Predator Kairomones Research Articles

A flavonol present in cocoa [(−)epicatechin] enhances snail memory

Dietary consumption of flavonoids (plant phytochemicals) may improve memory and neuro-cognitive performance, though the mechanism is poorly understood. Previous work has assessed cognitive effects in vertebrates; here we assess the suitability of Lymnaea stagnalis as an invertebrate model to elucidate the effects of flavonoids on cognition. (-)Epicatechin (epi) is a flavonoid present in cocoa, green tea and red wine. We studied its effects on basic snail behaviours (aerial respiration and locomotion), long-term memory (LTM) formation and memory extinction of operantly conditioned aerial respiratory behaviour. We found no significant effect of epi exposure (15 mg l(-1)) on either locomotion or aerial respiration. However, when snails were operantly conditioned in epi for a single 0.5 h training session, which typically results in memory lasting ~3 h, they formed LTM lasting at least 24 h. Snails exposed to epi also showed significantly increased resistance to extinction, consistent with the hypothesis that epi induces a more persistent LTM. Thus training in epi facilitates LTM formation and results in a more persistent and stronger memory. Previous work has indicated that memory-enhancing stressors (predator kairomones and KCl) act via sensory input from the osphradium and are dependent on a serotonergic (5-HT) signalling pathway. Here we found that the effects of epi on LTM were independent of osphradial input and 5-HT, demonstrating that an alternative mechanism of memory enhancement exists in L. stagnalis. Our data are consistent with the notion that dietary sources of epi can improve cognitive abilities, and that L. stagnalis is a suitable model with which to elucidate neuronal mechanisms.

Responses of three species of mosquito larvae to the presence of predatory dragonfly and damselfly larvae

AbstractAlthough predators have been extensively used in the biological control of mosquito larvae, their efficacy will be reduced if the larvae are able to detect and respond to their presence. This ability to detect and respond to the unseen presence of dragonfly or damselfly larvae was investigated for the larvae of three mosquito species (all Diptera: Culicidae) to see whether they either altered their rate of development or their feeding behaviour. The development of Culex quinquefasciatus Say and Culiseta longiareolata Macquart larvae was not affected by exudates from either predator, but Culex sinaiticus Kirkpatrick developed significantly slower when reared in the presence of a caged dragonfly larva and produced adults that were significantly smaller, indicating that they probably reduced feeding activity to make themselves less detectable to the predator. This only occurred when the dragonflies were fed in situ (in the presence of the mosquito larva) and not when removed for feeding, so that although this removed predator kairomones, other cues such as vibrations caused by movement of the predator may also be involved. In addition, the mosquito larvae responded to dragonfly larvae, but not to damselfly larvae. The depth of the water in which the mosquito larvae were reared had no effect on their response to the dragonfly. All three mosquito species significantly increased surface filter‐feeding, when a predator was present in the water (compared with controls where no predator was present), at the expense of bottom scraping. In Cx. sinaiticus (but not the other two species), surface filter‐feeding was greater when a dragonfly was present, compared with a damselfly. In the experimental conditions of one predator per 250 ml water, all three mosquito species were thus able to detect dragonfly and damselfly larvae (and distinguish between the two), but their response varied among species.

Social snails: the effect of social isolation on cognition is dependent on environmental context

Social isolation is often considered to have negative effects on cognitive function in a wide range of species. Here we assess how environmental context alters the effect of isolation on long-term memory formation (24 h) in the pond snail Lymnaea stagnalis. We operantly trained snails to reduce aerial respiration in hypoxia following exposure to one of three social conditions: (1) maintained and trained in groups; (2) maintained in groups, trained in isolation; or (3) maintained and trained in isolation. In addition, snails also experienced four stress exposure levels: control, exposure to low calcium availability, predator kairomone exposure during training or a combination of low calcium and predator kairomones. Snails isolated during training alone demonstrated no difference in memory formation compared with the snails trained in groups. Maintaining snails in social isolation for 8 days prior to training had a neutral effect on memory in control conditions or in the presence of predator kairomones alone. However, social isolation enhanced long-term memory formation in snails exposed to low calcium conditions, a stress that blocks memory formation in snails maintained in groups. Conversely, when exposed to low calcium and predator kairomones combined, grouped snails normally demonstrate long-term memory, but following maintenance in isolation long-term memory was blocked. Therefore, the effect of social isolation on cognitive function is highly dependent on the environmental context in which it is experienced.

Behavioral plasticity in an invaded system: non-native whelks recognize risk from native crabs

Inducible defenses have the potential to affect both invasion success and the structure of invaded communities. However, little is known about the cues used for risk-recognition that influence the expression of inducible defenses in invasive prey, because they involve a novel threat. In laboratory experiments, we investigated behavioral defenses induced by a native crab on two invasive oyster drills (marine whelks Urosalpinx cinerea and Ocinebrina inornata). Both drills hid more often and reduced their feeding rates when they detected predators consuming conspecific prey. Examination of the responses of U. cinerea to specific cue sources (predator kairomones, conspecific alarm cues) indicated that this species had the strongest responses to cues from injured conspecifics, but that it did recognize the novel crab predator. Our observation of native predator (per se) recognition by an invasive marine prey is novel. In addition, we observed that neither species of drill reduced their defensive behavior to reflect predation risk shared by a group of prey. The lack of density dependence in risk-assessment could cause populations of invasive prey to transmit both quantitatively and qualitatively different community effects over the course of an invasion as abundance changes. Together, these findings demonstrate several ways that the risk-assessment strategies could be important in establishment and post-establishment dynamics of invasive prey.

Interaction between environmental stressors mediated via the same sensory pathway

The great pond snail, Lymnaea stagnalis, is a calciphile, requiring approximately 20 mg/l dissolved calcium for natural populations to live long and prosper. However, despite population survival we have previously demonstrated that acute exposure for 1 week to low environmental calcium (20 mg/l) acts as a stressor on the snail, blocking long-term memory (LTM) formation. This response to calcium availability is mediated by the snail directly sensing the calcium concentration in its environment using a sensory structure called the osphradium. In addition to sensing the calcium environment, the osphradium also mediates the response to predator kairomones which has an opposite effect on memory i.e. kairomone exposure during training enhances LTM formation. Here we demonstrate how these two stressors (low calcium availability and predator kairomones), that alter memory formation in opposing directions via the same sensory system, interact when experienced simultaneously.

Rotifer population spread in relation to food, density and predation risk in an experimental system

1. Despite the popular use of diffusion models to predict the spatial spread of populations over time, we currently know little about how diffusion rates change with the state of the environment or the internal condition of individuals. To address this gap in our understanding, we measured rates of spread for many populations of the rotifer Brachionus calyciflorus in a suite of well-replicated experiments. 2. In one set of experiments, we manipulated food availability and population density along a continuous range of densities. In a second set, we manipulated the internal state of entire populations via food deprivation and exposure to predator kairomones. 3. Across replicate populations, diffusion rates were positively correlated with conspecific density. Diffusion rates were negatively correlated with food availability, especially when conspecific density was high. Diffusion rates of food-deprived populations or those exposed to predation risk were lower than controls. 4. Our results provide direct experimental evidence that rates of population spread are conditional on population density, food availability, body condition and predation risk.

Microgeographical variability in long-term memory formation in the pond snail, Lymnaea stagnalis

The ability to learn and form long-term memory (LTM) can enhance an animal’s fitness, for example by allowing it to remember predators, food sources or conspecific interactions. Here we used the great pond snail, Lymnaea stagnalis, to assess whether variability among natural populations in memory-forming capabilities occurs on a microgeographical scale. We used four populations from two different habitat types separated by 1–20 km: two from large, permanent canals and two from small, fluctuating drainage ditches. Of the four populations tested, only one, from a small drainage ditch, formed LTM lasting 24 h after a 0.5 h operant training session to reduce aerial respiration in hypoxic conditions when trained in pond water alone. Each of the four populations demonstrated the same memory retention capability over 2 consecutive years, indicating temporal stability within each population tested. Despite this lack of a consistent ability for LTM formation among populations in pond water, all populations tested demonstrated LTM formation in the presence of predator kairomones, from both tench, Tinca tinca, a predatory fish present at the large canal sites, and crayfish, Pacifastacus leniusculus, known to extend memory in a Dutch L. stagnalis population. Therefore, while we found differences between populations in LTM retention after training in pond water, the response to predator kairomones during training, an ecologically relevant stressor, appears highly conserved in this species, enabling all populations to form LTM.

Toxic Prey and Predator Avoidance: Responses of Toxic Newts to Chemical Stimuli from a Predator and Injured Conspecifics

Abstract Predator avoidance behavior minimizes predation risk because the prey never enters the perceptual field of the predator. For toxic species, avoiding potential predators indiscriminately is unlikely to be the best predator avoidance strategy because many predators will be incapable of consuming the toxin. We investigated the role of chemical-based avoidance behavior in predator-prey interactions between a toxic prey species, the Rough-skinned Newt (Taricha granulosa), and its major predator, the Common Garter Snake (Thamnophis sirtalis). Terrestrial newts avoided predator kairomones only when the predator had recently consumed a conspecific, but did not avoid damage-released alarm cues. These results indicate newts may be able to chemically differentiate between toxin-resistant and toxin-sensitive snakes in the same population and avoid only those snakes actively preying upon their cohort.

Prey risk assessment depends on conspecific density

In many systems, the number of prey killed by predators increases with prey density. This in turn generates higher levels of the indirect signals that prey use to assess predation risk. A model developed by Peacor (2003) showed that prey that respond to predator cues without accounting for conspecific density will consistently over‐ or under‐estimate risk and therefore invest improperly in anti‐predator defense. We tested this model using Rana temporaria tadpoles as prey and Aeshna cyanea dragonfly larvae as predators. As assumed by the model, prey reduced risky activity with increasing concentrations of predator kairomones and increased activity at high prey density. However, prey did not react to changes in cue or density if the ratio of cue‐to‐density remained constant. Prey therefore monitored their per capita risk, strongly supporting Peacor's model.

Experimental evidence that induced defenses promote coexistence of zooplanktonic populations

Theoretical predictions suggest that adaptive phenotypic plasticity, and induced defenses in particular, exert a stabilizing effect on ecological systems and increase the likelihood of species coexistence. Nonetheless, up to now, there is little empirical support for this hypothesized mechanism of diversity preservation. We experimentally assessed the effects of induction of plastic morphological responses triggered by a predator kairomone, on patterns of co-occurrence of two herbivore populations of rotifers (Brachionus calyciflorus and B. havanaensis) sharing resources (Chlorella vulgaris) and predators (Asplanchna brightwelli). To our knowledge, this is the first experimental work conducted at the population level where noninduced and induced states of same prey species are obtained through manipulating the level of predator signal. Our objective was to assess the consequences of induced defenses on the mean population density, population variability, evenness and likelihood of persistence of competitor populations. Our results show that induced defenses promote species coexistence through increasing the likelihood of persistence and evenness of competing populations, over a gradient of resource availability.

Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectusThe present review is one in the special series of reviews on animal–plant interactions.

The interaction between predator and prey is an evolutionary arms race, for which early detection by either party is often the key to success. In aquatic ecosystems, olfaction is an essential source of information for many prey and predators and a number of cues have been shown to play a key role in trait-mediated indirect interactions in aquatic communities. Here, we review the nature and role of predator kairomones, chemical alarm cues, disturbance cues, and diet cues on the behaviour, morphology, life history, and survival of aquatic prey, focusing primarily on the discoveries from the last decade. Many advances in the field have been accomplished: testing the survival value of those chemicals, providing field validation of laboratory results, understanding the extent to which chemically mediated learning may benefit the prey, understanding the role of these chemicals in mediating morphological and life-history adaptations, and most importantly, the selection pressures leading to the evolution of chemical alarm cues. Although considerable advances have been made, several key questions remain, the most urgent of which is to understand the chemistry behind these interactions.

Gene up-regulation in response to predator kairomones in the water flea, Daphnia pulex

BackgroundNumerous cases of predator-induced polyphenisms, in which alternate phenotypes are produced in response to extrinsic stimuli, have been reported in aquatic taxa to date. The genus Daphnia (Branchiopoda, Cladocera) provides a model experimental system for the study of the developmental mechanisms and evolutionary processes associated with predator-induced polyphenisms. In D. pulex, juveniles form neckteeth in response to predatory kairomones released by Chaoborus larvae (Insecta, Diptera).ResultsPrevious studies suggest that the timing of the sensitivity to kairomones in D. pulex can generally be divided into the embryonic and postembryonic developmental periods. We therefore examined which of the genes in the embryonic and first-instar juvenile stages exhibit different expression levels in the presence or absence of predator kairomones. Employing a candidate gene approach and identifying differentially-expressed genes revealed that the morphogenetic factors, Hox3, extradenticle and escargot, were up-regulated by kairomones in the postembryonic stage and may potentially be responsible for defense morph formation. In addition, the juvenile hormone pathway genes, JHAMT and Met, and the insulin signaling pathway genes, InR and IRS-1, were up-regulated in the first-instar stage. It is well known that these hormonal pathways are involved in physiological regulation following morphogenesis in many insect species. During the embryonic stage when morphotypes were determined, one of the novel genes identified by differential display was up-regulated, suggesting that this gene may be related to morphotype determination. Biological functions of the up-regulated genes are discussed in the context of defense morph formation.ConclusionsIt is suggested that, following the reception of kairomone signals, the identified genes are involved in a series of defensive phenotypic alterations and the production of a defensive phenotype.

Behavioral avoidance of injured conspecific and predatory chemical stimuli by larvae of the aquatic caddisfly Hesperophylax occidentalis

Prey animals often encounter situations that hinder their ability to conduct normal fitness-enhancing behaviors. Mating and foraging are frequently interrupted by predator vigilance and avoidance, and antipredator behavior. Many caddisfly larvae build protective cases that are carried with them throughout the aquatic life cycle. However, they are still vulnerable to predation, yet it is unknown the extent caddisflies use chemical cues for predator recognition and avoidance. We exposed larval caddisfly Hesperophylax occidentalis (Banks, 1908) to predatory, conspecific, and heterospecific chemical cues to determine if caddisfly larvae can use chemical stimuli alone for predator recognition and avoidance. Exposure to predator and injured conspecific chemicals elicited significant decreases in activity, while exposure to injured and uninjured heterospecific chemicals yielded no significant change in activity. The extended latency to move following exposure to predator kairomones indicates larval caddisflies utilize chemical cues for predator recognition and avoidance, and a similar decrease in movement associated with exposure to injured conspecifics suggests the presence of a chemical alarm cue.

Developmental plasticity compensates for selected low levels of behavioural avoidance in a freshwater snail

The way in which an organism responds behaviourally to environmental stimuli may either be innate (i.e. expressed without the need for previous experience) or affected by prior experience; but the relative importance of these two mechanisms in controlling antipredator behaviour is, as yet, unclear. We investigated how the avoidance behaviour of juvenile great pond snails, Lymnaea stagnalis (L.), artificially selected for either high or low innate avoidance behaviour, where the snail crawls above the waterline in response to predation cues, differed in terms of their response to prolonged exposure to predator kairomones during their development. Specifically, we tested: (1) whether snails from lines selected for low response showed enhanced crawl-out behaviour following exposure to predator kairomones during development; and (2) whether snails from high-response lines were able to increase their response further when raised in predator kairomone or whether these snails were constrained in their response. Following developmental exposure to kairomones from a predatory fish (i.e. tench, Tinca tinca L.), low-response snails showed an increased avoidance response when exposed to predation (i.e. predator kairomone plus alarm cues), equivalent to that seen in lines selected for high innate responses. In contrast, snails from high-response selection lines showed no change in crawl-out behaviour. These findings suggest that for antipredator behaviour, developmental exposure can compensate for the selected reduction in innate response in L. stagnalis , and that there may be constraints limiting the maximum level of crawl-out behaviour.

Attachment strength, aggregation and movement of the zebra mussel (Dreissena polymorpha, Bivalvia) in the presence of potential predators

We carried out laboratory experiments to study the behaviour of zebra mussels in the presence of predators with different feeding habits: the roach Rutilus rutilus (an efficient molluscivore), the racer goby Neogobius gymnotrachelus, the crayfish Orconectes limosus (facultative molluscivores), and the perch Perca fluviatilis (prefers other kinds of food). We studied three size (length) classes of mussels: small ( 17mm). We measured attachment strength and numbers of individuals forming aggregations after 6-d exposure to predators, as well as horizontal and vertical distances moved by mussels after 24h of exposure. Attachment strength and tendency to form aggregations of small and medium mussels increased in the presence of roach. Medium mussels exposed to perch were also more strongly attached than those in the control treatment (no predators). Large mussels were unaffected by any predators. Predators did not affect horizontal distances moved by all sizes of mussels. Small individuals exposed to roach reduced their upward movement. In most cases, the lack of responses to perch (a non-molluscivore) ruled out any potential influence of fish movements or faeces upon mussels, suggesting an effect of predator kairomones. The exception was the attachment of medium individuals, which also responded to the presence of perch. In this case, responses to other stimuli, e.g. fish movements, could be involved.

Salamander evolution across a latitudinal cline in gape‐limited predation risk

General predictions of community dynamics require that insights derived from local habitats can be scaled up to explain phenomena across geographic scales. Across these larger spatial extents, adaptation can play an increasing role in determining the outcome of species interactions. If local adaptation is common, then our ability to generalize measures of species interaction strength across communities will be limited without an additional understanding of the genetic variation underlying interaction traits. In the context of predator–prey interactions, prey individuals commonly are expected to reduce risky foraging behaviors and subsequent growth under predation threat. However, rapid growth into a large body size can defend against gape‐limited predators, creating a tradeoff between increased predation risk due to elevated foraging activity and decreased predation risk due to large size. Here I combine field observations, natural selection experiments, and common garden assays to understand potential adaptations of spotted salamander Ambystoma maculatum larvae to gape‐limited and gape‐unconstrained predators. Field observations and natural selection trials suggested antagonistic selection on prey body size among ponds dominated by gape‐limited predator salamanders A. opacum and gape‐unconstrained beetle larvae Dytiscus. In common garden experiments, prey from sites with high gape‐limited predation risk grew larger than those from other sites, suggesting the evolution of rapid growth into a prey size refuge. Larvae from all sites grew to a large size when exposed to the gape‐limited N. viridescens predator's kairomones. Hence, induced rapid growth into a size refuge may be an adaptive response to gape‐limited predation risk. Results point to an important role for cross‐community generalizations based on functional classifications of predators by their gape constraints and inter‐site genetic variation in prey growth rates and behaviors.

Plastic phenotypes of antennule shape in Bosmina longirostris controlled by physical stimuli from predators

Three antennule morphotypes in the small cladoceran Bosmina longirostris have been considered to be hereditarily rigid phenotypes. However, we found that monoclonal populations of Bosmina collected from a Japanese lake were composed of individuals with all three antennule types when grown under laboratory conditions. This suggests that each of the morphotypes represents a phenotype of the species. A morphotype named ‚‚pellucida’’ observed in the monoclonal cultures has been considered to be effective in avoiding copepod predations. We therefore hypothesized that the morphotype is induced by factors from the predator, cyclopoid copepod. To test this hypothesis, a laboratory experiment was conducted in which the monoclonal individuals were exposed to the kairomones of the copepod Acanthocyclops with or without physical contacts with the predator. The morphotype was not altered when Bosmina was exposed to the predator kairomone alone, but to direct predation by the copepod. This suggests that the antennule type of B. longirostris is controlled by physical stimuli from the copepod. The individual death rate of B. longirostris resulting from a copepod strike is low, even though the population dynamics of the animals are often governed by copepod predation. This may have made the physical stimuli of attempted predations useful factors for the prey Bosmina.

Taxon‐specific reaction norms to predator cues in a hybridDaphniacomplex

Summary1. Previous studies have shown that interspecific hybridisation is common among taxa from theDaphnia galeata/hyalina/cucullataspecies complex. We investigated the influence of predator kairomones on the morphology and life histories of nine clones belonging to three taxa (pureD. galeata, F1hybrids betweenD. galeataandD. hyalina, and backcrossedD. hyalina) of this species complex. Predators exerting positive (fish) and negative (Chaoboruslarvae) size‐selective predation were tested.2. The most responsive traits were size at maturity and size of neonates. Despite large between‐clone variation, discriminant analysis revealed that the three taxa were distinct from each other in key life‐history traits. F1hybrids did not react in an intermediate way compared to the other taxa: the multivariate distances between F1hybrids and either taxon were larger than between pureD. galeataand backcrossedD. hyalina.3. The average plasticity (calculated across all traits) was similar for all three taxa. With regard to the size at maturity and neonate body size, the strength of the response was a function of the intrinsic values of these traits expressed in the control. For example, for size at maturity, smaller individuals showed a significantly stronger reaction toChaoboruskairomones than larger ones.4. Finally, we monitored seasonal changes in body size, egg number and population density of pureD. galeataand F1hybrids in Greifensee (Switzerland). The two taxa experienced similar seasonal changes in body size but, on some sampling dates, they differed in mean egg number. The observed seasonal changes inDaphniabody size were consistent with what would be expected if the predator assemblage shifted from fish toChaoborusover the course of the summer. The fluctuations in the frequencies ofDaphniataxa, however, were not related to seasonal variation inDaphniabody size.5. Experimental data suggest that temporally heterogeneous predation regimes might be an important condition stabilising the co‐occurrence ofDaphniahybrids with parental taxa. Predation regimes, however, cannot solely explain dynamic changes in taxon frequency in Greifensee.

Linking predator kairomones and turbulence: synergistic effects and ultimate reasons for phenotypic plasticity in Daphnia cucullata

The seasonal change in helmet size in Daphnia cucullata has been studied for over one century. Recently it has been shown that helmets in D. cucullata, which have been found to reduce predator caused mortality, can be induced by chemical cues released by several predatory invertebrates. However, it also has been shown that tur- bulence induces this trait. The relation and interplay of both inducing cues is not known. Here we present results from lab experiments showing that predator cues and turbulence can act synergistically. Both factors in combination induced significantly larger responses, compared to each factor alone, and helmets reached the maximum sizes found in natural lakes. This result might help to explain the observation of large helmets in this species in nature. The ultimate reason behind the turbulence induction is yet unknown. We link both induction factors to predation, as the ultimate reason, by testing the hypothesis that D. cucullata can respond to turbulence produced by swimming invertebrates. We found that helmet growth increased significantly in direct contact to both the heterospecific Daphnia magna and the predator Cyclops sp. Treat- ments which accounted for chemical cues alone did not increase helmet growth in re- sponse to cues from D. magna ,o rCyclops under these conditions. Together, these re- sults indicate that D. cucullata is able to respond to mechanical cues produced by swimming invertebrates. Thus, our study suggests that both chemical cues and turbu- lence generated by predatory invertebrates might act synergistically to induce helmets as effective protection against invertebrate predation.

Inhibition of development of anti‐predator morphology in the small cladoceran Bosmina by an insecticide: impact of an anthropogenic chemical on prey–predator interactions

Summary1. The combined effect of the insecticide carbaryl and the predator (Leptodora kindtii) kairomone was assessed on the development of protuberant morphology in the small cladoceran Bosmina fatalis, a feature which evolved originally as a response to the kairomone. The experiment showed that Bosmina changed its morphology in response to the kairomone, but development was inhibited by carbaryl at a sub‐lethal concentration even in the presence of the kairomone. At the same time, reduction of fecundity was observed in animals exposed to carbaryl.2. A short‐term feeding experiment (B. fatalis versus Leptodora) indicated that such low concentrations of the insecticide had no impact on predation by Leptodora. Thus, it is suggested that the inhibition of development of anti‐predatory defences in Bosmina can increase its vulnerability to predation.3. Such disturbance of chemical communication by the insecticide reduces the individual survival rate of prey Bosmina in the environment with high predator density. On the other hand, reduction of fecundity may result in decreased population growth rate of animals.4. The impact of the insecticide on the anti‐predator morphology in Bosmina (inhibition) was opposite to that in Daphnia (enhancement). This suggests that biochemical induction processes in the development of anti‐predatory morphology are evolutionally different between Daphnia and Bosmina.