Differentiated phenotypic plasticity in larvae of the cannibalistic salamander Hynobius retardatus

Alternative phenotypes in natural populations can arise from either genetic polymorphism or an environmentally induced phenotype, that is, polyphenism. Evolutionary models of polyphenism developed by theoretical studies predict that polyphenism is favored when there are environment-dependent fitness trade-offs between alternatives and that the threshold frequency for a facultative switch between alternative phenotypes is adjusted in accordance with different selection regimes. The broad-headed (alternative) larval morph of Hynobius retardatus, which is induced by crowding with conspecifics or heterospecific anuran (Rana pirica) larvae, is a representative example of cannibalistic polyphenism. Morph induction by such proximate factors must reflect evolutionary (conditional frequency-dependent) processes. To clarify the role of frequency-dependent processes in polyphenism, I investigated the occurrence rate of the broad-headed morph under experimental crowding conditions (low conspecific, high conspecific, and high heterospecific densities) using larvae from eight natural populations with different larval densities of conspecifics and heterospecifics, and found interpopulational differences in the expression of the morph. Thus, there is a larval density-dependent equilibrium frequency of the morph in each pond, suggesting that the local switch point for morph induction was modified by selection to produce evolved differences between ponds. The evolution of such interpond differences has three necessary conditions: (1) There are pond-dependent fitness trade-offs between alternatives, (2) The maintenance of the morph is costly, and (3) The presence of conspecific or, especially, heterospecific larvae provides a reliable cue to the receiver.     

Predator-induced morphological defenses in marine zooplankton: a larval case study

While there are numerous reports of predator-induced morphological defenses for freshwater zooplankton, freshwater larvae, and benthic marine animals, a literature search revealed no reports of predator-induced morphological defenses for marine zooplankton. Rarity of predator-induced morphological defenses in marine zooplankton would imply a difference in predation risks compared to those experienced by freshwater organisms and benthic marine adults, whereas the presence of such plasticity in defenses would imply that risks are modified by developmental responses. This study reports a predator-induced change in defenses and vulnerability of a marine planktonic larva. Specifically, when reared in the presence of zoea larvae of Cancer spp., veliger larvae of the intertidal snail Littorina scutulata developed significantly smaller shell apertures and rounder shells than did cohort veligers reared in the absence of predator cues. Pairwise predation trials demonstrated that veligers reared with caged zoeas throughout development had greater survival than predator-naive veligers during short-term exposure to zoeas. The development of predator-induced morphological defenses by some marine larvae introduces a range of testable hypotheses on developmental plasticity that reduces vulnerability of planktonic larvae and other marine zooplankton to predators.     

Factors which affect the occurrence of cannibalism and the broad-headed "cannibal" morph in larvae of the salamander Hynobius retardatus

Cannibalism in amphibian larvae may be suppressed among siblings in comparison to distant relatives or nonkin, even when a "cannibal" morph that can consume conspecifics shows adaptive advantages. Two experimental studies were undertaken to analyze factors which affect the frequency of cannibalism and the occurrence of the broad-headed "cannibal" morph in larvae of the salamander Hynobius retardatus. The first experiment investigated whether or not the broad-headed "cannibal" morph is only induced after performing cannibalism. Because the broad-headed "cannibal" morph was observed in larval populations that showed no cannibalism, it was concluded that the "cannibal" morph could be induced without actual cannibalism. Second, possible factors affecting the occurrence of the broad-headed "cannibal" morph were analyzed with respect to the density of larvae, level of food supply, and kinship among larvae, alone or in combination. Appearance of the broad-headed "cannibal" morph was affected by interactive effects of density2kinship: although the morph was induced significantly more often at a higher density if the conspecifics were distantly or not related, it was strongly suppressed even at high density if larval kinship was very close or among siblings. In contrast, the frequency of cannibalism was independently affected by larval density, level of food supply, and kinship among larvae: it was significantly larger at high than at low larval densities, at low than at high food supply, and in mixed-sibling groups than in pure sibships. These results suggest that the "cannibal" morphs in H. retardatus are induced even without cannibalism at a high density of conspecifics in mixed-sibling groups, but the occurrence of this morph, which continuously consumes conspecifics, is suppressed among siblings.     

Fish predation selects for reduced foraging activity

Despite the importance of foraging activity for the growth/predation risk trade-off, studies that demonstrated predator-induced survival selection on foraging activity under semi-natural conditions are relatively rare. Here, we tested for fish-induced selection for reduced foraging activity in two larval Enallagma damselflies using a field enclosure experiment. Fish imposed considerable mortality in both damselfly species and survival selection on foraging activity could be detected in Enallagma geminatum. We did not detect selection in Enallagma hageni, probably because this species already was not eating very much in the absence of fish compared to E. geminatum. Both species responded strongly to the presence of predators by reducing their foraging activity. The documented survival selection on foraging activity was detected despite the already low activity levels in fish lake prey species and despite strong predator-induced plasticity in this trait.     

The deadly effects of "nonlethal" predators

Nonconsumptive predator effects are widespread and include plasticity as well as general stress responses. Caged predators are often used to estimate nonconsumptive effects, and numerous studies have focused on the larval stages of animals with complex life cycles. However, few of these studies test whether nonconsumptive predator effects, including stress responses, are exclusively sublethal. Nor have they assessed whether these effects extend beyond the larval stage, affecting success during stressful life-history transitions such as metamorphosis. We conducted experiments with larvae of a dragonfly (Leucorrhinia intacta) that exhibits predator-induced plasticity to assess whether the mere presence of predators affects larval survivorship, metamorphosis, and adult body size. Larvae exposed to caged predators with no ability to attack them had higher levels of mortality. In the second experiment, larvae reared with caged predators had higher rates of metamorphic failure, but there was no effect on adult body size. Our results suggest that stress responses induced by exposure to predator cues increase the vulnerability of prey to other mortality factors, and that mere exposure to predators can result in significant increases in mortality.     

Geographic variation in a predator-induced defense and its genetic basis

Predator-induced morphological defenses are a well-known form of phenotypic plasticity, but we continue to have a limited understanding of geographic variation in these responses and its genetic basis. Here we examine genetic variation and geographic differentiation in the inducible defenses of tadpoles (Rana pirica) in response to predatory salamander larvae (Hynobius retardatus). To do so, we crossed male and female frogs from a "mainland" Japanese island having predaceous salamanders and a more isolated island not having predaceous salamanders and raised resulting offspring in the presence and absence of H. retardatus. Mainland tadpoles exhibited a higher capacity to express the inducible morphology (a more bulgy body) than those from the predator-free island, and expression of the bulgy morph in mainland-island hybrids produced phenotypes that were intermediate to those produced by pure crosses. In addition, parental sex had no effect on expression of the bulgy morph. Our results support the hypothesis that geographic variation in inducible defenses is linked to the additive effects of autosomal alleles that are shaped by differences in historical exposure to the inducing predator.     

Novel features of an inducible defense system in larval tree frogs (Hyla chrysoscelis)

Organisms in aquatic ecosystems must often tolerate variable environmental conditions, including an uncertain risk of predation. Individuals that can maintain plastic defenses against predation will increase their survival when predators are present, but will not incur the costs of these defenses when the risk of predation is low and the defense is not induced. Larvae of the pond-breeding anuran Hyla chrysoscelis develop a conspicuous phenotype in the presence of predators consisting of a brightly colored tail and a deeper tail fin. In this study, I attempted to identify the source of the chemical signal that induces this defensive morphology in this species. I tested whether metabolites alone, originating from the prey but passing through the predator, were able to induce the same morphological response as the combination of alarm signals released directly by attacked conspecifics, and metabolites. I used morphometric and tail conspicuousness data to assess tadpole response to the perceived risk of predation by larval odonate predators (Anax junius). I also tested whether this inducing cue could be recognized across species by measuring the morphological response of H. chrysoscelis tadpoles exposed to cues emitted when tadpoles of a closely related genus (Pseudacris crucifer) were consumed. Tadpoles exhibited a clean graded response of both overall shape and tail morphology in response to all cues, corresponding to their relative reliability as indicators of a risk of predation. H. chrysoscelis tadpoles were also able to respond to cues emitted when tadpoles of a closely related genus were consumed by predators. These results illustrate that tadpoles of this species are able to respond to metabolites alone without alarm signals, and that interspecific chemical communication is a primary mechanism for predator avoidance in this inducible defense system.     

Threat-sensitive learning of predators by larval mosquitoes <Emphasis Type="Italic">Culex restuans</Emphasis>

A prerequisite for prey to show adaptive behavioural responses to predators is that the prey has the ability to recognise predators as threats. While predator recognition can be innate in many situations, learning is often essential. For many aquatic species, one common way to learn about predators is through the pairing of a novel predator odour with alarm cues released from injured conspecifics. One study with fish demonstrated that this mode of learning not only allows the prey to recognise the predatory cues as a threat, but also mediates the level of threat associated with the predator cues (i.e. threat-sensitive learning). When the prey is exposed to the novel predator with a high concentration of alarm cues, they subsequently show a high intensity of antipredator response to the predator cues alone. When exposed to the predator with a low concentration of alarm cues, they subsequently show a low-intensity response to the predator cues. Here, we investigated whether larval mosquitoes Culex restuans have the ability to learn to recognise salamanders as a threat through a single pairing of alarm cues and salamander odour and also whether they would learn to respond to salamander cues in a threat-sensitive manner. We conditioned individual mosquitoes with water or a low, medium or high concentration of crushed conspecific cues (alarm cues) paired with salamander odour. Mosquitoes exposed to salamander odour paired with alarm cues and subsequently exposed to salamander odour alone responded to the salamander as a threat. Moreover, the intensity of antipredator response displayed during the conditioning phase matched the response intensity during the testing phase. This is the first demonstration of threat-sensitive learning in an aquatic invertebrate.     

Why run and hide when you can divide? Evidence for larval cloning and reduced larval size as an adaptive inducible defense

Predator-induced cloning (asexual reproduction), with reduced size as consequence of cloning, suggests a novel adaptation to the threat of predation. Although cloning is a common reproductive strategy of many plants and animals, cloning in response to stimuli from predators has, at present, been documented only in the larvae (plutei) of the sand dollar, Dendraster excentricus. Other studies report larval cloning in echinoderms under optimal conditions of food and temperature. A burst of asexuality should be favored when environmental conditions are conducive to growth, but it is less clear that cloning is advantageous when conditions indicate risk from predators. This study tested the hypothesis that the small size of predator-induced clones reduces vulnerability during encounters with planktivorous fish. Successful cloning was inferred from an increase in larval density, a reduction in larval size and stage, and some direct observations of budding. All clones were smaller than uncloned sibling larvae, suggesting an advantage against visual predators. Pair-wise predation trials demonstrated that planktivorous fish ate more uncloned sibling plutei than small clones. These results offer a new ecological context for asexual reproduction: rapid size reduction as a defense. If the identifiable cues for cloning in echinoderm larvae (food and predators) are linked in nature, then larval cloning may be a response to a single ecological scenario rather than two separate and unrelated conditions.     

Case selection by a limnephilid caddisfly [Potamophylax latipennis (Curtis)] in response to different predators

Some organisms use morphological structures obtained by behavioural processes to lower mortality by predation. We test whether larvae of the limnephilid caddisfly Potamophylax latipennis (Curtis) vary their responses to the presence of different predators (dragonfly naiads, fire salamander larvae or brown trout) by choosing organic or mineral cases. We offered both case types to larvae, and simulated differences in predation risk using water conditioned with chemicals from the different predators. Our results show that Potamophylax larvae detect and discriminate predators using water-borne chemical cues and alter their choice of case type according to the perceived predation risk. Moreover, the distribution of larvae bearing cases of different anti-predator value matches the spatial variation in predation risk in the field.     

Induced defensive responses by the bivalve Mytilus edulis to predators with different attack modes

Predators such as crabs, whelks, and sea stars attack their bivalve prey in different ways, and predator-induced defenses are an important means of protection. The degree to which induced defenses are specific to different predators, however, remains largely unknown. In laboratory experiments (June to August 1998), we raised mussels (Mytilus edulis L.) in the presence of a drilling predator [the whelk Nucella lapillus (L.)] or a crushing predator [the crab Carcinus maenas (L.)] to determine whether induced changes in prey shell thickness, size, or shape occurred and whether changes were predator-specific. Over a 2 month period, juvenile mussels were exposed to waterborne cues from actively feeding crabs or whelks. Mussels produced thicker shell lips in response to both predators relative to control mussels raised in their absence, and the difference was significantly greater in response to whelks than to crabs. Mussels exposed to whelks showed significantly smaller increases in shell length and width and total wet weight than did mussels exposed to crabs. Thus, there may be a trade-off between shell thickness and linear shell growth and a potential delay in attaining a size refuge from predation. Received: 4 August 1999 / Accepted: 31 January 2000     

Variable predation risk and the dynamic nature of mosquito antipredator responses to chemical alarm cues

Summary. Predation is a pervasive selective agent highly variable in space and time. Due to the costs associated with antipredator responses, prey would be at a selective advantage if they respond to predation threats with an intensitfy matching the threat posed by the predator. Many aquatic organisms have been shown to use chemical alarm cues present in the water to assess the level of risk in their environment. This includes mosquito larvae which show antipredator responses to conspecific alarm cues. In this study, we investigated the nature of the responses of larval mosquitoes Culex restuans to those cues. In our initial observations, we showed pond/population differences in the response intensity of C. restuans to alarm cues. In experiment 1, we showed that the response intensity to alarm cues could be increased by increasing the background level of risk in the mosquitoes’ environment (by adding salamander predators) and once turned on, the response intensity to alarm cues was likely maintained for the remainder of the mosquitoes’ aquatic life. In experiments 2 and 3, we investigated if the increase in response intensity to alarm cues was directly correlated with the level of background risk in the mosquitoes’ environment. When given increasing levels of background risk, mosquito larvae subsequently showed a graded response to conspecific alarm cues. This series of experiments demonstrates that the response intensity of larval mosquitoes to a standard concentration of alarm cues is not fixed, but rather dependent on the background level of risk in the environment. An understanding of the background level of risk is particularly important for comparing antipredator responses of prey between habitats.     

Adaptive prey behavior and the dynamics of intraguild predation systems

Intraguild predation constitutes a widespread interaction occurring across different taxa, trophic positions and ecosystems, and its endogenous dynamical properties have been shown to affect the abundance and persistence of the involved populations as well as those connected with them within food webs. Although optimal foraging decisions displayed by predators are known to exert a stabilizing influence on the dynamics of intraguild predation systems, few is known about the corresponding influence of adaptive prey decisions in spite of its commonness in nature. In this study, we analyze the effect that adaptive antipredator behavior exerts on the stability and persistence of the populations involved in intraguild predation systems. Our results indicate that adaptive prey behavior in the form of inducible defenses act as a stabilizing mechanism and show that, in the same direction that adaptive foraging, enhances the parameter space in which species can coexist through promoting persistence of the IG-prey. At high levels of enrichment, the intraguild predation system exhibits unstable dynamics and zones of multiples attractors. In addition, we show that the equilibrium density of the IG-predator could be increased at intermediate values of defense effectiveness. Finally we conclude that adaptive prey behavior is an important mechanism leading to species coexistence in intraguild predation systems and consequently enhancing stability of food webs.     

Time constraints mediate predator-induced plasticity in immune function, condition, and life history

The simultaneous presence of predators and a limited time for development imposes a conflict: accelerating growth under time constraints comes at the cost of higher predation risk mediated by increased foraging. The few studies that have addressed this tradeoff have dealt only with life history traits such as age and size at maturity. Physiological traits have largely been ignored in studies assessing the impact of environmental stressors, and it is largely unknown whether they respond independently of life history traits. Here, we studied the simultaneous effects of time constraints, i.e., as imposed by seasonality, and predation risk on immune defense, energy storage, and life history in lestid damselflies. As predicted by theory, larvae accelerated growth and development under time constraints while the opposite occurred under predation risk. The activity of phenoloxidase, an important component of insect immunity, and investment in fat storage were reduced both under time constraints and in the presence of predators. These reductions were smaller when time constraints and predation risk were combined. This indicates that predators can induce sublethal costs linked to both life history and physiology in their prey, and that time constraints can independently reduce the impact of predator-induced changes in life history and physiology.     

Comparison of laboratory rates of predation of five species of marine fish larvae by three planktonic invertebrates: effects of larval size on vulnerability

Rates of predation by the invertebrates Aurelia aurita, Thysanoessa raschi and Euchaeta norvegica on larval stages of cod (Gadus morhua L.), flunder (Platichthys flesus L.), plaice (Pleuronectes platessa L.), herring (Clupea harengus L.), and turbot (Scophthalmus maximus L.) were determined. Experiments were conducted in late winter and early spring 1982 with predators collected in Loch Etive, Scotland and prey obtained from several locations in Great Britain. Early stages of the smallest species, cod, flounder and turbot, tended to be most vulnerable to all three predators, while the early stages of the larger species, plaice and herring, and older stages of all species, were less vulnerable. For all stages and species of larvae, predation rates by the three predators were most closely related to larval length and escape swimming speed. Larval length itself was closely correlated to indices of larval escape ability. Low predation rates on large larvae by E. norvegica could be due to handling difficulties, whereas for A. aurita and T. raschi these low rates were due to escape abilities of the larger larvae. Prey movement is an important stimulus eliciting predation in E. norvegica but not in A. aurita or T. raschi.     

How flexible is phenotypic plasticity? Developmental windows for trait induction and reversal

Inducible defenses allow prey to modulate their phenotypic responses to the level of predation risk in the environment and reduce the cost of constitutive defenses. Inherent in this statement is that prey must alter their phenotypes during development in order to form these defenses. This has lead many ecologists and evolutionary biologists to call for studies that examine developmental plasticity to provide insights into the importance of development in controlling the trajectories of trait formation, the integration of phenotypes over ontogeny, and the establishment of developmental windows for trait formation and reversal. By moving away from studies that focus on a single point in development, we can obtain a more complete understanding of the phenotypic decisions and limitations of prey. We exposed freshwater snails (Helisoma trivolvis) to environments in which predatory water bugs (Belostoma flumineum) were always absent, always present, or added and removed at different points in development. We discovered that snails formed morphological defenses against water bugs. Importantly, after the initial induction of defenses, snails showed similar developmental trajectories as snails reared without predators. Further, the snails possessed wide developmental windows for inducible defenses that extended past sexual maturity. However, being induced later in development appeared to have an associated cost (i.e., decreased shell thickness) that was not found when water bugs were always present. This epiphenotype (i.e., new shell formation as an extension of the current shell) suggests that resource limitation plays an important role in responses to temporal variation in predation risk and may have critical ecological costs that limit the benefits of the inducible defense. Lastly, the ability of snails to completely reverse their defenses was limited to early in ontogeny due to the constraints associated with modular growth of shell material. In sum, we demonstrate that taking a developmental perspective is extremely valuable for understanding the ecology of inducible defenses.     

Costs of brood parasitism and the lack of defenses on the yellow-winged blackbird - shiny cowbird system

The shiny cowbird (Molothrus bonariensis) is a generalist brood parasite that lays either white-immaculate or spotted egg morphs in eastern Argentina and Uruguay. Some hosts accept both morphs, others accept spotted eggs and reject the white morph, but no host has been found to accept white eggs and reject spotted ones. It has been suggested that the yellow-winged blackbird (Agelaius thilius) may be that type of host. The finding of a white acceptor-spotted rejector species would help to explain the occurrence and maintenance of the parasite egg polymorphism. We studied the incidence of shiny cowbird parasitism on this host, its costs for their reproductive success and the presence of antiparasitic defenses in the yellow-winged blackbird - shiny cowbird system. The parasite affected the reproductive success of the host in two ways. Cowbirds punctured host eggs causing a reduction in clutch size, and yellow-winged blackbirds deserted their nests whenever they suffered high egg loss. In addition, parasitized nests suffered higher predation during the nestling stage, but not during egg stages, indicating that the difference found was related to the presence of the cowbird chick, and not to higher exposure of parasitized nests to both parasites␣and predators. Despite the costs imposed by the parasite, yellow-winged blackbirds have not evolved antiparasitic defenses. This host did not reject any egg morph of the shiny cowbird nor desert parasitized nests unless it had suffered high egg loss. Current explanations for the host lack of defenses, the “time lag” and the “equilibrium” hypothesis, are discussed. Received: 29 August 1997 / Accepted after revision: 10 January 1998     

Species-specific antipredator capacities and prey refuges: interactions between piscivorous perch (Perca fluviatilis) and juvenile perch and roach (Rutilus rutilus)

The outcome of predator-prey interactions depends on the characteristics of predators and prey as well as the structure of the environment. In a replicated field enclosure experiment, we tested the effects of quantity and quality of different prey refuges (no structure, structure forming a partial refuge, and structure forming a complete refuge) on the interaction between piscivorous perch (Perca fluviatilis) and juvenile perch and roach (Rutilus rutilus). We quantified the behaviour of the predators and the prey and predator-induced prey mortality. The piscivores stayed in or close to the prey refuge and were more dispersed in the presence than in the absence of prey refuges. Survival of juvenile perch and roach decreased in the presence of predators and was higher for juvenile roach than for juvenile perch. In addition, juvenile perch survival increased with refuge efficiency Roach formed schools which were denser in the presence of predators, had a higher swimming speed (both in the open water and in the refuge) and used a larger area than juvenile perch. Both prey species decreased their distance to the prey refuge and increased the proportion of their time spent in the refuge in the presence of predators. The number of switches between the open-water habitat and the prey refuge was higher for juvenile roach than for juvenile perch. Juvenile perch used different parts of the prey refuge in a flexible way depending both on presence of predators and refuge type whereas juvenile roach used the different parts of the prey refuge in fixed proportions over all refuge treatments. Our results suggest that juvenile roach had a overall higher capacity to avoid predation than juvenile perch. However, in the presence of qualitatively different prey refuges juvenile perch responded to predators with more flexible refuge use than juvenile roach. The differences in antipredator capacities of juvenile perch and roach when subjected to piscivorous perch predation may depend on differences in life history patterns of the two species.     

The ghost of predation future: threat-sensitive and temporal assessment of risk by embryonic woodfrogs

Amphibians are able to learn to recognize their future predators during their embryonic development (the ghost of predation future). Here, we investigate whether amphibian embryos can also acquire additional information about their future predators, such as the level of threat associated with them and the time of day at which they would be the most dangerous. We exposed woodfrog embryos (Rana sylvatica) to different concentrations of injured tadpole cues paired with the odor of a tiger salamander (Ambystoma tigrinum) between 1500 and 1700 hours for five consecutive days and raised them for 9 days after hatching. First, we showed that embryos exposed to predator odor paired with increasing concentrations of injured cues during their embryonic development subsequently display stronger antipredator responses to the salamander as tadpoles, thereby demonstrating threat-sensitive learning by embryonic amphibians. Second, we showed that the learned responses of tadpoles were stronger when the tadpoles were exposed to salamander odor between 1500 and 1700 hours, the time at which the embryos were exposed to the salamander, than during earlier (1100–1300 hours) or later (1900–2100 hours) periods. Our results highlight the amazing sophistication of learned predator recognition by prey and emphasize the importance of temporal considerations in experiments examining risk assessment by prey.     

Patterns of shell repair in articulate brachiopods indicate size constitutes a refuge from predation

The cost of overcoming prey defenses relative to the value of internal tissues is a key criterion in predator/prey interactions. Optimal foraging theory predicts: (1) specific sizes of prey will result in the best returns to predators, and (2) there will often be a size at which the cost/benefit balance is low enough to effectively exclude predation. Data presented here on styles of repaired shell damage and size at which injury had been sustained was collected from samples of terebratulide brachiopods from the Antarctic Peninisula (Liothyrella uva), Falkland Islands (Magellania venosa and Terebratella dorsata) and Chile (M. venosa). The predominant form of damage on shells was indicative of predators attacking the valve margins. The modal size for repaired damage was more than 10 mm smaller than the modal size for the overall size distribution in each species and there were no repaired attacks in the largest size classes of any species. These data suggest that size forms a refuge from predation, as would be predicted by optimal foraging theory. The optimal sizes that predators appeared to attack vary between species, as do the sizes that provided a refuge from predation. High levels of multiple repairs (19% of the M. venosa population from the Falkland Islands sampled had 2 or more repairs) suggest that the mortality following attack is low, suggesting that many predators abandon their attacks.