Conspecific Alarm Cues Research Articles

Speed kills? Migrating sea lamprey increase speed when exposed to an antipredator cue but make worse short-term decisions

There is growing evidence that a natural repellent, injury-released alarm cues, can be used to guide the movements of invasive fishes to achieve management goals. However, because this process involves perception, downstream cognitive processing of sensory information affects decisions regarding expression of antipredator behavior. Response habituation, wherein repeated or continuous exposure to a cue reduces behavioral response rates, is an oft-cited challenge for use of predation cues as conservation tools. Habituation may be delayed or prevented by altering the concentration and/or the temporal pattern of odor release (pulses of odor vs continuous application). We examined the effects of varying odor concentration and exposure regime (continuous vs pulsed) on behavioral response of adult sea lamprey (Petromyzon marinus) to conspecific alarm cue in a two-choice maze. We found that exposure to alarm cue induced more frequent and rapid upstream movement, regardless of exposure regime. There was also clear evidence of a speed-accuracy tradeoff, wherein sea lamprey that took longer to arrive at the bifurcation in the maze were more likely to avoid the arm activated with alarm cue. We could not ascertain the value of increasing concentration or pulsing the alarm cue on preventing habituation, as habituation did not occur. We hypothesize dishabituation to the alarm cue occurred immediately prior to testing due to handling that may have inadvertently simulated an unsuccessful predator attack. If true, incorporating dishabituating stimuli may prove a useful means to maintain the efficacy of alarm cue when applied as a repellent to manipulate the movements of sea lamprey.

Yellowtail damselfish Chrysiptera parasema can associate predation risk with the acoustic call of a heterospecific damselfish following pairing with conspecific alarm cues.

The ability to detect and respond to the presence of predation risk is under intense selection, especially for small-bodied fishes. Damselfishes (Pomacentridae) use auditory vocalizations during inter- and intrasexual interactions, but it is not known if they can use vocalizations in the context of predator-prey interactions. Here, we test if yellowtail damselfish, Chrysiptera parasema, can learn to associate the territorial vocalization of heterospecific humbug damselfish Dascyllus aruanus with predation risk. In conditioning trials yellowtail damselfish were presented with the territorial call of humbug damselfish while either blank water (control treatment) or chemical alarm cue derived from damaged skin of conspecific yellowtail damselfish was introduced. In conditioning trials, fish exposed to alarm cue exhibited increased activity and spent more time in the water column relative to fish that received the control treatment. After a single conditioning trial, conditioned fish were exposed again to the territorial call of humbug damselfish. Fish conditioned with the call + alarm cue showed increased activity and spent more time in the water column relative to fish that had been conditioned with the control treatment. These data indicate associative learning of an auditory stimulus with predation risk in a species that regularly uses auditory signalling in other contexts. Recordings of conditioning and test trials failed to detect any acoustic calls produced by test fish in response to the perception of predation risk. Thus, although yellowtail damselfish can associate risk with auditory stimuli, we found no evidence that they produce an alarm call.

Is thermal sensitivity affected by predation risk? A case study in tadpoles from ephemeral environments.

Changes in environmental temperature may induce variations in thermal tolerance and sensitivity in ectotherm organisms. These variations generate plastic responses that can be analyzed by examining their Thermal Performance Curves (TPCs). Additionally, some performance traits, like locomotion, could be affected by other factors such as biological interactions (e.g., predator-prey interaction). Here, we evaluate if the risk of predation modifies TPCs in Mendoza four-eyed frog (Pleurodema nebulosum, Burmeister, 1861) and Guayapa's four-eyed frog (Pleurodema guayapae, Barrio, 1964), two amphibian species that occur in ephemeral ponds in arid environments. We measured thermal tolerances and maximum swimming velocity at six different temperatures in tadpoles under three situations: control, exposure to predator chemical cues, and exposure to conspecific alarm cues. TPCs were fitted using General Additive Mixed Models. We found that curves of tadpoles at risk of predation differed from those of control mainly in thermal sensitivity parameters. Our work confirms the importance of biotic interactions have in thermal physiology.

Temperature during embryonic development in brown trout influences juvenile behaviour in encounters with predators

AbstractVariation in thermal conditions during embryogenesis can have far‐reaching impact throughout ontogeny and may give rise to behavioural variation. Many animals, such as salmonids, exhibit behavioural trade‐offs related to foraging and predator avoidance. How embryonic temperature affects these behaviours has remained unexplored. Not only abiotic conditions during embryogenesis but also biotic factors such as predator conditioning may affect fish behaviour, especially anti‐predator responses. We examined how elevated temperatures and predator odours throughout embryogenesis affect the behaviour of 28–37 mm young‐of‐the‐year brown trout (Salmo trutta) in encounters with predators, namely Atlantic salmon (Salmo salar; 20 cm) and burbot (Lota lota; 40 cm). Juvenile brown trout were more active and aggressive if they were incubated in warmer water as eggs than if they were incubated in colder water, and trout remained inactive longer when encountering predators if they were cold incubated. Brown trout were less active and aggressive when an Atlantic salmon was present than when a burbot or no predator was present. Behavioural responses did not differ between trout that had been subjected to water with versus without predator odours during embryogenesis, possibly because brown trout were not subjected to conspecific alarm cues during egg incubation. This study shows that thermal conditions during embryogenesis can influence fish behaviour early in life and thus contribute to behavioural variation, with potential effects on life history. Considering the rapid warming of northern regions, elevated embryonic temperatures may contribute substantially to variation in salmonid behaviour in the near future.

Transgenerational plasticity of exploratory behavior and a hidden cost of mismatched risk environments between parental sexes

We require a better understanding of the relative contribution of different modes of non-genetic inheritance in behavioral trait development. Thus, we investigate variation in exploratory behavior, which is ecologically relevant and a target of selection. The metabolic hypothesis predicts exploratory behavior to be size-dependent across taxa. This size-dependency is cancelled out under high perceived risk, allowing us to determine the transgenerationally integrated estimated level of risk. Using fathead minnows Pimephales promelas, we manipulated perceived risk in mothers, fathers, caring males and offspring through continuous exposure to either conspecific alarm cues or to a control water treatment. In 1000 four-month old offspring, we determined body sizes and exploratory behavior. Perceived high risk in mothers, followed by personal risk, was most effective in eliminating size-dependent behavior whereas effects of paternal risk on offspring behavioral development were substantially weaker. When maternal risk is high, environmental mismatches between parents prevented offspring from responding appropriately to personal high risk. The environment of the caring male also impacted offspring behavior to a greater extent than that of its genetic parents. Our study highlights the high relative importance of maternal, personal and caring male risk environments and showcases potential costs of an environmental mismatch between parental sexes.

Carbon nanofibers caused oxidative stress and disrupted anti-predator responses in common spiny loach

Carbon nanofibers, recently recognized pollutants, have been heavily used among the nanomaterials in many industries. Due to the poor suspension-stability, carbon nanofibers tend to sediment at the bottom of waterbodies and hence can be consumed by the bottom-dwellers. The current investigation evaluates the impact of carbon nanofibers at concentrations between 0.1 and 10 mg L−1 on the common bottom dweller spiny loach Lepidocephalichthys thermalis inhabiting Indian rivers. Carbon nanofiber exposure elevated the activities of the hepatic antioxidant enzymes superoxide dismutase, catalase, peroxidase and glutathione S-transferase, as oxidative stress markers. The fish behaviour patterns were examined by testing the effect of carbon nanofibers on predator recognition ability using kairomones, conspecific alarm cues, and dietary cues. The carbon nanofiber-exposed fish showed a loss of predator-recognition abilities. The results collectively demonstrated the carbon nanofiber driven hepatic oxidative damage and impaired predator-recognition ability in L. thermalis. The investigation, first of its kind, highlights the toxic potential of the carbon nanofibers on benthic fishes.

Widespread learned predator recognition to an alien predator across populations in an amphibian species

Alien predators are a major cause of decline and extinction of species worldwide, since native organisms are rarely equipped with specific antipredatory strategies to cope with them. However, phenotypic plasticity and learned predator recognition may help prey populations to survive novel predators. Here we examine geographical variation in the learning ability of larval spadefoot toads (Pelobates cultripes) to recognize invasive predatory crayfish (Procambarus clarkii). We compare the learning-mediated behavioural responses of tadpoles from six populations across two regions in Spain (central and southern), with different histories of exposure to the presence of the invasive species. Two of the populations showed innate recognition of chemical cues from the invasive crayfish, whereas three of them learned to recognize such cues as a threat after conditioning with conspecific alarm cues. Learning abilities did not differ among southern populations, but they did among central populations. We assessed patterns of genetic variation within and among these two regions through microsatellite markers and found low genetic divergence among the southern populations but greater differentiation among the central ones. We hypothesize that similar responses to the invasive crayfish in southern populations may have arisen from a combination of extended historical exposure to this introduced predator (~ 50 y) and higher levels of gene flow, as they inhabit a highly interconnected pond network. In contrast, populations from central Spain show lower connectivity, have been exposed to the invasive crayfish for a shorter period of time, and are more divergent in their plastic responses.

Metabolic constraints and individual variation shape the trade-off between physiological recovery and antipredator responses in adult sockeye salmon.

Metabolic scope represents the aerobic energy budget available to an organism to perform non-maintenance activities (e.g., escape a predator, recover from a fisheries interaction, compete for a mate). Conflicting energetic requirements can give rise to ecologically relevant metabolic trade-offs when energy budgeting is constrained. The objective of this study was to investigate how aerobic energy is utilized when individual sockeye salmon (Oncorhynchus nerka) are exposed to multiple acute stressors. To indirectly assess metabolic changes in free swimming individuals, salmon were implanted with heart rate biologgers. Animals were then exercised to exhaustion or briefly handled as a control, and allowed to recover from this stressor for 48-h. During the first two hours of the recovery period, individual salmon were exposed to 90ml of conspecific alarm cues or water as a control. Heart rate was recorded throughout the recovery period. Recovery effort and time was higher in exercised fish, relative to control fish, whereas exposure to an alarm cue had no effect on either of these metrics. Individual routine heart rate was negatively correlated with recovery time and effort. Together, these findings suggest that metabolic energy allocation towards exercise recovery (i.e., an acute stressor; handling, chase, etc.) trumps antipredator responses in salmon, although individual variation may mediate this effect at the population level. This article is protected by copyright. All rights reserved.

Olfactory sensitivity and threat-sensitive responses to alarm cue in an invasive fish

Establishing how invasive animals perceive and manage the threat of predation improves our understanding of why certain species rapidly invade unfamiliar environs where others do not. The threat-sensitive response hypothesis predicts that prey that modulate their antipredator behavior in response to the perceived intensity of the threat will have a selective advantage. We investigated the behavioral and olfactory antipredator responses of migrating invasive sea lamprey to varying concentrations of a conspecific alarm cue in the laboratory and field. We hypothesized the odor indicates the presence and location of predation risk on river shorelines, allowing sea lamprey to either alter their migratory path and/or movement timing to reduce exposure to the predator. Migratory sea lampreys exhibited threat-sensitivity in space-use both in the laboratory and nature by increasingly avoiding areas as the concentration of alarm cue increased when safe space was available (areas without the alarm cue). The intensity of the avoidance at higher concentrations was greater in the field. Electrophysiological recordings from the olfactory organ confirmed a concomitant increase in signal output to the olfactory bulb of the brain when exposed to increased alarm cue concentrations. However, increasing the alarm cue concentration did not alter the animal’s motivation to move upstream in either avoidable risk or unavoidable risk scenarios. Exposure to alarm cue affected decisions regarding how to move, but not whether to move. Knowledge of how the animal uses the cue in nature reveals ways to use the cue to manipulate movement and achieve conservation goals.

Atorvastatin and gemfibrozil alter zebrafish behavior

ABSTRACT The pharmaceuticals atorvastatin and gemfibrozil are prescribed for the treatment of high blood cholesterol. Atorvastatin has been detected in surface waters at a concentrations of 250 ng/L while gemfibrozil at 0.5 μg/L. We tested the effects of atorvastatin and gemfibrozil individually and in combination on the swimming behavior and response of zebrafish (Danio rerio) to a conspecific alarm cue. We also measured whole-body cortisol and the effect of the alarm on metabolic rate. Fish exposed to nominal concentrations of 0.075 and 7.5 μg/L atorvastatin showed exaggerated responses to the alarm. In contrast, a high gemfibrozil concentration (nominal: 250 μg/L) alone and in combination with atorvastatin inhibited the alarm response suggesting an antagonistic effect. Neither drug affected total cortisol. After exposure to the alarm chemical the metabolic rate of control fish increased, but all other treatments decreased. This study shows that these drugs can effect behaviour at environmentally relevant concentrations.

On the use of antibiotics in plasticity research: Gastropod shells unveil a tale of caution.

Through phenotypic plasticity, individual genotypes can produce multiple phenotypes dependent on the environment. In the modern world, anthropogenic influences such as man-made pharmaceuticals are increasingly prevalent. They might alter observable patterns of plasticity and distort our conclusions regarding the adaptive potential of natural populations. Antibiotics are nowadays nearly ubiquitous in aquatic environments and prophylactic antibiotic use is also becoming more common to optimize animal survival and reproductive output in artificial settings. In the well-studied plasticity model system Physella acuta, prophylactic erythromycin treatment acts against gram-positive bacteria and thereby reduces mortality. Here, we study its consequences for inducible defence formation in the same species. In a 2 × 2 split-clutch design, we reared 635 P. acuta in either the presence or absence of this antibiotic, followed by 28-day exposure to either high or low predation risk as perceived through conspecific alarm cues. Under antibiotic treatment, risk-induced increases in shell thickness, a well-known plastic response in this model system, were larger and consistently detectable. Antibiotic treatment reduced shell thickness in low-risk individuals, suggesting that in controls, undiscovered pathogen infection increased shell thickness under low risk. Family variation in risk-induced plasticity was low, but the large variation in responses to antibiotics among families suggests different pathogen susceptibility between genotypes. Lastly, individuals that developed thicker shells had reduced total mass, which highlights resource trade-offs. Antibiotics thus have the potential to uncover a larger extent of plasticity, but might counterintuitively distort plasticity estimates for natural populations where pathogens are a part of natural ecology.

Commentary: using prey naïveté to inform ecological management.

Commentary: using prey naïveté to inform ecological management.

Does atrazine induce changes in predator recognition, growth, morphology, and metamorphic traits of larval skipper frogs (Euphlyctis cyanophlyctis)?

Atrazine, an info disruptor, interferes with the olfaction of aquatic organisms by impairing the chemosensory system. Consequently, it affects behavior, physiology, and growth increases mortality and infections, and suppresses the immune system of aquatic animals. In this study, we wanted to determine the sensitivity of larval Euphlyctis cyanophlyctis to different concentrations of atrazine by assessing their antipredator behavior, growth, morphology, and metamorphic traits. The results indicate that exposure to atrazine did not affect the survival of tadpoles. However, it caused retarded growth at higher concentrations. Interestingly, the antipredator behavior of tadpoles toward conspecific alarm cues decreased in a dose-dependent manner with an increase in the concentration of atrazine. Tadpoles exposed to low concentrations of atrazine had deeper, wider bodies and tails while those exposed to higher concentrations had shallower and narrower bodies with shallower tail muscles. However, at low and moderate concentrations atrazine did not affect size at metamorphosis, it extended the larval duration at higher concentrations.

Sea Lamprey Alarm Cue Comprises Water- and Chloroform- Soluble Components

A diversity of aquatic organisms manage predation risk by avoiding waters activated with conspecific alarm cues, a chemical mixture released from injuries. The sea lamprey (Petromyzon marinus) is a nocturnal migratory species that relies on its alarm cue to navigate around areas of predation risk when moving through river channels. Identification of the cue’s chemistry would allow managers to harness this innate behavioral response to guide migrating sea lamprey to traps (invasive population in the Laurentian Great Lakes) or to fish passage devices where dams block migrations in their native range. We pursued isolation of the sea lamprey alarm cue through behaviorally guided fractionation, fractionating the alarm cue into water-soluble and chloroform-soluble fractions, each of which elicited a substantial avoidance response. Recombining the two fractions restored full reactivity, suggesting the alarm cue mixture contains components that exhibit high solubility in water (e.g., nitrogenous compounds), chloroform (e.g., lipids), or perhaps materials that dissolve readily in either solvent. We further screened 13 individual compounds or pure isolates and 6 sub-fractions from the water-soluble fraction and found one of the pure isolates, isoleucine, evoked an avoidance response on its own, but not consistently when found in other mixtures. In a third experiment, we observed no behavioral response after recombining 32 compounds isolated and identified from the water-soluble fraction. These results confirm other suggestions that the process of elucidating alarm cue constituents is challenging. However, we suggest the pursuit is worthwhile given the strong evidence for the utility of alarm cues for use in the conservation and management of fishes and other aquatic organisms.

Neuromorphological and behavioural effects of early developmental exposure to alarm cue on captive-reared Atlantic salmon (Salmo salar)

Behavioural plasticity plays an important role in an organism's ability to adapt to captive settings, but a lack of perceived predation risk during early development in captivity can lead to diminished anti-predator behaviours. Here, we used Atlantic salmon ( Salmo salar) to test whether early developmental exposure to alarm cues (pre-exposure) led to (1) a developmentally plastic response to alarm cue in yearling and (2) an observable change in neural investment. We exposed fry to either a conspecific alarm cue (pre-exposed fish) or control water (non-exposed fish) and measured activity related to anti-predator behaviour such as time spent motionless, number of aggressive acts, and time spent associated with shelter. We found no indication of a developmentally plastic response to early alarm cue exposure, but we found that pre-exposed fish developed relatively smaller olfactory bulbs compared to non-exposed fish. Our results demonstrate the importance of and ability to exploit plastic responses in captive-reared Atlantic salmon and highlight the need to link behaviour with neuromorphological changes.

Ignorance is not bliss: evolutionary naiveté in an endangered desert fish and implications for conservation.

Predator naiveté has been invoked to explain the impacts of non-native predators on isolated populations that evolved with limited predation. Such impacts have been repeatedly observed for the endangered Pahrump poolfish, Empetrichthys latos, a desert fish species that evolved in isolation since the end of the Pleistocene. We tested Pahrump poolfish anti-predator responses to conspecific chemical alarm cues released from damaged epidermal tissue in terms of fish activity and water column position. Pahrump poolfish behavioural responses to conspecific alarm cues did not differ from responses to a dechlorinated tap water control. As a positive control, the well-studied fathead minnow, Pimephales promelas, showed significant alarm cue responses in terms of reduced activity and lowered water column position. The density of epidermal club cells, the presumptive source of alarm cues, was significantly lower in Pahrump poolfish relative to fathead minnows. Therefore, anti-predator competence mediated by conspecific alarm cues does not seem to be a component of the ecology of Pahrump poolfish. These findings provide a proximate mechanism for the vulnerability of Pahrump poolfish to non-native predators, with implications for the conservation and management of insular species.

Assessing effects of predator density and diversity on neophobia in Trinidadian guppies

Neophobic predator avoidance, where prey actively avoid novel stimuli, is thought to allow prey to cope with the inability to predict predation risk (i.e. uncertainty) while reducing the costs associated with learning. Recent studies suggest that neophobia is elicited as a response to unpredictable and elevated mean predation risk, and is linked to experience with diverse novel cues. However, no research has disentangled the effects of predator density and diversity on neophobia. We conditioned Trinidadian guppies (Poecilia reticulata) to high- or low-diversity predator model treatments paired with high, intermediate, or low concentrations of conspecific alarm cues as a proxy for predator density. We tested behavioural responses to a novel stimulus vs. a water control to determine differences in neophobia among treatments. We found that neophobic shoaling behaviour was shaped by mean risk (predator density). However both density and diversity shaped neophobic freezing, and to a weaker extent, neophobic area use. Our research suggests that predator diversity might elicit neophobic responses in guppies, but only when mean risk is high enough. The relationship between neophobia and components of predation risk is becoming increasingly relevant as ecological uncertainty becomes more prevalent with increasing climate change, anthropogenic impacts, and invasive species.

Pre- and Postnatal Predator Cues Shape Offspring Anti-predatory Behavior Similarly in the Bank Vole

Prey animals can assess the risks predators present in different ways. For example, direct cues produced by predators can be used, but also signals produced by prey conspecifics that have engaged in non-lethal predator-prey interactions. These non-lethal interactions can thereby affect the physiology, behavior, and survival of prey individuals, and may affect offspring performance through maternal effects. We investigated how timing of exposure to predation-related cues during early development affects offspring behavior after weaning. Females in the laboratory were exposed during pregnancy or lactation to one of three odor treatments: (1) predator odor (PO) originating from their most common predator, the least weasel, (2) odor produced by predator-exposed conspecifics, which we call conspecific alarm cue (CAC), or (3) control odor (C). We monitored postnatal pup growth, and we quantified foraging and exploratory behaviors of 4-week-old pups following exposure of their mothers to each of the three odour treatments. Exposure to odors associated with predation risk during development affected the offspring behavior, but the timing of exposure, i.e., pre- vs. postnatally, had only a weak effect. The two non-control odors led to different behavioral changes: an attraction to CAC and an avoidance of PO. Additionally, pup growth was affected by an interaction between litter size and maternal treatment, again regardless of timing. Pups from the CAC maternal treatment grew faster in larger litters; pups from the PO maternal treatment tended to grow faster in smaller litters. Thus, in rodents, offspring growth and behavior are seemingly influenced differently by the type of predation risk perceived by their mothers.

Paternal care effects outweigh gamete-mediated and personal environment effects during the transgenerational estimation of risk in fathead minnows

BackgroundIndividuals can estimate risk by integrating prenatal with postnatal and personal information, but the relative importance of different information sources during the transgenerational response is unclear. The estimated level of risk can be tested using the cognitive rule of risk allocation, which postulates that under consistent high-risk, antipredator efforts should decrease so that individual metabolic requirements can be satisfied. Here we conduct a comprehensive study on transgenerational risk transmission by testing whether risk allocation occurs across 12 treatments that consist of different maternal, paternal, parental care (including cross-fostering) and offspring risk environment combinations in the fathead minnow Pimephales promelas, a small cyprinid fish with alloparental care. In each risk environment, we manipulated perceived risk by continuously exposing individuals from birth onwards to conspecific alarm cues or a control water treatment. Using 2810 1-month old individuals, we then estimated shoaling behaviour prior to and subsequent to a novel mechanical predator disturbance.ResultsOverall, shoals estimating risk to be high were denser during the prestimulus period, and, following the risk allocation hypothesis, resumed normal shoaling densities faster following the disturbance. Treatments involving parental care consistently induced densest shoals and greatest levels of risk allocation. Although prenatal risk environments did not relate to paternal care intensity, greater care intensity induced more risk allocation when parents provided care for their own offspring as opposed to those that cross-fostered fry. In the absence of care, parental effects on shoaling density were relatively weak and personal environments modulated risk allocation only when parental risk was low.ConclusionsOur study highlights the high relative importance of parental care as opposed to other information sources, and its function as a mechanism underlying transgenerational risk transmission.

Running away or running to? Do prey make decisions solely based on the landscape of fear or do they also include stimuli from a landscape of safety?

Predator-prey interactions are a key part of ecosystem function, and non-consumptive effects fall under the landscape of fear theory. Under the landscape of fear, the antipredator responses of prey are based on the spatial and temporal distribution of predatory cues in the environment. However, the aversive stimuli (fear) are not the only stimuli prey can utilize when making behavioral decisions. Prey might also be using attractive stimuli that represent safety to guide decision making. Using a novel, orthogonal design, we were able to spatially separate aversive and attractive stimuli to determine whether prey are utilizing safety cues to navigate their environment. Crayfish Faxonius rusticus were placed in the center of a behavioral arena. Aversive stimuli of either predatory bass Micropterus salmoides cues or conspecific alarm cues increased along the x-axis of the behavioral arena. Safety cues (shelters) increased along the y-axis by decreasing the number of shelter openings in this direction. Crayfish were allowed two phases to explore the arena: one without the fearful stimuli and one with the stimuli. Linear mixed models were conducted to determine whether movement behaviors and habitat utilization were affected by the phase of the trial and the type of aversive stimuli. Crayfish responded more strongly to alarm cues than to fear cues, with only alarm cues significantly impacting habitat utilization. When responding to alarm cues, crayfish used safety cues as well as fear cues to relocate themselves within the arena. Based on these results, we argue that crayfish utilize a landscape of safety in conjunction with a landscape of fear when navigating their environment.