Experience and social environment influence the ability of young brown trout to forage on live novel prey

Efficient feeding is crucial for the growth, survival and reproductive success of most animals. In artificial-rearing environments, however, animals are deprived of many stimuli normally experienced in the wild, which may alter feeding behaviour, and thus influence their survival and reproductive success upon release in nature. In a laboratory experiment, we investigated the effect of hatchery rearing on the ability of brown trout, Salmo trutta, to capture and consume a novel live prey item. Hatchery-reared and wild-caught trout, originating from the same river, were fed single black crickets, either in isolation or in visual and olfactory contact with another hatchery-reared or wild-caught fish. Total consumption, time to first bite and feeding efficiency were monitored. Wild-caught trout ate more, were quicker to attack, and consumed attacked prey more efficiently than hatchery-reared fish. Food consumption and efficiency increased in both wild and hatchery-reared trout during the experiment. We propose that the differences in feeding ability between wild-caught and hatchery-reared brown trout were mainly due to differences in previous experience of feeding on live prey. Wild-caught trout tended to eat more and sooner when in visual contact with another fish than when in isolation. This trend was not seen for the hatchery-reared fish, which may be due to environmental differences between the hatchery and the natural stream. The initial inability of hatchery-reared fish to forage on live prey may reduce their success when released in the wild, especially when in competition with resident wild fish. Copyright 2001 The Association for the Study of Animal Behaviour.     

The effects of perceived competition and parasitism on the foraging behaviour of the upland bully (Eleotridae)

Prey choice by fish is subject to many constraints, some of which may interact to determine the relative preference of fish for prey with different profitabilities. The constraining effects of parasitism and perceived competition on foraging behaviour were examined in the upland bully, Gobiomorphus breviceps . In the laboratory, bullies faced with a choice of prey items of two different sizes chose the larger prey significantly more often than the smaller ones. The presence of a conspecific fish near the source of large prey significantly reduced the bullies'preference for larger prey. Neither the size of the test fish, nor the number of digenean metacercarial cysts they harboured, had any influence on their relative preference for larger prey, or on how that preference was dampened by the presence of a competitor. The threat of competition appears to be a more important constraint on prey choice in upland bullies than parasitism.     

Social learning of prey location in hatchery-reared Atlantic salmon

Naïve, hatchery-reared Atlantic salmon Salmo salar parr were paired with demonstrators that had been pre-trained to accept live prey from the surface or from the benthos. After 6 days of observing demonstrators through a clear perspex partition the naïve fish's benthic foraging skills were tested. The results revealed that hatchery-reared Atlantic salmon can be taught to target benthic prey items by observation alone and social learning protocols can be utilized to dramatically increase benthic foraging success. The results are discussed with reference to refining hatchery-rearing practices with a view to improving the post-release survival of hatchery fishes. The role of learning, and in particular social learning, in the development foraging behaviour is highlighted.     

Prey selection by experienced and naive juvenile Atlantic salmon

Both in foraging groups and in a sequential prey encounter context, learning had a visible effect on the pattern of selection for three live prey types ( Ecdyonurus larvae, Hydropsyche larvae, and Gammarus ) by juvenile Atlantic salmon Salmo salar . Compared to wild-caught fish, naive, hatchery-reared fish that had not been exposed to natural prey ate Hydropsyche larvae in a remarkably low proportion, and consumed a higher proportion of Gammarus. Ecdyonurus experienced a high and rather steady predation rate across the experience gradient, but after a short period of experience with live prey the consumption rate for Hydropsyche increased drastically, and that of Gammarus decreased, matching the selection pattern exhibited by wild fish. Individual fish offered prey in a sequential encounter context increased consumption rates of all the prey types as they gained experience, but the improvement was higher for the prey that were less consumed initially. Fish became more selective as they approached satiation, conforming to the prediction of optimal foraging theory that higher predator's energy requirements, as well as low food availability, result in reduced selectivity. The results also suggest that fish from distinct populations can differ in the degree of diet selectivity according to their energetic requirements for growth. The fast learning response of Atlantic salmon parr towards novel prey probably allows fish to maintain a high foraging efficiency when faced with frequent changes in the availability of different prey types.     

Habitat-related predation on juvenile wild-caught and hatchery-reared red drum Sciaenops ocellatus (Linnaeus)

We examined the patterns of habitat-specific mortality for newly settled red drum (Sciaenops ocellatus) using an experimental mesocosm approach. Experiments were designed to analyze prey vulnerability and fish rearing-type (wild-caught or hatchery-reared) in estuarine habitats of varying structural complexity including marsh (Spartina alterniflora Loisel), oyster reef (Crassostrea virginica Gmelin), seagrass (Halodule wrightii Aschers), and nonvegetated sand bottom. We used two different predators, pinfish (Lagodon rhomboides Linnaeus) and spotted seatrout (Cynoscion nebulosus Cuvier). For both predators, vulnerability of wild-caught red drum was significantly lower in structurally complex habitats such as seagrass and oyster reef; the highest vulnerability was associated with the nonvegetated bottom. This habitat effect was not apparent for hatchery-reared prey. In trials using a combination of both rearing-types, there was no significant habitat effect on prey selection, but hatchery-reared red drum suffered higher overall mortality than wild-caught fish from pinfish predators. In these trials, spotted seatrout did not select for either prey type. Differences we observed in prey vulnerability were likely caused by behavioral differences between wild-caught and hatchery-reared red drum. Our results reinforce the conclusion that structural complexity in estuarine habitats increases survival of newly settled fishes. Our data also suggest that hatchery-reared red drum may be more vulnerable to predation than natural fishes, and that survival of stocked fish may be enhanced through habitat-related behavior modification.     

Role of diet and experience in the development of feeding behaviour in largemouth bass, Micropterus salmoides

Two groups of largemouth bass, Micropterus salmoides , were reared in the laboratory. One group was reared on an artificial, passive diet (frozen brine shrimp) whereas the second was reared on a natural, active diet (cultured zooplankton). Observations on the development of feeding behaviour indicated that the motor patterns and duration (number of weeks in the behavioural repertoire) of the feeding acts did not differ between fry reared on the two diets. While feeding on their respective diets, natural-diet fry performed significantly more orientations and bites, the two major early feeding acts, than did the artificial-diet fry. When tested with live fish prey, fish reared on the natural diet performed fewer orientations and strikes and captured more prey per fry than did the artificial-diet fry. Natural-diet fry had a significantly better net efficiency (captures minus strikes minus orientations) than did artificial-diet fry. Diet, experience, and length (T.L.) of fry affected their predator efficiency significantly. We argue that providing hatchery-reared bass fry with an opportunity to prey on live forage fish once or twice before their release would enhance their survival and eventual recruitment into natural populations.     

Feeding on Profitable and Unprofitable Prey: Comparing Behaviour of Growth-Enhanced Transgenic and Normal Coho Salmon (Oncorhynchus kisutch)

We compared the performance of normal and growth hormone‐transgenic coho salmon feeding on surface drifting edible and inedible novel prey items in various social environments. With an inherently higher appetite, we predicted that transgenic fish would be more willing to feed on novel prey, and that visual company with another fish would enhance this difference further. Transgenic and normal fish, of similar size and age, were equally willing to attack both the edible (live insects) and inedible (artificial angling lure flies) prey, but transgenic fish did so faster and were more likely to make repeated attacks. Transgenic fish managed to seize and consume the edible prey after fewer attacks than did normal fish. However, swallowing of prey took longer than for normal fish. More transgenic individuals interacted with the inedible prey compared with normal salmon, and initially, transgenic fish in visual company with another fish also interacted more with the prey than single transgenic or any constellation of normal focal fish. With repeated exposures, the number of individuals attacking and the number of interactions with the prey decreased. These responses were stronger in transgenic fish, partly explained by the initially low response in normal fish. The observed differences are most likely the consequences of elevated levels of growth hormone in transgenic fish generating enhanced feeding motivation and reinforcement capacity. In a natural environment, the performance of a growth hormone‐transgenic fish may therefore depend on the relative abundance of profitable vs. unprofitable prey, as well as the presence of other transgenic individuals.     

Predator density and competition modify the benefits of group formation in a shoaling reef fish

Synthesis Predation risk experienced by individuals living in groups depends on the balance between predator dilution, competition for refuges, and predator interference or synergy. These interactions operate between prey species as well: the benefits of group living decline in the presence of an alternative prey species. We apply a novel model‐fitting approach to data from field experiments to distinguish among competing hypotheses about shifts in predator foraging behavior across a range of predator and prey densities. Our study provides novel analytical tools for analyzing predator foraging behavior and offers insight into the processes driving the dynamics of coral reef fish. Studies of predator foraging behavior typically focus on single prey species and fixed predator densities, ignoring the potential importance of complexities such as predator dilution; predator‐mediated effects of alternative prey; heterospecific competition; or predator–predator interactions. Neglecting the effects of prey density is particularly problematic for prey species that live in mixed species groups, where the beneficial effects of predator dilution may swamp the negative effects of heterospecific competition. Here we use field experiments to investigate how the mortality rates of a shoaling coral reef fish (a wrasse: Thalassoma amblycephalum), change as a result of variation in: 1) conspecific density, 2) density of a predator (a hawkfish: Paracirrhites arcatus), and 3) presence of an alternative prey species that competes for space (a damselfish: Pomacentrus pavo). We quantify changes in prey mortality rates from the predator's perspective, examining the effects of added predators or a second prey species on the predator's functional response. Our analysis highlights a model‐fitting approach that discriminates amongst multiple hypotheses about predator foraging in a community context. Wrasse mortality decreased with increasing conspecific density (i.e. mortality was inversely density‐dependent). The addition of a second predator doubled prey mortality rates, without significantly changing attack rate or handling time – i.e. there was no evidence for predator interference. The presence of a second prey species increased wrasse mortality by 95%; we attribute this increase either to short‐term apparent competition (predator aggregation) or to a decrease in handling time of the predator (e.g. through decreased wrasse vigilance). In this system, 1) prey benefit from intraspecific group living though a reduced predation risk, and 2) the benefit of group living is reduced in the presence of an alternative prey species.     

Differences in Lateral Line Morphology between Hatchery- and Wild-Origin Steelhead

Despite identification of multiple factors mediating salmon survival, significant disparities in survival-to-adulthood among hatchery- versus wild-origin juveniles persist. In the present report, we explore the hypothesis that hatchery-reared juveniles might exhibit morphological defects in vulnerable mechanosensory systems prior to release from the hatchery, potentiating reduced survival after release. Juvenile steelhead (Oncorhynchus mykiss) from two different hatcheries were compared to wild-origin juveniles on several morphological traits including lateral line structure, otolith composition (a proxy for auditory function), and brain weight. Wild juveniles were found to possess significantly more superficial lateral line neuromasts than hatchery-reared juveniles, although the number of hair cells within individual neuromasts was not significantly different across groups. Wild juveniles were also found to possess primarily normal, aragonite-containing otoliths, while hatchery-reared juveniles possessed a high proportion of crystallized (vaterite) otoliths. Finally, wild juveniles were found to have significantly larger brains than hatchery-reared juveniles. These differences together predict reduced sensitivity to biologically important hydrodynamic and acoustic signals from natural biotic (predator, prey, conspecific) and abiotic (turbulent flow, current) sources among hatchery-reared steelhead, in turn predicting reduced survival fitness after release. Physiological and behavioral studies are required to establish the functional significance of these morphological differences.     

Bitterling as models for studies of sperm competition

The plight of the world fish stocks is all too well documented. As part of an ongoing attempt to bolster fish stocks for both commercial and conservation purposes, many fish are reared in captivity and released into the wild. It is well known that hatchery‐reared fish have low post‐release survival compared with wild fish of similar age. Part of the reason for this high mortality is that hatchery fish show deficits in virtually all aspects of their behaviour, including prey selection and predator avoidance. Much behaviour requires repeated experience so that it may become fine‐tuned to prevailing circumstances via learning during development. It has been suggested that inappropriate behaviour is encouraged when fish are reared in the unnatural surroundings of the hatchery. However, hatchery fish can be taught to recognise live, novel prey items and predators and the rate of learning is increased in the presence of a more knowledgeable conspecifics. Here we present data showing how social learning protocols can be used to dramatically increase foraging success in juvenile Atlantic salmon. We also outline related aspects of our ongoing research and discuss some of the possibilities for altering hatchery practices to maximize post‐release survival.     

The role of social learning in conservation and fisheries reintroductions

The plight of the world fish stocks is all too well documented. As part of an ongoing attempt to bolster fish stocks for both commercial and conservation purposes, many fish are reared in captivity and released into the wild. It is well known that hatchery‐reared fish have low post‐release survival compared with wild fish of similar age. Part of the reason for this high mortality is that hatchery fish show deficits in virtually all aspects of their behaviour, including prey selection and predator avoidance. Much behaviour requires repeated experience so that it may become fine‐tuned to prevailing circumstances via learning during development. It has been suggested that inappropriate behaviour is encouraged when fish are reared in the unnatural surroundings of the hatchery. However, hatchery fish can be taught to recognise live, novel prey items and predators and the rate of learning is increased in the presence of a more knowledgeable conspecifics. Here we present data showing how social learning protocols can be used to dramatically increase foraging success in juvenile Atlantic salmon. We also outline related aspects of our ongoing research and discuss some of the possibilities for altering hatchery practices to maximize post‐release survival.     

Predator-induced diapause in Daphnia magna may require two chemical cues

The production of diapausing eggs by Daphnia magna stimulated by fish exudates can be explained as an anti-predator defence ensuring genome protection in periods of high risk from fish predation. The combined effects on the induction of D. magna diapause of an “alarm” chemical originating from injured conspecific prey and fish kairomones were tested. The results of the experiment showed that the cues when present together promote both the production of ephippial eggs and male formation, indicating their role in the synchronization of the entire mode of Daphnia sexual reproduction. Ephippial eggs were only produced in the presence of both fish kairomone and conspecific alarm chemicals, while male offspring occurred in the treatments where both, one or none of the cues were present. However, production of males was the highest when both cues were provided. D. magna responded similarly to the tested cues whether or not the hypothetical alarm substance associated with predator odour came from Daphnia specimens actually eaten by fish or from crushed conspecific individuals. However, chemicals from crushed chironomid larvae combined with fish kairomones did not induce a similar response in D. magna. The relative advantage of utilization of alarm cues or predator kairomones in the induction of defence responses in prey organisms is discussed. Received: 8 June 1998 / Accepted: 11 January 1999     

Interactions between adult and larval bluegill sunfish: positive and negative effects

Adult fish may affect the growth and survival of conspecific larvae through a variety of pathways, including negative interactions via competition for shared limiting resources or via predation (i.e., cannibalism), and positive interactions due to the consumption of larval predators and via resource enhancement (i.e., presence of adults increases availability of larval prey). To examine the overall effect of adult bluegill sunfish (Lepomis macrochirus) on larval bluegill, we conducted a field experiment in which we manipulated adult densities and quantified larval growth and survival, prey abundance, invertebrate predator abundance, and cannibalism. The presence of adult bluegill had a negative effect on final larval mass. This response was consistent with competition for zooplankton prey. Adult bluegill reduced the abundance of large zooplankton (e.g., Chaoborus and Daphnia), which were the dominant prey of bluegill larvae in the absence of adults. Larvae in the no-adult treatment also had significantly more prey in their stomachs compared to larvae in the presence of adults. Larval survival was maximized at intermediate adult densities and the overall production of larvae peaked at intermediate adult densities. The higher larval survival at intermediate adult densities is attributed to a reduction in invertebrate predators in treatments with adult bluegill; invertebrate predators experienced an 80% reduction in the presence of adult fish. Decreased larval survival at the highest adult density was not due to resource limitation and may be due to cannibalism, which was not directly observed in our study, but has been observed in other studies.     

Socializing makes thick-skinned individuals: on the density of epidermal alarm substance cells in cyprinid fish, the crucian carp (Carassius carassius)

In cyprinid fish, density of epidermal club cells (i.e. alarm substance cells) has been found to vary between lakes with different predator fauna. Because predators can be labelled with chemical cues from prey, we questioned if club cell density could be controlled indirectly by predators releasing prey cues. In particular, we suspected a possible feedback mechanism between chemical alarm signals and their cellular source. We raised crucian carp singly and in groups of four. For both rearing types, fish were exposed to skin extracts of either conspecifics or brown trout (without club cells), and provided either low or high food rations. Independent of rearing type, condition factor and club cell density increased with food ration size, but no change was found in club cell density following exposure to conspecific alarm signals. However, the density of club cells was found significantly higher for fish raised in groups than for fish raised alone. We conclude that an increased condition factor results in more club cells, but crucian carp may also possess an awareness of conspecific presence, given by higher club cell densities when raised in groups. This increase in club cell density may be induced by unknown chemical factors released by conspecifics.     

Environmental enrichment and prior experience of live prey improve foraging behaviour in hatchery‐reared Atlantic salmon

Atlantic salmon salmo salar L. parr were reared for 3 months under standard hatchery conditions or in a structurally enriched tank (containing plants, rocks and novel objects). Half of each of these fish had prior exposure to live prey in the form of live bloodworm while the other half were fed hatchery‐pellets. After 12 days all fish were tested on a novel live prey item (brine shrimp). A significant interaction between the two factors (prior exposure to live prey and rearing condition) revealed that foraging performance was only enhanced in fish that had been reared in a complex environment and exposed to live prey. It appears that the ability to generalize from one live prey type to another is only enhanced in fish that had been reared in an enriched environment. The findings support the assertion that the provision of enriched environments in combination with exposure to live prey prior to release may significantly improve the post‐release survival rates of hatchery‐reared fishes. As both the environmental enrichment and the prior foraging experience procedures were comparatively simple, the provision of such pre‐release experiences are likely to prove cost effective to hatcheries.     

How does the presence of a conspecific individual change the behavioral game that a predator plays with its prey?

Behavioral games predators play among themselves may have profound effects on behavioral games predators play with their prey. We studied the behavioral game between predators and prey within the framework of social foraging among predators. We tested how conspecific interactions among predators (little egret) change the predator–prey behavioral game and foraging success. To do so, we examined foraging behavior of egrets alone and in pairs (male and female) in a specially designed aviary consisting of three equally spaced pools with identical initial prey (comet goldfish) densities. Each pool was comprised of a risky microhabitat, rich with food, and a safe microhabitat with no food, forcing the fish to trade off food and safety. When faced with two versus one egret, we found that fish significantly reduced activity in the risky habitat. Egrets in pairs suffered reduced foraging success (negative intraspecific density dependence) and responded to fish behavior and to their conspecific by changing their visiting regime at the different pools—having shorter, more frequent visits. The time egret spent on each visit allowed them to match their long-term capture success rate across the environment to their capture success rate in the pool, which satisfies one aspect of optimality. Overall, egrets in pairs allocated more time for foraging and changed their foraging tactics to focus more on fish under cover and fish ‘peeping’ out from their shelter. These results suggest that both prey and predator show behavioral flexibility and can adjust to changing conditions as needed in this foraging game.     

Female predatory response to conspecific males and heterospecific prey in the praying mantis <Emphasis Type="Italic">Mantis religiosa</Emphasis>: evidence for discrimination of conspecific males

Sexual cannibalism, the attack and consumption of the opposite sex by a conspecific during courtship, copulation, or soon after copulation, is widespread among invertebrates, but the causes of this behavior are not fully understood. We examine the mistaken identity hypothesis, which posits that non-copulatory cannibalism occurs because females do not recognize conspecific males as potential mates. This hypothesis predicts indiscriminate predatory behavior by females towards conspecific males and heterospecific prey. This prediction remains largely unexamined. We tested this prediction in the praying mantis Mantis religiosa (Mantodea: Mantidae) through two behavioral experiments. In experiment 1, we presented targets in isolation to females: dead conspecific males or dead common prey items from the field (grasshopper Chrysochraon dispar). In experiment 2, we presented simultaneous live targets to females: conspecific males and grasshoppers. In both experiments, we varied female mating status (virgin vs. mated). Results indicate some degree of attack discrimination by the females. In experiment 1, the females were significantly more likely to strike at the grasshoppers, and showed a shorter latency to strike at grasshoppers. In experiment 2, females tended to preferentially strike at the grasshoppers, although this result fell short of statistical significance. Female discrimination between the males and grasshoppers may be explained, in part, by the size difference between the males and grasshoppers. Female mating status did not affect the occurrence or latency to strike in either experiment. These results fail to strongly support the prediction of indiscriminate predatory behavior by females, while contributing to a broader taxonomic assessment of the mistaken identity hypothesis.     

Costs and benefits of freezing behaviour in the harvestman Eumesosoma roeweri (Arachnida, Opiliones)

Animals present an enormous variety of behavioural defensive mechanisms, which increase their survival, but often at a cost. Several animal taxa reduce their chances of being detected and/or recognized as prey items by freezing (remaining completely motionless) in the presence of a predator. We studied costs and benefits of freezing in immature Eumesosoma roeweri (Opiliones, Sclerosomatidae). Preliminary observations showed that these individuals often freeze in the presence of the syntopic predatory spider Schizocosa ocreata (Araneae, Lycosidae). We verified that harvestmen paired with predators spent more time freezing than when alone or when paired with a conspecific. Then, we determined that predator chemical cues alone did not elicit freezing behaviour. Next, we examined predator behaviour towards moving/non-moving prey and found that spiders attacked moving prey significantly more, suggesting an advantage of freezing in the presence of a predator. Finally, as measure of the foraging costs of freezing, we found that individuals paired with a predator for 2 h gained significantly less weight than individuals paired with a conspecific or left alone. Taken together, our results suggest that freezing may protect E. roeweri harvestmen from predatory attacks by wolf spiders, but at the cost of reduced food and/or water intake.     

Interactive effects of predation risk and conspecific density on the nutrient stoichiometry of prey

The mere presence of predators (i.e., predation risk) can alter consumer physiology by restricting food intake and inducing stress, which can ultimately affect prey‐mediated ecosystem processes such as nutrient cycling. However, many environmental factors, including conspecific density, can mediate the perception of risk by prey. Prey conspecific density has been defined as a fundamental feature that modulates perceived risk. In this study, we tested the effects of predation risk on prey nutrient stoichiometry (body and excretion). Using a constant predation risk, we also tested the effects of varying conspecific densities on prey responses to predation risk. To answer these questions, we conducted a mesocosm experiment using caged predators (Belostoma sp.), and small bullfrog tadpoles (Lithobates catesbeianus) as prey. We found that L. catesbeianus tadpoles adjust their body nutrient stoichiometry in response to predation risk, which is affected by conspecific density. We also found that the prey exhibited strong morphological responses to predation risk (i.e., an increase in tail muscle mass), which were positively correlated to body nitrogen content. Thus, we pose the notion that in risky situations, adaptive phenotypic responses rather than behavioral ones might partially explain why prey might have a higher nitrogen content under predation risk. In addition, the interactive roles of conspecific density and predation risk, which might result in reduced perceived risk and physiological restrictions in prey, also affected how prey stoichiometry responded to the fear of predation.     

鳜鱼视觉特性及其对捕食习性适应的研究III．视觉对猎物运动和形状的反应

作者采用行为学方法测定了伏击型凶猛鱼类鳜鱼视觉对猎物运动和形状特征的反应特性.鳜鱼对3种不同体形饵料鱼有最强的跟踪反应和攻击反应,对虾则有较强的跟踪反应而几乎没有攻击反应,对蜻蜒幼虫仅有不强的跟踪反应而完全没有攻击反应.它对低速(v≤5cm/s)一连续和等间歇不连续运动的饵料鱼有较强的跟踪反应和攻击反应,对中速和高速(v≥10cm/s)连续运动的饵料鱼有最强的跟踪反应而几乎没有或完全没有攻击反应,对中速和高速等间歇不连续运动的饵料鱼则有最强的跟踪反应和最强的攻击反应.它对不连续运动的a、b、c、d、e、f6种形状均有跟踪反应,但近距离跟踪反应的强度与形状特征有关系,对不连续运动的b、c、d3种形状完全没有攻击反应,而对不连续运动的a、e、f3种形状则有依次增强的攻击反应.鳜鱼视觉可对猎物运动进行远距离的识别,并决定其对猎物的远距离跟踪反应.且其视觉仅能对猎物的大致形状进行近距离识别,并决定其对猎物的近距离跟踪反应和攻击反应.