Mouse alarm pheromone shares structural similarity with predator scents.

Sensing the chemical warnings present in the environment is essential for species survival. In mammals, this form of danger communication occurs via the release of natural predator scents that can involuntarily warn the prey or by the production of alarm pheromones by the stressed prey alerting its conspecifics. Although we previously identified the olfactory Grueneberg ganglion as the sensory organ through which mammalian alarm pheromones signal a threatening situation, the chemical nature of these cues remains elusive. We here identify, through chemical analysis in combination with a series of physiological and behavioral tests, the chemical structure of a mouse alarm pheromone. To successfully recognize the volatile cues that signal danger, we based our selection on their activation of the mouse olfactory Grueneberg ganglion and the concomitant display of innate fear reactions. Interestingly, we found that the chemical structure of the identified mouse alarm pheromone has similar features as the sulfur-containing volatiles that are released by predating carnivores. Our findings thus not only reveal a chemical Leitmotiv that underlies signaling of fear, but also point to a double role for the olfactory Grueneberg ganglion in intraspecies as well as interspecies communication of danger.

Identification of pyridine analogs as new predator-derived kairomones.

In the wild, animals have developed survival strategies relying on their senses. The individual ability to identify threatening situations is crucial and leads to increase in the overall fitness of the species. Rodents, for example have developed in their nasal cavities specialized olfactory neurons implicated in the detection of volatile cues encoding for impending danger such as predator scents or alarm pheromones. In particular, the neurons of the Grueneberg ganglion (GG), an olfactory subsystem, are implicated in the detection of danger cues sharing a similar chemical signature, a heterocyclic sulfur- or nitrogen-containing motif. Here we used a "from the wild to the lab" approach to identify new molecules that are involuntarily emitted by predators and that initiate fear-related responses in the recipient animal, the putative prey. We collected urines from carnivores as sources of predator scents and first verified their impact on the blood pressure of the mice. With this approach, the urine of the mountain lion emerged as the most potent source of chemical stress. We then identified in this biological fluid, new volatile cues with characteristic GG-related fingerprints, in particular the methylated pyridine structures, 2,4-lutidine and its analogs. We finally verified their encoded danger quality and demonstrated their ability to mimic the effects of the predator urine on GG neurons, on mice blood pressure and in behavioral experiments. In summary, we were able to identify here, with the use of an integrative approach, new relevant molecules, the pyridine analogs, implicated in interspecies danger communication.

Whole-body cortisol increases after direct and visual contact with a predator in zebrafish, Danio rerio

Ornamental fish may be severely affected by a stressful environment. Stressors impair the immune response, reproduction and growth rate; thus, the identification of possible stressors will aid to improve the overall quality of ornamental fish. The aim of this study was to determine whole-body cortisol of adult zebrafish, Danio rerio, following visual or direct contact with a predator species. Zebrafish were distributed in three groups: the first group, which consisted of zebrafish reared completely isolated of the predator, was considered the negative control; the second group, in which the predator, Parachromis managuensis was stocked together with zebrafish, was considered the positive control; the third group consisted of zebrafish stocked in a glass aquarium, with direct visual contact with the predator. The mean whole-body cortisol concentration in zebrafish from the negative control was 6.78 +/- 1.12 ng g(-1), a concentration statistically lower than that found in zebrafish having visual contact with the predator (9.26 +/- 0.88 ng g(-1)) which, in turn, was statistically lower than the mean whole-body cortisol of the positive control group (12.35 +/- 1.59 ng g(-1)). The higher whole-body cortisol concentration found in fish from the positive control can be attributed to the detection, by the zebrafish, of relevant risk situations that may involve a combination of chemical, olfactory and visual cues. One of the functions of elevated cortisol is to mobilize energy from body resources to cope with stress. The elevation of whole-body cortisol in fish subjected to visual contact with the predator involves only the visual cue in the recognition of predation risk. We hypothesized that the zebrafish could recognize predator characteristics in P managuensis, such as length, shape, color and behavior. Nonetheless, the elevation of whole-body cortisol in zebrafish suggested that the visual contact of the predator may elicit a stress response in prey fish. This assertion has a strong practical application concerning the species distribution in ornamental fish markets in which prey species should not be allowed to see predator species. Minimizing visual contact between prey and predator fish may improve the quality, viability and welfare of small fish in ornamental fish markets. (c) 2007 Elsevier B.V. All rights reserved.

Chemical cues related to conspecific size in pintado catfish, Pseudoplatystoma coruscans

The pintado (Pseudoplatystoma coruscans) is a ferocious carnivorous catfish with evident cannibalistic behaviour; its nocturnal habits are related to its ability to use predominately chemical sensorial modalities. This study investigated whether the pintado distinguishes conspecifics of different body sizes using chemical cues, which may reflect different physiological conditions such as hunger or stress. Pintados were observed when receiving water conditioned by either larger or similar-size conspecifics. A control group consisted of pintados receiving unconditioned water. Twelve repetitions were used for each condition. Feeding-like behaviours were investigated in the receiver fish and showed that they responded only to the conditioned water. Furthermore, a higher frequency of responses occurred when the water was conditioned by a similar-size conspecific. Thus, it is concluded that pintados are able to recognize conspecific size by chemical cues related to size and that this ability contributes to the individual's decision making on whether to approach or to avoid the conspecific.

Disturbance chemical cues determine changes in spatial occupation by the convict cichlid Archocentrus nigrofasciatus

I studied the effect of disturbance chemical cues on fish that make trade-offs between foraging in an open area and remaining in a safe refuge. I used convict cichlids Archocentrus nigrofasciatus that were either visually exposed to a predator (n = 8) or exposed to water conditioned by chemical cues from disturbed conspecifics (n = 8). Fish visually exposed to a predator decreased their ingestion rate and spent more time in the refuge than in the foraging area, while fish receiving water from frightened conspecifics did not alter their ingestion rate or time spent in the refuge and foraging site, but increased their spatial occupation (i.e., motion). These results suggest that convict cichlids recognized the predator by visual cues. Moreover, disturbance cues are a form of threatening public information that may increase fish spatial occupation due to increased exploring behaviour; but is not sufficiently alarming to alter feeding or increase refuge use. (C) 2004 Elsevier B.V. All rights reserved.

The scent of stress: Pintado catfish differentially respond to chemical cues from stressed conspecifics

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Black sea urchins evaluate predation risk using chemical signals from a predator and injured con- and heterospecific prey

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)

The 'club' cell and behavioural and physiological responses to chemical alarm cues in the Nile tilapia

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Predator and Heterospecific Stimuli Alter Behavior in Cattle

Wild and domestic ungulates modify their behavior in the presence of olfactory and visual cues of predators but investigations have not exposed a domestic species to a series of cues representing various predators and other ungulate herbivores.We used wolf (Canis lupus), mountain lion (Puma concolor), and mule deer (Odocoileus hemionus) stimuli (olfactory and visual), and a control (no stimuli) to experimentally test for differences in behavior of cattle (Bos taurus) raised in Arizona. We measured (1) vigilance, (2) foraging rates, (3) giving up density (GUD) of high quality foods and (4) time spent in high quality forage locations in response to location of stimuli treatments. In general, we found a consistent pattern in that wolf and deer treatments caused disparate results in all 4 response variables. Wolf stimuli significantly increased cattle vigilance and decreased cattle foraging rates; conversely, deer stimuli significantly increased cattle foraging rate and increased cattle use of high quality forage areas containing stimuli. Mountain lion stimuli did not significantly impact any of the 4 response variables. Our findings suggest that domestic herbivores react to predatory stimuli, can differentiate between stimuli representing two predatory species, and suggest that cattle may reduce antipredatory behaviour when near heterospecifics.

The scent of stress: Pintado catfish differentially respond to chemical cues from stressed conspecifics

We examined whether pintado catfish (Pseudoplatystoma corruscans) can discriminate between scents of non-injured conspecifics stressed by a predator or by confinement and how fish use this information in the trade-off between feeding and predator avoidance. In the confinement stress condition, fish ingested the food, whereas in the predator stress condition, fish did not eat. This finding and comparisons of the latency to food ingestion and the time spent swimming between the confinement and predator-stress conditions indicated that pintado catfish can discriminate between conspecifics stressed by a predator or confinement using chemical cues, and use this information for adjusting the trade-off between food intake and predator avoidance.

The role of chemotactile cues in interspecific interactions among Central-European arthropod communities

In einem Ökosystem beeinflussen sich Tiere gegenseitig in erster Linie durch direkte Interaktionen. Ihr Verhalten kann aber auch indirekt durch chemotaktile Stoffe die andere Tiere in der Umwelt hinterlassen beeinflusst werden. Vergleichbar zu direkten Interaktionen können indirekt ausgelöste Verhaltensänderungen einen starken Einfluss auf Populationsdynamiken und Gemeinschaftsstrukturen eines Ökosystems haben. Obwohl das daran gehegte Interesse der Ökologen in den letzten Jahrzenten stark gestiegen ist, fehlen immer noch Studien, welche über mehrere Arten hinweg versuchen die übergreifende Relevanz von chemotaktilen Stoffen herauszufinden. Im Rahmen meiner Doktorarbeit untersuchte ich daher wie sich mehrere mitteleuropäische Arthropodenarten, abhängig von deren interspezifischen Räuber-Beute- und Konkurrenzbeziehungen, mittels chemotaktiler Stoffe beeinflussen können. Mithilfe unterschiedlicher Verhaltensversuche konnte ich empirisch nachweisen, dass verschiedene Arthropoden chemotaktile Stoffe zu ihrem eigenen Vorteil nutzen können. Außerdem zeigen meine Ergebnisse, dass die Verhaltensänderungen artspezifisch und abhängig von den jeweiligen Lebenszyklen und den damit verbundenen Eigenschaften (z.B. Körpergröße, Häufigkeit oder Rangordnung) der beteiligten Arten sind. Ich vermute daher, dass Arthropoden chemotaktile Stoffe ihrer Gegenspieler wahrnehmen und interpretieren können. Eine Verhaltensänderung scheint jedoch nur dann statt zu finden wenn ein Nichtreagieren starke Fitnesskosten mit sich führen würde. Zusammenfassend zeigen die Ergebnisse meiner Doktorarbeit, wie wichtig es ist, die Bedeutung von chemotaktilen Stoffen innerhalb vieler Arten einer Gemeinschaft zu testen, um die den Verhaltensänderungen zugrundeliegenden Ursachen identifizieren zu können. Dies wiederum stellt die Grundlage, um die ökologische Relevanz von chemotaktilen Stoffen und deren mögliche Effekte auf Ökosystemfunktionen besser zu verstehen.

Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor)

Global declines in amphibians likely have multiple causes, including widespread pesticide use. Our knowledge of pesticide effects on amphibians is largely limited to short-term (4-d) toxicity tests conducted under highly artificial conditions to determine lethal concentrations (LC50). We found that if we used slightly longer exposure times (10–16 d), low concentrations of the pesticide carbaryl (3–4% of LC504-d) killed 10–60% of gray treefrog (Hyla versicolor) tadpoles. If predatory cues also were present, the pesticide became 2–4 times more lethal, killing 60–98% of tadpoles. Thus, under more realistic conditions of increased exposure times and predatory stress, current application rates for carbaryl can potentially devastate gray treefrog populations. Further, because predator-induced stress is ubiquitous in animals and carbaryl's mode of action is common to many pesticides, these negative impacts may be widespread in nature.

Antipredator behavior and cue recognition by multiple Everglades prey to a novel cichlid predator

Novel predator introductions are thought to have a high impact on native prey, especially in freshwater systems. Prey may fail to recognize predators as a threat, or show inappropriate or ineffective responses. The ability of prey to recognize and respond appropriately to novel predators may depend on the prey’s use of general or specific cues to detect predation threats.We used laboratory experiments to examine the ability of three native Everglades prey species (Eastern mosquitofish, flagfish and riverine grass shrimp) to respond to the presence, as well as to the chemical and visual cues of a native predator (warmouth) and a recentlyintroduced non-native predator (African jewelfish). We used prey from populations that had not previously encountered jewelfish. Despite this novelty, the native warmouth and nonnative jewelfish had overall similar predatory effects, except on mosquitofish, which suffered higher warmouth predation. When predators were present, the three prey taxa showed consistent and strong responses to the non-native jewelfish, which were similar in magnitude to the responses exhibited to the native warmouth. When cues were presented, fish prey responded largely to chemical cues, while shrimp showed no response to either chemical or visual cues. Overall, responses by mosquitofish and flagfish to chemical cues indicated low differentiation among cue types, with similar responses to general and specific cues. The fact that antipredator behaviours were similar toward native and non-native predators suggests that the susceptibility to a novel fish predator may be similar to that of native fishes, and prey may overcome predator novelty, at least when predators are confamilial to other common and longer-established non-native threats.

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

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

Predator nonconsumptive effects on prey recruitment weaken with recruit density, supplementary material

We investigated the nonconsumptive effects (NCEs) of predatory dogwhelks (Nucella lapillus) on intertidal barnacle (Semibalanus balanoides) recruitment through field experiments on the Gulf of St. Lawrence coast and the Atlantic coast of Nova Scotia, Canada. We studied the recruitment seasons (May-June) of 2011 and 2013. In 2011, the Gulf coast had five times more nearshore phytoplankton (food for barnacle larvae and recruits) during the recruitment season and yielded a 58% higher barnacle recruit density than the Atlantic coast at the end of the recruitment season. In 2013, phytoplankton levels and barnacle recruit density were similar on both coasts and also lower than for the Gulf coast in 2011. Using the comparative-experimental method, the manipulation of dogwhelk presence (without allowing physical contact with prey) revealed that dogwhelk cues limited barnacle recruitment under moderate recruit densities (Atlantic 2011/2013 and Gulf 2013) but had no effect under a high recruit density (Gulf 2011). Barnacle recruits attract settling larvae through chemical cues. Thus, the highest recruit density appears to have neutralized dogwhelk effects. This study suggests that the predation risk perceived by settling larvae may decrease with increasing recruit density and that prey food supply may indirectly influence predator NCEs on prey recruitment.