in the relative contribution of subsequent acceleratory bouts to maximal sprint speed on the broad and narrow dowel.

Acceleration↗

The quick and the fast: the evolution of acceleration capacity in Anolis lizards.

Although of prime ecological relevance, acceleration capacity is a poorly understood locomotor performance trait in terrestrial vertebrates. No empirical data exist on which design characteristics determine acceleration capacity among species and whether these design traits influence other aspects of locomotor performance. In this study we explore how acceleration capacity and sprint speed have evolved in Anolis lizards. We investigate whether the same or different morphological traits (i.e., limb dimensions and muscle mass) correlate with both locomotor traits. Within our sample of Anolis lizards, relative sprint speed and acceleration capacity coevolved. However, whereas the variation in relative acceleration capacity is primarily explained by the variation in relative knee extensor muscle mass, the variation in relative sprint speed is correlated to the variation in relative femur, tibia, and metatarsus length as well as knee extensor muscle mass. The fact that the design features required to excel in either performance trait partly overlap might explain the positive correlation between the variation in relative sprint speed and acceleration capacity. Furthermore, our data show how similar levels of sprint performance can be achieved through different morphological traits (limb segment lengths and muscle mass) suggesting that redundant mapping has potentially played a role in mitigating trade-offs.

Acceleration↗

Ontogeny of performance in vertebrates.

When competing for food or other resources, or when confronted with predators, young animals may be at a disadvantage relative to adults because of their smaller size. Additionally, the ongoing differentiation and growth of tissues and the development of sensory-motor integration during early ontogeny may constrain performance. Because ectothermic vertebrates show different growth regimes and energetic requirements when compared to endothermic vertebrates, differences in the ontogenetic trajectories of performance traits in these two groups might be expected. However, both groups of vertebrates show similar patterns of changes in performance with ontogeny. Evidence for compensation, resulting in relatively high levels of performance in juveniles relative to adults, appears common for traits related to locomotor and defensive behaviors. However, there is little evidence for compensation in traits associated with feeding and foraging. We suggest that this difference may be due to different selective regimes operating on locomotor versus feeding traits. As a result, relatively high levels of locomotor performance in juveniles and relatively high levels of feeding performance in adults are observed across a wide range of vertebrate groups.

Animals↗

Scaling of suction feeding performance in the catfish Clarias gariepinus.

Ontogenetic changes in the absolute dimensions of the cranial system together with changes in kinematics during prey capture can cause differences in the spatiotemporal patterns of water flow generated during suction feeding. Because the velocity of this water flow determines the force that pulls prey toward and into the mouth cavity, this can affect suction feeding performance. In this study, size-related changes in the suction-induced flow patterns are determined. To do so, a mathematical suction model is applied to video recordings of prey capturing Clarias gariepinus ranging in total length from 111 to 923 mm. Although large C. gariepinus could be expected to have increasing peak velocities of water flow compared with small individuals, the results from the hydrodynamic model show that this is not the case. Yet, when C. gariepinus becomes larger, the expansive phase is prolonged, resulting in a longer sustained flow. This flow also reaches farther in front of the mouth almost proportionally with head size. Forward dynamical simulations with spherical prey that are subjected to the calculated water flows indicate that the absolute distance from which a given prey can be sucked into the mouth as well as the maximal prey diameter increase substantially with increasing head size. Consequently, the range of potential prey that can be captured through suction feeding will become broader during growth of C. gariepinus. This appears to be reflected in the natural diet of this species, where both the size and the number of evasive prey increase with increasing predator size.

Animals↗

Ontogenetic scaling of bite force in lizards and turtles.

Because selection on juvenile life-history stages is likely strong, disproportionately high levels of performance (e.g., sprint speed, endurance, etc.) might be expected. Whereas this phenomenon has been demonstrated with respect to locomotor performance, data for feeding are scarce. Here, we investigate the relationships among body dimensions, head dimensions, and bite force during growth in lizards and turtles. We also investigate whether ontogenetic changes in bite performance are related to changes in diet. Our analyses show that, for turtles, head dimensions generally increase with negative allometry. For lizards, heads scale as expected for geometrically growing systems. Bite force generally increased isometrically with carapace length in turtles but showed significant positive allometry relative to body dimensions in lizards. However, both lizards and turtles display positive allometric scaling of bite force relative to some measures of head size throughout ontogeny, suggesting (1) strong selection for increased relative bite performance with increasing head size and (2) intrinsic changes in the geometry and/or mass of the jaw adductors during growth. Whereas our data generally do not provide strong evidence of compensation for lower absolute levels of performance, they do show strong links among morphology, bite force, and diet during growth.

Animals↗

Movement control strategies during jumping in a lizard (Anolis valencienni).

Whereas maximal performance is subjected to specific control criteria, sub-maximal movements theoretically allow for an infinite number of control strategies. Yet sub-maximal movements are predominant in the locomotor repertoire of most organisms and often little understood. Previous data on sub-maximal vertical jumping in humans has suggested that a movement effectiveness criterion might best explain the observed control strategy employed. Here we test the generality of this criterion in jumping by inducing lizards to jump both at a range of distances as well as a range of take-off angles. Our results show that while movement effectiveness appears to best explain jumping for different take-off angles, a 'push harder' strategy (i.e. mostly increasing the force output of the system), is used in the control of distance jumping. Thus, our data support the generality of the movement effectiveness criterion for vertical jumping, but not for distance jumping. Sub-maximal distance jumping in the lizard Anolis valencienni appears to be governed by a relatively simple control strategy that allows a rapid response. This accords well to the ecological circumstances in which long jumps are typically used (escape from predators).

Animals↗

Comparisons of aquatic versus terrestrial predatory strikes in the pitviper, Agkistrodon piscivorus.

Recent studies comparing terrestrial versus aquatic locomotion in animals have shown that changes in kinematics, muscular activation patterns, and performance across media are often dramatic. Surprisingly, however, despite the importance of feeding to the survival of most animals, few studies have compared differences in feeding behaviour between media. The present study compares prey-capture behaviour, strike success, strike velocity and acceleration, and prey-capture kinematics in a semi-aquatic pitviper (Agkistrodon piscivorus) when capturing both terrestrial (mice) and aquatic (fish) prey in a standardized laboratory setting. Strike velocity and acceleration did not differ significantly between media, but instead were positively correlated with initial prey distance. By contrast, the kinematics of terrestrial and aquatic strikes differed significantly in several aspects: max gape angle during the retraction phase, angular velocity of mouth closing during the strike, and the initial head angle before the strike. Terrestrial strikes were associated with higher gape angles during the retraction phase, higher angular velocities of mouth closure, and a more inclined head angle at the onset of the strike. Finally, strike success differed significantly between strike types, with terrestrial strikes being considerably more successful than aquatic strikes. Strike success likely differed due to the relatively slow mouth-closing velocity of aquatic strikes.

Acceleration↗

Comparative functional analysis of the hyolingual anatomy in lacertid lizards.

The tongue is often considered a key innovation in the evolution of a terrestrial lifestyle as it allows animals to transport food items through the oral cavity in air, a medium with low density and viscosity. The tongue has been secondarily coopted for a wide diversity of functions, including prey capture, drinking, breathing, and defensive behaviors. Within basal lizard groups, the tongue is used primarily for the purpose of prey capture and transport. In more derived groups, however, the tongue appears specialized for chemoreceptive purposes. Here we examine the tongue structure and morphology in lacertid lizards, a group of lizards where the tongue is critical to both food transport and chemoreception. Because of the different mechanical demands imposed by these different functions, regional morphological specializations of the tongue are expected. All species of lacertid lizards examined here have relatively light tongue muscles, but a well developed hyobranchial musculature that may assist during food transport. The intrinsic musculature, including verticalis, transversalis, and longitudinalis groups, is well developed and may cause the tongue elongation and retraction observed during chemoreception and drinking. The papillary morphology is complex and shows clear differences between the tongue tips and anterior fore-tongue, and the more posterior parts of the tongue. Our data show a subdivision between the fore- and hind-tongue in both papillary structure and muscular anatomy likely allowing these animals to use their tongues effectively during both chemoreception and prey transport. Moreover, our data suggest the importance of hyobranchium movements during prey transport in lacertid lizards.

Animals↗

Prey capture kinematics of ant-eating lizards.

While morphological and behavioral feeding specializations are obvious in many vertebrate groups, among lizards there appear to be few dietary specialists. By comparing the prey capture kinematics and overall feeding behavior in two highly specialized ant-eating lizards (Moloch horridus and Phrynosoma platyrhinos) with those of two closely related dietary generalists (Pogona vitticeps and Uma notata), we investigate whether dietary specialization has been accompanied by changes in the function and use of the feeding system. We quantified kinematic variables from high-speed video recordings (200-250 frames s(-1)) of each species feeding on ants. Prey capture was strikingly different in M. horridus to that of other species, being characterized by a suite of unusual behaviors including the lack of a body lunge, faster tongue protrusion, reduced prey processing and, most notably, the ability to modulate the slow open phase of the gape cycle. In concert, these traits make a single feeding event in M. horridus faster than that in any other iguanian lizard studied to date. Prey capture behavior in P. platyrhinos is kinematically more similar to U. notata and P. vitticeps than to M. horridus, but the ant specialists are similar in that both lack distinct prey processing behaviors, resulting in faster overall capture and feeding events. While ant feeding in P. vitticeps is faster than feeding on other prey, the duration of a single feeding event is still four times longer than in either ant specialist, because of extensive prey processing. Additionally, a phylogenetic comparison of ant specialist lizards with dietary generalists revealed that ant-eating lizards require significantly less time to capture and process prey. Thus there are not only significant behavioral modifications in these ant-eating lizards, but also multiple strategies among specialists, suggesting differing selective pressures or phylogenetic constraints in the evolution of ant eating in lizards.

Animals↗

Scaling of suction-feeding kinematics and dynamics in the African catfish, Clarias gariepinus.

Scaling effects on the kinematics of suction feeding in fish remain poorly understood, at least partly because of the inconsistency of the results of the existing experimental studies. Suction feeding is mechanically distinct from most other type of movements in that negative pressure inside the buccal cavity is thought to be the most important speed-limiting factor during suction. However, how buccal pressure changes with size and how this influences the speed of buccal expansion is unknown. In this paper, the effects of changes in body size on kinematics of suction feeding are studied in the catfish Clarias gariepinus. Video recordings of prey-capturing C. gariepinus ranging in total length from 111 to 923 mm were made, from which maximal displacements, velocities and accelerations of several elements of the cranial system were determined. By modelling the observed expanding head of C. gariepinus as a series of expanding hollow elliptical cylinders, buccal pressure and power requirement for the expansive phase of prey capture were calculated for an ontogenetic sequence of catfish. We found that angular velocities decrease approximately proportional with increasing cranial size, while linear velocities remain more or less constant. Although a decreasing (angular) speed of buccal expansion with increasing size could be predicted (based on calculations of power requirement and the expected mass-proportional scaling of available muscular power in C. gariepinus), the observed drop in (angular) speed during growth exceeds these predictions. The calculated muscle-mass-specific power output decreases significantly with size, suggesting a relatively lower suction effort in the larger catfish compared with the smaller catfish.

Africa↗

A functional morphological approach to the scaling of the feeding system in the African catfish, Clarias gariepinus.

Effects of size are pervasive and affect nearly all aspects of the biology of animals and plants. Theoretical scaling models have been developed to predict the effects of size on the functioning of musculo-skeletal systems. Although numerous experimental studies have investigated the effects of size on the movements of skeletal elements during locomotion and feeding in vertebrates, relatively little is known about the scaling of the muscles and bones responsible for the actual movements. Here, we examine the scaling of external morphology, skeletal elements of the feeding system, and a number of cranial muscles to understand how this may affect the movements observed during suction feeding in the African catfish, Clarias gariepinus. The results show that neither the head nor the cranial elements themselves scale according to geometric similarity models. Relative to head size, distinct changes in the mass and configuration of the feeding structures takes place. Unexpectedly, different cranial muscles show different scaling patterns that ultimately all lead to a positive allometry of muscle cross-sectional area relative to fish head size. This suggests that (1) the scaling of the cranial elements cannot be predicted a priori based on the scaling of external head dimensions and (2) the scaling of the feeding system is optimised towards high force output in the larger animals. An analysis of the consequences of the observed changes in morphology with size on performance traits, including bite force and jaw closing velocity, suggests a tight link between the scaling of the feeding system and the natural diet of these fish. Whereas for smaller size classes the system is tuned towards high bite forces, for animals with cranial lengths greater than 65 mm the scaling of the feeding system appears to be dictated by the hydrodynamic constraints on suction feeding.

Africa↗