The functional morphology of lingual prey capture in a scincid lizard,Tiliqua scincoides (Reptilia: Squamata)

We investigated the functional morphology of lingual prey capture in the blue‐tongued skink, Tiliqua scincoides, a lingual‐feeding lizard nested deep within the family Scincidae, which is presumed to be dominated by jaw‐feeding. We used kinematic analysis of high‐speed video to characterize jaw and tongue movements during prey capture. Phylogenetically informed principal components analysis of tongue morphology showed that, compared to jaw‐feeding scincids and lacertids, T. scincoides and another tongue‐feeding scincid, Corucia zebrata, are distinct in ways suggesting an enhanced ability for hydrostatic shape change. Lingual feeding kinematics show substantial quantitative and qualitative variation among T. scincoides individuals. High‐speed video analysis showed that T. scincoides uses significant hydrostatic elongation and deformation during protrusion, tongue‐prey contact, and retraction. A key feature of lingual prey capture in T. scincoides is extensive hydrostatic deformation to increase the area of tongue‐prey contact, presumably to maximize wet adhesion of the prey item. Adhesion is mechanically reinforced during tongue retraction through formation of a distinctive “saddle” in the foretongue that supports the prey item, reducing the risk of prey loss during retraction.     

Modulation of prey capture kinematics and the role of lingual sensory feedback in the lizard Pogona vitticeps

Most organisms feed on a variety of prey that may differ dramatically in their physical and behavioural characteristics (e.g. mobility, mass, texture, etc.). Thus the ability to modulate prey capture behaviour in accordance with the characteristics of the food appears crucial. In animals that use rapid tongue movements to capture prey (frogs and chameleons), the coordination of jaws and tongue is based on visual cues gathered prior to the prey capture event. However, most iguanian lizards have much slower tongue-based prey capture systems suggesting that sensory feedback from the tongue may play an important role in coordinating jaw and tongue movements. We investigated the modulation of prey capture kinematics in the agamid lizard Pogona vitticeps when feeding on a range of food items differing in their physical characteristics. As the lizard is a dietary generalist, we expected it to be able to modulate its prey capture kinematics as a function of the (mechanical) demands imposed by the prey. Additionally, we investigated the role of lingual sensory feedback by transecting the trigeminal sensory afferents. Our findings demonstrated that P. vitticeps modulates its prey capture kinematics according to specific prey properties (e.g. size). In addition, transection of the trigeminal sensory nerves had a strong effect on prey capture kinematics. However, significant prey type effects and prey type by transection effects suggest that other sources of sensory information are also used to modulate the prey capture kinematics in P. vitticeps.     

Tadpole–odonate larvae interactions: influence of body size and diel rhythm

Several studies have shown that prey and predator body size may affect the outcome of predator–prey interactions. However, few studies have taken in account the changes on predator–prey interactions over 24 h. In a tropical freshwater system I evaluated how predator and prey size, and their diel rhythm in activity influenced the interaction between Physalaemus pustulosus tadpoles and dragonfly larvae. Tadpoles of different size classes were exposed to two size classes of the dragonfly larvae Rhionaeschna spec. Feeding trials were conducted during day and night. Tadpole activity showed a diel rhythm and affected size-selective predation of the smallest dragonfly larvae, but not of the larger ones. Predator and prey size had a significant effect on the prey survivorship and prey size had a significant effect on the preference of the predator. The interaction between both factors was significant, indicating that they did not operate independently. I conclude that the predator–prey interactions between odonate larvae and anuran tadpoles were mainly affected by the size of the prey and the predator, and less by the diel activity pattern of the prey.     

Integrated diversification of locomotion and feeding in labrid fishes

An organism''s performance of any ecological task involves coordination of multiple functional systems. Feeding performance is influenced by locomotor abilities which are used during search and capture of prey, as well as cranial mechanics, which affect prey capture and processing. But, does this integration of functional systems manifest itself during evolution? We asked whether the locomotor and feeding systems evolved in association in one of the most prominent and diverse reef fish radiations, the Labridae. We examined features of the pectoral fins that affect swimming performance and aspects of the skull that describe force and motion of the jaws. We applied a recent phylogeny, calculated independent contrasts for 60 nodes and performed principal components analyses separately on contrasts for fin and skull traits. The major axes of fin and skull diversification are highly correlated; modifications of the skull to amplify the speed of jaw movements are correlated with changes in the pectoral fins that increase swimming speed, and increases in force capacity of the skull are associated with changes towards fins that produce high thrust at slow speeds. These results indicate that the labrid radiation involved a strong connection between locomotion and feeding abilities.     

Zooplankton capture by a coral reef fish: an adaptive response to evasive prey

Synopsis High-speed cinematography and video using modified Schlieren optics and laser illumination helped elicit details of prey capture mechanisms used by Chromis viridis while feeding on calanoid copepods and Artemia. Chromis viridis is capable of a ram-jaw, low-suction feeding, as well as a typical suction feeding behavior described for other species of planktivores. By adjusting the degree of jaw protrusion and amount of suction used during a feeding strike, this fish can modulate its feeding strikes according to the prey type being encountered. The ram-jaw feeding mode enables C. viridis to capture highly evasive calanoid copepods within 6 to 10 msec. The use of specialized feeding behavior for evasive prey and the ability to vary feeding behavior are adaptations for feeding on evasive prey.     

Mechanisms of selectivity in a nocturnal fish: a lack of active prey choice

Fish that feed on individual zooplankton usually exhibit strong selectivity for large prey. Such selectivity can result from the predator’s active choice of larger prey or from differential encounter rate due to lower detectability of small prey, or both. In diurnal fishes, selectivity is thought to be determined mostly by active choice. In spite of a lack of direct observations, active choice is also considered the prevailing mechanism of prey selectivity in nocturnal fishes. Our objective was to resolve this mechanism in the highly selective, nocturnal zooplanktivorous fish Apogon annularis. Laboratory experiments indicated that the fish’s encounter rate with small prey was lower than that with large prey and that its selectivity became stronger with decreasing light intensity. Feeding efficiency, defined as the ratio between feeding and encounter rates, ranged 41–89% and was positively correlated with prey size. When feeding on a mixture of prey sizes, the fish fed on each size group at a rate similar to that of its feeding on the respective size alone, indicating that selectivity in A. annularis was due to size-dependent encounter rate and differential feeding efficiency. A low visual acuity in A. annularis, as inferred from its inability to detect small prey (<0.9 mm in length), together with the low abundance of large zooplankton in situ, can explain the dominance of differential encounter over active choice in this nocturnal coral-reef fish.     

Linking cranial morphology to prey capture kinematics in three cleaner wrasses: Labroides dimidiatus,Larabicus quadrilineatus,and Thalassoma lutescens

Cleaner fishes are well known for removing and consuming ectoparasites off other taxa. Observers have noted that cleaners continuously “pick” ectoparasites from the bodies of their respective client organisms, but little is known about the kinematics of cleaning. While a recent study described the jaw morphology of cleaners as having small jaw‐closing muscles and weak bite forces, it is unknown how these traits translate into jaw movements during feeding to capture and remove ectoparasites embedded in their clients. Here, we describe cranial morphology and kinematic patterns of feeding for three species of cleaner wrasses. Through high‐speed videography of cleaner fishes feeding in two experimental treatments, we document prey capture kinematic profiles for Labroides dimidiatus, Larabicus quadrilineatus, and Thalassoma lutescens. Our results indicate that cleaning in labrids may be associated with the ability to perform low‐displacement, fast jaw movements that allow for rapid and multiple gape cycles on individually targeted items. Finally, while the feeding kinematics of cleaners show notable similarities to those of “picker” cyprinodontiforms, we find key differences in the timing of events. In fact, cleaners generally seem to be able to capture prey twice as fast as cyprinodontiforms. We thus suggest that the kinematic patterns exhibited by cleaners are indicative of picking behavior, but that “pickers” may be more kinematically diverse than previously thought. J. Morphol. 276:1377–1391, 2015. © 2015 Wiley Periodicals, Inc.     

A forceful upper jaw facilitates picking-based prey capture: biomechanics of feeding in a butterflyfish,Chaetodon trichrous

Biomechanical models of feeding mechanisms elucidate how animals capture food in the wild, which, in turn, expands our understanding of their fundamental trophic niche. However, little attention has been given to modeling the protrusible upper jaw apparatus that characterizes many teleost species. We expanded existing biomechanical models to include upper jaw forces using a generalist butterflyfish, Chaetodon trichrous (Chaetodontidae) that produces substantial upper jaw protrusion when feeding on midwater and benthic prey. Laboratory feeding trials for C. trichrous were recorded using high-speed digital imaging; from these sequences we quantified feeding performance parameters to use as inputs for the biomechanical model. According to the model outputs, the upper jaw makes a substantial contribution to the overall forces produced during mouth closing in C. trichrous. Thus, biomechanical models that only consider lower jaw closing forces will underestimate total bite force for this and likely other teleost species. We also quantified and subsequently modeled feeding events for C. trichrous consuming prey from the water column versus picking attached prey from the substrate to investigate whether there is a functional trade-off between prey capture modes. We found that individuals of C. trichrous alter their feeding behavior when consuming different prey types by changing the timing and magnitude of upper and lower jaw movements and that this behavioral modification will affect the forces produced by the jaws during prey capture by dynamically altering the lever mechanics of the jaws. In fact, the slower, lower magnitude movements produced during picking-based prey capture should produce a more forceful bite, which will facilitate feeding on benthic attached prey items, such as corals. Similarities between butterflyfishes and other teleost lineages that also employ picking-based prey capture suggest that a suite of key behavioral and morphological innovations enhances feeding success for benthic attached prey items.     

Facilitation between herons and smallmouth bass foraging on common prey

Understanding how multiple predators affect one another and their shared prey is an increasingly important goal for ecologists examining predator–prey dynamics and food-web structure. In a field experiment, we examined the outcome of interactions between terrestrial and freshwater predators foraging for the same prey in two temperate North American streams. We used a factorial design to examine the combined foraging effects of herons and smallmouth bass on striped shiners and central stonerollers. We found that there was facilitation between the two predators, resulting in risk-enhancement for the prey species, with particularly pronounced effects on the smallest (<70 mm) size classes. Facilitation is the least well-documented predator–predator interaction and has not been quantitatively demonstrated for freshwater and terrestrial predators. Our results indicate that bass may gain a net benefit from the presence of wading birds such as herons and egrets, and that concerns about the negative effects of birds on fish stocks through competition may be unwarranted.     

Jaw and hyolingual movements during prey transport in varanid lizards: effects of prey type

The ability to modulate feeding kinematics in response to prey items with different functional properties is likely a prerequisite for most organisms that feed on a variety of food items. Variation in prey properties is expected to reveal variation in feeding function and the functional role of the different phases in a transport cycle. Here we describe the kinematics of prey transport of two varanid species, Varanus niloticus and Varanus ornatus. These species were selected for analysis because of their highly specialised hyolingual system and food transport mechanism (inertial food transport). In these animals, tongue and hyoid movements are expected to make no, or only a minor, contribution to prey transport. We observed statistically significant prey type effects that could be associated with prey properties such as mass, size and mobility. These data show that both species are capable of modulating the kinematics of food transport in response to different prey types. Moreover, not only the kinematics of the jaws were modulated in response to prey characteristics but also the anterior/posterior movements of the tongue and hyoid. This suggests a more important role of the tongue and hyolingual movements in these animals than previously suspected. In contrast, head movements were rather stereotyped and were not modulated in response to changes in prey type.     

Predator–prey systems in streams and rivers

Many predator–prey systems are found in environments with a predominantly unidirectional flow such as streams and rivers. Alterations of natural flow regimes (e.g., due to human management or global warming) put biological populations at risk. The aim of this paper is to devise a simple method that links flow speeds (currents) with population retention (persistence) and wash-out (extinction). We consider systems of prey and specialist, as well as generalist, predators, for which we distinguish the following flow speed scenarios: (a) coexistence, (b) persistence of prey only or (c) predators only (provided they are generalists), and (d) extinction of both populations. The method is based on a reaction–advection–diffusion model and traveling wave speed approximations. We show that this approach matches well spread rates observed in numerical simulations. The results from this paper can provide a useful tool in the assessment of instream flow needs, estimating the flow speed necessary for preserving riverine populations.     

Self-optimization, community stability, and fluctuations in two individual-based models of biological coevolution

We compare and contrast the long-time dynamical properties of two individual-based models of biological coevolution. Selection occurs via multispecies, stochastic population dynamics with reproduction probabilities that depend nonlinearly on the population densities of all species resident in the community. New species are introduced through mutation. Both models are amenable to exact linear stability analysis, and we compare the analytic results with large-scale kinetic Monte Carlo simulations, obtaining the population size as a function of an average interspecies interaction strength. Over time, the models self-optimize through mutation and selection to approximately maximize a community potential function, subject only to constraints internal to the particular model. If the interspecies interactions are randomly distributed on an interval including positive values, the system evolves toward self-sustaining, mutualistic communities. In contrast, for the predator–prey case the matrix of interactions is antisymmetric, and a nonzero population size must be sustained by an external resource. Time series of the diversity and population size for both models show approximate 1/f noise and power-law distributions for the lifetimes of communities and species. For the mutualistic model, these two lifetime distributions have the same exponent, while their exponents are different for the predator–prey model. The difference is probably due to greater resilience toward mass extinctions in the food-web like communities produced by the predator–prey model.      

Premaxillary movements in cyprinodontiform fishes: an unusual protrusion mechanism facilitates "picking" prey capture

Premaxillary protrusion is hypothesized to confer a number of feeding advantages to teleost fishes; however, most proposed advantages relate to enhanced stealth or suction production during prey capture. Cyprinodontiformes exhibit an unusual form of premaxillary protrusion where the descending process of the premaxilla does not rotate anteriorly to occlude the sides of the open mouth during prey capture. Instead, the premaxilla is protruded such that it gives the impression of a beak during prey capture. We quantified premaxillary kinematics during feeding in four cyprinodontiform taxa and compared them with three percomorph taxa to identify any performance consequences of this protrusion mechanism. Individual prey capture events were recorded using digital high-speed video at 250-500 frames per second (n4 individuals, 4 strikes per individual). Species differed in the timing of movement and the maximum displacement of the premaxilla during the gape cycle and in the contribution of the premaxilla to jaw closing. Cyprinodontiform taxa produced less premaxillary protrusion than the percomorph taxa, and were consistently slower in the time to maximum gape. Further, it appears cyprinodontiforms can alter the contribution of the premaxilla to mouth closure on an event-specific basis. We were able to demonstrate that, within at least one species, this variability is associated with the location of the prey (bottom vs. water column). Cyprinodontiform upper jaw movements likely reflect increased dexterity associated with a foraging ecology where prey items are "picked" from a variety of locations: the bottom, water column, or surface. We postulate that dexterity requires slow, precisely controlled jaw movements; thus, may be traded off for some aspects of suction-feeding performance, such as protrusion distance and speed.     

Feeding performance of the Hawaiian sleeper,Eleotris sandwicensis (Gobioidei: Eleotridae): correlations between predatory functional modulation and selection pressures on prey

The eleotrid fish Eleotris sandwicensis inhabits lower reaches of streams in the Hawaiian Archipelago, where it feeds on juveniles of native amphidromous gobiid fishes migrating upstream from the ocean. Using high‐speed video and geometric modelling, we evaluated the feeding kinematics and performance of E. sandwicensis on free swimming prey, including two species with juveniles of different characteristic sizes, and compared successful and unsuccessful strikes. With fast jaw movements and a highly expansive buccal cavity, E. sandwicensis achieves high suction performance that enables the capture of elusive prey. Our analyses indicated that the species with larger juveniles (Sicyopterus stimpsoni) could be captured from a distance of up to 18.6% of the predator's body length (BL), but capture of the smaller species (Awaous guamensis) required a closer distance (12.2% BL). Predator–prey distance appears to be the predominant factor determining strike outcome during feeding on juvenile A. guamensis. However, during feeding on juvenile S. stimpsoni, E. sandwicensis shows modulations of strike behaviour that correlate with capture success. Moreover, the ability of E. sandwicensis to capture larger prey fish from longer distances suggests a potential biomechanical basis underlying observations that predation by eleotrids imposes significant selection against large body size in juvenile gobies. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 359–374.     

Feeding with speed: prey capture evolution in cichilds

The diversity of both the locomotor and feeding systems in fish is extensive, although little is known about the integrated evolution of the two systems. Virtually, all fish swim to ingest prey and all open their buccal cavity during prey capture, but the relationship between these two ubiquitous components of fish feeding strikes is unknown. We predicted that there should be a positive correlation between ram speed (RS) and maximum gape (MG) because the accuracy of a predatory strike goes down with an increase in RS and fish with larger mouths eat larger, more evasive prey. For 18 species of neotropical cichlids, we used phylogenetic-independent contrasts to study the relationship between the predator closing speed (RS) and mouth size (MG) during prey capture. To provide a robust comparative framework, we augmented existing phylogenetic information available from the mitochondrial cytochrome b gene with sequences from the S7 nuclear ribosomal intron for these species. Then, we captured high-speed (500 images per second), lateral view feeding sequences of each species by using a digital video camera and measured both RS and MG. Uncorrected species values of MG and RS were positively and significantly correlated. When accounting for any of the set of phylogenetic relationships recovered, the independent contrasts of RS and MG remained significantly, and positively, correlated. This tight evolutionary coupling highlights what is likely a common relationship between locomotor behaviour and feeding kinematics in many organisms.     

Rapid prey evolution and the dynamics of two-predator food webs

Traits affecting ecological interactions can evolve on the same time scale as population and community dynamics, creating the potential for feedbacks between evolutionary and ecological dynamics. Theory and experiments have shown in particular that rapid evolution of traits conferring defense against predation can radically change the qualitative dynamics of a predator–prey food chain. Here, we ask whether such dramatic effects are likely to be seen in more complex food webs having two predators rather than one, or whether the greater complexity of the ecological interactions will mask any potential impacts of rapid evolution. If one prey genotype can be well-defended against both predators, the dynamics are like those of a predator–prey food chain. But if defense traits are predator-specific and incompatible, so that each genotype is vulnerable to attack by at least one predator, then rapid evolution produces distinctive behaviors at the population level: population typically oscillate in ways very different from either the food chain or a two-predator food web without rapid prey evolution. When many prey genotypes coexist, chaotic dynamics become likely. The effects of rapid evolution can still be detected by analyzing relationships between prey abundance and predator population growth rates using methods from functional data analysis.     

The effects of intraspecific competition on the prey capture behavior and kinematics of the bluegill sunfish, Lepomis macrochirus

Competition has broad effects on fish and specifically the effects of competition on the prey capture kinematics and behavior are important for the assessment of future prey capture studies in bony fishes. Prey capture kinematics and behavior in bony fishes have been shown to be affected by temperature and satiation. The densities at which bony fish are kept have also been shown to affect their growth, behavior, prey selection, feeding and physiology. We investigated how density induced intraspecific competition for food affects the prey capture kinematics of juvenile bluegill sunfish, Lepomis macrochirus. High speed video was utilized to film five bold individuals feeding at three different densities representing different levels of intraspecific competition. We hypothesized that: (1) the feeding kinematics will be faster at higher levels of competition compared to lower levels of competition, and (2) bluegill should shift from more suction-based feeding towards more ram-based feeding with increasing levels of competition in order to outcompete conspecifics for a prey item. We found that, with increased intraspecific competition, prey capture became faster, involving more rapid jaw opening and therefore greater inertial suction, shorter mouth closing times, and shorter gape cycles. Furthermore, the attack velocity of the fish increased with increasing competition, however a shift towards primarily ram based feeding was not confirmed. Our study demonstrates that prey capture kinematics are affected by the presence of conspecifics and future studies need to consider the effects of competition on prey capture kinematics.     

The integration of locomotion and prey capture in vertebrates: Morphology, behavior, and performance

For most vertebrates, locomotion is a fundamental componentof prey capture. Despite this ubiquitous link, few studies havequantified the integration of these complex systems. Severalvariables related to locomotor performance, including maximumspeed, acceleration, deceleration, maneuverability, accuracy,and approach stability, likely influence feeding performancein vertebrates. The relative importance of these measures ofperformance, however, depends on the ecology of the predator.While factors such as morphology and physiology likely definethe limits of these variables, other factors such as motivationof the predator, prey type, and habitat structure can also influenceperformance. Understanding how these variables relate to feedingunder a given suite of ecological conditions is central to understandingpredator–prey interactions, and ultimately how locomotionand feeding have co-evolved. The goals of this article are todiscuss several variables of locomotor performance related toprey capture, present new data on the relationship between locomotorand feeding morphology in fishes, discuss the evolution of preycapture in cichlid fishes, and outline some future directionsfor research. While suction feeding is a primary mechanism ofprey capture in fishes, swimming is vital for accurately positioningthe mouth relative to the prey item. Many fishes decelerateduring prey capture using their body and fins, but the pectoralfins have a dominant role in maintaining approach stability.This suggests that fishes employing high-performance suctionfeeding (relatively small mouth) will have larger pectoral finsto facilitate accurate and stable feeding. I provide new dataon the relationship between pectoral fin morphology and maximumgape in centrarchid fishes. For seven species, pectoral finarea was significantly, and negatively, correlated with maximumgape. This example illustrates that the demands from one complexsystem (feeding) can influence another complex system (locomotion).Future studies that examine the morphological, physiological,and functional evolution of locomotion involved in prey captureby aquatic and terrestrial vertebrates will provide insightinto the origin and consequences of diversity.     

Joint evolution of predator body size and prey-size preference

We studied the joint evolution of predator body size and prey-size preference based on dynamic energy budget theory. The predators’ demography and their functional response are based on general eco-physiological principles involving the size of both predator and prey. While our model can account for qualitatively different predator types by adjusting parameter values, we mainly focused on ‘true’ predators that kill their prey. The resulting model explains various empirical observations, such as the triangular distribution of predator–prey size combinations, the island rule, and the difference in predator–prey size ratios between filter feeders and raptorial feeders. The model also reveals key factors for the evolution of predator–prey size ratios. Capture mechanisms turned out to have a large effect on this ratio, while prey-size availability and competition for resources only help explain variation in predator size, not variation in predator–prey size ratio. Predation among predators is identified as an important factor for deviations from the optimal predator–prey size ratio.     

Lyapunov functions for Lotka–Volterra predator–prey models with optimal foraging behavior

 The theory of optimal foraging predicts abrupt changes in consumer behavior which lead to discontinuities in the functional response. Therefore population dynamical models with optimal foraging behavior can be appropriately described by differential equations with discontinuous right-hand sides. In this paper we analyze the behavior of three different Lotka–Volterra predator–prey systems with optimal foraging behavior. We examine a predator–prey model with alternative food, a two-patch model with mobile predators and resident prey, and a two-patch model with both predators and prey mobile. We show that in the studied examples, optimal foraging behavior changes the neutral stability intrinsic to Lotka–Volterra systems to the existence of a bounded global attractor. The analysis is based on the construction and use of appropriate Lyapunov functions for models described by discontinuous differential equations. Received: 23 March 1999