Improving anti‐predator responses of hatchery reared salmonids by social learning

Predation shortly after release is the main source of mortality among hatchery‐reared fish used to restore or enhance endangered salmonid populations. We found, that hatchery‐reared salmonid young originating from endangered stocks have weak innate responses to their natural fish predators. The ability to avoid predation in fish can be improved through social learning from experienced to naïve individuals. Huge benefits would be achieved, if social learning processes could be successfully applied on a large scale to enhance viability of hatchery fish prior to release into the wild. By using model predators together with chemical cues from real predators we tested if social learning could be used to train hatchery‐reared salmonid young to avoid fish predators. As there are clear differences in social behaviour among the salmonid species, we first examined whether these differences affect the probability and efficiency of learning anti‐predator skills from trained demonstrators. We compared anti‐predator responses of observers (fish trained by using experienced fish as demonstrators) with those of control fish, which had been ‘trained’ by untrained naïve conspecifics. We also examined how the efficiency of social learning depends on the ratio of experienced to naïve fish involved in social transmission trials. The results of these experiments will give guidelines how social learning could be utilized in developing hatchery scale training protocols.     

Social enhancement and social inhibition of foraging behaviour in hatchery-reared Atlantic salmon

The results of two experiments showed that observation of a trained conspecific Atlantic salmon Salmo salar significantly increased the rate at which naïve hatchery-reared fish accepted novel, live prey items, whereas the presence of an untrained conspecific actually decreased learning rates due to social inhibition. Pre-release training involving exposure of hatchery-reared fish to live prey items in the presence of pre-trained demonstrators would result in a significant enhancement in their foraging success on release and help prevent starvation, which is thought to be one of the principal causes of post-release mortality in hatchery-reared fishes.     

Social Transfer of Predation Risk Information Reduces Food Locating Ability in European Minnows (Phoxinus phoxinus)

Little is known about how food location ability of animals is affected by social information of predation risk. This question was therefore addressed in an experimental study where naïve ‘observer’ European minnows (Phoxinus phoxinus) were allowed to search for food in a maze in the presence or absence of a predator (Salmo trutta). Observer minnows were accompanied by conspecific demonstrators which had previously been trained in the same maze either in the presence or absence of the predator. Observer minnows were most likely to locate food when the predator was absent both during their trial and during the pre‐training of demonstrators. When demonstrators had been trained with predators, observer success in locating the food was halved, although they were never exposed to predation risk themselves. When observers were exposed to predation risk their probability of locating food was further reduced regardless of the experience of their demonstrators. Our results show that predation risk can affect the foraging ability of minnows both directly and indirectly through social information from conspecifics. We conclude that social information may influence and constrain individual behavioural decisions, especially in rapidly changing environments where private information is often insufficient.     

Predator‐Naïve Brown Trout (Salmo trutta) Show Antipredator Behaviours to Scent from an Introduced Piscivorous Mammalian Predator Fed Conspecifics

Introduced mammalian predators may pose a high risk for native and naïve prey populations, but little is known about how native fish species may recognize and respond to scents from introduced mammalian predators. We investigated the role of diet‐released chemical cues in facilitating predator recognition, hypothesizing that native brown trout (Salmo trutta) would exhibit antipredator behaviours to faeces scents from the introduced American mink (Neovision vison) fed conspecifics, but not to non‐trout diets. In treatments‐control and replicate stream tank experiments, brown trout showed significant antipredator responses to faeces scent from mink fed conspecifics, but not to faeces scent from mink fed a non‐trout diet (chicken), or the non‐predator food control, Eurasian beaver (Castor fiber). We conclude that native and naïve brown trout show relevant antipredator behaviours to an introduced mammalian predator, presumably based on diet‐released conspecific alarm cues and thereby estimate the predation risk.     

Social Influence on Early Foraging of Domestic Chicks (Gallus gallus) in a Near-to-Nature Procedure

The aim of this study was to investigate the social influence of single chicks with different foraging experience on the behaviour of their group members during the first days after hatching. In contrast to the duplicate cage procedure normally used in social learning studies, four naïve group members could freely interact with a tutor or a control chick in an enriched 20-m² test arena. This arena contained two types of food caches with differently coloured food. The tutor was 3 d older than its group members and was trained to feed from one of the two food cache types, whereas the control chick was not familiar with the characteristics of the test arena and was either of the same age or 3 d older than its group members. During the first 9 d after hatching, the foraging activity of 32 chick groups was tested in 15 trials per group. Groups with a 3 d older but inexperienced control chick had the least foraging success whilst groups with a naïve control chick of the same age compared more favourably with the groups with experienced tutors than with groups that included older control chicks. In a second experiment, a tutor compartment was introduced into the test arena in order to compare a situation of unrestricted contact possibilities with the duplicate cage procedure in which tutor and bystanders are separated by a Perspex divider. The tutor compartment was opened for some test groups, allowing free interaction between tutor and naïve chicks. Those chicks which could only watch the tutor through the Perspex developed a preference for the tutor’s food type and discovered this food type as fast as the chicks of groups with unrestricted interactions. However, a relatively large proportion of groups (3 out of 8) did not develop successful foraging behaviour at all, whereas the successful groups showed longer feeding latencies during the subsequent trials than groups which had unrestricted contact with their tutor. This indicates an inhibiting effect of the duplicate cage procedure. It is concluded that when testing chicks of a few days of age, a distinction should be made between (i) the social influence on food particle preferences and (ii) the social influence on learning where to find food. This is important for generalizations taken from duplicate cage procedures without any environmental enrichment, as this restrictive setting only allows detection of food particle preferences.     

The relationship between dominance behaviour and growth as a function of habitat stability and community complexity: a test using salmon and trout

Predation shortly after release is the main source of mortality among hatchery‐reared fish used to restore or enhance endangered salmonid populations. We found, that hatchery‐reared salmonid young originating from endangered stocks have weak innate responses to their natural fish predators. The ability to avoid predation in fish can be improved through social learning from experienced to naïve individuals. Huge benefits would be achieved, if social learning processes could be successfully applied on a large scale to enhance viability of hatchery fish prior to release into the wild. By using model predators together with chemical cues from real predators we tested if social learning could be used to train hatchery‐reared salmonid young to avoid fish predators. As there are clear differences in social behaviour among the salmonid species, we first examined whether these differences affect the probability and efficiency of learning anti‐predator skills from trained demonstrators. We compared anti‐predator responses of observers (fish trained by using experienced fish as demonstrators) with those of control fish, which had been 'trained' by untrained naïve conspecifics. We also examined how the efficiency of social learning depends on the ratio of experienced to naïve fish involved in social transmission trials. The results of these experiments will give guidelines how social learning could be utilized in developing hatchery scale training protocols.     

Social Learning of a Novel Foraging Task by Big Brown Bats (Eptesicus fuscus)

Acquiring information via observation of others can be an efficient way to respond to changing situations or learn skills, particularly for inexperienced individuals. Many bat species are gregarious, yet few studies have investigated their capacity for learning from conspecifics. We tested whether big brown bats (Eptesicus fuscus) can learn a novel foraging task by interacting with knowledgeable conspecifics. In experimental trials 11 na?ve bats (7 juveniles, 4 adults) interacted freely with trained bats that were capturing tethered mealworms, while in control trials 11 na?ve bats (7 juveniles, 4 adults) flew with untrained bats. Na?ve bats were then assessed for their ability to capture tethered mealworms. While no bat in the control group learned the task, a significant number of experimental bats, including juveniles with little or no experience foraging, showed evidence of learning. Eighty-two per cent of experimental bats and 27% of control bats directed feeding buzzes (echolocation calls associated with prey capture) at the mealworm. Furthermore, seven experimental bats (64%) showed evidence of learning by attacking and/or capturing the mealworm, while no bat in the control group attacked or captured the prey. Analyses of high-speed stereo video recordings revealed increased interaction with demonstrators among bats attacking or capturing the mealworm. At the time they displayed evidence of learning, bats flew closer together during feeding buzzes than during other portions of trials. Our results demonstrate that social interaction with experienced bats, and listening to feeding buzzes in particular, may play an integral role in development of foraging skills in bats.     

Cover Caption

It is often assumed that learning improves foraging, but its direct benefits are not often examined. We demonstrate the contribution of learning to the foraging success of desert ants when a trained colony successfully competes against a naïve one. The outcome also depends on the relative group size. Desert Cataglyphis ants search individually for food (mostly dead prey) without laying pheromone trails (see pages 241-250). The cover photo shows a Cataglyphis niger worker searching for food in its typical sandy habitat. Photo provided Arik Dorfman.     

Responses of tadpoles to hybrid predator odours: strong maternal signatures and the potential risk/response mismatch

Previous studies have established that when a prey animal knows the identity of a particular predator, it can use this knowledge to make an ‘educated guess'' about similar novel predators. Such generalization of predator recognition may be particularly beneficial when prey are exposed to introduced and invasive species of predators or hybrids. Here, we examined generalization of predator recognition for woodfrog tadpoles exposed to novel trout predators. Tadpoles conditioned to recognize tiger trout, a hybrid derived from brown trout and brook trout, showed generalization of recognition of several unknown trout odours. Interestingly, the tadpoles showed stronger responses to odours of brown trout than brook trout. In a second experiment, we found that tadpoles trained to recognize brown trout showed stronger responses to tiger trout than those tadpoles trained to recognize brook trout. Given that tiger trout always have a brown trout mother and a brook trout father, these results suggest a strong maternal signature in trout odours. Tadpoles that were trained to recognize both brown trout and brook trout showed stronger response to novel tiger trout than those trained to recognize only brown trout or only brook trout. This is consistent with a peak shift in recognition, whereby cues that are intermediate between two known cues evoke stronger responses than either known cue. Given that our woodfrog tadpoles have no evolutionary or individual experience with trout, they have no way of knowing whether or not brook trout, brown trout or tiger trout are more dangerous. The differential intensity of responses that we observed to hybrid trout cues and each of the parental species indicates that there is a likely mismatch between risk and anti-predator response intensity. Future work needs to address the critical role of prey naivety on responses to invasive and introduced hybrid predators.     

Social learning improves survivorship at a life-history transition

During settlement, one of the main threats faced by individuals relates to their ability to detect and avoid predators. Information on predator identities can be gained either through direct experience or from the observation and/or interaction with others, a process known as social learning. In this form of predator recognition, less experienced individuals learn from experienced members within the social group, without having to directly interact with a predator. In this study, we examined the role of social learning in predator recognition in relation to the survival benefits for the damselfish, Pomacentrus wardi, during their settlement transition. Specifically, our experiments aimed to determine if P. wardi are capable of transmitting the recognition of the odour of a predator, Pseudochromis fuscus, to conspecifics. The experiment also examined whether there was a difference in the rate of survival between individuals that directly learnt the predator odour and those which acquired the information through social learning compared to naïve individuals. Results show that naïve P. wardi are able to learn a predator’s identity from experienced individuals via social learning. Furthermore, survival between individuals that directly learnt the predator’s identity and those that learnt through social learning did not significantly differ, with fish from both treatments surviving at least five times better than controls. These results demonstrate that experience may play a vital role in determining the outcome of predator–prey interactions, highlighting that social learning improves the ability of prey to avoid and/or escape predation at a life-history transition.     

Species-specific probe,based on 18S rDNA sequence,could be used for identification of the mucilage producer microalga <Emphasis Type="Italic">Gonyaulax fragilis</Emphasis> (Dinophyta)

Brook trout (Salvelinus fontinalis) in Appalachia experience prolonged periods of poor feeding conditions, particularly during summer and fall. To determine which prey organisms are important in sustaining brook trout populations, we monitored the feeding patterns of a population of brook trout over the course of 2 years with an emphasis on seasonal change. We employed a bioenergetics model to estimate whether or not each fish had obtained enough energy to meet daily metabolic demand. As a result, qualitative comparisons between fish feeding above maintenance ration (successfully feeding fish) and fish feeding below maintenance ration (unsuccessfully feeding fish) were possible. With the exception of winter, brook trout derived significantly more energy from terrestrial organisms than aquatic organisms. During each season, successfully feeding brook trout fed on greater proportions of specific prey types. Terrestrial Coleoptera and Lepidoptera consistently proved to be important prey during warmer seasons, while large organisms such as vertebrates and crayfish appeared to be important during winter. Our findings suggest that terrestrial organisms are more important than aquatic organisms in sustaining brook trout populations. Further, certain large and abundant terrestrial taxa are critical in providing energy to brook trout.     

More than a corridor: use of a main stem stream as supplemental foraging habitat by a brook trout metapopulation

Coldwater fishes in streams, such as brook trout (Salvelinus fontinalis), typically are headwater specialists that occasionally expand distributions downstream to larger water bodies. It is unclear, however, whether larger streams function simply as dispersal corridors connecting headwater subpopulations, or as critical foraging habitat needed to sustain large mobile brook trout. Stable isotopes (δ¹³C and δ¹⁵N) and a hierarchical Bayesian mixing model analysis was used to identify brook trout that foraged in main stem versus headwater streams of the Shavers Fork watershed, West Virginia. Headwater subpopulations were composed of headwater and to a lesser extent main stem foraging individuals. However, there was a strong relationship between brook trout size and main stem prey contributions. The average brook trout foraging on headwater prey were limited to 126 mm standard length. This size was identified by mixing models as a point where productivity support switched from headwater to main stem dependency. These results, similar to other studies conducted in this watershed, support the hypothesis that productive main stem habitat maintain large brook trout and potentially facilitates dispersal among headwater subpopulations. Consequently, loss of supplementary main stem foraging habitats may explain loss of large, mobile fish and subsequent isolation of headwater subpopulations in other central Appalachian watersheds.     

Predator–prey naïveté, antipredator behavior,and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non‐consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non‐native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non‐native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non‐consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non‐native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter‐related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non‐native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non‐native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.     

Do Low-Mercury Terrestrial Resources Subsidize Low-Mercury Growth of Stream Fish? Differences between Species along a Productivity Gradient

Low productivity in aquatic ecosystems is associated with reduced individual growth of fish and increased concentrations of methylmercury (MeHg) in fish and their prey. However, many stream-dwelling fish species can use terrestrially-derived food resources, potentially subsidizing growth at low-productivity sites, and, because terrestrial resources have lower MeHg concentrations than aquatic resources, preventing an increase in diet-borne MeHg accumulation. We used a large-scale field study to evaluate relationships among terrestrial subsidy use, growth, and MeHg concentrations in two stream-dwelling fish species across an in-stream productivity gradient. We sampled young-of-the-year brook trout (Salvelinus fontinalis) and Atlantic salmon (Salmo salar), potential competitors with similar foraging habits, from 20 study sites in streams in New Hampshire and Massachusetts that encompassed a wide range of aquatic prey biomass. Stable isotope analysis showed that brook trout used more terrestrial resources than Atlantic salmon. Over their first growing season, Atlantic salmon tended to grow larger than brook trout at sites with high aquatic prey biomass, but brook grew two-fold larger than Atlantic salmon at sites with low aquatic prey biomass. The MeHg concentrations of brook trout and Atlantic salmon were similar at sites with high aquatic prey biomass and the MeHg concentrations of both species increased at sites with low prey biomass and high MeHg in aquatic prey. However, brook trout had three-fold lower MeHg concentrations than Atlantic salmon at low-productivity, high-MeHg sites. These results suggest that differential use of terrestrial resource subsidies reversed the growth asymmetry between potential competitors across a productivity gradient and, for one species, moderated the effect of low in-stream productivity on MeHg accumulation.     

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.     

Generalization of learned predator recognition: an experimental test and framework for future studies

While some prey species possess an innate recognition of their predators, others require learning to recognize their predators. The specific characteristics of the predators that prey learn and whether prey can generalize this learning to similar predatory threats have been virtually ignored. Here, we investigated whether fathead minnows that learned to chemically recognize a specific predator species as a threat has the ability to generalize their recognition to closely related predators. We found that minnows trained to recognize the odour of a lake trout as a threat (the reference predator) generalized their responses to brook trout (same genus as lake trout) and rainbow trout (same family), but did not generalize to a distantly related predatory pike or non-predatory suckers. We also found that the intensity of antipredator responses to the other species was correlated with the phylogenetic distance to the reference predator; minnows responded with a higher intensity response to brook trout than rainbow trout. This is the first study showing that prey have the ability to exhibit generalization of predator odour recognition. We discuss these results and provide a theoretical framework for future studies of generalization of predator recognition.     

First Documentation of Cultural Transmission of Predator Recognition by Larval Amphibians

Predation is a pervasive selective agent shaping a prey's behaviour, morphology and life history. To survive, prey animals have to respond adaptively to predation threats and this can be achieved through learned predator recognition. Cultural transmission of predator recognition is likely a widespread means of learning in social animals, including mammals, birds and fishes. However, no studies have investigated the cultural transmission of predator recognition in amphibians. In our study, we examined whether naïve woodfrog (Rana sylvatica) tadpoles can acquire the recognition of the odour of a predatory tiger salamander (Ambystoma tigrinum) from experienced conspecifics. After conditioning some tutors to recognize salamander odour, we paired naïve observer tadpoles with either a salamander‐naïve or salamander‐experienced tutor and exposed the pairs to either salamander odour or a water control. Observers were subsequently tested alone for a response to salamander odour. We found that when given salamander odour, observer tadpoles that were paired with a salamander‐experienced tutor successfully learned to recognize the salamander odour as a threat, whereas the observers paired with salamander‐naïve tutors did not. Likewise, tadpoles exposed to the water control did not learn to recognize the salamander regardless of whether they were paired with a naïve or experienced tutor. This is the first study demonstrating cultural transmission of predator recognition in an amphibian species.     

Trout affect the density, activity and feeding of a larval plethodontid salamander

1. Ecologists have struggled to describe general patterns in the impacts of predators on stream prey, particularly at large, realistic spatial and temporal scales. Among the confounding variables in many systems is the presence of multiple predators whose interactions can be complex and unpredictable. 2. We studied the interactions between brook trout (Salvelinus fontinalis) and larval two‐lined salamanders (Eurycea bislineata), two dominant vertebrate predators in New England stream systems, by examining patterns of two‐lined salamander abundance in stream reaches above and below waterfalls that are barriers to fish dispersal, by measuring the effects of trout on salamander density and activity using a large‐scale manipulation of brook trout presence, and by conducting a small‐scale laboratory experiment to study how brook trout and larval two‐lined salamanders affect each other's prey consumption. 3. We captured more salamanders above waterfalls, in the absence of trout, than below waterfalls where trout were present. Salamander density and daytime activity decreased following trout addition to streams, and salamander activity shifted from aperiodic to more nocturnal with fish. Analysis of stomach contents from our laboratory experiment revealed that salamanders eat fewer prey with trout, but trout eat more prey in the presence of salamanders. 4. We suggest that as predators in streams, salamanders can influence invertebrate prey communities both directly and through density‐ and trait‐mediated interactions with other predators.     

Non‐native trout limit native brook trout access to space and thermal refugia in a restored large‐river system

We used direct observation via snorkeling surveys to quantify microhabitat use by native brook (Salvelinus fontinalis) and non‐native brown (Salmo trutta) and rainbow (Onchorynchus mykiss) trout occupying natural and restored pool habitats within a large, high‐elevation Appalachian river, United States. Permutational multivariate analysis of variance (PERMANOVA) and subsequent two‐way analysis of variance (ANOVA) indicated a significant difference in microhabitat use by brook and non‐native trout within restored pools. We also detected a significant difference in microhabitat use by brook trout occupying pools in allopatry versus those occupying pools in sympatry with non‐native trout—a pattern that appears to be modulated by size. Smaller brook trout often occupied pools in the absence of non‐native species, where they used shallower and faster focal habitats. Larger brook trout occupied pools with, and utilized similar focal habitats (i.e. deeper, slower velocity) as, non‐native trout. Non‐native trout consistently occupied more thermally suitable microhabitats closer to cover as compared to brook trout, including the use of thermal refugia (i.e. ambient–focal temperature >2°C). These results suggest that non‐native trout influence brook trout use of restored habitats by: (1) displacing smaller brook trout from restored pools, and (2) displacing small and large brook trout from optimal microhabitats (cooler, deeper, and lower velocity). Consequently, benefits of habitat restoration in large rivers may only be fully realized by brook trout in the absence of non‐native species. Future research within this and other large river systems should characterize brook trout response to stream restoration following removal of non‐native species.     

Cytogenetic identification of genomic elements of brook trout (Salvelinus fontinalis) in the karyotype of Arctic char (Salvelinus alpinus) from the aquaculture broodstock

Growing interest of Arctic char (Salvelinus alpinus) aquaculture in Europe, and the fact that it can easily hybridize with brook trout (Salvelinus fontinalis) resulting in fertile progeny, led us to investigate fish from the farmed stocks. Chromosomes of sampled Arctic char were examined using conventional and molecular cytogenetic (FISH) techniques in order to determine possible contamination of genomic elements of brook trout. Investigated fish possessed karyotypes composed of 80–82 chromosomes and up to three chromosome fragments. Using staining methods and FISH approach enabled identification of the brook trout chromosomes in the eight out of twenty‐two examined Arctic char. Specific location of AT‐, GC‐ positive and NOR sites observed on chromosomes as well as chromosome fragments in the karyotypes of several individuals points on past chromosomal rearrangements in fish from examined broodstock. Based on our results, it may be assumed that individuals with the brook trout genomic elements, although phenotypically identified as Arctic chars, were hybrids. Our results highlights that special care should be taken to protect gene pools of brook trout and Arctic char in farms where both species are cultured.