Asset protection in juvenile salmon: how adding biological realism changes a dynamic foraging model

The "asset-protection principle" created by Clark is based ona dynamic programming model and states that individuals should(1) become more averse to predation risk as they accumulatefitness assets but (2) generally be more willing to acceptpredation risk later in the foraging season. To test whetherthese predictions hold under biologically meaningful foraging parameters, I constructed a dynamic model of the optimal trade-offbetween foraging and predator avoidance in juvenile salmon.The model incorporates temperature and body-size dependentbio-energetic constraints typical for juvenile fish, whichgrow by orders of magnitude over a season. In its simplestform using seasonally constant growth potential and a linear over-winter survival function, my results equal those of Clark'smodel. Adding a fitness function and environmental data fromfield studies accentuates the asset-protection effect and fundamentallychanges the seasonal pattern of optimal effort. Simulationof typical poor feeding conditions in mid-summer yields theprediction of increased foraging in the spring in anticipationof worsening conditions. Increasing overall predation riskresults in smaller fish at the end of the season with a trade-offbetween summer and winter survival. The model generates testablepredictions for juvenile salmon and provides insights for otherorganisms (particularly poikilotherms) that are subject tosize-dependent or seasonally changing foraging dynamics.     

Vertical Position Reflects Increased Feeding Motivation in Growth Hormone Transgenic Coho Salmon (Oncorhynchus kisutch)

Growth hormone (GH) gene transgenesis has allowed the production of salmon with an inherently increased growth potential, on average two to threefold higher compared with daily specific growth rates observed in normal, non‐transgenic fish. This difference quickly results in animals of very different sizes at age, and is associated with specific morphological effects and enhanced appetites in transgenic animals. However, less is known of the feeding and antipredator behaviour of GH‐transgenic fish, information that can help with predictions of potential ecological consequences of release or escape of transgenic fish into the wild. In a series of experiments, transgenic (T) and normal (N) coho salmon of varying age and size (from 0.5 to 40 g, 3.5–21 mo) were studied singly, in pairs, and in groups during feeding and simulated predation threat. Vertical position generally did not differ between T and N fry, but at larger size (>4 g) T fish remained closer to the surface than N fish both during feeding and predatory attacks, probably as a consequence of inherent differences in feeding motivation and later reinforcement by associative learning. This difference in vertical position was not the result of competition as it remained even after either fish in the pair had been removed. In nature, where predators may attack from above (birds) or below (fish), this kind of behaviour may translate into higher risk of predation, which could increase mortality and lower the fitness of transgenic fish, unless their increased growth rate can compensate for the increased risk‐taking.     

Predation risk and resource abundance mediate foraging behaviour and intraspecific resource partitioning among consumers in dominance hierarchies

Dominance hierarchies and the resulting unequal resource partitioning among individuals are key mechanisms of population regulation. The strength of dominance hierarchies can be influenced by size‐dependent tradeoffs between foraging and predator avoidance whereby competitively inferior subdominants can access a larger proportion of limiting resources by accepting higher predation risk. Foraging‐predation risk tradeoffs also depend on resource abundance. Yet, few studies have manipulated predation risk and resource abundance simultaneously; consequently, their joint effect on resource partitioning within dominance hierarchies are not well understood. We addressed this gap by measuring behavioural responses of masu salmon Oncorhynchus masou ishikawae to experimental manipulations of predation risk and resource abundance in a natural temperate forest stream. Responses to predation risk depended on body size and social status such that larger fish (often social dominants) exhibited more risk‐averse behaviour (e.g. lower foraging and appearance rates) than smaller subdominants after exposure to a simulated predator. The magnitude of this effect was lower when resources were elevated, indicating that dominant fish accepted a higher predation risk to forage on abundant resources. However, the influence of resource abundance did not extend to the population level, where predation risk altered the distribution of foraging attempts (a proxy for energy intake) from being skewed towards large individuals to being skewed towards small individuals after predator exposure. Our results imply that size‐dependent foraging–predation risk tradeoffs can weaken the strength of dominance hierarchies by allowing competitively inferior subdominants to access resources that would otherwise be monopolized.     

Structural complexity and fish body size interactively affect habitat optimality

Predator–prey interactions are strongly influenced by habitat structure, particularly in coastal marine habitats such as seagrasses in which structural complexity (SC) may vary over small spatial scales. For seagrass mesopredators such as juvenile fishes, optimality models predict that fitness will be maximized at levels of SC that enhance foraging but minimize predation risk, both of which are functions of body size. We tested the hypothesis that in eelgrass (Zostera marina) habitat, optimal SC for juvenile giant kelpfish (Heterostichus rostratus), an abundant eelgrass mesopredator in southern California, changes through ontogeny. To do this, we quantified eelgrass SC effects on habitat associations, relative predation risk, and foraging efficiency for three size classes of juvenile giant kelpfish. We found that habitat selection differed with fish size: small fish selected dense eelgrass, whereas larger fish selected sparse eelgrass. Small kelpfish experienced the lowest relative predation risk in dense eelgrass but also had higher foraging efficiency in dense eelgrass, suggesting that dense eelgrass is selected by these fish because it minimizes risk and maximizes potential for growth. Surprisingly, larger kelpfish did not experience lower predation risk than small kelpfish. However, larger kelpfish experienced higher foraging efficiency in sparse eelgrass vs. dense eelgrass, suggesting that they select sparse eelgrass to maximize foraging efficiency. Our study highlights that trade-offs between predation risk and foraging can occur within a single habitat type, that studies should consider how habitat value changes through ontogeny, and that seagrass habitat value may be maximal when within-patch variability in SC is high.     

Growth history and intrinsic factors influence risk assessment at a critical life transition for a fish

Making the appropriate decision in the face of predation risk dictates the fate of prey, and predation risk is highest at life history boundaries such as settlement. At the end of the larval phase, most coral reef fishes enter patches of reef containing novel predators. Since vision is often obscured in the complex surroundings, chemical information released from damaged conspecific is used to forewarn prey of an active predator. However, larvae enter the reef environment with their own feeding and growth histories, which will influence their motivation to feed and take risks. The present study explored the link between recent growth, feeding history, current performance and behavioural risk taking in newly settling stages of a coral reef damselfish (Pomacentrus amboinensis). Older and larger juveniles in good body condition had a stronger response to chemical alarm cues of injured conspecifics; these fish spent a longer time in shelter and displayed a more dramatic decrease in foraging behaviour than fish in lower body condition. Feeding experiments supported these findings and emphasized the importance of body condition in affecting risk assessment. Evidently, larval growth history and body condition influences the likelihood of taking risks under the threat of predation immediately after settlement, thereby affecting the probability of survival in P. amboinensis.     

Ontogenetic variations in the type and size of prey consumed by juvenile coho,Oncorhynchus kisutch,and chinook,O. tshawytscha,salmon

Synopsis Stomach contents of juvenile coho,Oncorhynchus kisutch, and chinook,O. tshawytscha, salmon collected in purse seines off the coast of Washington and Oregon were examined for variations related to predator size. There was a general trend toward increasing consumption of fish with increasing body size, due mainly to the increase in northern anchovy biomass consumed by the larger salmon. Most of the major prey taxa showed significant differences among the size classes examined for both salmon species. There was a direct relationship between predator and prey size for both coho and chinook, but considerable variation was found in prey length consumed within each size class. Prey width did not provide as good a fit as prey length for either species. In general, coho consumed larger fish prey in relation to their body length than chinook but there were substantial differences by month or year of collection.     

Salamander evolution across a latitudinal cline in gape-limited predation risk

General predictions of community dynamics require that insights derived from local habitats can be scaled up to explain phenomena across geographic scales. Across these larger spatial extents, adaptation can play an increasing role in determining the outcome of species interactions. If local adaptation is common, then our ability to generalize measures of species interaction strength across communities will be limited without an additional understanding of the genetic variation underlying interaction traits. In the context of predator–prey interactions, prey individuals commonly are expected to reduce risky foraging behaviors and subsequent growth under predation threat. However, rapid growth into a large body size can defend against gape-limited predators, creating a tradeoff between increased predation risk due to elevated foraging activity and decreased predation risk due to large size. Here I combine field observations, natural selection experiments, and common garden assays to understand potential adaptations of spotted salamander Ambystoma maculatum larvae to gape-limited and gape-unconstrained predators. Field observations and natural selection trials suggested antagonistic selection on prey body size among ponds dominated by gape-limited predator salamanders A. opacum and gape-unconstrained beetle larvae Dytiscus . In common garden experiments, prey from sites with high gape-limited predation risk grew larger than those from other sites, suggesting the evolution of rapid growth into a prey size refuge. Larvae from all sites grew to a large size when exposed to the gape-limited N. viridescens predator's kairomones. Hence, induced rapid growth into a size refuge may be an adaptive response to gape-limited predation risk. Results point to an important role for cross-community generalizations based on functional classifications of predators by their gape constraints and inter-site genetic variation in prey growth rates and behaviors.     

Effects of body size and predators on intracohort competition in wild and domesticated juvenile salmon in a stream

Competition between masu salmon (Oncorhynchus masou) of wild and aquaculture origin was investigated. Fry were individually marked and released in stream enclosures with and without a piscivorous predator. The aim was to assess the effects of predators and salmon body size on survival and growth of the two types of fish under natural conditions. The presence of predaceous Japanese huchen (Hucho perryi) resulted in lower mean growth rates of surviving fry. Relatively large fish survived and grew better than relatively small fish in the absence of predators, but not in their presence. This probably indicates an indirect effect of predation risk on within-cohort competitive behavior among salmon juveniles, with larger fish forced to give up their position as superior competitors. Domesticated fish survived in larger numbers and grew much faster than wild fish, irrespective of predator presence. Comparison with similar field studies revealed a pattern that the pre-experimental environment influenced the outcome of competition between wild and domesticated juvenile salmon. Domesticated fish were superior competitors even in the absence of an initial size advantage, which commonly gives a further advantage to hatchery-raised fish in natural streams. Therefore, caution dictates to avoid the release or escape of such fish into the wild.     

Group‐Size Effect on Vigilance and Foraging in a Predator‐Free Population of Feral Goats (Capra hircus) on the Isle of Rum,NW Scotland

Many previous studies have found that as group size increases, individual vigilance levels decrease and forage intake increases (group‐size effect), but few such studies have considered the impact of within‐group interactions and other confounding factors on the direction of group‐size effects. A free‐ranging population of feral goats (Capra hircus), with little predation threat, was studied on the Isle of Rum (northwest Scotland), from Jun. to Nov. 2000, to investigate the effects of group size on individual vigilance levels and foraging efficiency after taking into account the effect of confounding factors (e.g. sex, season, time of day, habitat, predation risk) and within‐group interactions (via changes in movement rates while feeding). Our results show that, while group size exerted a negative influence on individual vigilance levels and a positive effect on movement rate, foraging efficiency never increased with group size and even decreased at certain times of day. There was no sex difference in individual vigilance in feral goats, but foraging efficiency was higher in females than in males. Goats were more vigilant in fall than in summer. The results imply that the benefits for foraging obtained from the reduced vigilance level in larger groups may be constrained or offset by increased interaction (or competition) within larger groups even in a population that faces negligible predation risk.     

Invertebrate mesopredators are larger in streams with fish

Species with complex life cycles (e.g., aquatic larvae, terrestrial adults) are expected to shorten the time spent in the larval stage if mortality risks are high, a trade-off that lowers predation risk at the cost of reduced time for growth and thus smaller adult size. We tested these predictions by comparing the timing of and size at emergence for two relatively large and common invertebrate mesopredator species (Isoperla montana and Rhyacophila vibox) that inhabit small coastal streams, with and without predatory fish, in eastern Canada. Contrary to expectations based on predation risk–foraging trade-off theory, individuals of both invertebrate species tended to be larger rather than smaller in streams with fish than in fishless streams. The patterns were consistent, however, with the expected ecological effects of top predators on food webs, where fish lower abundances of invertebrate mesopredators, increasing resource availability and thus growth rates for the remaining individuals. We conclude that variation among streams in size at emergence is better explained by the impact of fish on resource availability than to behavioural or life history trade-offs occurring under risk of predation.     

Disruption of seasonality in growth hormone-transgenic coho salmon (Oncorhynchus kisutch) and the role of cholecystokinin in seasonal feeding behavior

Seasonal variation in daily food intake is a well-documented phenomenon in many organisms including wild-type coho salmon where the appetite is noticeably reduced during periods of decreased day length and low water temperature. This reduction may in part be explained by altered production of cholecystokinin (CCK) and growth hormone (GH). CCK is a hormone produced in the brain and gut that mediates a feeling of satiety and thus has an inhibitory effect on food intake and foraging behaviour. Growth hormone (GH) enhances feeding behaviour and consequently growth, but its production is reduced during winter. The objectives of this study were: first, to compare the seasonal feeding behaviour of wild and GH-transgenic coho salmon; second, to determine the behavioural effect of blocking the action of CCK (by using devazepide) on the seasonal food intake; and third, to measure CCK expression in brain and gut tissues between the two genotypes across seasons. We found that, in contrast to wild salmon, food intake in transgenic salmon was not reduced during winter indicating that seasonal control of appetite regulation has been disrupted by constitutive production of GH in transgenic animals. Blocking of CCK increased food intake in both genotypes in all seasons. The increase was stronger in wild genotypes than transgenic fish; however blocking CCK in wild-type fish in winter did not elevate appetites to levels observed in the summer. The response to devazepide was generally faster in transgenic than in wild salmon with more rapid effects observed during summer than during winter, possibly due to a higher temperature in summer. Overall, a seasonal effect on CCK mRNA levels was observed in telencephalon with levels during winter being higher compared to the summer in wild fish, but with no seasonal effect in transgenic fish. No differences in seasonal CCK expression were found in hypothalamus. Higher levels of CCK were detected in the gut of both genotypes in winter compared to summer. Thus, CCK appears to mediate food intake among seasons in both wild-type and GH-transgenic salmon, and an altered CCK regulation may be responsible at least in part for the seasonal regulation of food intake.     

An asymmetric producer-scrounger game: body size and the social foraging behavior of coho salmon

A tension between cooperation and conflict characterizes the behavioral dynamics of many social species. The foraging benefits of group living include increased efficiency and reduced need for vigilance, but social foraging can also encourage theft of captured prey from conspecifics. The payoffs of stealing prey from others (scrounging) versus capturing prey (producing) may depend not only on the frequency of each foraging strategy in the group but also on an individual’s ability to steal. By observing the foraging behavior of juvenile coho salmon (Oncorhynchus kisutch), we found that, within a group, relatively smaller coho acted primarily as producers and took longer to handle prey, and were therefore more likely to be targeted by scroungers than relatively larger coho. Further, our observations suggest that the frequency of scrounging may be higher when groups contained individuals of different sizes. Based on these observations, we developed a model of phenotype-limited producer-scrounger dynamics, in which rates of stealing were structured by the relative size of producers and scroungers within the foraging group. Model simulations show that when the success of stealing is positively related to body size, relatively large predators should tend to be scroungers while smaller predators should be producers. Contrary to previous models, we also found that, under certain conditions, producer and scrounger strategies could coexist for both large and small phenotypes. Large scroungers tended to receive the highest payoff, suggesting that producer-scrounger dynamics may result in an uneven distribution of benefits among group members that—under the right conditions—could entrench social positions of dominance.     

Oxygen uptake of growth hormone transgenic coho salmon during starvation and feeding

Oxygen uptake of growth hormone transgenic coho salmon Oncorhynchus kisutch was measured in individual fish with a closed-system respirometer and was compared with that of similar-sized non-transgenic control coho salmon during starvation and when fed a fixed ration or to satiation. Transgenic and control fish did not differ in their standard oxygen uptake after 4 days of starvation, although control fish had a higher routine oxygen uptake, scope for spontaneous activity and initial acclimation oxygen uptake. During feeding, transgenic fish ate significantly more than control fish, and had an overall oxygen uptake that was 1·7 times greater than control fish. When fish that had eaten the same per cent body mass were compared, transgenic fish had an oxygen uptake that was 1·4 times greater than control fish. Differences in oxygen uptake in growth hormone transgenic coho salmon and non-transgenic fish appear to be due to the effects of feeding, acclimation and activity level, and not to a difference in basal metabolism.     

School size affects individual feeding success in three-spined sticklebacks (Gastevosteus aculeatus L.)

The effect of school size on the feeding success of individual three-spined sticklebacks was studied. We found that the proportion of fish feeding on benthic prey increased with school size and that fish in large schools tended to start feeding sooner than fish in small schools. The total number of strikes also increased in larger schools. Despite this evidence for a foraging benefit associated with school membership we propose that improved feeding returns do not alone explain stickleback schooling.     

Development of net energy intake models for drift-feeding juvenile coho salmon and steelhead

We developed models to predict the effect of water velocity on prey capture rates and on optimal foraging velocities of two sympatric juvenile salmonids, coho salmon and steelhead. Mean fish size was ~80 mm, the size of age I+ coho and steelhead during their second summer in Southeast Alaska streams, when size overlap suggests that competition might be strongest. We used experimentally determined prey capture probabilities to estimate the effect of water velocity on gross energy intake rates, and we modeled prey capture costs using experimental data for search and handling times and published models of swimming costs. We used the difference between gross energy intake and prey capture costs to predict velocities at which each species maximized net energy intake rate. Predicted prey capture rates for both species declined from ~75 to 30–40 prey/h with a velocity increase from 0.30 to 0.60 m·s⁻¹. We found little difference between coho and steelhead in predicted optimum foraging velocities (0.29 m·s⁻¹ for coho and 0.30 m·s⁻¹ for steelhead). Although prey capture ability appears to be more important than are prey capture costs in determining optimum foraging velocities, capture costs may be important for models that predict fish growth. Because coho are assumed to pay a greater swimming cost due to a less hydrodynamic body form, we also modeled 10 and 25% increases in hydrodynamic drag to assess the effect of increased prey capture costs. This reduced optimum velocity by 0 and 0.01 m∙s⁻¹, respectively. Habitat segregation among equal-sized coho and steelhead does not appear to be related to the effects of water velocity on their respective foraging abilities.     

How feeding performance and energy intake change with a small increase in the body size of the three-spined stickleback

Changes in the foraging behaviour due to variation in the body size of the three-spined stickleback Gasterosteus aculeatus were investigated. All sizes of fish had a high probability of attacking prey whenever encountered. The probability of eating the prey increased with the size of the fish, as the larger fish had larger jaws and a greater stomach capacity. Therefore, as fish increased in size there was an increase in the probability of successful prey capture. The level of satiation did not have an effect on the prey handling time, which is contrary to other studies and is probably a result of the large prey sizes. The physical size of the prey meant that the handling times were long regardless of the motivational level of the fish. The larger fish took in more energy and at a faster rate, although the time to reach satiation was similar for all fish sizes. The advantage that large fish appear to have in successfully gaining large prey is negated by their greater metabolic requirement. The changes in feeding performance induced by small increases in body size could have important consequences for intraspecific competition, habitat Use and risk of predation.     

Seasonal variations in feeding range and flock structure of the Rook Corvus frugilegus in eastern Ireland

The feeding range and flock structure of Rooks showed temporal variations caused mainly by the dispersion of food and reproductive behaviour.
Feeding range was restricted in spring, autumn and early winter when food availability was high and Rooks were reproductively active. A large feeding range occurred in late summer and late winter, when food availability was either generally low or locally distributed and when Rooks were reproductively inactive. The occurrence of flocks common to several rookeries mirrored variations in feeding range; mixed rookery flocks were more common in late summer and late winter. Similarly, the size of the rookery (as measured by the number of nests) was related to feeding range only when Rooks were reproductively inactive and at such times larger rookeries had greater feeding ranges.
Flock structure showed similar seasonal variations; small widely spaced flocks predominated in summer, autumn, early winter and spring, whereas large dense flocks occurred in late winter. Diurnal variations in flock structure occurred within any one season. Both seasonal and diurnal variations in flock structure may be determined by the dispersion of the prey and the feeding strategy used to obtain it, reproductive behaviour and the risk of predation.     

Seasonal Trophic Niche Shift and Cascading Effect of a Generalist Predator Fish

Few studies have examined how foraging niche shift of a predator over time cascade down to local prey communities. Here we examine patterns of temporal foraging niche shifts of a generalist predator (yellow catfish, Pelteobagrus fulvidraco) and the abundance of prey communities in a subtropical lake. We predicted that the nature of these interactions would have implications for patterns in diet shifts and growth of the predator. Our results show significant decreases in planktivory and benthivory from late spring to summer and autumn, whereas piscivory increased significantly from mid-summer until late autumn and also increased steadily with predator body length. The temporal dynamics in predator/prey ratios indicate that the predation pressure on zooplankton and zoobenthos decreased when the predation pressure on the prey fish and shrimps was high. Yellow catfish adjusted their foraging strategies to temporal changes in food availability, which is in agreement with optimal foraging theory. Meanwhile the decrease in planktivory and benthivory of yellow catfish enabled primary consumers, such as zooplankton and benthic invertebrates, to develop under low grazing pressure via trophic cascading effects in the local food web. Thus, yellow catfish shifts its foraging niche to intermediate consumers in the food web to benefit the energetic demand on growth and reproduction during summer, which in turn indirectly facilitate the primary consumers. In complex food webs, trophic interactions are usually expected to reduce the strength and penetrance of trophic cascades. However, our study demonstrates strong associations between foraging niche of piscivorous fish and abundance of prey. This relationship appeared to be an important factor in producing top-down effects on both benthic and planktonic food webs.     

The foraging and antipredator behaviour of growth-enhanced transgenic Atlantic salmon

Growth rate has been established as a key parameter influencing foraging decisions involving the risk of predation. Through genetic manipulation, transgenic salmon bred to contain and transmit a growth hormone transgene are able to achieve growth rates significantly greater than those of unmanipulated salmon. Using such growth-enhanced transgenic Atlantic salmon, we directly tested the hypothesis that relative growth rates should be correlated with willingness to risk exposure to a predator. We used size-matched transgenic and control salmon in two experiments where these fish could either feed in safety, or in the presence of the predator. The first experiment constrained the predator behind a Plexiglas partition (no risk of mortality), the second required the fish to feed in the same compartment as the predator (a finite risk of mortality). During these experiments, transgenic salmon had rates of consumption that were approximately five times that of the control fish and rates of movement approximately double that of controls. Transgenic salmon also spent significantly more time feeding in the presence of the predator, and consumed absolutely more food at that location. When there was a real risk of mortality, control fish almost completely avoided the dangerous location. Transgenic fish continued to feed at this location, but at a reduced level. These data demonstrate that the growth enhancement associated with the transgenic manipulation increases the level of risk these fish are willing to incur while foraging. If the genetic manipulation necessary to increase growth rates is achievable through evolutionary change, these experiments suggest that growth rates of Atlantic salmon may be optimized by the risk of predation. Copyright 1999 The Association for the Study of Animal Behaviour.     

Individual growth and phase differentiation of lacustrine masu salmon, Oncorhynchus masou, under artificial rearing conditions

 In lacustrine masu salmon, Oncorhynchus masou, originated from anadromous fish and inhabiting an artificial lake (Shumarinai Lake), we examined the relationship between individual growth during the juvenile stage and phase differentiation under artificial rearing conditions. In females, the mean fork length of potential (subsequent) 1+ smolts and potential 1+ parr (1+ parr show fish that neither smolted nor matured until 1+ autumn) always differed after their first summer (0+ summer), the former being larger. In males, the juveniles that grew faster during their first spring became 0+ mature male parr. After their first summer, potential 1+ smolts were always larger in body length than potential 1+ mature parr and potential 1+ parr. These results were similar to previous reports of anadromous masu salmon, suggesting that the lacustrine masu salmon studied seems to have maintained the phase differentiation as in the original fish, likely because only 60 years have passed since the formation of the lacustrine population.