Epidermal 'alarm substance' cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation

Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator-prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.     

On the Meaning of Alarm Calls: A Review of Functional Reference in Avian Alarm Calling

A long‐standing question in animal communication is whether signals reveal intrinsic properties of the signaller or extrinsic properties of its environment. Alarm calls, one of the most conspicuous components of antipredator behaviour, intuitively would appear to reflect internal states of the signaller. Pioneering research in primates and fowl, however, demonstrated that signallers may produce unique alarm calls during encounters with different types of predators, suggesting that signallers through selective production of alarm calls provide to conspecific receivers information about predators in the environment. In this article, we review evidence for such ‘functional reference’ in the alarm calls of birds based on explicit tests of two criteria proposed in Macedonia & Evans’ (Ethology 93, 1993, 177) influential conceptual framework: (1) that unique alarm calls are given to specific predator categories, and (2) that alarm calls isolated from contextual information elicit antipredator responses from receivers similar to those produced during actual predator encounters. Despite the importance of research on birds in development of the conceptual framework and the ubiquity of alarm calls in birds, evidence for functionally referential alarm calls in this clade is limited to six species. In these species, alarm calls are associated with the type of predator encountered as well as variation in hunting behaviour; with defence of reproductive effort in addition to predators of adults; with age‐related changes in predation risk; and with strong fitness benefits. Our review likely underestimates the occurrence of functional reference in avian alarm calls, as incomplete application and testing of the conceptual framework has limited our understanding. Throughout, therefore, we suggest avian taxa for future studies, as well as additional questions and experimental approaches that would strengthen our understanding of the meaning of functional reference in avian alarm calls.     

Receiving behaviour is sensitive to risks from eavesdropping predators

Conspicuous signals may attract both intended receivers as well as unintended receivers such as predators. However, signalling individuals are not the only ones at risk when communicating, as the intended receiver may encounter eavesdropping predators that are attracted to the same signals. Here, we show that the house mouse (Mus domesticus) behaviourally responds to social signals (scents) as though receiving carries a risk of predation. We presented mice with their own scents (low social benefit to receiving) and those from an unknown “intruder” (high social benefit to receiving) under high (cat urine added) and low (water added) perceived predation risk. Mice traded-off the potential social benefits of receiving a signal against the costs of potential predator encounter. Receiving rates of both social signals (own and intruder) were high under low predation risk. Mice reduced receiving of both social signals when predation risk was increased; however, the effect was greater for their own low value scent than for the high social value intruder scent. Notably, rates of signalling did not vary with the level of perceived predation risk. Our findings suggest that mice traded-off the potential social benefits of receiving a signal (scent mark) against the costs of potential predator encounter. We suggest that, for some species, the costs of communication are borne more by the receivers than the signallers, and that the influence of risks to receivers on the design of communication systems may have been underestimated.     

Context‐dependent alarm signalling in an insect

Animals often respond to danger by raising alarm to inform others. Alarm signals come in many different forms, such as visual or mechanical display, sound or odour. Some animals produce vocal alarm signals that vary with the level of danger. For chemical alarm signals, virtually nothing is known about such context‐dependent signalling due to a general notion that alarm pheromones have fixed compositions. Here, we show that larvae of the Western Flower Thrips (Frankliniella occidentalis) produce an alarm pheromone whose composition varies with the level of danger they face: the presence of a relatively harmless predator or a very dangerous predator, that is either actually attacking or not. The frequency of alarm pheromone excretion increases with the level of danger. Moreover, the composition of excreted alarm pheromone varies in the relationship between total and relative amount of the putative two components, decyl acetate (DAc) and dodecyl acetate (DDAc). When pheromone is excreted with a predator present but not attacking, the percentage DDAc increases with the total amount of pheromone. When a predator does attack, however, the relationship between percentage DDAc and total amount of pheromone is reversed. Taken together, the alarm signal of thrips larvae appears to be context dependent, which to our knowledge is the first report of context‐dependent composition of an alarm pheromone.     

Learned Recognition of Heterospecific Alarm Signals: The Importance of a Mixed Predator Diet

A wide diversity of aquatic organisms release alarm signals upon being attacked by a predator. Alarm signals may 'warn' nearby individuals of danger. Moreover, the signals may be important in facilitating learned recognition of unknown stimuli. It is common for different prey species to respond to each other's chemical alarm signals. In many cases, the responses are learned but no learning mechanisms have been identified to date. In this study we tested whether prey fish can learn the identity of an unknown alarm signal when they detect it in association with conspecific alarm cues in the diet of a predator. Chemical alarm cues are known to be conserved in the diet of predators. We conditioned fathead minnows ( Pimephales promelas ) with chemical stimuli from predatory yellow perch ( Perca flavescens ) fed a mixed diet of minnows and brook stickleback ( Culaea inconstans ), perch fed a mixed diet of swordtails ( Xiphophorus helleri ) and stickleback or distilled water. Minnows were subsequently exposed to chemical alarm cues of injured stickleback alone. Those minnows previously conditioned with perch fed a mixed diet of minnows and stickleback increased their use of shelter and 'froze' significantly more than minnows previously conditioned with perch fed a diet of swordtails and stickleback or those exposed to distilled water. These data demonstrate a mechanism by which minnows can learn the identity of a heterospecific alarm signal.     

Foot-thumping as an alarm signal in macropodoid marsupials: prevalence and hypotheses of function

• 1 Alarm signalling as a means to reduce predation risk is an important component of the behavioural repertoire of many species. It has previously been noted that many of the macropodoid marsupials (kangaroos, wallabies and rat‐kangaroos) produce a foot‐thump, an audible signal created by striking the ground with one or both feet, that is most likely an alarm signal.
• 2 The prevalence of foot‐thumping within the macropodoids and hypotheses of its function as an alarm signal have been poorly documented. To address this issue, we investigate the prevalence of foot‐thumping in macropodoids and interpret possible function according to current alarm signalling theory. Evidence for foot‐thumping was found in almost all macropodoids. In light of this, the behaviour appears to be a conservative trait that may have arisen alongside or followed the evolution of bipedal locomotion, and suggests that this trait carries significant benefits that transcend ecological and predation differences among species.
• 3 Nine alarm signal hypotheses were explored in order to determine the function of foot‐thumping in macropodoid marsupials. However, the existing evidence for consistent function remains inconclusive. Therefore, a series of predictions were developed to provide the foundation for future research to investigate more thoroughly the function of foot‐thumping in macropodoid marsupials.

     

Heterospecific recognition of referential alarm calls in two species of lemur

ABSTRACT

Alarm vocalizations are a common feature of the mammalian antipredator response. The meaning and function of these calls vary between species, with some species using calls to reference-specific categories of predators. Species can also use more than just the calls of conspecifics to detect threat, ‘eavesdropping’ on other species’ signalling to avoid predation. However, the evidence to date for both referential signalling and eavesdropping within primates is limited. We investigated two sympatric populations of wild lemur, the Coquerel’s sifaka Propithecus coquereli and the common brown lemur Eulemur fulvus, presenting them with playbacks of predator calls, conspecific alarm calls and heterospecific lemur alarm calls, and recorded their behavioural responses following the playbacks. Results suggest that the Coquerel’s sifaka may have functionally referential alarm calls with high specificity for aerial predators, but there was no evidence for any referential nature of the other call investigated. Brown lemurs appear to have a mixed alarm system, with one call being specific with respect to aerial predators. The other call investigated appeared to reference terrestrial predators. However, it was also used in other contexts, so does not meet the criteria for functional reference. Both species showed evidence for heterospecific alarm call recognition, with both the Coquerel’s sifaka and the brown lemurs responding appropriately to heterospecific aerial alarm calls.     

Is Alarm Calling Risky? Marmots Avoid Calling from Risky Places

Alarm calling is common in many species. A prevalent assumption is that calling puts the vocalizing individual at increased risk of predation. If calling is indeed costly, we need special explanations for its evolution and maintenance. In some, but not all species, callers vocalize away from safety and thus may be exposed to an increased risk of predation. However, for species that emit bouts with one or a few calls, it is often difficult to identify the caller and find the precise location where a call was produced. We analyzed the spatial dynamics of yellow-bellied marmot (Marmota flaviventris) alarm calling using an acoustic localization system to determine the location from which calls were emitted. Marmots almost always called from positions close to the safety of their burrows, and, if they produced more than one alarm call, tended to end their calling bouts closer to safety than they started them. These results suggest that for this species, potential increased predation risk from alarm calling is greatly mitigated and indeed calling may have limited predation costs.     

Nestling presence affects the anti-predator response of adult superb fairy-wrens (Malurus cyaneus)

Nest predation accounts for the majority of nesting failure, and hence there has been strong selection on behaviour to reduce nest predation, including patterns of nest defence. Here, we test risk-taking behaviour to experimentally placed predators in the presence or absence of nestlings. We use the superb fairy-wren (Malurus cyaneus) to test the prediction that vigilance will be comparable with and without nestlings, but that alarm vocalisations will increase when nestlings are present. We found support for both predictions. Adult vigilance of predators was comparable with and without nestlings. Alarm vocalisation intensity was predicted by predator type and nestling presence, and was highest to the snake model in the presence of nestlings. These results point to selection for differentiated nest defence response in relation to predator type and the presence or absence of nestlings.     

Predators Are Attracted to the Olfactory Signals of Prey

Background

Predator attraction to prey social signals can force prey to trade-off the social imperatives to communicate against the profound effect of predation on their future fitness. These tradeoffs underlie theories on the design and evolution of conspecific signalling systems and have received much attention in visual and acoustic signalling modes. Yet while most territorial mammals communicate using olfactory signals and olfactory hunting is widespread in predators, evidence for the attraction of predators to prey olfactory signals under field conditions is lacking.

Methodology/Principal Findings

To redress this fundamental issue, we examined the attraction of free-roaming predators to discrete patches of scents collected from groups of two and six adult, male house mice, Mus domesticus, which primarily communicate through olfaction. Olfactorily-hunting predators were rapidly attracted to mouse scent signals, visiting mouse scented locations sooner, and in greater number, than control locations. There were no effects of signal concentration on predator attraction to their prey''s signals.

Conclusions/Significance

This implies that communication will be costly if conspecific receivers and eavesdropping predators are simultaneously attracted to a signal. Significantly, our results also suggest that receivers may be at greater risk of predation when communicating than signallers, as receivers must visit risky patches of scent to perform their half of the communication equation, while signallers need not.     

Dangerous liaisons: the predation risks of receiving social signals

Individuals are at risk when communicating because conspicuous signals attract both conspecifics and eavesdropping predators. This predation cost of communicating has typically been attributed to signalling individuals because of their conspicuous role, and is a core concept within sexual selection and communication ecology. But, if predators are attracted to signals, then receivers, both intended or otherwise, may also find themselves at risk of predation. Here, we review the theoretical basis and empirical evidence that receiving also carries a risk of predation. We distinguish between the risks of receiving and responding to signals, and we argue that receivers of signals that are long lived, are highly predictable in time or place and/or cannot be received quickly are likely to be at greater risk of predation compared to receivers of signals without these properties. We review recent empirical evidence from a variety of taxa that supports the hypothesis that receivers (including heterospecific prey) are aware of these risks and that they modify their behaviour to balance the risks against the benefits of receiving under predation threat. We also discuss the wider implications of risky receiving for receiving and signalling behaviour in prey, as well as for the prey's predators.     

Anti‐Predator Signals in the Chaffinch Fringilla coelebs in Response to Habitat Structure and Different Predator Types

Many animals respond to the presence of predators with conspicuous signals such as alarm calling. These signals may aid the detection of the predator by conspecifics or may deter the predator from attack. The advantages of such signals may be dependent upon predator type and habitat type. We measured signalling behaviours (alarm calling and tail flicking) in foraging chaffinches in response to different predator models (hawk and pigeon control, cat and plastic box as control). In addition we measured responses to a cat model when chaffinches were foraging in different habitat structures (obstructed vs. open). There was no difference in the number of individual chaffinches alarm calling in obstructed vs. open habitat, but birds tail flicked more in open habitat, suggesting that tail flicking acts as a visual signal to the predator or conspecifics and therefore unlike auditory cues is influenced by habitat structure. Chaffinches were also more likely to tail flick in response to the cat model than the other three models. Our results are consistent with the idea that animals may respond to ground predators, which spend a large amount of time observing prey before attack, by using signalling behaviours, such as tail flicking and alarm calling. Further work on prey selection by predators is needed to separate the functions of signalling behaviour in response to predators.     

Eavesdropping on heterospecific alarm calls: from mechanisms to consequences

Animals often gather information from other species by eavesdropping on signals intended for others. We review the extent, benefits, mechanisms, and ecological and evolutionary consequences of eavesdropping on other species' alarm calls. Eavesdropping has been shown experimentally in about 70 vertebrate species, and can entail closely or distantly related species. The benefits of eavesdropping include prompting immediate anti‐predator responses, indirect enhancement of foraging or changed habitat use, and learning about predators. Eavesdropping on heterospecifics can provide more eyes looking for danger, complementary information to that from conspecifics, and potentially information at reduced cost. The response to heterospecific calls can be unlearned or learned. Unlearned responses occur when heterospecific calls have acoustic features similar to that used to recognize conspecific calls, or acoustic properties such as harsh sounds that prompt attention and may allow recognition or facilitate learning. Learning to recognize heterospecific alarm calls is probably essential to allow recognition of the diversity of alarm calls, but the evidence is largely indirect. The value of eavesdropping on different species is affected by problems of signal interception and the relevance of heterospecific alarm calls to the listener. These constraints on eavesdropping will affect how information flows among species and thus affect community function. Some species are ‘keystone’ information producers, while others largely seek information, and these differences probably affect the formation and function of mixed‐species groups. Eavesdroppers might also integrate alarm calls from multiple species to extract relevant and reliable information. Eavesdropping appears to set the stage for the evolution of interspecific deception and communication, and potentially affects communication within species. Overall, we now know that eavesdropping on heterospecific alarm calls is an important source of information for many species across the globe, and there are ample opportunities for research on mechanisms, fitness consequences and implications for community function and signalling evolution.     

The consequences of crowned eagle central-place foraging on predation risk in monkeys

The African crowned eagle (Stepahnoaetus coronatus) is the primary predator for arboreal primates throughout sub-Saharan forests. Monkeys typically respond with alarm calls when they are aware of the presence of crowned eagles and such calls can be considered a corollary of predation risk within primate groups. Alarm calls from six species of monkeys were recorded across the home range of an eagle pair in Taï National Park, Côte d''Ivoire. Spatial and temporal variation in primate alarm calling was found to be related to eagle ranging behaviour according to the predictions of central-place foraging models. Radio-tracking data indicate that eagle activity is higher in the centre of their home range and monkey alarm-calling rates are correspondingly elevated near eagle nests as opposed to farther away. Alarm-calling rates are also temporally coupled with measures of eagle activity. There were considerable differences between the species in both rates and spatial patterns of alarm calling. The variation we measure in predation risk is expected to have consequences at the behavioural and population level.     

The signaller's dilemma: a cost-benefit analysis of public and private communication

Background

Understanding the diversity of animal signals requires knowledge of factors which may influence the different stages of communication, from the production of a signal by the sender up to the detection, identification and final decision-making in the receiver. Yet, many studies on signalling systems focus exclusively on the sender, and often ignore the receiver side and the ecological conditions under which signals evolve.

Methodology/Principal Findings

We study a neotropical katydid which uses airborne sound for long distance communication, but also an alternative form of private signalling through substrate vibration. We quantified the strength of predation by bats which eavesdrop on the airborne sound signal, by analysing insect remains at roosts of a bat family. Males do not arbitrarily use one or the other channel for communication, but spend more time with private signalling under full moon conditions, when the nocturnal rainforest favours predation by visually hunting predators. Measurements of metabolic CO₂-production rate indicate that the energy necessary for signalling increases 3-fold in full moon nights when private signalling is favoured. The background noise level for the airborne sound channel can amount to 70 dB SPL, whereas it is low in the vibration channel in the low frequency range of the vibration signal. The active space of the airborne sound signal varies between 22 and 35 meters, contrasting with about 4 meters with the vibration signal transmitted on the insect''s favourite roost plant. Signal perception was studied using neurophysiological methods under outdoor conditions, which is more reliable for the private mode of communication.

Conclusions/Significance

Our results demonstrate the complex effects of ecological conditions, such as predation, nocturnal ambient light levels, and masking noise levels on the performance of receivers in detecting mating signals, and that the net advantage or disadvantage of a mode of communication strongly depends on these conditions.     

Evolutionary novelty in communication between the sexes

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.     

Essay on Contemporary Issues in Ethology: Variation among Mammalian Alarm Call Systems and the Problem of Meaning in Animal Signals

Understanding the information conveyed by animal signals requires studies of both production and perception. It is important to determine the relationship between signal morphology and the circumstances of production, the way signaller behavior varies with motivational state and the role of context in mediating responses to signals. Alarm calls are well-suited to research of this type because they are widespread in birds and mammals and typically evoke unambiguous responses. We review studies of alarm calling in primates and ground-dwelling sciurid rodents, concentrating especially on whether these signal systems may be viewed as ‘functionally referential’, that is, as conveying sufficient information about an event for receivers to select appropriate responses. Comparisons of the physical, behavioral and habitat characteristics of these species suggest that incompatibility of the escape responses required to avoid different classes of predators may have been an important factor in the evolution of functionally referential alarm calls.     

Acoustic alarm signalling facilitates predator protection of treehoppers by mutualist ant bodyguards

Mutualism is a net positive interaction that includes varying degrees of both costs and benefits. Because tension between the costs and benefits of mutualism can lead to evolutionary instability, identifying mechanisms that regulate investment between partners is critical to understanding the evolution and maintenance of mutualism. Recently, studies have highlighted the importance of interspecific signalling as one mechanism for regulating investment between mutualist partners. Here, we provide evidence for interspecific alarm signalling in an insect protection mutualism and we demonstrate a functional link between this acoustic signalling and efficacy of protection. The treehopper Publilia concava Say (Hemiptera: Membracidae) is an insect that provides ants with a carbohydrate-rich excretion called honeydew in return for protection from predators. Adults of this species produce distinct vibrational signals in the context of predator encounters. In laboratory trials, putative alarm signal production significantly increased following initial contact with ladybeetle predators (primarily Harmonia axyridis Pallas, Coleoptera: Coccinellidae), but not following initial contact with ants. In field trials, playback of a recorded treehopper alarm signal resulted in a significant increase in both ant activity and the probability of ladybeetle discovery by ants relative to both silence and treehopper courtship signal controls. Our results show that P. concava treehoppers produce alarm signals in response to predator threat and that this signalling can increase effectiveness of predator protection by ants.     

Chemical Alarm Signals Enhance Survival of Brook Charr (Salvelinus fontinalis) During Encounters with Predatory Chain Pickerel (Esox niger)

A diversity of aquatic organisms release chemical alarm signals when attacked or captured by a predator. These alarm signals are thought to warn other conspecifics of danger and, consequently, may benefit receivers by increasing their survival. Here we experimentally investigated the differences in behaviour and survival of hatchery-reared juvenile brook charr Salvelinus fontinalis that had been exposed to either brook charr skin extract (experimental treatment) or a control of swordtail skin extract (control treatment). Charr exposed to conspecific skin extract exhibited a significant reduction in movement and/or altered their foraging behaviour in the laboratory when compared with charr exposed to swordtail skin extract. We also exposed charr to either water conditioned by a single brook charr disturbed by a predatory bird model or water conditioned by a single undisturbed brook charr. Charr exposed to disturbance signals reduced activity significantly more than charr exposed to chemical stimuli from undisturbed charr. These results demonstrate the existence of both damage-released alarm signals and disturbance signals in brook charr. Wild brook charr also responded to damage-released alarm cues under natural conditions. Charr avoided areas of a stream with minnow traps labelled with conspecific alarm cues vs. control cues. During staged encounters with chain pickerel Esox niger in the laboratory, predator-naive charr fry were better able to evade the predator if they were previously warned by an alarm signal, thus suggesting a survival benefit to receivers. Collectively, these results demonstrate that the presence of alarm signals in brook charr has important implications for understanding predator–prey interactions.     

Semantic communication in birds: evidence from field research over the past two decades

What do animal signals mean? This is a central question in studies on animal communication. Research into the semantics of animal signals began in 1980, with evidence that alarm calls of a non-human primate designated predators as external referents. These studies have challenged the historical assumption that such referential signaling is a unique feature of human language and produced a paradigm shift in animal communication research. Over the past two decades, an increasing number of field studies have revealed similar complexity in anti-predator communication of birds. The acoustic structures of avian alarm calls show a high degree of variation in pitch, duration, shape, and repetition rate. In addition to such distinct and graded variations, several birds combine discrete types of notes or calls into higher complex sequences. These variations in alarm calls are typically associated with the predator’s attributes, such as predator type and distance, and receivers respond to them with appropriate anti-predator behaviors. Although alarm calls of several bird species, as well as those of monkeys, appear to denote predator attributes, almost nothing is known about the cognitive processes that underlie the production and perception of these signals. In this review, I explore the existing evidence for referential signaling in birds and highlight the importance of the cognitive approach to animal communication research. I hope this review will promote further investigations of alarm-calling behavior in birds and will help enhance our understanding of the ecology and evolution of semantic communication.