Feeding and aggressive behaviours in juvenile coho salmon (Oncorhynchus kisutch) under chemically-mediated risk of predation

Summary Juvenile coho salmon (Oncorhynchus kisutch) spend the first year of their lives in their natal streams, where they may often hold feeding territories. They also face significant risk of predation by birds and fish, and should alter their behaviour to reduce risk of mortality when these predators are present. Although there is laboratory evidence that coho react to predator visual stimuli, chemoreception of avian predator presence has not previously been reported. We tested the influence of chemical stimuli of common merganser (Mergus merganser), preying on juvenile coho, on two aspects of coho territorial behaviour, foraging and aggression, in flow-through aquaria. After a mixture of merganser- and coho-conditioned water was introduced into the system, juvenile coho significantly reduced their attack distance on drifting prey. The fish also significantly decreased their aggressive behaviour directed towards mirrors (total number of acts, intensity of acts and time spent) when the same odour was present. They did not change their behaviour in either experiment after control introductions of water treated with fish alone. These results are interpreted within the framework of a trade-off between juvenile growth and mortality.     

Distribution and diet of juvenile Patagonian toothfish on the South Georgia and Shag Rocks shelves (Southern Ocean)

The distribution and diet of juvenile (<750 mm) Patagonian toothfish are described from four annual trawl surveys (2003–2006) around the island of South Georgia in the Atlantic sector of the Southern Ocean. Recruitment of toothfish varies inter-annually, and a single large cohort dominated during the four years surveyed. Most juveniles were caught on the Shag Rocks shelf to the NW of South Georgia, with fish subsequently dispersing to deeper water around both the South Georgia and Shag Rocks shelves. Mean size of juvenile toothfish increased with depth of capture. Stomach contents analysis was conducted on 795 fish that contained food remains and revealed that juvenile toothfish are essentially piscivorous, with the diet dominated by notothenid fish. The yellow-finned notothen, Patagonotothen guntheri, was the dominant prey at Shag Rocks whilst at South Georgia, where P. guntheri is absent, the dominant prey were Antarctic krill and notothenid fish. The diet changed with size, with an increase in myctophid fish and krill as toothfish grow and disperse. The size of prey also increased with fish size, with a greater range of prey sizes consumed by larger fish.     

The paradox of risk assessment: comparing responses of fathead minnows to capture-released and diet-released alarm cues from two different predators

Summary. Many aquatic prey are known to use chemical alarm cues to assess their risk of predation. In fishes, such alarm cues can be released either through damage of the epidermis during a predatory attack (capture-released) or through release from the predator feces (diet-released). In our study, we compared the importance of capture- versus diet-released alarm cues in risk assessment by fathead minnows (Pimephales promelas) that were na?ve to fish predators. We utilized two different fish predators: a specialized piscivore, the northern pike (Esox lucius) and a generalist predator, the brook trout (Salvelinus fontinalis). Handling time of pike consuming minnows was much shorter than for trout consuming minnows, likely resulting in less epidermal damage to the minnows during attacks by pike. In accordance with this, minnows showed a less intense antipredator response to capture-released cues from pike than capture-released cues from trout. This represents a paradox in risk assessment for the minnows as they respond to the specialized piscivore, the more dangerous predator, with a less intense antipredator response. In contrast, the minnows showed a stronger antipredator response to the specialized piscivore than to the generalist when given diet cues. This work highlights the need for researchers to carefully consider the nature of the information available to prey in risk assessment.     

Threat-sensitive predator avoidance in damselfish-trumpetfish interactions

Summary Predatory threat can vary during a predator-prey interaction as an attack escalates or among predators at different times. A Threat-sensitivity hypothesis is presented which predicts that prey individuals will trade-off predator avoidance against other activities by altering their avoidance responses in a manner that reflects the magnitude of the predatory threat. This hypothesis was tested in the field by presenting prey (threespot damselfish, Stegastes planifrons) with models of foraging predators (Atlantic trumpetfish, Aulostomus maculatus). During a presentation, damselfish displayed progressively stronger avoidance as predator models were brought nearer; response waned rapidly once predator models passed overhead. Larger predator models and those oriented in a strike pose evoked stronger avoidance reactions than smaller and non-attacking models, intermediate responses were evoked by size and orientation combinations that were intermediate in threat, and habituation was more common to weakly-threatening presentations. Smaller damselfish showed stronger avoidance of models than did larger damselfish. Nonavoidance activities, such as feeding and territorial defense, were curtailed during presentations or were more common during weakly threatening presentations. Approaches to the models, equated with mobbing, were more common among large damselfish, again reflecting degrees of vulnerability among different size prey individuals. These initial results indicate that damselfish threatened by predators respond in a graded manner that reflects the degree of threat posed by the predator, in accordance with the Threat-sensitivity hypothesis.     

Low-level copper exposures increase visibility and vulnerability of juvenile coho salmon to cutthroat trout predators

Copper contamination in surface waters is common in watersheds with mining activities or agricultural, industrial, commercial, and residential human land uses. This widespread pollutant is neurotoxic to the chemosensory systems of fish and other aquatic species. Among Pacific salmonids (Oncorhynchus spp.), copper-induced olfactory impairment has previously been shown to disrupt behaviors reliant on a functioning sense of smell. For juvenile coho salmon (O. kisutch), this includes predator avoidance behaviors triggered by a chemical alarm cue (conspecific skin extract). However, the survival consequences of this sublethal neurobehavioral toxicity have not been explored. In the present study juvenile coho were exposed to low levels of dissolved copper (5-20 microg/L for 3 h) and then presented with cues signaling the proximity of a predator. Unexposed coho showed a sharp reduction in swimming activity in response to both conspecific skin extract and the upstream presence of a cutthroat trout predator (O. clarki clarki) previously fed juvenile coho. This alarm response was absent in prey fish that were exposed to copper. Moreover, cutthroat trout were more effective predators on copper-exposed coho during predation trials, as measured by attack latency, survival time, and capture success rate. The shift in predator-prey dynamics was similar when predators and prey were co-exposed to copper. Overall, we show that copper-exposed coho are unresponsive to their chemosensory environment, unprepared to evade nearby predators, and significantly less likely to survive an attack sequence. Our findings contribute to a growing understanding of how common environmental contaminants alter the chemical ecology of aquatic communities.     

Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasterosteus spp.)

Summary In laboratory experiments, we tested the hypothesis that by living in larger shoals, juvenile threespine (Gasterosteus aculeatus) and blackspotted (G. wheatlandi) sticklebacks lower their risk of being parasitized by the crustacean ectoparasite Argulus canadensis. An increase in shoal size resulted in a lower average number of attacks received by individual fish, but had no negative effect on the attack performance (attack rate and attack success) of the parasites. In addition, more fish formed shoals and shoal sizes were larger in the presence of parasites. We conclude that ectoparasitism may have been a strong selective factor in the evolution of social behaviour in juvenile sticklebacks.     

Feeding ecology and niche segregation in oceanic top predators off eastern Australia

We examined the feeding ecology and niche segregation of the ten most abundant fish species caught by longline operations off eastern Australia between 1992 and 2006. Diets of 3,562 individuals were examined. Hook timer data were collected from a further 328 fish to examine feeding behaviour in relation to depth and time of day. Prey biomass was significantly related to predator species, predator length and year and latitude of capture. Although the fish examined fed on a mix of fish, squid and crustacea, fish dominated the diet of all species except small albacore (Thunnus alalunga) which fed mainly on crustacea and large swordfish (Xiphias gladius) and albacore which fed mainly on squid. Cannibalism was observed in lancetfish (Alepisaurus spp.). Multidimensional scaling identified three species groups based on their diet composition. One group consisted of yellowfin tuna (T. albacares), striped marlin (Tetrapturus audax) and dolphinfish (Coryphaena hippurus); a second group consisted of bigeye tuna (T. obesus), swordfish and albacore; and a third consisted of southern bluefin tuna (T. maccoyii) and blue shark (Prionace glauca). Of note was the separation of mako shark (Isurus oxyrhynchus) and lancetfish from all other predators. Prey length generally increased with increasing predator length although even large predators fed on a wide range of prey lengths including very small prey. Overall, differences in prey type and size, feeding times and depths were noted across the range of species examined to the extent that predators with overlapping prey, either in type or size, fed at different times of the diel period or at different depths. Taken together these data provide evidence for feeding niche segregation across the range of oceanic top predators examined.     

Performance level and efficiency of two differing predator-avoidance strategies depend on nutritional state of the prey fish

Animal prey has developed a variety of behavioural strategies to avoid predation. Many fish species form shoals in the open water or seek refuge in structurally complex habitats. Since anti-predator strategies bear costs and are energy-demanding, we hypothesised that the nutritional state of prey should modify the performance level and efficiency of such strategies. In aquaria either containing or lacking a structured refuge habitat, well-fed or food-deprived juvenile roach (Rutilus rutilus) were exposed to an open-water predator (pikeperch, Sander lucioperca). Controls were run without predators. In the presence of the predator, roach enhanced the performance of the anti-predator strategy and increased the use of the refuge habitat whereby food-deprived roach were encountered more often in the structure than well-fed roach. Nonetheless more starved than well-fed roach were fed upon by the predator. In the treatments offering only open-water areas, roach always formed dense shoals in the presence of the predator. The shoal density, however, was lower in starved roach. Starving fish in shoals experienced the highest predation mortality across all experimental treatments. The experiment confirmed the plasticity of the anti-predator behaviour in roach and demonstrated that food deprivation diminished the efficiency of shoaling more strongly than the efficiency of hiding. The findings may be relevant to spatial distribution of prey and predator–prey interactions under natural conditions because when prey are confronted with phases of reduced resource availability, flexible anti-predator strategies may lead to dynamic habitat use patterns.     

Induced defensive responses by the bivalve Mytilus edulis to predators with different attack modes

Predators such as crabs, whelks, and sea stars attack their bivalve prey in different ways, and predator-induced defenses are an important means of protection. The degree to which induced defenses are specific to different predators, however, remains largely unknown. In laboratory experiments (June to August 1998), we raised mussels (Mytilus edulis L.) in the presence of a drilling predator [the whelk Nucella lapillus (L.)] or a crushing predator [the crab Carcinus maenas (L.)] to determine whether induced changes in prey shell thickness, size, or shape occurred and whether changes were predator-specific. Over a 2 month period, juvenile mussels were exposed to waterborne cues from actively feeding crabs or whelks. Mussels produced thicker shell lips in response to both predators relative to control mussels raised in their absence, and the difference was significantly greater in response to whelks than to crabs. Mussels exposed to whelks showed significantly smaller increases in shell length and width and total wet weight than did mussels exposed to crabs. Thus, there may be a trade-off between shell thickness and linear shell growth and a potential delay in attaining a size refuge from predation. Received: 4 August 1999 / Accepted: 31 January 2000     

Predator inspection behaviour in three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>): body size,local predation pressure and cooperation

The apparently maladaptive tendency of fish to approach and inspect potential predators has been explained in terms of useful information gathering or as a signal to the predator that it has been seen. We examined this behaviour in 16 populations of wild-caught stickleback (Gasterosteus aculeatus) from ponds with and without predatory perch (Perca fluviatilis). Three large and three small individuals per population were each exposed to three model predators differing in realism. A final cooperative treatment entailed pairing subjects with a second individual from the same population, but of the alternative size class, during predator presentation. As might be expected, predator inspection behaviour was much greater in the predator-sympatric populations, and only these fish increased their level of inspection as the models became incrementally more realistic. This suggests that reductions occur in the level of costly inspection behaviour in populations without predators. Subject body size had no effect on inspection effort, which suggests a limited role for experience (we assumed larger fish to be older than smaller fish), at least over the relative age differences utilized. However, small predator-sympatric fish were the only subjects to increase inspection significantly when in a cooperative context, perhaps reflecting the inherent value of a relatively larger partner in this context. These results confirm that levels of predator inspection are both population- and situation-dependent, suggesting a trade-off in the potential costs and benefits of this behaviour.Communicated by C. St. Mary     

Predator choice in the field; grouping guppies, Poecilia reticulata, receive more attacks

Capture success of many predator species has been shown to decrease with increasing prey group size and it is therefore suggested that predators should choose to attack stragglers and/or small groups. Predator choice in the laboratory has shown mixed results with some species preferentially attacking large groups and others preferring to attack stragglers over groups. Such predator choices have not been tested in the field. In our study we presented a binary choice between a shoal of guppies and a single guppy to predators in pools in the Arima river, Trinidad. We observed attacks in 11 different pools from a total of 53 predators (20 acara cichlids, Aequidens pulcher, 32 pike cichlids, Crenicichla frenata, and one wolf-fish, Hoplias malabaricus) and found that all predators showed a strong preference for the shoal of guppies in terms of both first choice and total number of attacks. We discuss the implications of these preferences with regards to predator–prey interactions.     

Mean free-path length theory of predator–prey interactions: Application to juvenile salmon migration

Ecological theory traditionally describes predator–prey interactions in terms of a law of mass action in which the prey mortality rate depends on the density of predators and prey. This simplifying assumption makes population-based models more tractable but ignores potentially important behaviors that characterize predator–prey dynamics. Here, we expand traditional predator–prey models by incorporating directed and random movements of both predators and prey. The model is based on theory originally developed to predict collision rates of molecules. The temporal and spatial dimensions of predators–prey encounters are determined by defining movement rules and the predator's field of vision. These biologically meaningful parameters can accommodate a broad range of behaviors within an analytically tractable framework suitable for population-based models. We apply the model to prey (juvenile salmon) migrating through a field of predators (piscivores) and find that traditional predator–prey models were not adequate to describe observations. Model parameters estimated from the survival of juvenile chinook salmon migrating through the Snake River in the northwestern United States are similar to estimates derived from independent approaches and data. For this system, we conclude that survival depends more on travel distance than travel time or migration velocity.     

Parental investment and its ecological consequences in the solitary wasp Sceliphron assimile (Dahlbom) (Sphecidae)

Summary The sphecid wasp Sceliphron assimile Dahlbom builds mud cells whose volumes are positively correlated to maternal length, the relationship being highly significant for daughters (Fig. 1). However, small females build cells longer and wider in relation to their own body length than large females do (Fig. 3). Cell volume closely regulates the total weight of prey stocked per cell (Figs. 4, 10). Maternal length is directly related to prey size and inversely related to the number of prey stocked (Fig. 5). Female length, above a threshold of 19 mm, probably does not influence her chance of starting a nest (Fig. 6) but is strongly positively correlated to achieved fecundity. Large females have larger offspring and a higher proportion of daughters than small females do (Fig. 7), but this is largely controlled by maternal behaviour rather than by genetical mechanisms (Fig. 10). The results are in general agreement with those of Trivers and Hare (1976) for solitary wasps, but large progeny are cheaper to produce per unit weight than small ones, and for a given weight sons are cheaper to produce than daughters.     

Size matters: variation in the diet of chick and adult crested terns

We investigated ontogenetic, temporal and spatial patterns in the composition and size of prey in the diet of crested terns, Sterna bergii. Diet analyses indicated that crested terns are a generalist predator on surface-schooling clupeids (Australian anchovy Engraulis australis, sardine Sardinops sagax and blue sprat Spratelloides robustus), Degens leatherjacket Thamnaconus degeni, southern sea garfish Hyporhamphus melanochir, Australian herring Arripis georgianus, slender bullseye Parapriacanthus elongatus and barracouta Thyrsites atun. Ontogenetic differences in prey size indicated that adults are constrained in their foraging behaviour during the early chick-provisioning period by the need to self feed and select smaller prey that can be ingested by their chicks. Chicks consumed significantly higher proportions of clupeids than adults, which consumed mainly Degens leatherjackets and barracouta, suggesting that adults may select higher quality prey for their chicks compared to what they consume themselves. Spatial differences in prey composition were driven by differing proportions of sardine, Australian anchovy and Degens leatherjacket and could reflect local differences in the abundances of these prey. The size of prey taxa consumed by adults also reflected a North–South gradient in prey size. The large component of juvenile sardine in the diet of crested terns suggests future dietary measures may inform fisheries managers about changes in local juvenile sardine abundance. These data could assist in highlighting any fishery-related decreases in sardine recruitment and help ensure commercial fishing practices address principals of Ecologically Sustainable Development developed for Australian fisheries.     

Interactions between fangblennies (Plagiotremus rhinorhynchus) and their potential victims: fooling the model rather than the client?

Lepidophagous (scale-eating) blue-striped fangblennies (Plagiotremus rhinorhynchus Bleeker 1852) are often found sympatrically with the bluestreak cleaner wrasse (Labroides dimidiatus Valenciennes 1839). They have some resemblance to the juvenile L. dimidiatus and have previously been reported as aggressive cleaner wrasse mimics. We observed 14 P. rhinorhynchus on a small area in the barrier reef near Hoga Island, Indonesia to assess the effects of client size on the behaviour and attack success of fangblennies: our results suggest that fangblennies are selective with regard to victim size; fish avoided by the fangblennies are significantly larger than those not avoided and attack success is significantly higher at intermediate victim size classes. The behaviour of the victims also has a significant direct effect on the foraging success of the fangblennies; where the potential victim posed, 63.6% were ignored by the fangblenny and only 7.4% of attacks were successful on posing fish as opposed to a surprise attack success rate of 71.6%. Overall, victims which exhibited the pose behaviour were significantly smaller in size. It appears likely that the predatory strategy of these fangblennies varies with victim size and that mimicry plays a minor role in attracting potential victims. We suggest that in common with other mimetic fish the resemblance of fangblennies to juvenile bluestreak cleaner wrasse allows them to actively hunt in areas where adult cleaners are common thus, indirectly improving their feeding opportunities.     

Prey capture by Pisaster brevispinus (Asteroidea: Echinodermata) on soft substrate

Observations on the subtidal seastar Pisaster brevispinus (Stimpson) indicate that this predator can extend the central tube feet into sand-mud substrate for a distance roughly equal to the radius of the seastar. Field and laboratory evidence demonstrates the use of the elongated tube feet by the asteroid for the capture of burrowed prey items. A relationship between predator size and the size of juveniles of the deep-burrowing clam Tresus nuttallii taken as prey is a product of the ability of larger seastars to extend the tube feet further into the substrate and capture deeper prey. The role of P. brevispinus as an important subtidal predator along the Pacific Coast of North America is discussed.     

Threat-sensitive generalization of predator recognition by larval amphibians

Despite the importance of acquired predator recognition in mediating predator–prey interactions, we know little about the specific characteristics that prey use to distinguish predators from non-predators. Recent experiments with mammals and fish indicate that some prey lacking innate predator recognition have the ability to display anti-predator responses upon their first encounter with those predators if they are similar to predators that the prey has recently learned to recognize. This phenomenon is referred to as generalization of predator recognition. In this experiment, we documented for the first time that larval amphibians (woodfrog, Rana sylvatica) have the ability to generalize the recognition of known predators to closely related novel predators. Moreover, we demonstrated that this ability is dependent on the level of risk associated with the known predator. When red-bellied newt, Cynops pyrrhogaster (known predator), was paired with simulated low risk, tadpoles displayed fright responses to newts and novel tiger salamanders, Ambystoma tigrinum, but not to novel African clawed frogs, Xenopus laevis. However, when the newt was paired with simulated high risk, tadpoles generalized their responses to both tiger salamanders and African clawed frogs. Larval anurans seem to have a wider generalization frame than other animals.     

Underwater and above-water search patterns of an Arctic seabird: reduced searching at small spatiotemporal scales

How predators vary search patterns in response to prey predictability is poorly known. For example, marine invertebrates may be predictable but of low energy value, while fish may be of higher energy value but unpredictable at large (pelagic schools) or small (solitary benthics) spatial scales. We investigated the search patterns of the thick-billed murre (Uria lomvia), an Arctic seabird feeding on invertebrates, pelagic fish, or benthic fish. Foraging ranges at the Coats Island colony are generally smaller (<240 min per trip) than at larger colonies, and many birds specialize in foraging tactics and diet. Underwater search times for benthic fish were higher than for pelagic fish or invertebrates while above-water search times for pelagic fish were higher than for benthic fish or invertebrates. There were few stops during trips. Total trip time, flying time, number of flights, and number of dives were intercorrelated and increased with prey energy content, suggesting that longer trips involved fewer prey encounters due to selection of higher-quality, but rarer, prey items. Flight times were not Lévy-distributed and seabirds may have used area-restricted searches. The high degree of specialization, apparent absence of information center effects, and reduced above-water searching times may be linked to the relatively small colony size and the resulting short commuting distances to feeding areas, leading to greater prey predictability. We concluded that prey predictability over various scales affected predator search patterns.     

The role of turbidity as a constraint on predator-prey interactions in aquatic environments

Many of the world's most productive aquatic ecosystems usually contain turbid water. Paradoxically, many fish species that live in these habitats are also those that often rely on vision to detect their predators and their prey. For these fish, turbidity will reduce the distance at which predator-prey interactions occur, and there should be a reduction in the opportunity for behavioural modification to control the risk of predation. Under these conditions, we predict that most antipredator behaviour will become ineffective and that predator-prey interactions in turbid water will be primarily characterised by the direct effects of predator consumption of prey, rather than behavioural modification reducing the growth rates of prey. This hypothesis was tested in two laboratory experiments. The first experiment investigated how water turbidity, risk of predation, and their interaction affect habitat choice decisions by fathead minnows (Pimephales promelas). These data demonstrate that fathead minnows reduce their use of dangerous habitats, but that this effect is diminished in turbid water. A second experiment examined mortality patterns when these fish were preyed upon by yellow perch (Perca flavescens) in clear and turbid water. Absolute mortality rates were unaffected by visibility, but patterns of mortality were random in turbid water and skewed towards smaller individuals in clear water. Combined, these results support our hypothesis and suggest that the impact of predation risk will be reduced in turbid aquatic ecosystems. Received: 23 May 1996 / Accepted after revision: 18 November 1996     

Habitat use by juvenile Atlantic cod (Gadus morhua) in the presence of an actively foraging and non-foraging predator

Experiments were conducted in the autumn and winter of 1992/93 to examine habitat use by juvenile (age 0+) Atlantic cod, Gadus morhua L., before, during and following exposure to a passive or actively foraging predator (age 3+ cod). Experiments presented groups of juvenile cod (n=5 fish/group) with one of two combinations of three substrates; (1) gravel, sand, and a patch of artificial kelp (kelp), or (2) cobble, sand, and kelp. Cobble is known to provide juvenile cod with a refuge from predation. Kelp was used to test the hypothesis that juvenile cod associate with fleshy macroalgae in nature because of the safety it provides from predators. There was little difference in habitat use by juvenile cod before, during or following exposure to a passive predator. Under these conditions, juvenile cod appeared to prefer finer grained mineral substrates and avoided the kelp. The extent of the juvenile response to a passive predator was to avoid the predator's location in the experimental tank. In contrast, juvenile cod showed a significant shift in habitat use when exposed to an actively foraging predator, hiding in cobble or, when cobble was not available, in kelp. Use of both these habitats resulted in a significant reduction in predation risk to the juvenile cod. Our results suggest that: (1) an association with kelp provides safety from predation to juvenile cod, and (2) juvenile cod are capable for assessing the risk a predator represents and adjust their response accordingly.