Most bony fishes rely on suction mechanisms to capture and transport prey. Once captured, prey ar... more Most bony fishes rely on suction mechanisms to capture and transport prey. Once captured, prey are carried by water movement inside the oral cavity to a second set of jaws in the throat, the pharyngeal jaws, which manipulate the prey and assist in swallowing. Moray eels display much less effective suction-feeding abilities. Given this reduction in a feeding mechanism that is widespread and highly conserved in aquatic vertebrates, it is not known how moray eels swallow large fish and cephalopods. Here we show that the moray eel (Muraena retifera) overcomes reduced suction capacity by launching raptorial pharyngeal jaws out of its throat and into its oral cavity, where the jaws grasp the struggling prey animal and transport it back to the throat and into the oesophagus. This is the first described case of a vertebrate using a second set of jaws to both restrain and transport prey, and is the only alternative to the hydraulic prey transport reported in teleost fishes. The extreme mobility of the moray pharyngeal jaws is made possible by elongation of the muscles that control the jaws, coupled with reduction of adjacent gill-arch structures. The discovery that pharyngeal jaws can reach up from behind the skull to grasp prey in the oral jaws reveals a major innovation that may have contributed to the success of moray eels as apex predators hunting within the complex matrix of coral reefs. This alternative prey transport mode is mechanically similar to the ratcheting mechanisms used in snakes--a group of terrestrial vertebrates that share striking morphological, behavioural and ecological convergence with moray eels.
Synopsis The ability to expand the behavioral repertoire past seemingly rigid morphological featu... more Synopsis The ability to expand the behavioral repertoire past seemingly rigid morphological features enables animals to succeed in a variety of ecological contexts. The integration of morphology, performance, and behavior produces diverse animal feeding strategies. These different strategies reflect trade-offs between specialization, prey choice, and energetic expenditure, which have important consequences for understanding individual and population-level flexibility in response to environmental change. Here we examined the feeding strategies used by the Hawaiian monk seal (Neomonachus schauinslandi), an endangered marine predator. We tested how Hawaiian monk seal feeding strategies change in response to ecological context, specifically prey size and prey location at different depths. Seven captive Hawaiian monk seals were fed five prey types across a continuum of sizes, and prey were presented at three depths to represent surface, pelagic, and benthic feeding. Hawaiian monk seals u...
Animals use diverse feeding strategies to capture and consume prey, with many species switching b... more Animals use diverse feeding strategies to capture and consume prey, with many species switching between strategies to accommodate different prey. Many marine animals exhibit behavioral flexibility when feeding to deal with spatial and temporal heterogeneity in prey resources. However, little is known about flexibility in the feeding behavior of many large marine predators. Here, we documented the feeding behavior and kinematics of the critically endangered Hawaiian monk seal (Neomonachus schauinslandi, n=7) through controlled feeding trials. Seals were fed multiple prey types (e.g., night smelt, capelin, squid, and herring) that varied in size and shape to examine behavioral flexibility in feeding. Hawaiian monk seals primarily used suction feeding (91% of all feeding trials) across all prey types, but biting, specifically pierce feeding, was also observed (9% of all feeding trials). Suction feeding was characterized by shorter temporal events, a smaller maximum gape and gape angle,...
SUMMARY Animal movement and its muscular control are central topics in functional morphology. As ... more SUMMARY Animal movement and its muscular control are central topics in functional morphology. As experimentalists we often manipulate stimuli in a controlled setting or compare species to observe the degree of variation in movement and motor control of particular behaviors. Understanding and communicating the biological significance of these sources of variability requires a universal terminology that is presently lacking in the functional morphology literature. We suggest that `stereotypy' be used to refer to the degree of variability observed in a behavior across trials under a given set of conditions. The ability of an organism to alter its behavior across experimental treatments is referred to as `flexibility'. We discuss how there has been a tendency to confound the phenomenon of a behavior exhibiting low variability, which we refer to as stereotyped, with inflexibility, or the inability to alter the behavior in response to a change in stimulus. The degree of stereotypy and flexibility in a behavior need not be correlated, nor need they have a common underlying basis. Coordination, a term used to describe the relationship between different body parts during movement, can be stereotyped and can show flexibility. Stereotypy of coordination can be assessed by the strength of correlations between movements of two body parts. The influence of coordination coherence on behavioral performance has rarely been considered,and could shed light on how taxa differ in their ability to perform behaviors. We suggest definitions of the terms stereotypy, flexibility and coordination,and provide examples of how and when these terms could be used when discussing behavioral changes in functional morphology.
We examined the effects of variation in swimming speed, or &a... more We examined the effects of variation in swimming speed, or 'ram speed', on the feeding kinematics of juvenile Indo-Pacific tarpon, Megalops cyprinoides. Tarpon were filmed feeding on non-elusive prey at 500 images s(-1). Prey items were offered at one end of the filming tank, the opposite end where tarpon grouped, to encourage them to use a ram strategy to capture their prey. We describe tarpon as ram-suction feeders. Ram speed varied among strikes from 0.19 to 1.38 m/s and each individual produced speeds that spanned at least 0.9 m/s across trials. Although suction distances were much less variable, prey movement towards the predator was present in all feeding trials. There was a strong positive relationship between initial predator - prey distance and ram speed (r(2)=0.72, P<0.001). When tarpon initiated their strike from further away, they achieved higher ram speeds, but also took longer to capture their prey. All other timing variables were unaffected by ram speed whereas at higher ram speeds tarpon exhibited greater expansion of the mouth and buccal cavity. Greater buccal expansion accomplished in the same period of time implies that both the total volume of water captured and the water flow rate entering the mouth was greater in strikes at higher ram speeds. Our results demonstrate how feeding kinematics may vary as a function of ram speed, and how fish predators that lack jaw protrusion and have a large gape capacity can maximize their feeding success by altering their swimming speed.
Trade-offs are believed to impose major constraints on adaptive evolution, and they arise when mo... more Trade-offs are believed to impose major constraints on adaptive evolution, and they arise when modification of a trait improves one aspect of performance but incurs a cost in another. Here we show that performance costs that result from competing demands on one trait can be mitigated by compensatory changes in other traits, so long as performance has a complex basis. Numerical simulations indicate that increases in the number of traits that determine performance decrease the strength of performance trade-offs. In centrarchid fishes, multiple traits underlie suction feeding performance, and experimental data and hydrodynamic modeling show that combinations of traits evolve to increase the ability to feed on attached prey while mitigating costs to performance on evasive prey. Diet data for centrarchid species reveal a weak trade-off between these prey types, corroborating the results based on hydrodynamic modeling and suggesting that complexity in the functional basis of suction feeding performance enhances trophic diversification. Complexity may thus permit the evolution of combinations of high-performance behaviors that appear to violate underlying trade-offs, such as the ability to exert high suction forces with large gape. This phenomenon may promote morphological, functional, and ecological diversification in the face of the myriad selective demands organisms encounter.
SUMMARYWe present an analysis of prey capture functional morphology in eels by comparing two spec... more SUMMARYWe present an analysis of prey capture functional morphology in eels by comparing two species of moray eels, Muraena retifera and Echidna nebulosa (Family Muraenidae), to the American eel Anguilla rostrata (Family Anguillidae). The skulls of both moray species exhibited extreme reductions of several prominent components of the suction-feeding mechanism, including the hyoid bar, the sternohyoideus muscle and the pectoral girdle. Associated with these anatomical modifications, morays showed no evidence of using suction during prey capture. From 59 video sequences of morays feeding on pieces of cut squid we saw no hyoid depression and no movement of prey toward the mouth aperture during the strike, a widely used indicator of suction-induced water flow. This was in contrast to A. rostrata, which exhibited a robust hyoid, sternohyoideus muscle and pectoral girdle, and used suction to draw prey into its mouth. Average prey capture time in morays, about 500 ms, was roughly 10 times longer than in A. rostrata, and morays frequently reversed the direction of jaw and head rotation in the midst of the strike. We tested whether the absence of suction feeding reduces temporal constraints on feeding kinematics, permitting greater variance in traits that characterize timing and the extent of motion in the neurocranium, by comparing moray eel species with A. rostrata,two Centrarchids and a cichlid. Kinematic variance was roughly 5 times higher in morays than the suction-feeding species. Prey capture by suction demands a rapid, highly coordinated series of cranial movements and the loss of this mechanism appears to have permitted slower, more variable prey capture kinematics in morays. The alternative prey capture strategy in morays, biting,may be tied to their success as predators in the confined spaces of reef crevices where they hunt for cephalopods, crustaceans and fish.
Phenotypic convergence is a macroevolutionary pattern that need not be consistent across life his... more Phenotypic convergence is a macroevolutionary pattern that need not be consistent across life history. Ontogenetic transitions in dietary specialization clearly illustrate the dynamics of ecological selection as organisms grow. The extent of phenotypic convergence among taxa that share a similar ecological niche may therefore vary ontogenetically. Because ontogenetic processes have been shown to evolve, phylogenetic comparative methods can be useful in examining how the scaling of traits relates to ecology. Cleaning, a behavior in which taxa consume ectoparasites off clientele, is well represented among wrasses (Labridae). Nearly three-fourths of labrids that clean do so predominately as juveniles, transitioning away as adults. We examine the scaling patterns of 33 labrid species to understand how life-history patterns of cleaning relate to ontogenetic patterns of phenotypic convergence. We find that as juveniles, cleaners exhibit convergence in body and cranial traits that enhance ...
Most bony fishes rely on suction mechanisms to capture and transport prey. Once captured, prey ar... more Most bony fishes rely on suction mechanisms to capture and transport prey. Once captured, prey are carried by water movement inside the oral cavity to a second set of jaws in the throat, the pharyngeal jaws, which manipulate the prey and assist in swallowing. Moray eels display much less effective suction-feeding abilities. Given this reduction in a feeding mechanism that is widespread and highly conserved in aquatic vertebrates, it is not known how moray eels swallow large fish and cephalopods. Here we show that the moray eel (Muraena retifera) overcomes reduced suction capacity by launching raptorial pharyngeal jaws out of its throat and into its oral cavity, where the jaws grasp the struggling prey animal and transport it back to the throat and into the oesophagus. This is the first described case of a vertebrate using a second set of jaws to both restrain and transport prey, and is the only alternative to the hydraulic prey transport reported in teleost fishes. The extreme mobility of the moray pharyngeal jaws is made possible by elongation of the muscles that control the jaws, coupled with reduction of adjacent gill-arch structures. The discovery that pharyngeal jaws can reach up from behind the skull to grasp prey in the oral jaws reveals a major innovation that may have contributed to the success of moray eels as apex predators hunting within the complex matrix of coral reefs. This alternative prey transport mode is mechanically similar to the ratcheting mechanisms used in snakes--a group of terrestrial vertebrates that share striking morphological, behavioural and ecological convergence with moray eels.
Synopsis The ability to expand the behavioral repertoire past seemingly rigid morphological featu... more Synopsis The ability to expand the behavioral repertoire past seemingly rigid morphological features enables animals to succeed in a variety of ecological contexts. The integration of morphology, performance, and behavior produces diverse animal feeding strategies. These different strategies reflect trade-offs between specialization, prey choice, and energetic expenditure, which have important consequences for understanding individual and population-level flexibility in response to environmental change. Here we examined the feeding strategies used by the Hawaiian monk seal (Neomonachus schauinslandi), an endangered marine predator. We tested how Hawaiian monk seal feeding strategies change in response to ecological context, specifically prey size and prey location at different depths. Seven captive Hawaiian monk seals were fed five prey types across a continuum of sizes, and prey were presented at three depths to represent surface, pelagic, and benthic feeding. Hawaiian monk seals u...
Animals use diverse feeding strategies to capture and consume prey, with many species switching b... more Animals use diverse feeding strategies to capture and consume prey, with many species switching between strategies to accommodate different prey. Many marine animals exhibit behavioral flexibility when feeding to deal with spatial and temporal heterogeneity in prey resources. However, little is known about flexibility in the feeding behavior of many large marine predators. Here, we documented the feeding behavior and kinematics of the critically endangered Hawaiian monk seal (Neomonachus schauinslandi, n=7) through controlled feeding trials. Seals were fed multiple prey types (e.g., night smelt, capelin, squid, and herring) that varied in size and shape to examine behavioral flexibility in feeding. Hawaiian monk seals primarily used suction feeding (91% of all feeding trials) across all prey types, but biting, specifically pierce feeding, was also observed (9% of all feeding trials). Suction feeding was characterized by shorter temporal events, a smaller maximum gape and gape angle,...
SUMMARY Animal movement and its muscular control are central topics in functional morphology. As ... more SUMMARY Animal movement and its muscular control are central topics in functional morphology. As experimentalists we often manipulate stimuli in a controlled setting or compare species to observe the degree of variation in movement and motor control of particular behaviors. Understanding and communicating the biological significance of these sources of variability requires a universal terminology that is presently lacking in the functional morphology literature. We suggest that `stereotypy' be used to refer to the degree of variability observed in a behavior across trials under a given set of conditions. The ability of an organism to alter its behavior across experimental treatments is referred to as `flexibility'. We discuss how there has been a tendency to confound the phenomenon of a behavior exhibiting low variability, which we refer to as stereotyped, with inflexibility, or the inability to alter the behavior in response to a change in stimulus. The degree of stereotypy and flexibility in a behavior need not be correlated, nor need they have a common underlying basis. Coordination, a term used to describe the relationship between different body parts during movement, can be stereotyped and can show flexibility. Stereotypy of coordination can be assessed by the strength of correlations between movements of two body parts. The influence of coordination coherence on behavioral performance has rarely been considered,and could shed light on how taxa differ in their ability to perform behaviors. We suggest definitions of the terms stereotypy, flexibility and coordination,and provide examples of how and when these terms could be used when discussing behavioral changes in functional morphology.
We examined the effects of variation in swimming speed, or &a... more We examined the effects of variation in swimming speed, or 'ram speed', on the feeding kinematics of juvenile Indo-Pacific tarpon, Megalops cyprinoides. Tarpon were filmed feeding on non-elusive prey at 500 images s(-1). Prey items were offered at one end of the filming tank, the opposite end where tarpon grouped, to encourage them to use a ram strategy to capture their prey. We describe tarpon as ram-suction feeders. Ram speed varied among strikes from 0.19 to 1.38 m/s and each individual produced speeds that spanned at least 0.9 m/s across trials. Although suction distances were much less variable, prey movement towards the predator was present in all feeding trials. There was a strong positive relationship between initial predator - prey distance and ram speed (r(2)=0.72, P<0.001). When tarpon initiated their strike from further away, they achieved higher ram speeds, but also took longer to capture their prey. All other timing variables were unaffected by ram speed whereas at higher ram speeds tarpon exhibited greater expansion of the mouth and buccal cavity. Greater buccal expansion accomplished in the same period of time implies that both the total volume of water captured and the water flow rate entering the mouth was greater in strikes at higher ram speeds. Our results demonstrate how feeding kinematics may vary as a function of ram speed, and how fish predators that lack jaw protrusion and have a large gape capacity can maximize their feeding success by altering their swimming speed.
Trade-offs are believed to impose major constraints on adaptive evolution, and they arise when mo... more Trade-offs are believed to impose major constraints on adaptive evolution, and they arise when modification of a trait improves one aspect of performance but incurs a cost in another. Here we show that performance costs that result from competing demands on one trait can be mitigated by compensatory changes in other traits, so long as performance has a complex basis. Numerical simulations indicate that increases in the number of traits that determine performance decrease the strength of performance trade-offs. In centrarchid fishes, multiple traits underlie suction feeding performance, and experimental data and hydrodynamic modeling show that combinations of traits evolve to increase the ability to feed on attached prey while mitigating costs to performance on evasive prey. Diet data for centrarchid species reveal a weak trade-off between these prey types, corroborating the results based on hydrodynamic modeling and suggesting that complexity in the functional basis of suction feeding performance enhances trophic diversification. Complexity may thus permit the evolution of combinations of high-performance behaviors that appear to violate underlying trade-offs, such as the ability to exert high suction forces with large gape. This phenomenon may promote morphological, functional, and ecological diversification in the face of the myriad selective demands organisms encounter.
SUMMARYWe present an analysis of prey capture functional morphology in eels by comparing two spec... more SUMMARYWe present an analysis of prey capture functional morphology in eels by comparing two species of moray eels, Muraena retifera and Echidna nebulosa (Family Muraenidae), to the American eel Anguilla rostrata (Family Anguillidae). The skulls of both moray species exhibited extreme reductions of several prominent components of the suction-feeding mechanism, including the hyoid bar, the sternohyoideus muscle and the pectoral girdle. Associated with these anatomical modifications, morays showed no evidence of using suction during prey capture. From 59 video sequences of morays feeding on pieces of cut squid we saw no hyoid depression and no movement of prey toward the mouth aperture during the strike, a widely used indicator of suction-induced water flow. This was in contrast to A. rostrata, which exhibited a robust hyoid, sternohyoideus muscle and pectoral girdle, and used suction to draw prey into its mouth. Average prey capture time in morays, about 500 ms, was roughly 10 times longer than in A. rostrata, and morays frequently reversed the direction of jaw and head rotation in the midst of the strike. We tested whether the absence of suction feeding reduces temporal constraints on feeding kinematics, permitting greater variance in traits that characterize timing and the extent of motion in the neurocranium, by comparing moray eel species with A. rostrata,two Centrarchids and a cichlid. Kinematic variance was roughly 5 times higher in morays than the suction-feeding species. Prey capture by suction demands a rapid, highly coordinated series of cranial movements and the loss of this mechanism appears to have permitted slower, more variable prey capture kinematics in morays. The alternative prey capture strategy in morays, biting,may be tied to their success as predators in the confined spaces of reef crevices where they hunt for cephalopods, crustaceans and fish.
Phenotypic convergence is a macroevolutionary pattern that need not be consistent across life his... more Phenotypic convergence is a macroevolutionary pattern that need not be consistent across life history. Ontogenetic transitions in dietary specialization clearly illustrate the dynamics of ecological selection as organisms grow. The extent of phenotypic convergence among taxa that share a similar ecological niche may therefore vary ontogenetically. Because ontogenetic processes have been shown to evolve, phylogenetic comparative methods can be useful in examining how the scaling of traits relates to ecology. Cleaning, a behavior in which taxa consume ectoparasites off clientele, is well represented among wrasses (Labridae). Nearly three-fourths of labrids that clean do so predominately as juveniles, transitioning away as adults. We examine the scaling patterns of 33 labrid species to understand how life-history patterns of cleaning relate to ontogenetic patterns of phenotypic convergence. We find that as juveniles, cleaners exhibit convergence in body and cranial traits that enhance ...
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