Predator-induced Changes Research Articles

Local adaptation in trait-mediated trophic cascades.

Predator-induced changes in prey foraging can influence community dynamics by increasing the abundance of basal resources via a trait-mediated trophic cascade. The strength of these cascades may be altered by eco-evolutionary relationships between predators and prey, but the role of basal resources has received limited attention. We hypothesized that trait-mediated trophic cascade strength may be shaped by selection from trophic levels above and below prey. Field and laboratory experiments used snails (Nucella lapillus) from two regions in the Gulf of Maine (GoM) that vary in basal resource availability (e.g. mussels), seawater temperature, and contact history with the invasive green crab, Carcinus maenas. In field and laboratory experiments, Nucella from both regions foraged on mussels in the presence or absence of green crab risk cues. In the field, Nucella from the northern GoM, where mussels are scarce, were less responsive to risk cues and more responsive to seawater temperature than southern Nucella. In the lab, however, northern Nucella foraged and grew more than southern snails in the presence of risk, but foraging and growth were similar in the absence of risk. We suggest that adaptation to basal resource availability may shape geographical variation in the strength of trait-mediated trophic cascades.

Development under predation risk increases serotonin-signaling, variability of turning behavior and survival in adult fruit flies Drosophila melanogaster.

The development of high-throughput behavioral assays, where numerous individual animals can be analyzed in various experimental conditions, has facilitated the study of animal personality. Previous research showed that isogenic Drosophila melanogaster flies exhibit striking individual non-heritable locomotor handedness. The variability of this trait, i.e., the predictability of left-right turn biases, varies across genotypes and under the influence of neural activity in specific circuits. This suggests that the brain can dynamically regulate the extent of animal personality. It has been recently shown that predators can induce changes in prey phenotypes via lethal or non-lethal effects affecting the serotonergic signaling system. In this study, we tested whether fruit flies grown with predators exhibit higher variability/lower predictability in their turning behavior and higher survival than those grown with no predators in their environment. We confirmed these predictions and found that both effects were blocked when flies were fed an inhibitor (αMW) of serotonin synthesis. The results of this study demonstrate a negative association between the unpredictability of turning behavior of fruit flies and the hunting success of their predators. We also show that the neurotransmitter serotonin controls predator-induced changes in the turning variability of fruit flies, regulating the dynamic control of behavioral predictability.

The role of prey and predator identity in eliciting inducible defenses of Daphnia.

Predators can modify population and community dynamics not only through direct predation, but also through nonconsumptive effects. Predator-induced changes in the traits of prey species are important components of these nonconsumptive effects. While these are well studied in simplified one-predator one-prey settings, relatively little is known about how kairomones act on prey across heterogeneous aquatic ecosystems with diverse identities of predator and prey. Kairomones are, to some extent, predator specific, and can be classified as diet dependent or diet independent. This classification depends on whether the identity of the prey plays a role in eliciting a defense response. In an effort to elucidate how prey and predator identity determines the defense responses in water fleas, we used inducible morphology and life history traits of Daphnia mitsukuri as a model to systematically explore to what extent predator and prey identity, and species composition of the prey community determined the expression of inducible defenses, and to what extent predator-induced responses differed among genotypes. Our results showed that the defense responses of D. mitsukuri mainly relied on diet-dependent kairomones, which were not influenced by fish species identity but were highly dependent on the phylogenetic distances between D. mitsukuri and the prey ingested by fish. This phylogenetic signal is strong, with D. mitsukuri responding only to the kairomones of fish that feed on cladocerans. We also found that the amplitude of the responses to fish kairomones increased with the amount of cladoceran in the dietary community. We observed significant differences in defensive traits among three D. mitsukuri genotypes, but the differences were minor compared with the effects of kairomones themselves. The results of our systematic analyses point to the role of prey phylogeny in eliciting inducible defenses of D. mitsukuri, thereby enriching our understanding of nonconsumptive effects in aquatic ecosystems.

Induced defenses as a management tool: Shaping individuals to their environment

Many prey species can adjust morphology to reduce predation risk in response to predator cues. Enhancing prey defenses using predator cues may improve survival of cultivated species and enhance species restoration efforts, but assessment of such benefits at industrially relevant scales is needed. We examined how raising a model foundation species, oysters (Crassostrea virginica), under commercial hatchery conditions with cues from two common predator species can improve survival across a variety of predator regimes and environmental conditions. Oysters responded to predators by growing stronger shells than controls, but had subtle variations in shell characteristics depending on the predator species. Predator-induced changes significantly increased oyster survival up to 600% and survivorship was maximized when cue source was matched with local predator regime. Overall, our findings demonstrate the utility of using predator cues to enhance the survival of target species across landscapes and highlight the opportunity to employ nontoxic methods to control pest-based mortality.

Sub-chronic administration of fluoxetine does not alter prey-capture or predator avoidance behaviors in adult South African clawed frogs (Xenopus laevis).

Animals will halt foraging efforts and engage defensive behaviors in response to predator cues. Some researchers have proposed that the switch from appetitive to avoidance behavior resembles anxiety, but most work on this has been performed in a limited number of animal models, primarily zebrafish and rodents. We used adult South African clawed frogs (Xenopus laevis) to determine if the canonical anxiolytic fluoxetine alters predator-induced changes in appetitive and avoidance behavior in a laboratory-based trade-off task that mimics foraging/predator avoidance tradeoffs in the wild. We hypothesized that sub-chronic fluoxetine treatment (20 d) would not affect baseline behavior but would reverse predator-induced changes in food intake, appetitive and avoidance behavior, and the abundance of anxiety related gene transcripts in the optic tectum, a brain area central to ecological decision making in frogs. We found that fluoxetine significantly reduced baseline locomotion compared to vehicle-treated animals. Fluoxetine had no effect on appetitive and avoidance behaviors that were sensitive to predator cues in this assay and did not alter any of the anxiety-related transcripts in the tectum. We conclude that while peripheral sub-chronic administration of fluoxetine significantly reduces locomotion, it does not modify predator-induced changes in approach and avoidance behaviors in this assay. Our findings are not consistent with visual predator cues causing state anxiety in adult frogs.

Variable stoichiometric and macronutrient responses to lizard predation in Ozark glade grasshopper communities.

The General Stress Paradigm (GSP) predicts that prey body compositions should shift under chronic predation as prey increase body carbon and decrease body nitrogen content through dietary changes, heightened metabolism, reduced dietary efficiency, and the breakdown of nitrogen rich tissues to make labile carbohydrates available. In our study, we explored how the elemental and macronutrient content along with the morphology of three abundant Ozark glade grasshopper species differed between glades with and without predatory collared lizard (Crotaphytus collaris) populations. Our results indicated that lichen grasshoppers (Trimerotropis saxatilis) increased body C:N ratios in response to predators. Scudder's short-wing grasshoppers (Melanoplus scudderi) increased both body %C and %protein content, while the handsome grasshoppers (Syrbula admirabilis) did not significantly respond to the presence of collared lizards. None of the three grasshopper species showed morphological responses to predation. We also found that elemental and macronutrient content of grasshoppers was not always significantly correlated and was not associated with the same environmental factors, indicating a need to incorporate both perspectives in future research and utilize more accurate macromolecular assays. Overall, we found support for some aspects of the GSP in field-active animals and add to the growing body of evidence that predator-induced changes in prey body composition are more complex than predicted by the original GSP.

Stress hormone-mediated antipredator morphology improves escape performance in amphibian tadpoles

Complete functional descriptions of the induction sequences of phenotypically plastic traits (perception to physiological regulation to response to outcome) should help us to clarify how plastic responses develop and operate. Ranid tadpoles express several plastic antipredator traits mediated by the stress hormone corticosterone, but how they influence outcomes remains uncertain. We investigated how predator-induced changes in the tail morphology of wood frog (Rana sylvatica) tadpoles influenced their escape performance over a sequence of time points when attacked by larval dragonflies (Anax junius). Tadpoles were raised with no predator exposure, chemical cues of dragonflies added once per day, or constant exposure to caged dragonflies crossed with no exogenous hormone added (vehicle control only), exogenous corticosterone, or metyrapone (a corticosteroid synthesis inhibitor). During predation trials, we detected no differences after four days, but after eight days, tadpoles exposed to larval dragonflies and exogenous corticosterone had developed deeper tail muscles and exhibited improved escape performance compared to controls. Treatment with metyrapone blocked the development of a deeper tail muscle and resulted in no difference in escape success. Our findings further link the predator-induced physiological stress response of ranid tadpoles to the development of an antipredator tail morphology that confers performance benefits.

Prey vulnerability and predation pressure shape predator-induced changes in O2 consumption and antipredator behaviour

Predators regulate prey abundance (direct predation) as well as influencing their metabolism and behaviour (indirect effects) through the perception of risk. Antipredator traits are informed by individual experience of risk, which may vary over environmental gradients and through ontogeny. As prey grow, individual vulnerability generally diminishes, and the reduction in individual vulnerability with ontogenetic growth can potentially lead to size refugia, ultimately nullifying the impacts of direct predation. Despite the ecological importance of the indirect effects of predation and the disproportionate influence larger individuals have on ecological level processes, there has been little focus on the potential indirect effects of predation risk on invulnerable prey. Using a combination of field and laboratory experiments, we measured the changes in routine oxygen consumption of vulnerable and invulnerable size classes of the intertidal snail Nucella lapillus (dogwhelk), exposed to effluent from its crab predator Carcinus maenas. To test the potential influence of prior experience of predation risk, measurements were conducted on populations naturally exposed to different levels of predation pressure. Field results showed that only invulnerable snails modified their routine oxygen consumption in the presence of risk, and this occurred across all populations. Oxygen consumption rates in the laboratory, however, contradicted the pattern, with only vulnerable prey responding to the perception of risk. Metabolic responses of both vulnerable and invulnerable prey under field and laboratory conditions are discussed in the context of asset protection and prey energetic state. Observations of snail behaviour in the laboratory showed that dogwhelks from exposed shores, where predatory risk is higher, were more likely to exhibit antipredator behaviour. Importantly, our findings provide evidence that the indirect effects of predators remain influential even after prey are no longer susceptible to direct predation and add to the growing body of evidence highlighting the ecological importance of indirect predation.

Substrate-size choice in European eel (Anguilla anguilla) elvers is not altered by piscivore chemical cues.

The European eel Anguilla anguilla Linnaeus 1758 is critically endangered with recruitment estimated at 5-10% of historical levels. Enhancing survival of recruits is pivotal for conservation, and restoration should consider habitat choice of elvers ascending river systems. We experimentally show that newly ascended elvers choose small pebble habitat over finer and larger substrates, regardless of the presence or absence of piscivore chemical cues, indicating no predator-induced change in substrate choice. Enriching habitats with this substrate fraction should enhance eel recruitment as well as biodiversity at large.

Non-consumptive predator effects on prey population size: A dearth of evidence.

There is a large and growing interest in non-consumptive effects (NCEs) of predators. Diverse and extensive evidence shows that predation risk directly influences prey traits, such as behaviour, morphology and physiology, which in turn, may cause a reduction in prey fitness components (i.e. growth rate, survival and reproduction). An intuitive expectation is that NCEs that reduce prey fitness will extend to alter population growth rate and therefore population size. However, our intensive literature search yielded only 10 studies that examined how predator-induced changes in prey traits translate to changes in prey population size. Further, the scant evidence for risk-induced changes on prey population size have been generated from studies that were performed in very controlled systems (mesocosm and laboratory), which do not have the complexity and feedbacks of natural settings. Thus, although likely that predation risk alone can alter prey population size, there is little direct empirical evidence that demonstrates that it does. There are also clear reasons that risk effects on population size may be much smaller than the responses on phenotype and fitness components that are typically measured, magnifying the need to show, rather than infer, effects on population size. Herein we break down the process of how predation risk influences prey population size into a chain of events (predation risk affects prey traits, which affect prey fitness components and population growth rate, which affect prey population size), and highlight the complexity of each transition. We illustrate how the outcomes of these transitions are not straightforward, and how environmental context strongly dictates the direction and magnitude of effects. Indeed, the high variance in prey responses is reflected in the variance of results reported in the few studies that have empirically quantified risk effects on population size. It is therefore a major challenge to predict population effects given the complexity of how environmental context interacts with predation risk and prey responses. We highlight the critical need to appreciate risk effects at each level in the chain of events, and that changes at one level cannot be assumed to translate into changes in the next because of the interplay between risk, prey responses, and the environment. The gaps in knowledge we illuminate underscore the need for more evidence to substantiate the claim that predation risk effects extend to prey population size. The lacunae we identify should inspire future studies on the impact of predation risk on population-level responses in free-living animals.

Predator-induced changes in the chemical defence of a vertebrate.

1. Inducible defences are ubiquitous in the animal kingdom, but little is known about facultative changes in chemical defences in response to predators, especially so in vertebrates. 2. We tested for predator-induced changes in toxin production of larval common toads (Bufo bufo), which are known to synthesize bufadienolide compounds. 3. The experiment included larvae originating from three permanent and three temporary ponds reared in the presence or absence of chemical cues of three predators: dragonfly larvae, newts or fish. 4. Tadpoles raised with chemical cues of predation risk produced higher numbers of bufadienolide compounds and larger total bufadienolide quantities than predator-naive conspecifics. Further, the increase in intensity of chemical defence was greatest in response to fish, weakest to newts and intermediate to dragonfly larvae. Tadpoles originating from temporary and permanent ponds did not differ in their baseline toxin content or in the magnitude of their induced chemical responses. 5. These results provide the first compelling evidence for predator-induced changes in chemical defence of a vertebrate that may have evolved to enhance survival under predation risk.

Neuroendocrine modulation of predator avoidance/prey capture tradeoffs: Role of tectal NPY2R receptors

The optic tectum rapidly inhibits food intake when a visual threat is present. Anatomical and electrophysiological evidence support a role for neuropeptide Y (NPY), originating from cells in the thalamus, in the tectal inhibition of prey capture. Here we test the hypothesis that tectal NPY receptor type 2 (NPY2R) influences prey-capture and predator-avoidance responses in the African clawed frog, Xenopus laevis. We tested two questions: 1) Does tectal NPY administration decrease food intake and alter prey-capture behavior? 2) Does tectal administration of a NPY2R antagonist increase food intake, alter prey-capture behavior, and alter predator avoidance behavior? NPY microinjected bilaterally into the tecta failed to significantly alter food intake at any dose tested, although predator presence significantly reduced food intake. However, NPY differentially altered discrete components of prey capture including increasing the latency to contact food and reducing the amount of time in contact with food. These effects were blocked by the NPY2R antagonist BIIE0246. Additionally, BIIE0246 elevated food intake on its own after bilateral tectal microinjection. Furthermore, BIIE0246 reversed the reduction of food intake caused by exposure to a predator. Overall, these findings indicate that tectal NPY2R activation causes frogs to consume food more quickly, which may be adaptive in predator-rich environments. Blocking tectal NPY2R increases baseline food intake and reduces or eliminates predator-induced changes in prey capture and food intake.

Predator-induced changes of male and female mating preferences: innate and learned components.

While many mating preferences have a genetic basis, the question remains as to whether and how learning/experience can modify individual mate choice decisions. We used wild-caught (predator-experienced) and F1 laboratory-reared (predator-naïve) invasive Western mosquitofish Gambusia affinis from China to test whether mating preferences (assessed in a first mate choice test) would change under immediate predation threat. The same individuals were tested in a second mate choice test during which 1 of 3 types of animated predators was presented: 1) a co-occurring predator, 2) a co-evolved but not currently co-occurring predator, and 3) a non-piscivorous species as control. We compared preference scores derived from both mate choice tests to separate innate from experiential effects of predation. We also asked whether predator-induced changes in mating preferences would differ between sexes or depend on the choosing individual’s personality type and/or body size. Wild-caught fish altered their mate choice decisions most when exposed to the co-occurring predator whereas laboratory-reared individuals responded most to the co-evolved predator, suggesting that both innate mechanisms and learning effects are involved. This behavior likely reduces individuals’ risk of falling victim to predation by temporarily moving away from high-quality (i.e., conspicuous) mating partners. Accordingly, effects were stronger in bolder than shyer, large- compared with small-bodied, and female compared with male focal individuals, likely because those phenotypes face an increased predation risk overall. Our study adds to the growing body of literature appreciating the complexity of the mate choice process, where an array of intrinsic and extrinsic factors interacts during decision-making.

Sustained disruption of narwhal habitat use and behavior in the presence of Arctic killer whales

Although predators influence behavior of prey, analyses of electronic tracking data in marine environments rarely consider how predators affect the behavior of tracked animals. We collected an unprecedented dataset by synchronously tracking predator (killer whales, [Formula: see text] = 1; representing a family group) and prey (narwhal, [Formula: see text] = 7) via satellite telemetry in Admiralty Inlet, a large fjord in the Eastern Canadian Arctic. Analyzing the movement data with a switching-state space model and a series of mixed effects models, we show that the presence of killer whales strongly alters the behavior and distribution of narwhal. When killer whales were present (within about 100 km), narwhal moved closer to shore, where they were presumably less vulnerable. Under predation threat, narwhal movement patterns were more likely to be transiting, whereas in the absence of threat, more likely resident. Effects extended beyond discrete predatory events and persisted steadily for 10 d, the duration that killer whales remained in Admiralty Inlet. Our findings have two key consequences. First, given current reductions in sea ice and increases in Arctic killer whale sightings, killer whales have the potential to reshape Arctic marine mammal distributions and behavior. Second and of more general importance, predators have the potential to strongly affect movement behavior of tracked marine animals. Understanding predator effects may be as or more important than relating movement behavior to resource distribution or bottom-up drivers traditionally included in analyses of marine animal tracking data.

The interplay between resource supply and demand determines the influence of predation on prey body size

Predation has been shown to either increase or decrease the body mass of fish, as well as cause variable changes in growth rate. The mechanisms underlying these contrasting responses are not well understood. Here we compared intraspecific body size and growth responses to predation against a backdrop of 2006 estimates of asymptotic mass and growth constants (i.e., von Bertalanffy parameters) across species. We show that intraspecific responses can be quite large relative to interspecific variation and confirm that the magnitude and direction of body size responses is variable. We then employed the supply–demand (SD) model of body mass evolution to explore how predator-induced changes in resource demand or supply could alter body mass. The SD model predicts that any combination of increasing or decreasing body mass and increasing or decreasing growth rate is possible when predation risk is increased, which is consistent with the literature. Finally, we use three case studies to illustrate how the interplay of resource supply and resource demand determines the actual body mass and growth rate response to predation.

Social communication of predator-induced changes in Drosophila behavior and germ line physiology.

Behavioral adaptation to environmental threats and subsequent social transmission of adaptive behavior has evolutionary implications. In Drosophila, exposure to parasitoid wasps leads to a sharp decline in oviposition. We show that exposure to predator elicits both an acute and learned oviposition depression, mediated through the visual system. However, long-term persistence of oviposition depression after predator removal requires neuronal signaling functions, a functional mushroom body, and neurally driven apoptosis of oocytes through effector caspases. Strikingly, wasp-exposed flies (teachers) can transmit egg-retention behavior and trigger ovarian apoptosis in naive, unexposed flies (students). Acquisition and behavioral execution of this socially learned behavior by naive flies requires all of the factors needed for primary learning. The ability to teach does not require ovarian apoptosis. This work provides new insight into genetic and physiological mechanisms that underlie an ecologically relevant form of learning and mechanisms for its social transmission.

Influence of predator identity on the strength of predator avoidance responses in lobsters

The American lobster, Homarus americanus, is an important benthic consumer in the Gulf of Maine and supports an extremely valuable fishery in New England and eastern Canada. Meanwhile, there is substantial interest in restoring large predator fish species to the Gulf of Maine, and these predators may impact lobster populations both by consuming them and by inducing them to alter their behavior. Lobster tethering experiments were used to examine the susceptibility of a range of lobster size classes to predation in Saco Bay, Maine. The most susceptible sizes of lobsters were then exposed to three different fish predators (Atlantic striped bass Morone saxatilis, Atlantic cod Gadus morhua, and sea raven Hemitripterus americanus) separately in experimental mesocosm tanks. Juvenile lobsters moved less and spent more time in shelter when in the presence of cod or sea raven. By contrast, striped bass did not induce lobsters to alter their behavior. Striped bass are highly mobile, active pursuit predators, which are thought to induce weaker behavioral responses in prey than sit-and-pursue predators like sea ravens. Thus, differences in lobster sheltering behavior corresponded with differences in predator foraging behavior. These predator-induced changes in behavior can result in less foraging activity, which may translate into reduced lobster growth and reproduction. Efforts to model marine communities and ecosystems will benefit from a more holistic understanding of whether predators induced prey to modify their foraging behavior and habitat usage.

A novel paradigm for nonassociative long-term memory in Drosophila: predator-induced changes in oviposition behavior.

Learning processes in Drosophila have been studied through the use of Pavlovian associative memory tests, and these paradigms have been extremely useful in identifying both genetic factors and neuroanatomical structures that are essential to memory formation. Whether these same genes and brain compartments also contribute to memory formed from nonassociative experiences is not well understood. Exposures to environmental stressors such as predators are known to induce innate behavioral responses and can lead to new memory formation that allows a predator response to persist for days after the predator threat has been removed. Here, we utilize a unique form of nonassociative behavior in Drosophila where female flies detect the presence of endoparasitoid predatory wasps and alter their oviposition behavior to lay eggs in food containing high levels of alcohol. The predator-induced change in fly oviposition preference is maintained for days after wasps are removed, and this persistence in behavior requires a minimum continuous exposure time of 14 hr. Maintenance of this behavior is dependent on multiple long-term memory genes, including orb2, dunce, rutabaga, amnesiac, and Fmr1. Maintenance of the behavior also requires intact synaptic transmission of the mushroom body. Surprisingly, synaptic output from the mushroom body (MB) or the functions of any of these learning and memory genes are not required for the change in behavior when female flies are in constant contact with wasps. This suggests that perception of this predator that leads to an acute change in oviposition behavior is not dependent on the MB or dependent on learning and memory gene functions. Because wasp-induced oviposition behavior can last for days and its maintenance requires a functional MB and the wild-type products of several known learning and memory genes, we suggest that this constitutes a paradigm for a bona fide form of nonassociative long-term memory that is not dependent on associated experiences.

Predator-induced changes in the growth of eyes and false eyespots

The animal world is full of brilliant colours and striking patterns that serve to hide individuals or attract the attention of others. False eyespots are pervasive across a variety of animal taxa and are among nature's most conspicuous markings. Understanding the adaptive significance of eyespots has long fascinated evolutionary ecologists. Here we show for the first time that the size of eyespots is plastic and increases upon exposure to predators. Associated with the growth of eyespots there is a corresponding reduction in growth of eyes in juvenile Ambon damselfish, Pomacentrus amboinensis. These morphological changes likely direct attacks away from the head region. Exposure to predators also induced changes in prey behaviour and morphology. Such changes could prevent or deter attacks and increase burst speed, aiding in escape. Damselfish exposed to predators had drastically higher survival suffering only 10% mortality while controls suffered 60% mortality 72 h after release.

Morphological defense influences absolute, not relative, nonconsumptive effects in marine snails

Theory predicts that the strength of nonconsumptive predator effects (NCEs) depends on the state of individual prey and their vulnerability to predators. This prediction has rarely been tested, particularly with respect to interspecific variation in the vulnerability of closely related (i.e., within the same genus) guild members within a community. I examined the relationship between morphological vulnerability and predator-induced feeding suppression among 3 species of predatory whelks (Nucella spp.) that differ in their morphological defense—shell armor. Weaker-shelled species (N. ostrina and N. canaliculata) were more vulnerable to predation by crabs (Cancer productus) than the stronger-shelled species (N. lamellosa). Crab cues suppressed feeding in the most vulnerable species to a greater extent than the 2 less vulnerable species in absolute terms, but proportional decreases in feeding due to crab cues were no different among species. Thus, species-specific differences in feeding activity are maintained in the presence of crab cues, suggesting that the degree to which congeneric guild members transmit NCEs is related to constitutive levels of feeding activity rather than morphological defense. These results contrast with the commonly observed pattern of behavioral compensation for weaker morphological defenses in distantly related gastropod species and highlight the importance of examining the absolute and proportional predator-induced changes in behavior of different prey species. Key wor ds: antipredator behavior , food web, gastropod, nonconsumptive effect, trait compensation, trophic cascade. [Behav Ecol]