Passive bristling of mako shark scales in reversing flows.

Shark skin has been shown to reduce drag in turbulent boundary layer flows, but the flow control mechanisms by which it does so are not well understood. Drag reduction has generally been attributed to static effects of scale surface morphology, but possible drag reduction effects of passive or active scale actuation, or 'bristling', have been recognized more recently. Here, we provide the first direct documentation of passive scale bristling due to reversing, turbulent boundary layer flows. We recorded and analysed high-speed videos of flow over the skin of a shortfin mako shark, Isurus oxyrinchus These videos revealed rapid scale bristling events with mean durations of approximately 2 ms. Passive bristling occurred under flow conditions representative of cruise swimming speeds and was associated with two flow features. The first was a downward backflow that pushed a scale-up from below. The second was a vortex just upstream of the scale that created a negative pressure region, which pulled up a scale without requiring backflow. Both flow conditions initiated bristling at lower velocities than those required for a straight backflow. These results provide further support for the role of shark scale bristling in drag reduction.

Biomechanics of the jaw of the durophagous bonnethead shark.

Durophagy in chondrichthyan fishes is thought to entail a set of morphological characteristics, such as hypertrophied adductor muscles, molariform teeth, and high bite forces. However, these characteristics are not common to all durophagous chondrichthyans. In some durophagous chondrichthyans, the jaws are better suited biomechanically to resist bending in the area where prey is processed. Resistance to bending is in part, quantified by second moment of area (I), which uses the neutral axis of an object to analyze the arrangement of material. This study investigated whether the lower jaw of the bonnethead shark, Sphyrna tiburo, is more resistant to bending under the crushing/molariform teeth compared to the grasping teeth. Using computerized tomography (CT) scanning, the jaws of ten bonnethead sharks were visualized, then digitally resliced at identical positions along the jaw for all specimens. I increased along the lower jaw from anterior to posterior as the teeth transform from grasping to crushing, with the largest absolute increase occurring about the transition from grasping to crushing teeth. When the lower jaw is compared to that of a rod of similar cross-sectional area, the shape exceeds that of a rod by 1.6 to 5.7 times, meaning the shape of the jaw is better suited to resist bending than if the same size jaw was shaped as a solid rod. These results suggest the lower jaw of S. tiburo is adapted to resist bending more under the molariform teeth where crushing occurs than at the anterior grasping teeth.

Modulation of shark prey capture kinematics in response to sensory deprivation.

The ability of predators to modulate prey capture in response to the size, location, and behavior of prey is critical to successful feeding on a variety of prey types. Modulating in response to changes in sensory information may be critical to successful foraging in a variety of environments. Three shark species with different feeding morphologies and behaviors were filmed using high-speed videography while capturing live prey: the ram-feeding blacktip shark, the ram-biting bonnethead, and the suction-feeding nurse shark. Sharks were examined intact and after sensory information was blocked (olfaction, vision, mechanoreception, and electroreception, alone and in combination), to elucidate the contribution of the senses to the kinematics of prey capture. In response to sensory deprivation, the blacktip shark demonstrated the greatest amount of modulation, followed by the nurse shark. In the absence of olfaction, blacktip sharks open the jaws slowly, suggestive of less motivation. Without lateral line cues, blacktip sharks capture prey from greater horizontal angles using increased ram. When visual cues are absent, blacktip sharks elevate the head earlier and to a greater degree, allowing them to overcome imprecise position of the prey relative to the mouth, and capture prey using decreased ram, while suction remains unchanged. When visual cues are absent, nurse sharks open the mouth wider, extend the labial cartilages further, and increase suction while simultaneously decreasing ram. Unlike some bony fish, neither species switches feeding modalities (i.e. from ram to suction or vice versa). Bonnetheads failed to open the mouth when electrosensory cues were blocked, but otherwise little to no modulation was found in this species. These results suggest that prey capture may be less plastic in elasmobranchs than in bony fishes, possibly due to anatomical differences, and that the ability to modulate feeding kinematics in response to available sensory information varies by species, rather than by feeding modality.

Androgen receptors in the bonnethead, Sphyrna tiburo: cDNA cloning and tissue-specific expression in the male reproductive tract.

As demonstrated in past studies, androgens appear to play critical roles in regulating reproduction in male sharks. However, little is known about the cell-specific actions of androgens in these fishes. To address this, this study examined androgen targets in reproductive organs of a seasonally reproducing shark, the bonnethead (Sphyrna tiburo). A partial bonnethead AR cDNA clone was isolated and found to exhibit strong homology with known vertebrate ARs. Using RT-PCR and in situ hybridization, AR was found to be expressed in multiple cell types in the male bonnethead testis (premeiotic germ cells, Leydig-like interstitial cells, Sertoli cells, peritubular myoid cells, and mature spermatozoa) and gonadal ducts (stromal cells, luminal epithelial cells, mature spermatozoa). Furthermore, AR expression in these organs was found to vary temporally in relation to the seasonal reproductive cycle. Based on immunocytochemistry, the presence of AR protein in male bonnethead reproductive organs was largely consistent with patterns of AR gene expression with the single exception of mature spermatozoa, which exhibited consistently strong mRNA expression but only inconsistent and weak AR protein immunoreactivity. These results suggest important roles for androgens in regulating germ cell proliferation, hormone production, spermatid elongation, spermiation, and gonadal duct function in male bonnetheads. In addition, high abundance of AR mRNA in bonnethead spermatozoa suggest the potential for de novo protein synthesis following spermiation/copulation and/or a role for AR mRNA in early embryonic development, both of which have been proposed to explain the occurrence of mRNA transcripts in spermatozoa from various vertebrates.

Feeding biomechanics of the cownose ray, Rhinoptera bonasus, over ontogeny.

Growth affects the performance of structure, so the pattern of growth must influence the role of a structure and an organism. Because animal performance is linked to morphological specialization, ontogenetic change in size may influence an organism's biological role. High bite force generation is presumably selected for in durophagous taxa. Therefore, these animals provide an excellent study system for investigating biomechanical consequences of growth on performance. An ontogenetic series of 27 cownose rays (Rhinoptera bonasus) were dissected in order to develop a biomechanical model of the feeding mechanism, which was then compared with bite forces measured from live rays. Mechanical advantage of the feeding apparatus was generally conserved throughout ontogeny, while an increase in the mass and cross-sectional area of the jaw adductors resulted in allometric gains in bite force generation. Of primary importance to forceful biting in this taxon is the use of a fibrocartilaginous tendon associated with the insertion of the primary jaw adductor division. This tendon may serve to redirect muscle forces anteriorly, transmitting them within the plane of biting. Measured bite forces obtained through electrostimulation of the jaw adductors in live rays were higher than predicted, possibly due to differences in specific tension of actual batoid muscle and that used in the model. Mass-specific bite forces in these rays are the highest recorded for elasmobranchs. Cownose rays exemplify a species that, through allometric growth of bite performance and morphological novelties, have expanded their ecological performance over ontogeny.

Feeding performance of king Mackerel, Scomberomorus cavalla.

Feeding performance is an organism's ability to capture and handle prey. Although bite force is a commonly used metric of feeding performance, other factors such as bite pressure and strike speed are also likely to affect prey capture. Therefore, this study investigated static bite force, dynamic speeds, and predator and prey forces resulting from ram strikes, as well as bite pressure of the king mackerel, Scomberomorus cavalla, in order to examine their relative contributions to overall feeding performance. Theoretical posterior bite force ranged from 14.0-318.7 N. Ram speed, recorded with a rod and reel incorporated with a line counter and video camera, ranged from 3.3-15.8B L/s. Impact forces on the prey ranged from 0.1-1.9 N. Bite pressure, estimated using theoretical bite forces at three gape angles and tooth cross-sectional areas, ranged from 1.7-56.9 MPa. Mass-specific bite force for king mackerel is relatively low in comparison with other bony fishes and sharks, with relatively little impact force applied to the prey during the strike. This suggests that king mackerel rely on high velocity chases and high bite pressure generated via sharp, laterally compressed teeth to maximize feeding performance.

Constructional morphology within the head of hammerhead sharks (sphyrnidae).

The study of functional trade-offs is important if a structure, such as the cranium, serves multiple biological roles, and is, therefore, shaped by multiple selective pressures. The sphyrnid cephalofoil presents an excellent model for investigating potential trade-offs among sensory, neural, and feeding structures. In this study, hammerhead shark species were chosen to represent differences in head form through phylogeny. A combination of surface-based geometric morphometrics, computed tomography (CT) volumetric analysis, and phylogenetic analyses were utilized to investigate potential trade-offs within the head. Hammerhead sharks display a diversity of cranial morphologies where the position of the eyes and nares vary among species, with only minor changes in shape, position, and volume of the feeding apparatus through phylogeny. The basal winghead shark, Eusphyra blochii, has small anteriorly positioned eyes. Through phylogeny, the relative size and position of the eyes change, such that derived species have larger, more medially positioned eyes. The lateral position of the external nares is highly variable, showing no phylogenetic trend. Mouth size and position are conserved, remaining relatively unchanged. Volumetric CT analyses reveal no trade-offs between the feeding apparatus and the remaining cranial structures. The few trade-offs were isolated to the nasal capsule volume's inverse correlation with braincase, chondrocranial, and total cephalofoil volume. Eye volume also decreased as cephalofoil width increased. These data indicate that despite considerable changes in head shape, much of the head is morphologically conserved through sphyrnid phylogeny, particularly the jaw cartilages and their associated feeding muscles, with shape change and morphological trade-offs being primarily confined to the lateral wings of the cephalofoil and their associated sensory structures.

Feeding in billfishes: inferring the role of the rostrum from a biomechanical standpoint.

Perhaps the most striking feature of billfishes is the extreme elongation of the premaxillary bones forming their rostra. Surprisingly, the exact role of this structure in feeding is still controversial. The goal of this study is to investigate the use of the rostrum from a functional, biomechanical and morphological standpoint to ultimately infer its possible role during feeding. Using beam theory, experimental and theoretical loading tests were performed on the rostra from two morphologically different billfish, the blue marlin (Makaira nigricans) and the swordfish (Xiphias gladius). Two loading regimes were applied (dorsoventral and lateral) to simulate possible striking behaviors. Histological samples and material properties of the rostra were obtained along their lengths to further characterize structure and mechanical performance. Intraspecific results show similar stress distributions for most regions of the rostra, suggesting that this structure may be designed to withstand continuous loadings with no particular region of stress concentration. Although material stiffness increased distally, flexural stiffness increased proximally owing to higher second moment of area. The blue marlin rostrum was stiffer and resisted considerably higher loads for both loading planes compared with that of the swordfish. However, when a continuous load along the rostrum was considered, simulating the rostrum swinging through the water, swordfish exhibited lower stress and drag during lateral loading. Our combined results suggest that the swordfish rostrum is suited for lateral swiping to incapacitate their prey, whereas the blue marlin rostrum is better suited to strike prey from a wider variety of directions.

Prey capture kinematics in batoids using different prey types: investigating the role of the cephalic lobes.

Cephalic lobes are novel structures found in some myliobatid stingrays. While undulatory batoids utilize the pectoral fins for prey capture and locomotion, lobed species partition locomotion to the pectoral fins, utilizing the lobes exclusively for prey capture. We investigated the use of the anterior pectoral fins and cephalic lobes in prey capture in five batoid species. The purpose of this study was to investigate the: (1) prey capture kinematics and use of the cephalic lobes in lobed and lobeless batoids; (2) role of the cephalic lobes in modulating capture behavior based on prey type. It was hypothesized that lobed species would display unique capture behaviors resulting in faster and more successful capture of prey, and display greater modulation in capture behavior. Findings showed that lobed species used only the head region for capture, were faster at pouncing and tenting, but slower at mouth opening. The cephalic lobes were more movable than the anterior pectoral fins of lobeless species. Modulation occurred in all species. Elusive prey increased tent duration for the lobeless species, increased mouth opening duration in the lobed Aetobatus narinari, and were farther away from the mouth than non-elusive prey during biting for all species. All species had few prey escapes. Overall, species with cephalic lobes captured prey faster but did not display increased modulatory ability or feeding success. The cephalic lobes help localize prey capture to the head region, speeding up the prey capture event and maintaining an efficient capture rate despite having less flexible pectoral fins.

Movable shark scales act as a passive dynamic micro-roughness to control flow separation.

Shark scales on fast-swimming sharks have been shown to be movable to angles in excess of 50°, and we hypothesize that this characteristic gives this shark skin a preferred flow direction. During the onset of separation, flow reversal is initiated close to the surface. However, the movable scales would be actuated by the reversed flow thereby causing a greater resistance to any further flow reversal and this mechanism would disrupt the process leading to eventual flow separation. Here we report for the first time experimental evidence of the separation control capability of real shark skin through water tunnel testing. Using skin samples from a shortfin mako Isurus oxyrinchus, we tested a pectoral fin and flank skin attached to a NACA 4412 hydrofoil and separation control was observed in the presence of movable shark scales under certain conditions in both cases. We hypothesize that the scales provide a passive, flow-actuated mechanism acting as a dynamic micro-roughness to control flow separation.

Multisensory integration and behavioral plasticity in sharks from different ecological niches.

The underwater sensory world and the sensory systems of aquatic animals have become better understood in recent decades, but typically have been studied one sense at a time. A comprehensive analysis of multisensory interactions during complex behavioral tasks has remained a subject of discussion without experimental evidence. We set out to generate a general model of multisensory information extraction by aquatic animals. For our model we chose to analyze the hierarchical, integrative, and sometimes alternate use of various sensory systems during the feeding sequence in three species of sharks that differ in sensory anatomy and behavioral ecology. By blocking senses in different combinations, we show that when some of their normal sensory cues were unavailable, sharks were often still capable of successfully detecting, tracking and capturing prey by switching to alternate sensory modalities. While there were significant species differences, odor was generally the first signal detected, leading to upstream swimming and wake tracking. Closer to the prey, as more sensory cues became available, the preferred sensory modalities varied among species, with vision, hydrodynamic imaging, electroreception, and touch being important for orienting to, striking at, and capturing the prey. Experimental deprivation of senses showed how sharks exploit the many signals that comprise their sensory world, each sense coming into play as they provide more accurate information during the behavioral sequence of hunting. The results may be applicable to aquatic hunting in general and, with appropriate modification, to other types of animal behavior.

The morphology of the cephalic lobes and anterior pectoral fins in six species of batoids.

Many benthic batoids utilize their pectoral fins for both undulatory locomotion and feeding. Certain derived, pelagic species of batoids possess cephalic lobes, which evolved from the anterior pectoral fins. These species utilize the pectoral fins for oscillatory locomotion while the cephalic lobes are used for feeding. The goal of this article was to compare the morphology of the cephalic lobes and anterior pectoral fins in species that possess and lack cephalic lobes. The skeletal elements (radials) of the cephalic lobes more closely resembled the radials in the pectoral fin of undulatory species. Second moment of area (I), calculated from cephalic lobe radial cross sections, and the number of joints revealed greater flexibility and resistance to bending in multiple directions as compared to pectoral fin radials of oscillatory species. The cephalic lobe musculature was more complex than the anterior pectoral fin musculature, with an additional muscle on the dorsal side, with fiber angles running obliquely to the radials. In Rhinoptera bonasus, a muscle presumably used to help elevate the cephalic lobes is described. Electrosensory pores were found on the cephalic lobes (except Mobula japonica) and anterior pectoral fins of undulatory swimmers, but absent from the anterior pectoral fins of oscillatory swimmers. Pore distributions were fairly uniform except in R. bonasus, which had higher pore numbers at the edges of the cephalic lobes. Overall, the cephalic lobes are unique in their anatomy but are more similar to the anterior pectoral fins of undulatory swimmers, having more flexibility and maneuverability compared to pectoral fins of oscillatory swimmers. The maneuverable cephalic lobes taking on the role of feeding may have allowed the switch to oscillatory locomotion and hence, a more pelagic lifestyle.

Feeding biomechanics and theoretical calculations of bite force in bull sharks (Carcharhinus leucas) during ontogeny.

Evaluations of bite force, either measured directly or calculated theoretically, have been used to investigate the maximum feeding performance of a wide variety of vertebrates. However, bite force studies of fishes have focused primarily on small species due to the intractable nature of large apex predators. More massive muscles can generate higher forces and many of these fishes attain immense sizes; it is unclear how much of their biting performance is driven purely by dramatic ontogenetic increases in body size versus size-specific selection for enhanced feeding performance. In this study, we investigated biting performance and feeding biomechanics of immature and mature individuals from an ontogenetic series of an apex predator, the bull shark, Carcharhinus leucas (73-285cm total length). Theoretical bite force ranged from 36 to 2128N at the most anterior bite point, and 170 to 5914N at the most posterior bite point over the ontogenetic series. Scaling patterns differed among the two age groups investigated; immature bull shark bite force scaled with positive allometry, whereas adult bite force scaled isometrically. When the bite force of C. leucas was compared to those of 12 other cartilaginous fishes, bull sharks presented the highest mass-specific bite force, greater than that of the white shark or the great hammerhead shark. A phylogenetic independent contrast analysis of anatomical and dietary variables as determinants of bite force in these 13 species indicated that the evolution of large adult bite forces in cartilaginous fishes is linked predominantly to the evolution of large body size. Multiple regressions based on mass-specific standardized contrasts suggest that the evolution of high bite forces in Chondrichthyes is further correlated with hypertrophication of the jaw adductors, increased leverage for anterior biting, and widening of the head. Lastly, we discuss the ecological significance of positive allometry in bite force as a possible "performance gain" early in the life history of C. leucas.

Largemouth bass (Micropterus salmoides) switch feeding modalities in response to sensory deprivation.

Animals use a suite of sensory modalities to precisely locate and capture prey. While numerous studies have examined the effects of sensory deprivation on the behaviors leading to prey capture and while it is generally believed that information in the pre-strike period determines the way fish capture prey, this study is the first to examine the contribution of sensory information to jaw kinematics during capture. Largemouth bass were filmed using high-speed videography while capturing live mosquitofish. Bass were examined intact, with visual deprivation under infrared light, and with lateral line deprivation following treatment with cobalt chloride. Deprived of visual cues, this visual ram-feeding predator switches towards suction-based feeding to successfully capture prey. They approach prey slowly but open their mouths more rapidly, which has been shown to result in greater buccal pressure, causing their prey to move a greater distance at a more rapid velocity as they are being drawn into the predators' mouths. Deprived of lateral line cues, bass have higher forward velocities during capture and capture prey earlier in the gape cycle. This study demonstrates that sensory pre-strike information directly affects the capture modality employed by fishes and that fish can modulate between ram and suction not only by adjusting the amount of ram by increasing or decreasing their movements, but also by actively increasing the amount of suction used. These results suggest that the ability to modulate feeding behavior may allow animals to not only exploit a broader breadth of prey items, but also to be capable of doing so in a wider variety of environments.

Biology meets engineering: the structural mechanics of fossil and extant shark teeth.

The majority of studies on the evolution and function of feeding in sharks have focused primarily on the movement of cranial components and muscle function, with little integration of tooth properties or function. As teeth are subjected to sometimes extreme loads during feeding, they undergo stress, strain, and potential failure. As attributes related to structural strength such as material properties and overall shape may be subjected to natural selection, both prey processing ability and structural parameters must be considered to understand the evolution of shark teeth. In this study, finite element analysis was used to visualize stress distributions of fossil and extant shark teeth during puncture, unidirectional draw (cutting), and holding. Under the loading and boundary conditions here, which are consistent with bite forces of large sharks, shark teeth are structurally strong. Teeth loaded in puncture have localized stress concentrations at the cusp apex that diminish rapidly away from the apex. When loaded in draw and holding, the majority of the teeth show stress concentrations consistent with well designed cantilever beams. Notches result in stress concentration during draw and may serve as a weak point; however they are functionally important for cutting prey during lateral head shaking behavior. As shark teeth are replaced regularly, it is proposed that the frequency of tooth replacement in sharks is driven by tooth wear, not tooth failure. As the tooth tip and cutting edges are worn, the surface areas of these features increase, decreasing the amount of stress produced by the tooth. While this wear will not affect the general structural strength of the tooth, tooth replacement may also serve to keep ahead of damage caused by fatigue that may lead to eventual tooth failure.

Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico.

The feeding anatomy, behavior and diet of the whale shark Rhincodon typus were studied off Cabo Catoche, Yucatan Peninsula, Mexico. The filtering apparatus is composed of 20 unique filtering pads that completely occlude the pharyngeal cavity. A reticulated mesh lies on the proximal surface of the pads, with openings averaging 1.2mm in diameter. Superficial to this, a series of primary and secondary cartilaginous vanes support the pads and direct the water across the primary gill filaments. During surface ram filter feeding, sharks swam at an average velocity of 1.1m/s with 85% of the open mouth below the water's surface. Sharks on average spent approximately 7.5h/day feeding at the surface on dense plankton dominated by sergestids, calanoid copepods, chaetognaths and fish larvae. Based on calculated flow speed and underwater mouth area, it was estimated that a whale shark of 443 cm total length (TL) filters 326 m(3)/h, and a 622 cm TL shark 614 m(3)/h. With an average plankton biomass of 4.5 g/m(3) at the feeding site, the two sizes of sharks on average would ingest 1467 and 2763 g of plankton per hour, and their daily ration would be approximately 14,931 and 28,121 kJ, respectively. These values are consistent with independently derived feeding rations of captive, growing whale sharks in an aquarium. A feeding mechanism utilizing cross-flow filtration of plankton is described, allowing the sharks to ingest plankton that is smaller than the mesh while reducing clogging of the filtering apparatus.

Young's modulus and hardness of shark tooth biomaterials.

To date, the majority of studies on feeding mechanics in sharks have focused on the movement of cranial components and muscle function, with little attention to tooth properties or function. Attributes related to mechanical properties, such as structural strength, may also be subjected to natural selection. Additionally it is necessary to characterize these properties in order to construct biomechanical models of tooth function. The goal of this study was to determine hardness and elastic modulus for the shark tooth materials enameloid, osteodentine, and orthodentine. Five teeth each from one carcharhiniform species, the bonnethead Sphyrna tiburo, and one lamniform, the sand tiger shark Carcharias taurus, were utilized for nanoindentation testing. Each tooth was sectioned transversely, air-dried, and polished. Both enameloid and dentine were tested on each tooth via a Berkovich diamond tip, with nine 2 microm deep indentations per material. t-Tests were used to determine if there were differences in hardness and Young's modulus between the tooth materials of the two species. There was no significant difference between the two species for the material properties of enameloid, however both hardness and Young's modulus were higher for osteodentine than for orthodentine. This may be due to differences in microanatomy and chemical composition, however this needs to be studied in greater detail.

Bite force and performance in the durophagous bonnethead shark, Sphyrna tiburo.

Bite force, a measure of performance, can be used to link anatomical form and function. Earlier studies have shown bite force to have a significant influence on dietary constraints and ontogenetic shifts in resource utilization. The bonnethead shark, Sphyrna tiburo, is a durophagous member of the family Sphyrnidae. Its diet in South Florida waters consists almost entirely of blue crabs, which are crushed or ingested whole. This abundant coastal predator's feeding mechanism is specialized for the consumption of hard prey, including a modified biting pattern and molariform teeth. The goals of this research were to (1) characterize the mechanical function of the feeding mechanism of S. tiburo through biomechanical modeling of biting and in vivo bite force measurements; (2) compare the bite force of S. tiburo with those of other fishes; and (3) identify functional constraints on prey capture by comparing the bite force of S. tiburo with the fracture properties of its primary prey item, blue crabs. Maximum theoretical bite force ranged from 25.7 N anteriorly to 107.9 N posteriorly. S. tiburo has the second lowest mass specific bite force for any fish studied to date, and its posterior mechanical advantage of 0.88 is lower than other durophagous chondrichthyans, indicating that this independent evolutionary acquisition of durophagy was not accompanied by the associated morphological changes found in other durophagous cartilaginous fishes. Blue crab fracture forces (30.0-490.0 N) range well above the maximum bite force of S. tiburo, suggesting that prey material properties functionally constrain dietary ecology to some degree.

Functional morphology of the feeding apparatus, feeding constraints, and suction performance in the nurse shark Ginglymostoma cirratum.

The nurse shark, Ginglymostoma cirratum, is an obligate suction feeder that preys on benthic invertebrates and fish. Its cranial morphology exhibits a suite of structural and functional modifications that facilitate this mode of prey capture. During suction-feeding, subambient pressure is generated by the ventral expansion of the hyoid apparatus and the floor of its buccopharyngeal cavity. As in suction-feeding bony fishes, the nurse shark exhibits expansive, compressive, and recovery kinematic phases that produce posterior-directed water flow through the buccopharyngeal cavity. However, there is generally neither a preparatory phase nor cranial elevation. Suction is generated by the rapid depression of the buccopharyngeal floor by the coracoarcualis, coracohyoideus, and coracobranchiales muscles. Because the hyoid arch of G. cirratum is loosely connected to the mandible, contraction of the rectus cervicis muscle group can greatly depress the floor of the buccopharyngeal cavity below the depressed mandible, resulting in large volumetric expansion. Suction pressures in the nurse shark vary greatly, but include the greatest subambient pressures reported for an aquatic-feeding vertebrate. Maximum suction pressure does not appear to be related to shark size, but is correlated with the rate of buccopharyngeal expansion. As in suction-feeding bony fishes, suction in the nurse shark is only effective within approximately 3 cm in front of the mouth. The foraging behavior of this shark is most likely constrained to ambushing or stalking due to the exponential decay of effective suction in front of the mouth. Prey capture may be facilitated by foraging within reef confines and close to the substrate, which can enhance the effective suction distance, or by foraging at night when it can more closely approach prey.

Relative importance of growth and behaviour to elasmobranch suction-feeding performance over early ontogeny.

Development of the ability to capture prey is crucial to predator survival. Trends in food-capture performance over early ontogeny were quantified for leopard sharks Triakis semifasciata and whitespotted bamboosharks Chiloscyllium plagiosum by measuring suction pressure and flow in front of the mouth during feeding. At any size, C. plagiosum produce greater subambient pressure and ingest more rounded water parcels. Maximum subambient pressure scaled with negative allometry in T. semifasciata and was accompanied by an increase in the time to reach maximum gape. Despite a similar trend in buccal expansion timing, maximum pressure in C. plagiosum scaled with isometry and was accompanied by an earlier onset of hyoid depression and a positive allometric increase in buccal reserve volume. Growth was the primary factor responsible for developmental trends in both species, with size-independent behavioural changes contributing little to overall performance variability. Ontogenetic dietary shifts are predicted for both species as a consequence of size-dependent changes in performance. Chiloscyllium plagiosum becomes anatomically and behaviourally canalized towards suction feeding, limiting the effective range of prey capture and possibly necessitating stalking. Triakis semifasciata, by contrast, retains the flexibility to employ both ram and suction and therefore captures more elusive prey with age.