Heterospecific Alarm Cues Research Articles

Variation in Defensive Strategies of Brown Frogs against Conspecific and Heterospecific Alarm Cues

Chemical cues released upon injury play a crucial role in mediating antipredator responses in many aquatic species. Prey populations capable of exploiting information from different sources may enhance their fitness, although the factors determining this ability are not always clear. In this study, we investigated the antipredator responses to both conspecific and heterospecific injury cues (i.e., alarm cues) in three brown frog species: Rana dalmatina, Rana latastei, and Rana temporaria. We recorded two tadpole defensive behaviours: the proportion of time spent inactive and the distance covered. Responses to a native odonate predator were used as a positive control. Tadpoles of R. dalmatina showed a clear decrease in activity in response to both con- and heterospecific cues, similar to their reaction to predator cues. Tadpoles of R. latastei slightly decreased activity in response to alarm cues from both agile frog species but did not react to common frog cues. Finally, R. temporaria exhibited high sensitivity to conspecific cues and a weak response to heterospecific cues. The phylogenetic-relatedness hypothesis seems to explain the observations for both R. latastei and R. temporaria, while for R. dalmatina, the ecological coexistence hypothesis, given its overlapping distribution with the other two species, seems to better explain the data. However, since the invoked hypotheses are not mutually exclusive, further analysis of other populations of these species is necessary to confirm the generality of these findings and to better understand the role of environmental factors in shaping these antipredator responses.

Heterospecific eavesdropping on disturbance cues of a treefrog.

Alarm signals and cues are crucial to animal survival and vary greatly across species. Eavesdropping on heterospecific alarm signals and cues can provide eavesdroppers with information about potential threats. In addition to acoustic alarm signals, evidence has accumulated that chemical alarm cues and disturbance cues can also play a role in alerting conspecifics to potential danger in adult anurans (frogs and toads). However, there is very little known about whether disturbance cues are exploited by heterospecifics. In the present study, we conducted a binary choice experiment and a prey chemical discrimination experiment, respectively, to test the responses of a sympatric anuran species (red webbed treefrogs, Rhacophorus rhodopus) and a sympatric predator species (Chinese green tree vipers, Trimeresurus stejnegeri) to disturbance odors emitted by serrate-legged small treefrogs (Kurixalus odontotarsus). In the binary choice experiment, we found that the presence of disturbance odors did not significantly trigger the avoidance behavior of R. rhodopus. In the prey chemical discrimination experiment, compared with odors from undisturbed K. odontotarsus (control odors) and odorless control, T. stejnegeri showed a significantly higher tongue-flick rate in response to disturbance odors. This result implies that disturbance odor cues of K. odontotarsus can be exploited by eavesdropping predators to detect prey. Our study provides partial evidence for heterospecific eavesdropping on disturbance cues and has an important implication for understanding heterospecific eavesdropping on chemical cues of adult anurans.

The role of donor and receiver size in the response to public cues in Hart’s rivulus, Anablepsoides hartii

Abstract Aquatic prey use chemical alarm cues as public information sources to optimize behavioural decisions. Recent studies suggest that the contextual value of these cues is shaped by their source, the size of the donor relative to the receiver, and the size of the receiver itself. Here, we exposed Hart’s rivulus (Anablepsoides hartii) to conspecific or heterospecific alarm cues from donors that were either smaller or larger than the mean focal rivulus size. Smaller rivulus reduced foraging in response to conspecific and heterospecific cues, regardless of donor size. However, larger rivulus exhibited no reduction in foraging towards small conspecific cues and increased foraging towards small heterospecific cues. Additionally, while conspecific donors elicited strong predator avoidance, rivulus exhibited stronger responses to large vs. small heterospecific cues. Our results demonstrate that the value of alarm cues is shaped by the interacting effects of receiver size and the size and species of cue donors.

Behavioural responses to con- and heterospecific alarm cues by an alien and a coexisting native fish

The monkey goby Neogobius fluviatilis is an invasive Ponto-Caspian fish that enters habitats of the native gudgeon Gobio gobio in European freshwaters, likely belonging to the same prey guild. Their abilities to detect and avoid predation have been poorly understood, although these traits may contribute to the competitive advantage and drive the invasion success of the goby. We tested intra- and interspecific responses of fish from sympatric populations to damage-released alarm cues (skin extract) in laboratory. Both species of fish responded to conspecific and heterospecific cues, but their responses to conspecifics were more diverse (changed social distancing among individuals, reduced vertical and horizontal movement) than those elicited by heterospecifics (changed social distancing only). Moreover, the fish differed in their anti-predation behaviour: the gudgeon increased whilst the monkey goby decreased inter-individual distances and only the gudgeon exhibited thigmotaxis and reduced mobility in response to the conspecific cues. Interspecific differences show that the species exhibit distant anti-predation strategies. This might be associated with their phylogenetic distance and/or higher differentiation of their ecological niches than commonly assumed. Besides, our results suggest that alien species be included in the interspecific exchange of information in local fish assemblages.

Living in mixed species groups promotes predator learning in degraded habitats

Living in mix-species aggregations provides animals with substantive anti-predator, foraging and locomotory advantages while simultaneously exposing them to costs, including increased competition and pathogen exposure. Given each species possess unique morphology, competitive ability, parasite vulnerability and predator defences, we can surmise that each species in mixed groups will experience a unique set of trade-offs. In addition to this unique balance, each species must also contend with anthropogenic changes, a relatively new, and rapidly increasing phenomenon, that adds further complexity to any system. This complex balance of biotic and abiotic factors is on full display in the exceptionally diverse, yet anthropogenically degraded, Great Barrier Reef of Australia. One such example within this intricate ecosystem is the inability of some damselfish to utilize their own chemical alarm cues within degraded habitats, leaving them exposed to increased predation risk. These cues, which are released when the skin is damaged, warn nearby individuals of increased predation risk and act as a crucial associative learning tool. Normally, a single exposure of alarm cues paired with an unknown predator odour facilitates learning of that new odour as dangerous. Here, we show that Ambon damselfish, Pomacentrus amboinensis, a species with impaired alarm responses in degraded habitats, failed to learn a novel predator odour as risky when associated with chemical alarm cues. However, in the same degraded habitats, the same species learned to recognize a novel predator as risky when the predator odour was paired with alarm cues of the closely related, and co-occurring, whitetail damselfish, Pomacentrus chrysurus. The importance of this learning opportunity was underscored in a survival experiment which demonstrated that fish in degraded habitats trained with heterospecific alarm cues, had higher survival than those we tried to train with conspecific alarm cues. From these data, we conclude that redundancy in learning mechanisms among prey guild members may lead to increased stability in rapidly changing environments.

Behavioral response of juvenile silver and bighead carp to conspecific and heterospecific alarm cues

Predation is an important factor influencing the strength and success of a year class in many prey fishes. Many adaptations, including chemical cues, benefit shoaling groups by informing members of a possible impending predatory threat. Bighead (Hypophthalmichthys nobilis) and silver carps (Hypophthalmichthys molitrix) are widely dispersed invasive fishes that spend much of their first year at a size vulnerable to predation. The objective of this study was to evaluate the fright response of juvenile bighead and silver carps when exposed to alarm cues from conspecific and heterospecific fishes. Groups of carps were exposed to 5 mL of alarm cue from either bighead carp, silver carp, golden shiner (Notemigonus crysoleucas), or fathead minnow (Pimephales promelas). Behavior was recorded before and after the application of the treatment. Our results indicate that both species were unable to recognize chemical alarm cues from North American cypriniforms, yet both were able to recognize conspecific alarm cues. However, the two species of bigheaded carps respond to conspecific chemicals differently. Silver carp increase distance among individuals, whereas bighead carp reduce distance between individuals. Both show a reduction in activity after chemical application. Though both species recognize conspecific alarm cues, bighead carp exhibit similar fright patterns when exposed to alarm chemicals of silver carp, yet no behavioral responses were detected in silver carp when exposed to alarm chemicals of bighead carp. An understanding of fright response in bighead and silver carps aids understanding of predator interactions and ecological roles of these fishes, and can be utilized in population management applications.

Behavioural differences and interactions between two sessile bivalves forming mixed-species assemblages

Behavioural differences and interactions between two sessile bivalves forming mixed-species assemblages

Strong behavioural defensive responses of endemic Rana latastei tadpoles induced by a native predator's odour

Abstract Prey species must constantly acquire information on predator identity, abundance and dangerousness from the environment. In aquatic habitats, this information is mainly propagated by water‐borne chemical signals, either predator‐specific odours or prey alarm cues. Anuran larvae innately respond to conspecific alarm cues and are able to associate them to predator cues during their lifetime. In this study, we investigated the anti‐predatory responses of endemic Italian agile frog (Rana latastei) tadpoles exposed to either conspecific or heterospecific alarm cues and a native predator's (Anax imperator larvae) odour. Pre‐and post‐stimulus behaviours of each tadpole were recorded by a digital camera and analysed by a source executable software for image‐based tracking. We found that Italian agile frog tadpoles responded to fasted dragonfly odour by strongly reducing their activity, both in terms of the amount of time they spent active and path length covered in comparison to control groups. Contrary to previous studies, predators' diet had a negligible effect on tadpole response and our experiment did not bring any evidence of the phylogenetic‐relatedness hypothesis. The innate or early‐in‐development recognition of dragonfly larvae is clearly adaptive and may increase tadpole survival with relatively low costs, but, at the same time, may increase the risk of ignoring novel potential threats.

Innate responses to conspecific and heterospecific alarm cues in the endangered eastern cape redfin Pseudobarbus afer.

We examined innate responses to conspecific and heterospecific alarm cues in a small cyprinid minnow, the Eastern Cape redfin Pseudobarbus afer. We found that redfins respond to conspecific skin extract, which contains alarm chemicals, and showed that their preferred response is to hide in refugia. Redfins also respond to skin extract from an allopatric, distantly related minnow species, the chubbyhead barb Enteromius anoplus indicating that neither sympatry nor close phylogenetic relationships are necessary for recognition of heterospecific alarm cues. Although both conspecific and heterospecific alarm cues induced similar responses, the response to heterospecific cues was less intense. This may be explained by a trade-off between selection to maximise threat recognition and selection to avoid the costs of responding to irrelevant cues, or by differences in chemical structures of alarm cues between species. These findings have implications for the conservation of this Endangered fish species and for freshwater fishes throughout Africa.

Retention of learned predator recognition in embryonic and juvenile rainbow trout

Abstract Minimizing predation risk, especially for young or naïve individuals, can be achieved by learning to recognize predators. Embryonic learning may optimize survival by allowing for the earliest possible response to predation threats posthatch. However, predatory threats often change over an individual’s lifetime, and using old information can be detrimental if it becomes outdated. Adaptive forgetting allows an individual to discount obsolete information in decision-making and instead emphasize newer, more relevant information when responding to predation threats. Little is known about the extent to which young individuals can learn and forget information about predation threats. Here we demonstrate that rainbow trout 1) are capable of learning from both conspecific and heterospecific alarm cues as embryos, newly hatched larvae, and free-swimming larvae, 2) exhibit adaptive forgetting of predator information at all stages, and 3) display dynamic adaptive forgetting based on the ontogeny of learning. Specifically, fish that learned information as embryos retained the information for longer periods than those that learned the same information as newly hatched alevins.

Chemically-induced plasticity in early life history ofPalaemon argentinus: are chemical alarm cues conserved within palaemonid shrimps?

Most aquatic animals use infochemicals from both conspecifics and heterospecifics to assess local predation risks and enhance predator detection. Released substances from injured conspecifics and other species (chemical alarm cues) are reliable cues to indicate an imminent danger in a specific habitat and often mediate the development of inducible defenses. Amphibian and fish embryos have been shown to acquire this information while at the embryonic stage of development, in relation to the developing nervous system and sensory development. With the exception of Daphnia, there is no information on chemically mediated responses to alarm cues in embryos of any crustacean groups. Therefore, we tested whether embryo exposure to chemical cues simulating predation on conspecifics or heterospecifics (closely related, non-coexisting species), or a mixture of both, alters embryonic developmental time, size and morphology of the first larval instar in Palaemon argentinus (Crustacea: Decapoda). Embryonic exposure to chemical alarm cues from conspecifics shortened the embryonic developmental time and elicited larger larvae with a longer rostrum. Rostrum length of the first larval instar changed independently of their size, thus elongated rostra can be considered a defensive feature. Embryonic developmental time was not altered by chemical alarm cues from either heterospecifics or the mixed cues treatment; however, exposure to these cues resulted in larger larvae compared with the control group. Chemically induced morphological plasticity in larvae in response to alarm cues from con- and heterospecifics suggests that such cues are conserved in palaemonids shrimps, providing embryos with an innate recognition of heterospecific alarm cues as predicted by the phylogenetic relatedness hypothesis.

Training for Translocation: Predator Conditioning Induces Behavioral Plasticity and Physiological Changes in Captive Eastern Hellbenders (Cryptobranchus alleganiensis alleganiensis) (Cryptobranchidae, Amphibia)

Translocations are stressful, especially when captive animals are naïve to natural stimuli. Captive eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) identify predatory fish as threats, but may be more vulnerable to predation and stress because of inexperience with them. We investigated the use of predator conditioning to prepare hellbenders, behaviorally and physiologically, for the presence of a common predator, largemouth bass (Micropterus salmoides). We reared hellbenders for 30 d with and without continuous exposure to largemouth bass kairomones and heterospecific alarm cues and found conditioned hellbenders became less active compared to unconditioned individuals (p = 0.017). After conditioning, we exposed hellbenders to water, a low concentration of kairomones, or a high concentration of kairomones in a closed respirometer system. We measured activity within respirometer chambers and routine metabolic rate. We found unconditioned hellbenders exposed to low and high concentrations of kairomones were 41% and 119% more active than conditioned animals (p = 0.002 and p < 0.001). Moreover, conditioned individuals had on average 6.5% lower metabolic rates across all three kairomone concentrations compared to unconditioned individuals (p = 0.017). Our data suggest that predator conditioning induces behavioral avoidance tactics and physiological changes that could improve future translocation efforts for hellbenders and other imperiled species.

Predator-induced neophobia in juvenile cichlids.

Predation is an important but often fluctuating selection factor for prey animals. Accordingly, individuals plastically adopt antipredator strategies in response to current predation risk. Recently, it was proposed that predation risk also plastically induces neophobia (an antipredator response towards novel cues). Previous studies, however, do not allow a differentiation between general neophobia and sensory channel-specific neophobic responses. Therefore, we tested the neophobia hypothesis focusing on adjustment in shoaling behavior in response to a novel cue addressing a different sensory channel than the one from which predation risk was initially perceived. From hatching onwards, juveniles of the cichlid Pelvicachromis taeniatus were exposed to different chemical cues in a split-clutch design: conspecific alarm cues which signal predation risk and heterospecific alarm cues or distilled water as controls. At 2 months of age, their shoaling behavior was examined prior and subsequent to a tactical disturbance cue. We found that fish previously exposed to predation risk formed more compact shoals relative to the control groups in response to the novel disturbance cue. Moreover, the relationship between shoal density and shoal homogeneity was also affected by experienced predation risk. Our findings indicate predator-induced, increased cross-sensory sensitivity towards novel cues making neophobia an effective antipredator mechanism.

Avoidance behavior in two sympatric planaria species: effects of conspecific and heterospecific chemical alarm cues

In many aquatic animals, predator avoidance can be stimulated by chemical cues, including those released by injured prey (alarm cues). Alarm cues of both conspecific and heterospecific origin have been identified within several fish taxa, where phylogenetic conservation of the cue-response complex is common. Turbellarian flatworms (planaria) are among the simplest animals known to respond to chemical cues released by injured conspecifics. We examined how two locally sympatric planaria species respond to conspecific and heterospecific chemical cues using macerated tissue suspensions. Brown (Girardia tigrina) and black (Dugesia dorotocephala) planaria both exhibited avoidance behavior when presented conspecific cues. Despite a significant twofold difference in body size (black > brown), stimulus prepared from a single (1×) individual of either species elicited avoidance. Increasing brown planaria cue concentration by macerating two individuals (2×) produced a significant increase in conspecific avoidance. Heterospecific stimuli produced asymmetric results. Black planaria avoided the brown planaria stimulus, but only in the higher concentration (2×) trials. Brown planaria did not consistently exhibit avoidance of the black planaria stimulus and some brown subjects approached and consumed black planarian tissues. Our results expand the demonstrated occurrence of alarm cues among planaria and suggest that avoidance behavior can be mediated by multiple environmental and intrinsic factors in freshwater Turbellaria.

Conspecific alarm cues affect interspecific aggression in cichlid fishes

Individuals have to respond simultaneously to different environmental factors often making trade-offs between conflicting demands necessary. Many freshwater ecosystems are resource-limited and both intra- and interspecific competitiveness is a common requirement to gain and defend resources necessary for reproduction. Although predation risk is an important selective force affecting behavioral decisions, little is known about the impact of predation risk on interspecific competition. Here, we investigate whether chemically mediated predation risk affects interspecific territorial aggression by the freshwater cichlid Pelvicachromis taeniatus. In our experiments, territorial P. taeniatus males were visually confronted with a territorial intruder: a heterospecific, sympatric cichlid (Benitochromis nigrodorsalis) which generally induced aggression in P. taeniatus. Predation risk for P. taeniatus was simulated by a concurrent release of conspecific chemical alarm cues. In control treatments, no chemical cues, dissolved heterospecific alarm cues, or aliquots of distilled water were provided during these aggressive encounters. The results show that interspecific aggression of territorial male P. taeniatus is significantly decreased under predation risk compared to the control treatments. This suggests that interspecific competition becomes less intense under concurrent predation risk. As this process could hinder competitive exclusion, predation risk may indirectly promote and stabilize biodiversity in natural ecosystems.

Chemical alarm cues are conserved within the coral reef fish family Pomacentridae.

Fishes are known to use chemical alarm cues from both conspecifics and heterospecifics to assess local predation risks and enhance predator detection. Yet it is unknown how recognition of heterospecific cues arises for coral reef fishes. Here, we test if naïve juvenile fish have an innate recognition of heterospecific alarm cues. We also examine if there is a relationship between the intensity of the antipredator response to these cues and the degree to which species are related to each other. Naïve juvenile anemone fish, Amphiprion percula, were tested to see if they displayed antipredator responses to chemical alarm cues from four closely related heterospecific species (family Pomacentridae), a distantly related sympatric species (Asterropteryx semipunctatus) and a saltwater (control). Juveniles displayed significant reductions in foraging rate when exposed to all four confamilial heterospecific species but they did not respond to the distantly related sympatric species or the saltwater control. There was also a strong relationship between the intensity of the antipredator response and the extent to which species were related, with responses weakening as species became more distantly related. These findings demonstrate that chemical alarm cues are conserved within the pomacentrid family, providing juveniles with an innate recognition of heterospecific alarm cues as predicted by the phylogenetic relatedness hypothesis.

Size‐mediated response to public cues of predation risk in a tropical stream fish

In order to investigate any size-dependent differences between behavioural patterns, wild-caught Hart's rivulus Rivulus hartii of varying sizes were exposed to chemical alarm cues extracted from the skin of conspecifics or heterospecific Poecilia reticulata, or a tank water control, in a series of laboratory trials. In response to conspecific alarm cues, R. hartii subjects of the range of body sizes tested exhibited consistent, size-independent antipredator behaviours that were characterized by decreased locomotory activity and foraging levels and increased refuging behaviour. Conversely, focal R. hartii demonstrated significant size-dependent trends in response to heterospecific alarm cues, with smaller individuals exhibiting antipredator responses and larger individuals shifting their behaviour to increased levels of activity consistent with a foraging, or predatory, response. These results show that the behavioural responses of individual R. hartii to publicly available chemical alarm cues from heterospecifics are mediated by the size of the receiver.

Cohabitation enhances the avoidance response to heterospecific alarm cues in a freshwater snail

Cohabitation enhances the avoidance response to heterospecific alarm cues in a freshwater snail

Active space of chemical alarm cue in natural fish populations

Abstract Chemical cues released from injured fish skin during a predator attack provide reliable information about the presence of predation risk. Here, I report estimates of the area avoided by littoral fishes after experimental release of chemical alarm cues in two small lakes in northern Minnesota. Minnow traps were labeled chemically with either water (control) or skin extract (chemical alarm cue) made from 2 cm2 of cyprinid skin (redbelly dace in experiment 1, fathead minnows in experiment 2). Traps labeled with water were placed 1, 2, or 8 m from traps labeled with alarm cue. After 2 h, water-traps that were either 1 or 2 m distant from an alarm-trap caught significantly fewer fish than water-traps 8 m distant from alarm-traps. Conspecific and heterospecific skin extract produced similar area avoidance by fathead minnows. Redbelly dace showed a larger active space in response to conspecific than heterospecific alarm cues. Brook stickleback showed reduced catches within 2 m of skin extract of fathead minnows. Overall, the radius of active space was between 2 and 8 m under lake conditions with average subsurface currents of 0.82 cm/s. These data are the first field estimates of active space of ostariophysan chemical alarm cues.

PHYLOGENETIC RELATEDNESS AND ECOLOGICAL INTERACTIONS DETERMINE ANTIPREDATOR BEHAVIOR

Interspecific recognition of alarm cues among guild members through "eavesdropping" may allow prey to fine-tune antipredator responses. This process may be linked to taxonomic relatedness but might also be influenced by local adaptation to recognize alarm cues from sympatric species. We tested this hypothesis using antipredator responses of a freshwater gastropod Lymnaea stagnalis (L.) to alarm cues from damaged conspecific and 10 heterospecific gastropod species. As predicted, the magnitude of antipredator response decreased significantly with increasing phylogenetic distance, but increased when species were naturally sympatric (defined as species cohabiting in the same water body) with the source population of L. stagnalis. The responses to sympatric species were higher overall, and the relationship between genetic distance and alarm cue response was stronger when tested with sympatric species. This is the first study to demonstrate that population sympatry influences innate antipredator responses to alarm cues from intraguild members and suggests that responses based on phylogenetic relationships can be modified through local adaptation. Such adaptation to heterospecific alarm cues suggests that species could be at a disadvantage when they encounter novel intraguild members resulting from species invasion or range expansion due to a reduction in the presence of reliable information about predation risk.