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.     

Disparity between Feeding Performance and Predicted Muscle Strength in the Pharyngeal Musculature of Black Drum, Pogonias cromis (Sciaenidae)

Synopsis Pogonias cromis, black drum, is the largest durophagous sciaenid and feeds almost exclusively on hard-shelled bivalves and gastropods using powerful pharyngeal jaws. I estimated pharyngeal jaw bite forces used to crush live molluscs during feeding trials from juvenile and young adult Pogonias cromis, and they are the highest yet documented for bony fishes. Crushing ability in P. cromis scaled with strong positive allometry suggesting large adult fish may have one of the strongest bites among vertebrates. Physiological estimates of pharyngeal muscle strength derived from muscle cross sectional area accounted for only half of the force generated during actual feeding performance trials. The significant disparity between feeding performance and pharyngeal muscle strength in P. cromis indicates the presence of novel biomechanical linkages that enhance crushing ability for feeding on hard-shelled molluscs. I present a biomechanical model in which the lower pharyngeal jaw architecture of P. cromis emulates a second class lever mechanism that can amplify muscle forces transmitted to the shell of the prey.     

Feeding behaviour and bite force of sabretoothed predators

The feeding behaviour of extinct sabretoothed predators (machaeroidines, nimravids, barbourofelids, machairodonts and thylacosmilines) is investigated using beam theory. Because bite force applied along the mandible should be proportional to the external dimension of the mandibular corpus, patterns of variation in these dimensions at interdental gaps will reflect the adaptation of the jaw to specific loads, related to killing methods. Comparison of the mandibular force profiles of sabretooths to those of extant conical‐toothed carnivorans of known feeding behaviour reveals that sabretooths had a powerful bite, as strong or stronger than extant felids of similar mandibular length. Loads exerted at the lower canine were better constrained in the sagittal plane than in extant conical‐toothed carnivorans, indicating that prey was efficiently restrained when the sabre bite was delivered. The mandibular symphysis is generally better buttressed dorsoventrally in dirk‐toothed sabretooths than in scimitar‐toothed sabretooths, implying different killing strategies for the two ecomorphs: dirktooths delivered powerful sabre bites on prey they restrained with their forelimbs, while scimitartooths delivered slashing sabre bites and may have used their incisor battery to subdue their prey. The mandibular symphysis of Smilodon fatalis is less buttressed dorsoventrally than that of other dirk‐toothed sabretooths, possibly as a consequence of the greater torsional stresses induced while feeding rapidly on carcasses in response to intense competition. The mandibular symphysis of Thylacosmilus atrox is better buttressed dorsoventrally in juveniles than in adults, suggesting that young marsupial sabretooths underwent an extended period of parental care as typically observed in modern felids and inferred for eutherian sabretooths. Finally, machaeroidines and the nimravid Nimravus brachyops are exceptional in exhibiting a degree of dorsoventral buttressing of the mandibular symphysis that is intermediate between advanced sabretooths and conical‐toothed felids but similar to the extant Neofelis nebulosa, suggesting that the latter taxon may be close to the ancestral condition of a new sabretooth radiation. © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145 , 393–426.     

Resource partitioning among top predators in a Miocene food web

The exceptional fossil sites of Cerro de los Batallones (Madrid Basin, Spain) contain abundant remains of Late Miocene mammals. From these fossil assemblages, we have inferred diet, resource partitioning and habitat of three sympatric carnivorous mammals based on stable isotopes. The carnivorans include three apex predators: two sabre-toothed cats (Felidae) and a bear dog (Amphicyonidae). Herbivore and carnivore carbon isotope (δ¹³C) values from tooth enamel imply the presence of a woodland ecosystem dominated by C₃ plants. δ¹³C values and mixing-model analyses suggest that the two sabre-toothed cats, one the size of a leopard and the other the size of a tiger, consumed herbivores with similar δ¹³C values from a more wooded portion of the ecosystem. The two sabre-toothed cats probably hunted prey of different body sizes, and the smaller species could have used tree cover to avoid encounters with the larger felid. For the bear dog, δ¹³C values are higher and differ significantly from those of the sabre-toothed cats, suggesting a diet that includes prey from more open woodland. Coexistence of the sabre-toothed cats and the bear dog was likely facilitated by prey capture in different portions of the habitat. This study demonstrates the utility of stable isotope analysis for investigating the behaviour and ecology of members of past carnivoran guilds.     

Behavior of juvenile pink salmon (Oncorhynchus gorbuscha Walbaum) toward novel prey: influence of ontogeny and experience

Synopsis The behavior of individual, juvenile pink salmon toward novel prey (Artemia salina) under laboratory conditions is described. Two aspects of predatory behavior, namely latency time to initial prey-capture attempt and prey-capture success, are quantified in relation to chronological age and feeding experience. Initially, mean latency time declined slightly with increasing age up to Day 19 (post-emergence from gravel), but increased sharply to an asymptote with further aging. Mean percentage capture success gradually increased from 7.88% on Day 1 to 92.9% on Day 45. Prior feeding experience on the prey resulted in a decline (to a stable level) in mean latency time in experienced fish compared to control fish. Mean percentage capture success was not significantly altered by prior feeding experience on the prey.     

Carcass Decoration Changes Web Structure and Prey Capture Rate in an Orb-Web Spider, Cyclosa mulmeinensis (Araneae, Araneidae)

Cyclosa spiders attach prey carcasses as decorations to their webs, but the functions of the carcasses are unclear and controversial. We investigated distinctive features of these webs in the field and conducted prey-capture experiments in the lab using the orb-web spider Cyclosa mulmeinensis. Webs with attached decoration had a significantly narrower mesh width than those without decoration and a higher degree of vertical asymmetry in the web’s shape. In the laboratory, webs without decorations trapped significantly more prey, even though other features of the webs were nearly identical. These results suggest that web decorations do not attract prey in this species, but might play other roles such as blinding predators to the spider’s presence.     

Biomechanical analyses of Cambrian euarthropod limbs reveal their effectiveness in mastication and durophagy

Durophagy arose in the Cambrian and greatly influenced the diversification of biomineralized defensive structures throughout the Phanerozoic. Spinose gnathobases on protopodites of Cambrian euarthropod limbs are considered key innovations for shell-crushing, yet few studies have demonstrated their effectiveness with biomechanical models. Here we present finite-element analysis models of two Cambrian trilobites with prominent gnathobases—Redlichia rex and Olenoides serratus—and compare these to the protopodites of the Cambrian euarthropod Sidneyia inexpectans and the modern American horseshoe crab, Limulus polyphemus. Results show that L. polyphemus, S. inexpectans and R. rex have broadly similar microstrain patterns, reflecting effective durophagous abilities. Conversely, low microstrain values across the O. serratus protopodite suggest that the elongate gnathobasic spines transferred minimal strain, implying that this species was less well-adapted to masticate hard prey. These results confirm that Cambrian euarthropods with transversely elongate protopodites bearing short, robust gnathobasic spines were likely durophages. Comparatively, taxa with shorter protopodites armed with long spines, such as O. serratus, were more likely restricted to a soft food diet. The prevalence of Cambrian gnathobase-bearing euarthropods and their various feeding specializations may have accelerated the development of complex trophic relationships within early animal ecosystems, especially the ‘arms race'' between predators and biomineralized prey.     

Why the Long Face? The Mechanics of Mandibular Symphysis Proportions in Crocodiles

Background

Crocodilians exhibit a spectrum of rostral shape from long snouted (longirostrine), through to short snouted (brevirostrine) morphologies. The proportional length of the mandibular symphysis correlates consistently with rostral shape, forming as much as 50% of the mandible’s length in longirostrine forms, but 10% in brevirostrine crocodilians. Here we analyse the structural consequences of an elongate mandibular symphysis in relation to feeding behaviours.

Methods/Principal Findings

Simple beam and high resolution Finite Element (FE) models of seven species of crocodile were analysed under loads simulating biting, shaking and twisting. Using beam theory, we statistically compared multiple hypotheses of which morphological variables should control the biomechanical response. Brevi- and mesorostrine morphologies were found to consistently outperform longirostrine types when subject to equivalent biting, shaking and twisting loads. The best predictors of performance for biting and twisting loads in FE models were overall length and symphyseal length respectively; for shaking loads symphyseal length and a multivariate measurement of shape (PC1– which is strongly but not exclusively correlated with symphyseal length) were equally good predictors. Linear measurements were better predictors than multivariate measurements of shape in biting and twisting loads. For both biting and shaking loads but not for twisting, simple beam models agree with best performance predictors in FE models.

Conclusions/Significance

Combining beam and FE modelling allows a priori hypotheses about the importance of morphological traits on biomechanics to be statistically tested. Short mandibular symphyses perform well under loads used for feeding upon large prey, but elongate symphyses incur high strains under equivalent loads, underlining the structural constraints to prey size in the longirostrine morphotype. The biomechanics of the crocodilian mandible are largely consistent with beam theory and can be predicted from simple morphological measurements, suggesting that crocodilians are a useful model for investigating the palaeobiomechanics of other aquatic tetrapods.     

Prey-induced changes to a predator's behaviour and morphology: Implications for shell-claw covariance in the northwest Atlantic

Whereas many plasticity studies demonstrate the importance of inducible defences among prey, far fewer investigate the potential role of inducible offences among predators. Here we ask if natural differences in a snail's shell hardness can induce developmental changes to a predatory crab's claw size. To do this, we fed Littorina obtusata snails from either thick- or thin-shelled populations to captive European green crabs Carcinus maenas. The crabs' shell-breaking behaviour dominated among those fed thin-shelled snails, whereas crabs fed thick-shelled snails mostly winkled flesh through the shell opening without damaging the shell itself (a.k.a. aperture-probing behaviour). Significantly, the size of crab crusher claws grew in proportion to the frequency of shell-crushing behaviour and, for a same shell-crushing frequency, crabs fed thick-shelled snails grew larger crusher claws than those fed thin-shelled snails after two experimental moults. Diet and behaviour had no effect on the growth of the smaller cutter claws of same individuals, providing good evidence that allometric changes to crusher claws were indeed a result of differential use while feeding. Findings indicate that both predation habits and claw sizes are affected by green crabs' diet, supporting the hypothesis that prey-induced phenotypic plasticity contributes to earlier accounts of shell-claw covariance between this predator and its Littorina prey in the wild.     

Habitat structural complexity mediates the foraging success of multiple predator species

We investigated the role of freshwater macrophytes as refuge by testing the hypothesis that predators capture fewer prey in more dense and structurally complex habitats. We also tested the hypothesis that habitat structure not only affects the prey-capture success of a single predator in isolation, but also the effectiveness of two predators combined, particularly if it mediates interactions between the predators. We conducted a fully crossed four-factorial laboratory experiment using artificial plants to determine the separate quantitative (density) and qualitative (shape) components of macrophyte structure on the prey-capture success of a predatory damselfly, Ischnura heterosticta tasmanica, and the southern pygmy perch, Nannoperca australis. Contrary to our expectations, macrophyte density had no effect on the prey-capture success of either predator, but both predators were significantly less effective in the structurally complex Myriophyllum analogue than in the structurally simpler Triglochin and Eleocharis analogues. Furthermore, the greater structural complexity of Myriophyllum amplified the impact of the negative interaction between the predators on prey numbers; the habitat use by damselfly larvae in response to the presence of southern pygmy perch meant they captured less prey in Myriophyllum. These results demonstrate habitat structure can influence multiple predator effects, and support the mechanism of increased prey refuge in more structurally complex macrophytes.     

Intralocality Variation in Feeding Biomechanics and Prey Use in Archosargus probatocephalus (Teleostei,Sparidae), with Implications for the Ecomorphology of Fishes

Archosargus probatocephalusin a Florida estuary was investigated to explore intraspecific variation in prey utilization and jaw biomechanics. Volumetric contribution of major prey types and seven biomechanical features of the oral jaws that characterize prey-capture and processing performance were contrasted between two locations within the estuary. At Mosquito Lagoon, where A. probatocephalusinhabited mostly oyster beds, mangroves and salt marshes, fish consumed mostly thick-shelled bivalves, gastropods, crabs, and tubiculous polychaetes and amphipods. In contrast, conspecifics at Indian River Lagoon that inhabited mostly seagrass beds and algal turf consumed predominantly algae, seagrass, epiphytic invertebrates and small bivalves and gastropods. Difference in magnitude of durophagy between locations was associated with differences in oral-jaw biomechanics. Analyses of covariance indicated that A. probatocephalusat Mosquito Lagoon had more massive jaw muscles and bones, than conspecifics at Indian River Lagoon. Variations in lever ratios for jaw-opening and jaw-closing between locations were not significant. It is hypothesized that intralocality differences in food habits have induced the development of feeding morphologies that enhance the ability of A. probatocephalusto successfully exploit locally dominant prey resources within the estuary. Plasticity of the feeding mechanism of A. probatocephalusmay buffer the species from the adverse effects of settling on heterogeneous habitats that contain variable prey resources such as those found within estuaries.     

Insights into the ecology and evolutionary success of crocodilians revealed through bite-force and tooth-pressure experimentation

Background

Crocodilians have dominated predatory niches at the water-land interface for over 85 million years. Like their ancestors, living species show substantial variation in their jaw proportions, dental form and body size. These differences are often assumed to reflect anatomical specialization related to feeding and niche occupation, but quantified data are scant. How these factors relate to biomechanical performance during feeding and their relevance to crocodilian evolutionary success are not known.

Methodology/Principal Findings

We measured adult bite forces and tooth pressures in all 23 extant crocodilian species and analyzed the results in ecological and phylogenetic contexts. We demonstrate that these reptiles generate the highest bite forces and tooth pressures known for any living animals. Bite forces strongly correlate with body size, and size changes are a major mechanism of feeding evolution in this group. Jaw shape demonstrates surprisingly little correlation to bite force and pressures. Bite forces can now be predicted in fossil crocodilians using the regression equations generated in this research.

Conclusions/Significance

Critical to crocodilian long-term success was the evolution of a high bite-force generating musculo-skeletal architecture. Once achieved, the relative force capacities of this system went essentially unmodified throughout subsequent diversification. Rampant changes in body size and concurrent changes in bite force served as a mechanism to allow access to differing prey types and sizes. Further access to the diversity of near-shore prey was gained primarily through changes in tooth pressure via the evolution of dental form and distributions of the teeth within the jaws. Rostral proportions changed substantially throughout crocodilian evolution, but not in correspondence with bite forces. The biomechanical and ecological ramifications of such changes need further examination.     

Bite Force in Four Pinniped Species from the West Coast of Baja California,Mexico, in Relation to Diet,Feeding Strategy,and Niche Differentiation

Behavioral foraging differences are known to aid in food resource partitioning in pinniped communities, but it is not known whether skull biomechanical efficiency also contributes to dietary niche partitioning. We tested this hypothesis in a community of four sympatric species of pinnipeds that co-occur along the coast of Baja California: California sea lion (Zalophus californianus), northern elephant seal (Mirounga angustirostris), harbor seal (Phoca vitulina), and Guadalupe fur seal (Arctocephalus townsendi). We tested whether their preferred prey items differed in resistivity to puncture and whether those differences were linked to the mass of the muscles of mastication and the biomechanical efficiency with which they can puncture prey items. For each prey species, we measure resistivity to puncture using texture profile analysis. We found that M. angustirostris consumes the most resistant prey and that A. townsendi consumes the least resistant. We estimated physiological cross-sectional area of the muscles of mastication for each pinniped and found that the same pair of species respectively has the largest and smallest theoretical value of muscular force. Finally, we estimated the bite force that each pinniped species requires to puncture its prey by solving Euler-Lagrange equations based on biomechanical lever model parameters measured from 3D digital models of the skulls. We also found differences in efficiency between the species. These data allowed us to classify the three ecomorphological types. Type 1 features a hydrodynamic skull with relatively low mandibular forces, characteristic of pelagic carnivore feeders such as A. townsendi. Type 2, represented by Z. californianus and M. angustirostris (both opportunistic feeders), is characterized by broad insertion areas for the mandibular muscles and strong teeth, permitting these predators to vary the prey target species as a function of prey availability. Type 3 features a less robust skull and a lower muscle efficiency, characteristic of benthic feeders such as P. vitulina. This evidence indicates that biomechanical differences between the species contribute to dietary niche construction.

     

Coordination of Behavioral Sequences Between Individuals During Prey Capture in a Social Spider, Anelosimus eximius

The analysis of collaborative predation sequences performed by groups of 10 individuals (females) in a nonterritorial permanent-social spider, A. eximius, shows that prey-captures are organized in successive steps. Spiders begin by throwing sticky silk, which hinders the prey in the web; they then throw dry silk, which completes the immobilization of the prey. The third step is characterized by bites that paralyze the prey that will be then carried. A concordance test reveals a coordination of the individual's acts that explains the collaborative prey-capture efficiency. No individual specialization in one type of act has been shown. On the contrary, by using living preys or artificially dead vibrated preys, we show that all individuals have equipotential behaviors. Furthermore, each spider is able to adjust its behavior to the state of the prey. Individuals already involved in prey transportation can again display bites or sticky silk throwing if the prey is artificially vibrated. This mechanism, which corresponds to stimergic processes responsible for self-organized phenomena, already described in social insects, permits a coordination of individual acts without the recourse of direct communication. These results permit us to understand better how individuals coordinate their acts and lead us to support the hypothesis that the transition between solitary species and social species in spiders could have been sudden.     

Animal-Borne Imaging Reveals Novel Insights into the Foraging Behaviors and Diel Activity of a Large-Bodied Apex Predator,the American Alligator (Alligator mississippiensis)

Large-bodied, top- and apex predators (e.g., crocodilians, sharks, wolves, killer whales) can exert strong top-down effects within ecological communities through their interactions with prey. Due to inherent difficulties while studying the behavior of these often dangerous predatory species, relatively little is known regarding their feeding behaviors and activity patterns, information that is essential to understanding their role in regulating food web dynamics and ecological processes. Here we use animal-borne imaging systems (Crittercam) to study the foraging behavior and activity patterns of a cryptic, large-bodied predator, the American alligator (Alligator mississippiensis) in two estuaries of coastal Florida, USA. Using retrieved video data we examine the variation in foraging behaviors and activity patterns due to abiotic factors. We found the frequency of prey-attacks (mean = 0.49 prey attacks/hour) as well as the probability of prey-capture success (mean = 0.52 per attack) were significantly affected by time of day. Alligators attempted to capture prey most frequently during the night. Probability of prey-capture success per attack was highest during morning hours and sequentially lower during day, night, and sunset, respectively. Position in the water column also significantly affected prey-capture success, as individuals’ experienced two-fold greater success when attacking prey while submerged. These estimates are the first for wild adult American alligators and one of the few examples for any crocodilian species worldwide. More broadly, these results reveal that our understandings of crocodilian foraging behaviors are biased due to previous studies containing limited observations of cryptic and nocturnal foraging interactions. Our results can be used to inform greater understanding regarding the top-down effects of American alligators in estuarine food webs. Additionally, our results highlight the importance and power of using animal-borne imaging when studying the behavior of elusive large-bodied, apex predators, as it provides critical insights into their trophic and behavioral interactions.     

Behavior of the rhabdocoel flatworm Mesostoma ehrenbergii in prey capture and feeding

The prey-capture and feeding behavior of the rhabdocoel flatworm Mesostoma ehrenbergii (Focke, 1836) was analyzed using a variety of live and dead prey, including Daphnia, mosquito larvae, and tubifex annelids. Prey-capture behavior was broken down into its individual components. Mesostoma could accommodate to and change its behavior depending on the size and type of prey. Mechanical rather than chemical cues were effective in inducing prey-capture behavior. No evidence for a special chemical paralysis as suggested by other workers was found. The apparent paralysis observed in cladocera such as Daphnia and mosquito larvae was, in part a behavioral response of the prey in ‘playing possum’ and also in part due to immobilization of the prey by the flatworm with mucous threads. This revised version was published online in July 2006 with corrections to the Cover Date.     

Evolution mediates the effects of apex predation on aquatic food webs

Ecological and evolutionary mechanisms are increasingly thought to shape local community dynamics. Here, I evaluate if the local adaptation of a meso-predator to an apex predator alters local food webs. The marbled salamander (Ambystoma opacum) is an apex predator that consumes both the spotted salamander (Ambystoma maculatum) and shared zooplankton prey. Common garden experiments reveal that spotted salamander populations which co-occur with marbled salamanders forage more intensely than those that face other predator species. These foraging differences, in turn, alter the diversity, abundance and composition of zooplankton communities in common garden experiments and natural ponds. Locally adapted spotted salamanders exacerbate prey biomass declines associated with apex predation, but dampen the top-down effects of apex predation on prey diversity. Countergradient selection on foraging explains why locally adapted spotted salamanders exacerbate prey biomass declines. The two salamander species prefer different prey species, which explains why adapted spotted salamanders buffer changes in prey composition owing to apex predation. Results suggest that local adaptation can strongly mediate effects from apex predation on local food webs. Community ecologists might often need to consider the evolutionary history of populations to understand local diversity patterns, food web dynamics, resource gradients and their responses to disturbance.     

‘A prey in the hand’, multi-prey capute behaviour in a sit-and-wait predator,Ranatra dispar (Heteroptera: Nepidae), the Water Stick Insect

The Water Stick Insect,Ranatra dispar, is shown to be able to capute and hold a number of prey simultaneously. Capture of prey characteristically occurs in 3 distinct patterns (Type 1, 2 and 3), each characterized by a different number of prey caught. The time since las feeding by the predator has a significant effect on wether the predator will capture more than one prey. Once feeding starts, there is a critical period during which, if an encounter takes place the predator will attempt to capture either a second or third prey. The critical peroid is longer, the higher the motivation level of the predator. It is suggested that this prey-capture behaviour potentially increase the size of a meal as groups of prey move past the stationary prdator.     

Effect of locomotor approach on feeding kinematics in the green anole (Anolis carolinensis)

Squamates are well-known models for studying to examine locomotor and feeding behaviors in tetrapods, but studies that integrate both behavioral activities remain scarce. Anolis lizards are a classical lineage to study the evolutionary relationships between locomotor behavior and complex structural features of the habitat. Here, we analyzed prey-capture behavior in one representative arboreal predator, Anolis carolinensis, to demonstrate the functional links between locomotor strategies and the kinematics of feeding. A. carolinensis uses two strategies to catch living insects on perches: Head-Up Capture and Jump Capture. In both cases, lizards use lingual prehension to capture the prey and the kinematic patterns of the trophic apparatus are not significantly influenced by the selected strategies. Therefore, to capture one prey type, movements of the trophic structures are highly fixed and A. carolinensis modulates the locomotor pattern to exploit the environment. Predation behavior in A. carolinensis integrates two different behavioral patterns: locomotor plasticity of prey-approach and biomechanical stereotypy of tongue prehension to successfully capture the prey.