Sound the alarm: learned association of predation risk with novel auditory stimuli by fathead minnows ( Pimephales promelas ) and glowlight tetras ( Hemigrammus erythrozonus ) after single simultaneous pairings with conspecific chemical alarm cues

Fathead minnows, Pimephales promelas, and glowlight tetras, Hemigrammus erythrozonus, were tested for their ability to associate predation risk with novel auditory stimuli after auditory stimuli were presented simultaneously with chemical alarm cues. Minnows and tetras gave a fright response when exposed to skin extract (alarm cue) and an artificial auditory sound stimulus, but no response to water (control) and sound, indicating that they did not have a pre-existing aversion to the auditory stimulus. When retested with sound stimuli alone, minnows and glowlight tetras that had previously been conditioned with water and sound showed no response, but those that had been conditioned with alarm cues and sound exhibited antipredator behaviour (reduced activity) in response to the auditory cue. This is the first known demonstration of learned association of an auditory cue with predation risk, and raises questions about the role of sound in mediating predator-prey interactions in fishes.     

Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish

Individuals that dare approach predators (predator inspection behaviour) may benefit by acquiring information regarding the potential threat of predation. Although information acquisition based on visual cues has been demonstrated for fish, it is unknown whether fish will inspect predators on the basis of chemical cues or whether such inspection behaviour results in information acquisition. Here, we first ascertained whether predator inspection behaviour can be mediated by chemical cues from predators by exposing groups of predator-naive glowlight tetras (Hemigrammus erythrozonus) to the chemical cues of a potential fish predator (convict cichlid Cichlasoma nigrofasciatum) that had been fed either tetras (which possess an alarm pheromone) or swordtails (Xiphophorus helleri, which lack Ostariophysan alarm pheromones). Tetras showed a significant increase in antipredator behaviour when exposed to the tetra-diet cue, but not when exposed to the swordtail-diet cue. Chemically mediated predator inspection behaviour was also affected. Both the latency to inspect and the minimum approach distance to the predator significantly increased, and the mean number of inspectors per predator inspection visit significantly decreased when tetras were exposed to the tetra-diet versus the swordtail-diet chemical cues. We then examined a potential benefit associated with chemically mediated predator inspection behaviour. Only tetras that were initially exposed to the tetra-diet cue and that had inspected the predator acquired the visual recognition of a convict cichlid as a predation threat. Our results thus demonstrate that (1) predator inspection behaviour in the glowlight tetra can be initiated by chemical cues, (2) chemically mediated inspection behaviour is affected by the presence of alarm pheromone, and (3) inspectors benefit by acquiring the recognition of novel predators. Copyright 1999 The Association for the Study of Animal Behaviour.     

Learned Recognition of Novel Predator Odour by Zebra Danios, Danio Rerio, Following Time-shifted Presentation of Alarm Cue And Predator Odour

Fishes in the superorder ostariophysi possess specialized epidermal cells that contain an alarm cue. Fish associate novel odours, such as the odour of a predator, with predation risk after a single, simultaneous exposure to the novel odour and alarm cue. Thereafter, the novel cue is recognized as an indicator of risk and its presence induces antipredator behaviour. Two common antipredator behaviours are reduction in activity and movement to the bottom. This phenomenon has been demonstrated many times in the laboratory setting for a variety of aquatic taxa. In nature however, the detection of novel predator odour may be time-shifted with respect to the detection of alarm cues. Is there a critical period immediately upon the detection of alarm cue in which associative learning can occur? We presented zebra danios, Danio rerio, with the odour of northern pike, Esox lucius, 5?min after presenting them with either alarm cue or water (control). During a predation event, 5?min is a long time. When later retested with pike odour alone, zebra fish conditioned with alarm cue significantly increased antipredator behaviour in terms of decreased activity and movement towards the bottom. Control fish did not recognize pike odour as dangerous when retested. These data show that learned recognition of predation risk is sufficiently robust to accommodate ecologically realistic temporal shifts in stimulus presentation.     

Physiological responses of topmouth gudgeon, <Emphasis Type="Italic">Pseudorasbora parva</Emphasis>, to predator cues and variation of current velocity

Predators, either through direct or indirect encounter and current velocity, are frequently stressful to fish living in stream waters. In nature, fish may experience both current velocity stress and predation danger simultaneously. Experiments were carried out to clarify to what extent predation risk (with reference to different types of predatory cues) and current velocity can induce physiological stress in a running-water dwelling fish, topmouth gudgeon (Pseudorasbora parva). Fish were exposed to an alarm substance, predator odor, and visual cue, as well to combinations of predation risk and elevated current velocities. Metabolic rate, ventilation rate and fish activity were measured. Results showed that irrespective of the type of encounter, the presence of predator imposed physiological stress on fish. Metabolic rate were 0.983 ± 0.312, 0.641 ± 0.151, 0.572 ± 0.063, and 0.277 ± 0.016 mg O₂ W⁻¹ h⁻¹ following presence of alarm substance, visual cue, predator odor and control, respectively. Dramatic changes in ventilation rate and activity affirmed that alarm substance induced the strongest stress, followed by predator odor and visual cue. Reactions appeared to mirror the extent of fish perceiving danger of predation. Predation risk together with current velocity induces stronger stress, much stronger than if the current velocity works as a single stressor. However, the interaction between predation risk and current velocity did not have a significant effect on metabolic function; magnitude of metabolic response to high current velocity might mask the metabolic response to predator presence. Small fish living in stream habitats that face local predation risk would spend higher energy expenditure that may have negative impacts on growth, and hence their fitness.     

Paternal effects in a wild‐type zebrafish implicate a role of sperm‐derived small RNAs

While the importance of maternal effects has long been appreciated, a growing body of evidence now points to the paternal environment having an important influence on offspring phenotype. Indeed, research on rodent models suggests that paternal stress leaves an imprint on the behaviour and physiology of offspring via nongenetic information carried in the spermatozoa; however, fish have been understudied with regard to these sperm‐mediated effects. Here, we investigated whether the zebrafish was subjected to heritable influences of paternal stress by exposing males to stressors (conspecific‐derived alarm cue, chasing and bright light) before mating and assessing the behavioural and endocrine responses of their offspring, including their behavioural response to conspecific‐derived alarm cue. We found that after males are exposed to stress, their larval offspring show weakened responses to stressors. Small RNA sequencing subsequently revealed that the levels of several small noncoding RNAs, including microRNAs, PIWI‐interacting RNAs and tRNA‐derived small RNAs, were altered in the spermatozoa of stressed fathers, suggesting that stress‐induced alterations to the spermatozoal RNA landscape may contribute to shaping offspring phenotype. The work demonstrates that paternal stress should not be overlooked as a source of phenotypic variation and that spermatozoal small RNAs may be important intergenerational messengers in fish.     

Differential responses to predator cues between two mosquito species breeding in different habitats

1. Natural selection favours females who can correctly assess the predation risk and hence avoid high‐risk oviposition sites and reduce the mortality rate of their offspring. In spite of the potential significance of such behaviour, relatively few studies have assessed the relationship between oviposition behaviour and predation risk. 2. The present study aimed to determine the sublethal effects of predators on oviposition site selection by gravid females, the foraging activity of larvae, and the life history traits of two mosquito species that breed in different habitats, Aedes albopictus Skuse (container breeder) and Culex tritaeniorhynchus Giles (wetland breeder). 3. Female C. tritaeniorhynchus avoided laying eggs at oviposition sites in the presence of a predator cue. In contrast, female A. albopictus laid eggs in both the absence and presence of the predator cue. 4. To examine the effects of predator cues on larval behaviour, experiments were conducted in the absence and presence of a predator cue. Although larval activity was lower in the presence of the predator cue than that in its absence in both species, C. tritaeniorhynchus responded to the predator cue more strongly than A. albopictus. Female A. albopictus that had been reared with caged predators exhibited an extended larval development period, whereas the adult C. tritaeniorhynchus reared in the presence of predators were smaller than those reared in their absence. 5. This finding might explain why C. tritaeniorhynchus avoid laying eggs in predator‐conditioned water, for example to increase the fitness of their offspring, but A. albopictus either cannot detect predator cues or are not sensitive to them.     

Conspecific alarm cue sensitivity by the estuarine calanoid copepod,Paracartia longipatella

Sensitivity to chemical cues associated with predation threat has been well observed in many freshwater zooplankters, yet few studies have highlighted such sensitivity in eury‐ and stenohaline metazoans. We aimed to assess sensitivity to conspecific chemical alarm cues in the estuarine copepod, Paracartia longipatella. Alarm cues associated with predation have been shown to have population level effects on certain zooplanktonic species. As such, we assessed the occurrence of such effects on population dynamics of P. longipatella over a 12 day period. Using experimental in situ mesocosms, we compared P. longipatella adult, copepodite and nauplii numbers between three treatments; one inoculated with conspecific alarm cues, one containing direct predation pressure (zooplanktivorous fish), and a control treatment containing no predation threat. Trends in population abundances were similar between the direct predation and alarm cue treatments for the six days of the experiment, decreasing in abundance. During the latter half of the study, however, P. longipatella abundances in the alarm cue treatment increased, while those in the presence of direct predation continued to decrease. In the treatment absent of any predation threat, P. longipatella abundances increased consistently over time for the duration of the study. We suggest that P. longipatella are indeed sensitive to conspecific alarm cues associated with predation threat. Furthermore, we propose that prolonged exposure to conspecific alarm cues in the absence of any real threat results in a reduction in sensitive to these cues.     

Anti-predator behaviour in response to conspecific chemical alarm cues in an esociform fish, <Emphasis Type="Italic">Umbra limi</Emphasis> (Kirtland 1840)

When a predators attack prey, damaged prey tissue releases chemical information that reliably indicates an actively foraging predator. Prey use these semiochemicals to cue anti-predator behaviour and reduce their probability of predation. Here, we test central mudminnows, Umbra limi (Kirtland 1840), for anti-predator behavioural responses to chemical cues in conspecific skin extract. In a field experiment, traps scented with mudminnow skin extract (alarm cue) caught fewer mudminnows than traps scented with water (control). Under controlled laboratory conditions, mudminnows showed a significant reduction in activity and movement to the bottom in response to alarm cues relative to water controls. Reduced activity and increased time on the bottom of the tank are both known components of an anti-predator response. Thus, based on field and lab data, mudminnows exhibited anti-predator behavioural responses to chemical alarm cues released by damaged epidermal tissue. Histological preparations of epidermal tissue did not reveal the presence of specialised “alarm substance” cells for the production of chemical alarm cues. This is the first report of an alarm reaction in an esociform, an order with a long evolutionary history of piscivory.     

Predator Inspection Behaviour in a Characin Fish: an Interaction between Chemical and Visual Information?

Recent evidence suggests that predator inspection behaviour by Ostariophysan prey fishes is regulated by both the chemical and visual cues of potential predators. In laboratory trials, we assessed the relative importance of chemical and visual information during inspection visits by varying both ambient light (visual cues) and predator odour (chemical cues) in a 2 × 2 experimental design. Shoals of glowlight tetras (Hemigrammus erythrozonus) were exposed to a live convict cichlid (Archocentrus nigrofasciatus) predator under low (3 lux) or high (50 lux) light levels and in the presence of the odour of a cichild fed tetras (with an alarm cue) or swordtails (Xiphophorus helleri, with an alarm cue not recognized by tetras). Tetras exhibited threat‐sensitive inspection behaviour (increased latency to inspect, reduced frequency of inspection, smaller inspecting group sizes and increased minimum approach distance) towards a predator paired with a tetra‐fed diet cue, regardless of light levels. Similar threat‐sensitive inspection patterns were observed towards cichlids paired with a swordtail‐fed diet cue only under high light conditions. Our data suggest that chemical cues in the form of prey alarm cues in the diet of the predator, are the primary source of information regarding local predation risk during inspection behaviour, and that visual cues are used when chemical information is unavailable or ambiguous.     

Detection of conspecific alarm cues by juvenile salmonids under neutral and weakly acidic conditions: laboratory and field tests

A variety of fishes possess damage-released chemical alarm cues, which play a critical role in the detection and avoidance of potential predation threats. Recently, we have demonstrated that the ability of fathead minnows (Pimephales promelas) and finescale dace (Phoxinus neogaeus) to detect and respond to conspecific alarm cues is significantly reduced under weakly acidic conditions (pH 6.0). Rainbow trout (Oncorhynchus mykiss) and brook charr (Salvelinus fontinalis) possess an analogous alarm cue system. However, it is unknown if the trout alarm cue system is likewise affected by relatively small changes in pH. In addition, previous studies have not verified this phenomenon under natural conditions. We conducted laboratory and field trials to examine the potential effects of acute exposure to weakly acidic (pH 6.0) conditions on the detection and response of conspecific alarm cues by juvenile trout. Our laboratory results demonstrate that while juvenile rainbow trout exhibit significant increases in antipredator behaviour under normal pH conditions (pH 7.0–7.2), they do not respond to the presence of conspecific chemical alarm cues (i.e. response is not different from controls) under weakly acidic conditions. Similarly, a wild strain of brook charr in their natural streams near Sudbury, Ontario, failed to detect conspecific alarm cues in a weakly acidic stream (mean pH 6.11) while they responded to these cues in a neutral stream (mean pH of 6.88). This is the first demonstration that relatively small changes in ambient pH can influence alarm responses under natural conditions. These data suggest significant, sub-lethal effects of acid precipitation on natural waterways.     

The ontogeny of chemically mediated antipredator responses of fathead minnows Pimephales promelas

The antipredator responses of adult and larval fathead minnows Pimephales promelas to chemical alarm cues prepared throughout ontogeny were tested using various behavioural assays. Larval epidermis was also examined during ontogeny using standard haematoxylin and eosin staining techniques. Adults elicited an antipredator response to chemical alarm cue made from larvae as young as 8–17 days post‐hatch. Interestingly, larvae did not possess visible club cells until 28–37 days post‐hatch and did not respond to conspecific chemical alarm cue until 48–57 days post‐hatch. These results suggest that chemical alarm cue may not be contained within club cells and that the components of larval and adult chemical alarm cue may be similar throughout ontogeny.     

Maternal predator‐exposure affects offspring size at birth but not telomere length in a live‐bearing fish

The perception of predation risk could affect prey phenotype both within and between generations (via parental effects). The response to predation risk could involve modifications in physiology, morphology, and behavior and can ultimately affect long‐term fitness. Among the possible modifications mediated by the exposure to predation risk, telomere length could be a proxy for investigating the response to predation risk both within and between generations, as telomeres can be significantly affected by environmental stress. Maternal exposure to the perception of predation risk can affect a variety of offspring traits but the effect on offspring telomere length has never been experimentally tested. Using a live‐bearing fish, the guppy (Poecilia reticulata), we tested if the perceived risk of predation could affect the telomere length of adult females directly and that of their offspring with a balanced experimental setup that allowed us to control for both maternal and paternal contribution. We exposed female guppies to the perception of predation risk during gestation using a combination of both visual and chemical cues and we then measured female telomere length after the exposure period. Maternal effects mediated by the exposure to predation risk were measured on offspring telomere length and body size at birth. Contrary to our predictions, we did not find a significant effect of predation‐exposure neither on female nor on offspring telomere length, but females exposed to predation risk produced smaller offspring at birth. We discuss the possible explanations for our findings and advocate for further research on telomere dynamics in ectotherms.     

Direct Exposure to Corticosterone During Embryonic Development Influences Behaviour in an Ovoviviparous Lizard

It is becoming increasingly clear that conditions experienced during embryonic development can be of major importance for traits subsequent to parturition or hatching. For example, in mammals, offspring from stressed mothers show a variety of changes in behavioural, morphological, and life‐history traits. The effects of maternal stress on trait development are believed to be mediated via transfer of glucocorticoids, the main hormones released during the stress response, from mother to offspring. However, also other physiological maternal responses during stress could be responsible for changes in offspring phenotype. We investigated the direct effects of corticosterone on offspring development, without other confounding factors related to increased maternal stress, by injection of corticosterone in eggs of the ovoviviparous lizard Lacerta vivipara. Corticosterone‐manipulated offspring did not show impaired development, reduced body size or body condition at parturition. However, corticosterone‐treated offspring showed altered anti‐predator behaviour, as measured by the time required to emerge from shelter after a simulated predator attack. Differential steroid exposure during development, possibly mediated by maternal stress response, may explain some of the variation in behaviour among individuals in natural populations.     

Predator Recognition and Learned Irrelevance in the Crayfish Orconectes virilis

When individuals of the crayfish Orconectes virilis detect an unlearned danger cue (alarm odor) and a novel cue (goldfish odor) at the same time, they form a learned association and behave as if the novel cue is associated with increased predation risk ( Hazlett et al. 2002 ). This study examined the potential for learned irrelevance in O. virilis and the circumstances under which blockage of the formation of a learned association could occur. If individuals experience a random pattern of alarm odor and goldfish odor over the days prior to the simultaneous detection of those two cues, no learned association is formed (= learned irrelevance). That is, there is no inhibition of responses to a food cue when goldfish odor is added if the crayfish has experienced a random pattern of the two cues. Learning was eliminated if the random pattern of cues was experienced before or after the simultaneous detection. To present the two cues (alarm and goldfish odors) to crayfish independently on separate days, the water containing goldfish odor had to be removed from the aquaria as the odor persisted at least 24 h. The importance of the learned irrelevance phenomenon on predator–prey interactions is discussed.     

The Dilution Effect and Differential Predation Following Brood Adoption in Free-ranging Convict Cichlids (Cichlasoma nigrofasciatum)

Parental investment in unrelated offspring is potentially maladaptive but may be promoted by natural selection if the presence of foreign young enhances the survival of the parents' own young. We experimentally augmented broods of free-ranging convict cichlids (Cichlasoma nigrofasciatum) to test whether survival of the adopting parents' young (fry) increases, in relation to that of control broods, after the addition of smaller foreign fry, and whether such an increase can be attributed to the effect of brood dilution acting alone or to a combination of brood dilution and the effect of differential predation on adopted young. Total fry survival did not differ between experimental (E) broods and control (C) broods, but E broods had significantly more large (host) fry after 5 days and 10 days than C broods did. In E broods, small (foreign) fry suffered higher rates of predation than large fry, indicating differential predation. In E broods starting at 7.0 and 7.5 mm standard length (SL), observed fry mortalities did not differ significantly from mortalities expected from the effect of brood dilution. However, E broods starting at 8.0 mm SL had significantly lower mortalities than expected, indicating that parents that adopt smaller foreign fry can increase the survival of their own fry by the combined effects of brood dilution and differential predation. Within E broods, growth of smaller foreign fry was significantly slower than that of larger host fry, suggesting that intra-brood agonistic behaviour affects access to food for smaller fry. Therefore, increased predation and reduced growth are two negative effects that act on fry of donor parents.     

The demographic and life‐history costs of fear: Trait‐mediated effects of threat of predation on Aedes triseriatus

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Brief communication: Prenatal and early postnatal stress exposure influences long bone length in adult rat offspring

Stress during the prenatal and early postnatal periods (perinatal stress, PS) is known to impact offspring cognitive, behavioral, and physical development, but effects on skeletal growth are not clear. Our objective was to analyze effects of variable, mild, daily PS exposure on adult offspring long bone length. Twelve pregnant rat dams were randomly assigned to receive variable stress from gestational days 14–21 (Prenatal group), postpartum days 2–9 (Postnatal), both periods (Pre–Post), or no stress (Control). Differences in adult offspring tibia and femur length were analyzed among treatment groups. Mean tibia length differed among groups for males (P = 0.016) and females (P = 0.009), and differences for femur length approached significance for males (P = 0.051). Long bone length was shorter among PS‐exposed offspring, especially those exposed to postnatal stress (Postnatal and Pre–Post groups). Results persisted when controlling for nose–tail length. These differences might reflect early stunting that is maintained in adulthood, or delayed growth among PS‐exposed offspring. This study suggests that PS results in shorter long bones in adulthood, independently of effects on overall body size. Stunting and growth retardation are major global health burdens. Our study adds to a growing body of evidence suggesting that PS is a risk factor for poor linear growth. Am J Phys Anthropol 149:307–311, 2012. © 2012 Wiley Periodicals, Inc.     

Predator-induced changes in morphology of a prey fish: the effects of food level and temporal frequency of predation risk

In a series of experiments, we investigated the effects of food availability and risk frequency on the dynamics of predator-induced changes in growth and morphology of prey fish using goldfish (Carassius auratus) as our test species. In experiment 1, we fed goldfish high or low food rations and exposed them to either alarm cues from conspecifics, cues from swordtails or a water control. After 60 days, goldfish in the alarm cue treatment significantly increased their body depth and body weight but had smaller body length than goldfish exposed to swordtails cues or water, likely reducing their vulnerability to gape-limited predators. Importantly, food level had an impact on the amplitude of the morphological changes. In experiment 2, goldfish were exposed to two different frequencies of predation cues or a water control for 50 days. The cues were either continued or discontinued from day 51 to 100, and all cues were resumed from day 101 to 150. We found that goldfish exposed to predation cues increased their depth and weight at a faster rate than did the goldfish exposed to water, and of particular significance was the fact that frequency of risk had an effect on the amplitude of the change. When the cues were interrupted, the increase in growth rate parameters was reduced to the level of the goldfish exposed to water. However, when the cues were resumed, the rate increased to match the growth rate of the goldfish that were continuously exposed to the cues. Finally, we staged encounters between goldfish of differing morphologies and yellow perch (Perca flavescens) and found that deep-bodied goldfish had better survival than the shallow-bodied ones. These experiments illustrate the dynamic nature of inducible morphological defences.     

Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring

There is growing evidence that maternal experience influences offspring via non-genetic mechanisms. When female three-spined sticklebacks (Gasterosteus aculeatus) were exposed to the threat of predation, they produced larger eggs with higher cortisol content, which consumed more oxygen shortly after fertilization compared with a control group. As juveniles, the offspring of predator-exposed mothers exhibited tighter shoaling behaviour, an antipredator defence. We did not detect an effect of maternal exposure to predation risk on the somatic growth of fry. Altogether, we found that exposure to an ecologically relevant stressor during egg formation had several long-lasting consequences for offspring, some of which might be mediated by exposure to maternally derived cortisol. These results support the hypothesis that female sticklebacks might influence the development, growth and behaviour of their offspring via eggs to match their future environment.     

Olfactorily-mediated cortisol response to chemical alarm cues in zebrafish Danio rerio

Chemical cues released as a by-product of predation mediate antipredator behaviour, but little is known about the physiological responses to olfactory detection of predation risk. In this study, zebrafish Danio rerio were exposed to either chemical alarm cues from conspecifics, or water (control). Compared with water controls, D. rerio exposed to alarm cues responded behaviourally with antipredator behaviours such as erratic dashing and an increase in time spent near the bottom of the test aquarium. Danio rerio were sacrificed 5 min after exposure to test cues (alarm cues or water). Enzyme-linked immunosorbent assay (ELISA) revealed whole-body levels of cortisol that were significantly higher for fish exposed to alarm cues (mean ± SE, 11.9 ± 3.4 ng g⁻¹) than control fish (1.5 ± 0.7 ng g⁻¹). These data provide a benchmark for future studies of the proximate mechanisms of olfactorily mediated antipredator responses, modelling effects on aquatic life in a changing climate and, as a model organism, Danio rerio can further our understanding of anxiety in humans.