Scaling of suction feeding performance in the catfish Clarias gariepinus

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

The dynamics of prey choice in fish: the importance of prey size and satiation

Over a number of decades the process of prey choice has been investigated using fishes as model predators. Using fishes for the model has allowed the proximate factors that determine how a mobile predator finds and chooses to eat the prey encountered within a variable 3‐D environment to be estimated. During prey choice a number of constraints exist, in particular most fish predators will eat their prey whole thus their jaws and gut create functional limitations once a prey has been attacked. By considering the relationship between the size of the prey and the predator's feeding apparatus and feeding motivation this study explores the link between mechanistic studies and theoretical, optimal foraging based predictions. How the prediction of prey choices made by the fish following prey encounter can be reconciled with what is likely to be found in the fish's stomach is discussed. This study uses a progression of empirical examples to illustrate how the limits of functional constraints and prey choice at different stages of motivation to feed can be taken into account to improve predictions of predator prey choice.     

Implications of the feeding current structure of Euchaeta rimana, a carnivorous pelagic copepod, on the spatial orientation of their prey

Many marine planktonic organisms create water currents to entrainand capture food items. Rheotactic prey entrained within thesefeeding currents often exibit escape reactions. If the directionof escape is away from the feeding current, the prey may successfullydeter predation. If the escape is towards the center of thefeeding current, the prey will be re-entrained towards its predatorand remain at risk of predation. The direction of escape isdependent on (i) the ability of the prey to escape in a directiondifferent than its pre-escape orientation and (ii) the orientationcaused by the interaction of the prey's body with the movingfluid. In this study, the change in orientation of Acartia hudsonicanauplii as a result of entrainment within the feeding currentof Euchaeta rimana, a planktonic predatory copepod, was examined,When escaping in still water, A.hudsonica nauplii were ableto vary their pre-escape direction by only 10. This allowsonly a limited ability to escape in a direction different thantheir pre-escape orientation. Analyses of the feeding currentof E.rimana show the flow speed to be most rapid in the centralregion with an exponential decrease in speed distally. In contrast,flow vorticity is minimal in the center of the feeding currentand maximal at 1.75 mm along the antennae. As a result, thedegree of rotation of the prey towards the center of the feedingcurrent shows a strong dependency on the prey's location withinthe feeding current. The feeding current of E.rimana rotatedthe prey 14 when near the center of the flow field and up to160 when located more distal in the feeding current Since theprey's escape abilities cannot compensate for the rotation dueto the flow, this mechanism will maintain the escaping preywithin the feeding current of their predator. Therefore, thefeeding current facilitates predatory copepods in capturingprey by (i) increasing the amount of water which passes overtheir sensors and through their feeding appendages and (ii)controlling the spatial orientation of their prey prior to escape.     

Suction feeding mechanics, performance, and diversity in fishes

Despite almost 50 years of research on the functional morphologyand biomechanics of suction feeding, no consensus has emergedon how to characterize suction-feeding performance, or its morphologicalbasis. We argue that this lack of unity in the literature isdue to an unusually indirect and complex linkage between themuscle contractions that power suction feeding, the skeletalmovements that underlie buccal expansion, the sharp drop inbuccal suction pressure that occurs during expansion, the flowof water that enters the mouth to eliminate the pressure gradient,and the forces that are ultimately exerted on the prey by thisflow. This complexity has led various researchers to focus individuallyon suction pressure, flow velocity, or the distance the preymoves as metrics of suction-feeding performance. We attemptto integrate a mechanistic view of the ability of fish to performthese components of suction feeding. We first discuss a modelthat successfully relates aspects of cranial morphology to thecapacity to generate suction pressure in the buccal cavity.This model is a particularly valuable tool for studying theevolution of the feeding mechanism. Second, we illustrate themultidimensional nature of suction-feeding performance in acomparison of bluegill, Lepomis macrochirus, and largemouthbass, Micropterus salmoides, two species that represent oppositeends of the spectrum of performance in suction feeding. As anticipated,bluegills had greater accuracy, lower peak flux into the mouth,and higher flow velocity and acceleration of flow than did bass.While the differences between species in accuracy of strikeand peak water flux were substantial, peak suction velocityand acceleration were only about 50% higher in bluegill, a relativelymodest difference. However, a hydrodynamic model of the forcesthat suction feeders exert on their prey shows that this differencein velocity is amplified by a positive effect of the smallermouth aperture of bluegill on force exerted on the prey. Ourmodel indicates that the pressure gradient in front of a fishthat is feeding by suction, associated with the gradient inwater velocity, results in a force on the prey that is largerthan drag or acceleration reaction. A smaller mouth apertureresults in a steeper pressure gradient that exerts a greaterforce on the prey, even when other features of the suction floware held constant. Our work shows that some aspects of suction-feedingperformance can be determined from morphology, but that thecomplexity of the behavior requires a diversity of perspectivesto be used in order to adequately characterize performance.     

Surface tension prey transport in shorebirds: how widespread is it?

Surface tension prey transport is a feeding mechanism employing the surface tension of water surrounding prey to transport prey from bill tip to mouth. Previously, it has been demonstrated only in the Red-necked Phalarope Phalaropus lobatus. On the basis of a model of the bill morphology necessary for this method of prey transport, I suggest that many species of shorebird should be capable of surface tension feeding. Laboratory investigations of the feeding mechanics of Wilson's Phalarope Phalaropus tricolor , Western Sandpiper Calidris mauri and Least Sandpiper Calidris minutilla demonstrated that all three use surface tension transport of prey when feeding in water. I examined interspecific variation in the performance of this feeding mechanism with a high-speed video system and a customized motion analysis system. Exploratory analyses indicated significant interspecific variation in distance the prey is transported per cycle of mandibular spreading, gape increase per unit transport, speed of transport, total number of cycles necessary to complete transport and total time to complete transport. The calidrid sandpipers also occasionally used other feeding mechanisms in conjunction with surface tension transport of prey. The discovery that these sandpipers, which normally obtain prey by probing, are capable of surface tension transport of prey implies that the capacity to employ this feeding mechanism may be widespread in the Scolopacidae and may have been a significant factor in the evolutionary radiation of phalaropes into aquatic environments.     

A discrete, stochastic model for microbial filter feeding: a model for feeding of ciliated protists on spatially uniform, nondepletable suspensions

Suspension-feeding ciliates, either bacteriovorous or planktonic, are adapted to feed on particulate food matter of size much smaller than their own size. These microorganisms collect their prey by generating water currents that draw prey toward their capture surfaces. Under such conditions food particles are treated in bulk, and captures of individual food particles from a suspension by individual single-celled organisms are discrete events that occur at random intervals of time. Each such event is followed by a sequence of additional events that also occur at random intervals of time. This sequence culminates in the incorporation of the digestible portion of the food particle into the cell's cytoplasm and the expulsion of the indigestible portion from the cell. In theory, the rate of the overall ingestion-digestion process can be limited by the passage of particles through any stage of this sequence of events. In this paper, we assume that only the initial events in the sequence, those that occur in the oral region of the cell, limit the rate of the ingestion-digestion process, and we develop a discrete, stochastic model of filter feeding based on that assumption. We use the model to show how advanced instrumentation, such as flow cytometry, can be used to measure parameters of the model and also to answer a number of important questions about the mechanism of filter feeding. We show also how the model can be applied to nonhomogeneous cell populations for which parameters of the model are distributed.     

How tetrapods feed in water: a functional analysis by paradigm

Mechanical theory is used to erect a paradigm predicting the manipulations used by carnivorous aquatic amphibians, reptiles, birds and mammals to catch, subdue, process and swallow their prey. These predictions are confirmed by observational evidence. Most aquatic predatory tetrapods use long, prehensile tooth-armed jaws as pincer jaws to snap shut onto the prey and catch and kill it, although some use the flexibility of long necks in spear fishing and some odontocetes may stun prey with sonar. Most do not have cutting or nipping dentitions as these cannot be used on prey which is freely floating. They use caniniform dentition to hold and kill prey, or in some cases crushing dentition to break open hard-shelled prey. They dismember prey by dynamic loading, snatching bites so quickly that the prey tears. They use shake feeding, shaking the prey apart from side to side above the water. If the prey is too large to lift above the water they use twist feeding, twisting pieces off. Small pieces are easily swallowed but larger pieces are held above the water and swallowed by tilting the head back in gravity feeding, or by jerking the head back and forth in incrtial feeding. Some animals use mobile jaws to pull prey back into the mouth in ratchet feeding. Filter feeding evades these problems by feeding on very small prey. The use of paradigms in functional analysis is discussed with special reference to this work. The paradigm method is shown to be the most suitable one. There has been repeated convergent and parallel evolution of adaptations to feed in water.     

The fine structure and function of the tentacle in Tokophrya infusionum

The feeding apparatus of Suctoria consists of long, thin, stiff tubes called tentacles. When a swimming prey attaches to the tip of the tentacle a number of events follow in rapid succession. The tentacle broadens, a stream of tiny granules starts to move upward at its periphery to the tip, the prey becomes immobilized and shortly thereafter the cytoplasm of the still living prey begins to flow through the center of the tentacle to the body of the predator. An electron microscope study of the tentacle in Tokophrya infusionum, a protozoan of the subclass Suctoria, has disclosed a number of structural details which help to clarify some of the mechanisms involved in this unusual way of feeding. Each tentacle is composed of two concentric tubes. The lumen of the inner tube is surrounded by 49 tubular fibrils most probably of contractile nature. In the inner tube the cytoplasm of the prey is present during feeding, and in the outer tube are small dense bodies. It was found that the dense bodies originate in the cytoplasm of Tokophrya. They have an elongate, missile-like appearance, pointed at one end, rounded at the other, and are composed of several distinct segments. At the tip of the tentacle they penetrate the plasma membrane, with their pointed ends sticking out. It is assumed that the missile-like bodies play a major role in the feeding process. Their composite structure suggests that they might contain a number of enzymes which most probably are responsible for the various events preceding the actual food intake.     

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.     

Feeding currents facilitate a mixotrophic way of life

Mixotrophy is common, if not dominant, among eukaryotic flagellates, and these organisms have to both acquire inorganic nutrients and capture particulate food. Diffusion limitation favors small cell size for nutrient acquisition, whereas large cell size facilitates prey interception because of viscosity, and hence intermediately sized mixotrophic dinoflagellates are simultaneously constrained by diffusion and viscosity. Advection may help relax both constraints. We use high-speed video microscopy to describe prey interception and capture, and micro particle image velocimetry (micro-PIV) to quantify the flow fields produced by free-swimming dinoflagellates. We provide the first complete flow fields of free-swimming interception feeders, and demonstrate the use of feeding currents. These are directed toward the prey capture area, the position varying between the seven dinoflagellate species studied, and we argue that this efficiently allows the grazer to approach small-sized prey despite viscosity. Measured flow fields predict the magnitude of observed clearance rates. The fluid deformation created by swimming dinoflagellates may be detected by evasive prey, but the magnitude of flow deformation in the feeding current varies widely between species and depends on the position of the transverse flagellum. We also use the near-cell flow fields to calculate nutrient transport to swimming cells and find that feeding currents may enhance nutrient uptake by ≈75% compared with that by diffusion alone. We argue that all phagotrophic microorganisms must have developed adaptations to counter viscosity in order to allow prey interception, and conclude that the flow fields created by the beating flagella in dinoflagellates are key to the success of these mixotrophic organisms.     

Potential impact of size-selective planktivory on phosphorus release by zooplankton

A laboratory model of phosphorus release by Daphnia rosea was implemented for published zooplankton data from lakes characterized by different abundances of size-selective planktivores. Size-selective feeding reduces average prey size and increases P release per unit biomass. At the system level, decreased prey standing crop associated with higher planktivore abundance could balance the size dependent increase in P release rate. However, estimates of both net reduction and net increase in rate of P release from zooplankton resulted from model application. Size-selective feeding might be important not only in energetic or evolutionary relationships between predator and prey but also in determination of the relative importance of different pathways of phosphorus flow through pelagic systems.     

Stomach fullness modulates prey size choice in the frillfin goby,Bathygobius soporator

Behaviours related to foraging and feeding in predator–prey systems are fundamental to our understanding of food webs. From the perspective of a predator, the selection of prey size depends upon a number of factors including prey vulnerability, prey size, and the predator's motivation to eat. Thus, feeding motivation and prey visual cues are supposed to influence predator decisions and it is predicted that prey selection by visual cues is modulated by the predator's stomach fullness prior to attacking a prey. This study was conducted using an animal model from the rocky shores ecosystem, a predatory fish, the frillfin goby Bathygobius soporator, and a benthic prey, the mottled shore crab Pachygrapsus transversus. Our results demonstrate that frillfin gobies are capable of visually evaluating prey size and that the size evaluation process is modulated by the level of stomach fullness. Predators with an empty stomach (0% fullness) attacked prey that was larger than the predicted optimal size. Partially satiated predators (50% stomach fullness) selected prey close to the optimal size, while fully satiated predators (100% stomach fullness) showed no preference for size. This finding indicates an integrative response of the predator that depends on the input of both internal and external sensory information when choosing prey. Predator perceptions of visual cues (prey size) and stomach fullness modulate foraging decisions. As a result, a flexible feeding behaviour emerges, evidencing a clearly adaptive response in line with optimal foraging theory predictions.     

Superfluous killing in spiders: a consequence of adaptation to food-limited environments?

The hypothesis that superfluous killing, partial consumption,and abandonment of prey is a consequence of adaptation to food-limited environments was tested in two feeding trials on a desert spider, Agelenopsis aperta. First, we made comparisons among populations inhabiting sites of high prey (HP) or low prey (LP) availabilitythat differed in their degree of genetic isolation. Typically,A. aperta entirely consumed one or two of the prey items itcaptured in a feeding bout. Additional prey were partiallyconsumed or abandoned without eating. Spiders from the geneticallyisolated HP population, however, captured fewer prey and showeda higher incidence of full feeding on prey than did individualsfrom the other populations. Only one spider from this populationcaptured a prey item that it failed to feed on, whereas spidersfrom LP populations failed to feed on high numbers of capturedprey. The greatest variability in feeding behavior was exhibitedin the HP population that experienced gene flow. The secondtest was based on the finding that aggressiveness is largelya sex-linked trait in A. aperta: the aggressiveness of thefemale parent only is inherited by male offspring, whereasboth parents contribute to this trait in female offspring.All female F₁ hybrids between LP and HP parental types exhibitedhigh levels of superfluous killing, as did male F₁ hybridsderived from LP females. F₁ hybrid males derived from HP femalesexhibited extremely low levels of superfluous killing. Superfluouskilling thus has its basis in the genetic control of levelsof aggression.     

Quantification of flow during suction feeding in bluegill sunfish

Nearly all aquatic-feeding vertebrates use some amount of suction to capture prey items. Suction prey capture occurs by accelerating a volume of water into the mouth and taking a prey item along with it. Yet, until recently, we lacked the necessary techniques and analytical tools to quantify the flow regime generated by feeding fish. We used a new approach; Digital Particle Image Velocimetery (DPIV) to measure several attributes of the flow generated by feeding bluegill sunfish. We found that the temporal pattern of flow was notably compressed during prey capture. Flow velocity increased rapidly to its peak within 20 ms of the onset of the strike, and this peak corresponded to the time that the prey entered the mouth during capture. The rapid acceleration and deceleration of water suggests that timing is critical for the predator in positioning itself relative to the prey so that it can be drawn into the mouth along with the water. We also found that the volume of water affected by suction was spatially limited. Only rarely did we measure significant flow beyond 1.75 cm of the mouth aperture (in 20 cm fish), further emphasizing the importance of mechanisms, like locomotion, that place the fish mouth in close proximity to the prey. We found that the highest flows towards the mouth along the fish midline were generated not immediately in front of the open mouth, but approximately 0.5 cm anterior to the mouth opening. Away from the midline the peak in flow was closer to the mouth. We propose that this pattern indicates the presence of a bow wave created by the locomotor efforts of the fish. In this scheme, the bow wave acts antagonistically to the flow of water generated by suction, the net effect being to push the region of peak flow away from the open mouth. The peak was located farther from the mouth opening in strikes accompanied by faster locomotion, suggesting faster fish created larger bow waves.     

Eating without hands or tongue: specialization, elaboration and the evolution of prey processing mechanisms in cartilaginous fishes

The ability to separate edible from inedible portions of prey is integral to feeding. However, this is typically overlooked in favour of prey capture as a driving force in the evolution of vertebrate feeding mechanisms. In processing prey, cartilaginous fishes appear handicapped because they lack the pharyngeal jaws of most bony fishes and the muscular tongue and forelimbs of most tetrapods. We argue that the elaborate cranial muscles of some cartilaginous fishes allow complex prey processing in addition to their usual roles in prey capture. The ability to manipulate prey has evolved twice along different mechanical pathways. Batoid chondrichthyans (rays and relatives) use elaborate lower jaw muscles to process armored benthic prey, separating out energetically useless material. In contrast, megacarnivorous carcharhiniform and lamniform sharks use a diversity of upper jaw muscles to control the jaws while gouging, allowing for reduction of prey much larger than the gape. We suggest experimental methods to test these hypotheses empirically.     

Chew,shake, and tear: Prey processing in Australian sea lions (Neophoca cinerea)

Pinnipeds generally target relatively small prey that can be swallowed whole, yet often include larger prey in their diet. To eat large prey, they must first process it into pieces small enough to swallow. In this study we explored the range of prey‐processing behaviors used by Australian sea lions (Neophoca cinerea) when presented with large prey during captive feeding trials. The most common methods were chewing using the teeth, shaking prey at the surface, and tearing prey held between the teeth and forelimbs. Although pinnipeds do not masticate their food, we found that sea lions used chewing to create weak points in large prey to aid further processing and to prepare secured pieces of prey for swallowing. Shake feeding matches the processing behaviors observed in fur seals, but use of forelimbs for “hold and tear” feeding has not been previously reported for other otariids. When performing this processing method, prey was torn by being stretched between the teeth and forelimbs, where it was secured by being squeezed between the palms of their flippers. These results show that Australian sea lions use a broad repertoire of behaviors for prey processing, which matches the wide range of prey species in their diet.     

Consequences of sexual selection on feeding in male jumping spiders (Araneae: Salticidae)

The chelicerae of male Myrmarachne plataleoides , a salticid spider from Sri Lanka, are about five times the length of those of conspecific females. Intrasexual selection is thought to account for this structural dimorphism. The elongation of the male's chelicerae has resulted in morphological and behavioural differences in the feeding process of males and females. Males, unlike females, lack a fang duct and cannot envenom prey. During feeding, males use their fangs to skewer prey. The prey's contents are extracted from the holes in its cuticle where the spider's fangs protrude through the prey near the spider's mouth.     

Functional groups in piscivorous fishes

Piscivory is a key ecological function in aquatic ecosystems, mediating energy flow within trophic networks. However, our understanding of the nature of piscivory is limited; we currently lack an empirical assessment of the dynamics of prey capture and how this differs between piscivores. We therefore conducted aquarium‐based performance experiments, to test the feeding abilities of 19 piscivorous fish species. We quantified their feeding morphology, striking, capturing, and processing behavior. We identify two major functional groups: grabbers and engulfers. Grabbers are characterized by horizontal, long‐distance strikes, capturing their prey tailfirst and subsequently processing their prey using their oral jaw teeth. Engulfers strike from short distances, from high angles above or below their prey, engulfing their prey and swallowing their prey whole. Based on a meta‐analysis of 2,209 published in situ predator–prey relationships in marine and freshwater aquatic environments, we show resource partitioning between grabbers and engulfers. Our results provide a functional classification for piscivorous fishes delineating patterns, which transcend habitats, that may help explain size structures in fish communities.     

The effect of spatial heterogeneity on the persistence of predator-prey interactions

The effect of spatially discontinuous environments on predator-prey systems is examined by using a computer simulation model. It is shown that increasing prey dispersal and decreasing predator dispersal do not necessarily have a stabilizing influence on the interaction, as had been concluded by previous workers. The stability of predator-prey interaction depends on the interaction of the dispersal process with normal reproduction and feeding of the predator and prey species.     

Unexpected effects of prey dimensions and morphologies on the size selective feeding by two bacterivorous flagellates (Ochromonas sp. and Spumella sp.)

Current models on protistan size-selective feeding assume that contact probability is the factor that largely explains observed food preferences. Contact probability is generally expected to be positively correlated with prey size and therefore to explain observed food selection for larger prey items. We critically tested these basic assumptions on size-selective feeding using the interception-feeding chrysomonad nanoflagellates Ochromonas sp. and Spumella sp. Mechanisms of differential feeding were studied during distinct stages of the selection process (i.e. contact probability, capture efficiency, ingestion efficiency, and differential digestion) by means of high-resolution video microscopy. Food selection was investigated using a mixture of microspheres ranging from 0.3-2.2 microm in diam., as well as a mixed bacterial community. In contrast to current model assumptions, the contact probability was highest for microspheres of intermediate size (0.9-1.2 microm), but was not generally positively correlated with prey size over the whole prey size range. Capture and ingestion also proved to be involved in size selection: these patterns were also independent of the food concentration (p = 0.968 for Ochromonas, p = 0.971 for Spumella). Even though the capture rate was significantly higher for attached flagellates than for swimming flagellates (p < 0.001), size selectivity was not affected (p > 0.05). Our results indicate that: (i) size selection is not actively regulated by these flagellates, but is a passive process; (ii) contact probability is not generally positively correlated with prey size, but shows a maximum for intermediate-sized prey in the prey size spectrum of 0.3-2.2 microm; and (iii) selection steps other than contact probability are crucial for size selection and should be integrated in models on size selection.