Fish Cues Research Articles

Effects of metolachlor and fish cues on tadpole antipredator behaviors

Antipredator behaviors are often crucial for animal survival. In environments impacted by humans, animals may be exposed to a wide array of chemical contaminants due to agriculture, industry, and other activities. Among other effects, these chemical contaminants may influence behaviors prey animals use to cope with predation risk, likely reducing survival by suppressing or even maladaptively reversing normal behavioral responses. Changes in behavioral responses could be the result of impaired detection of cues that indicate predator presence or altered behavioral plasticity in response to predator cues. In a laboratory experiment, we tested the effects of the commonly used herbicide metolachlor on the behavior of tadpoles of the American bullfrog (Lithobates catesbeianus) in both the absence and presence of water conditioned with cues (odor) of fish. We observed several behaviors in the tadpoles reflective of predator avoidance when exposed to combinations of metolachlor (0 or 80 ppb) and the presence or absence of fish cues. We found that metolachlor had size-dependent effects on tadpole activity levels, with larger tadpoles being much less active in the absence of metolachlor but similar in activity to small tadpoles when metolachlor was present. Fish cues similarly had size-dependent effects on multiple tadpole behaviors. Finally, hiding behavior and zone change (movement) behavior of tadpoles in response to fish cues varied depending on the presence of metolachlor and, in the case of zone changes, tadpole size. Our findings indicate that the presence of chemical contaminants has the potential to alter important antipredator behaviors. However, these effects are complex, and size may mediate the nature of the response to both chemical contaminants and predators.

In situ testing of candidate odorant cues in coral-reef fish: a new method with tests of dimethylsulfoniopropionate and betaines

In situ testing of candidate odorant cues directly in coral-reef communities has the advantage that, in principle, it permits the behavioral responses of all fish species to be evaluated in the species’ natural environments. The success of in situ testing depends critically, however, on a suitable method of odorant release. We provide here a proof-of-concept for a new method of release that (instead of using distilled water as an ejection medium) ejects odorant-containing local reef water remotely and silently over an extended time period using gravity as the motive force. The ejected water, being neutrally buoyant, remains in the reef community, dispersing in local currents. From our observations of fish behavior during ejection of candidate odorants in Curaçao reefs, we confirm that brown chromis (Chromis multilineata) are likely attracted to dimethylsulfoniopropionate (DMSP), and we obtain suggestive evidence that they are attracted to a mix of three betaines: glycine betaine, proline betaine, and trigonelline. Creole wrasse (Clepticus parrae) and yellowhead wrasse (Halichoeres garnoti) are likely repelled by DMSP. Many observed fish species gave no evidence of being affected by either DMSP or betaines.

One of these things is not like the other: Mixed predator cues result in lopsided phenotypic responses in a Neotropical tadpole.

Many organisms have evolved to produce different phenotypes in response to environmental variation. Dendropsophus ebraccatus tadpoles develop opposing shifts in morphology and coloration when they are exposed to invertebrate vs vertebrate predators. Each of these alternate phenotypes are adaptive, conferring a survival advantage against the predator with which tadpoles were reared but imposing a survival cost with the mismatched predator. Here, we measured the phenotypic response of tadpoles to graded cues and mixed cues of both fish and dragonfly nymphs. Prey species like D. ebraccatus commonly co-occur with both of these types of predators, amongst many others as well. In our first experiment, tadpoles increased investment in defensive phenotypes in response to increasing concentrations of predator cues. Whereas morphology only differed in the strongest predation cue, tail spot coloration differed even at the lowest cue concentration. In our second experiment, tadpoles reared with cues from both predators developed an intermediate yet skewed phenotype that was most similar to the fish-induced phenotype. Previous studies have shown that fish are more lethal than dragonfly larvae; thus tadpoles responded most strongly to the more dangerous predator, even though the number of prey consumed by each predator was the same. This may be due to D. ebraccatus having evolved a stronger response to fish or because fish produce more kairomones than do dragonflies for a given amount of food. We demonstrate that not only do tadpoles assess predation risk via the concentration of predation cues in the water, they produce a stronger response to a more lethal predator even when the strength of cues is presumed to be identical.

Lack of anti-predator recognition in a marine isopod under the threat of an invasive predatory crab

The prey naïveté hypothesis suggests that the failure of prey to recognize novel predators as a threat is caused by a lack of anti-predator adaptations. We tested this hypothesis in a unique natural setting, where the isopod Idotea balthica encountered the rapidly spreading invasive crab, Rhithropanopeus harrissii. Earlier research had indicated high mortality of the isopods during exposure to R. harrissii. The isopod exerted no co-evolutionary history with any littoral crabs and thus the strong impact could be caused by lack of pre-adaptations towards the new predator species. We tested this hypothesis by studying the anti-predator responses of the isopods with water-born cues of R. harrissii and of the native predatory fish Perca fluviatilis. Compared to control water, the isopods lowered their activity when exposed to the fish cue. Instead crab cue did not induce anti-predator behaviour. We also tested the hypothesis that mortality caused by novel predator, similar to predation by P. fluviatilis, would result in differential selection for the two sexes and contribute to the evolution of personalities. However, we found no differences in anti-predator behaviour nor in mortality between the sexes or personalities of the isopods. The outcomes reveal an interesting evolutionary scenario, where predation by a local predator induce soft selection on prey characteristics, but an invasive species cause hard selection without differentiating between prey individuals. Our study—conducted in the dawn of the population outbreak of R. harrissii—provides an excellent reference point for studies resolving the evolutionary impacts of invasive predators on naïve prey.

Habitat isolation and the cues of three remote predators differentially modulate prey colonization dynamics in pond landscapes.

Recent evidence suggests predators may change colonization rates of prey in nearby predator-free patches as an example of context-dependent habitat selection. Such remote predator effects can be positive when colonizers are redirected to nearby patches (habitat compression), or negative when nearby patches are avoided (risk contagion). However, it is unknown to what extent such responses are predator- and prey-specific and change with increasing distance from predator patches. We evaluated how cues of fish, backswimmers and dragonfly larvae affect habitat selection in replicated pond landscapes with predator-free patches located at increasing distances from a predator patch. We found evidence for risk contagion and compression, but spatial colonization patterns were both predator- and prey-specific. The mosquito Culex pipiens and water beetle Hydraena testacea avoided patches next to patches with dragonfly larvae (i.e. risk contagion). Predator-free patches next to patches with backswimmers were avoided only by mosquitoes. Mosquitoes preferentially colonized patches at some distance from a fish or backswimmer patch (i.e. habitat compression). Colonization patterns of beetles also suggested habitat compression, although reward contagion could not be fully excluded as an alternative explanation. Water beetles preferred the most isolated patches regardless of whether predators were present in the landscape, showing that patch position in a landscape alone affects colonization. We conclude that habitat selection can be a complex product of patch isolation and the combined effects of different local and remote cues complicate current attempts to predict the distribution of mobile organisms in landscapes.

Higher, Faster, Better: Maternal Effects Shorten Time Lags and Increase Morphological Defenses in Daphnia lumholtzi Offspring Generations

Prey species can respond to the presence of predators by inducing phenotypic plastic traits which form morphological, life history or behavioral defenses. These so-called inducible defenses have evolved within a cost-benefit framework. They are only formed when they are needed, and costs associated with defenses are saved when predators are not present. However, a disadvantage compared to permanent defenses are lag phases between predator perception and the full formation of defenses. This may be especially important when the predation risk persists for longer periods, e.g., outlasts one generation and challenges prey offspring. We hypothesized that transgenerational induced phenotypic plasticity reduces lag phases in situations where hazards threaten specimens over several generations. We tested this in three generations of the freshwater crustaceanDaphnia lumholtziusing the three-spined sticklebackGasterosteus aculeatusas predator. In the presence of chemical cues from fishD. lumholtziexpresses elongated head and tail spines. In the F0 generation defenses are constraint by a comparatively long lag phase and are not developed prior to the 3rd instar. In the F1, and F2 of induced animals this lag phase is shortened and defenses are developed upon birth. We show that induction of TGP in the mothers takes place already during the juvenile stages and transfers to the offspring generation in forms of shortened time lags and enhanced trait expression. When progeny is additionally exposed to fish cues as embryos, the addition of maternal and embryonic effects further enhances the magnitude of defense expression. Our findings detail a distinguished strategy of transgenerational phenotypic plasticity which allows to shorten lag phases of trait changes in phenotypic plasticity.

Toxic Microcystis aeruginosa alters the resource allocation in Daphnia mitsukuri responding to fish predation cues.

Many prey organisms adaptively respond to predation risk by inducible defenses with underlying tradeoffs in resource allocation. Cyanobacterial blooms expose zooplankton to poor food conditions, affecting the herbivores' fitness. Given the interferences on resources allocation and life history traits, poor-quality cyanobacteria are predicted to affect the adaptive predator-induced responses in zooplankton. Here, we exposed two clones (i.e., clones SH and ZJ) of the cladoceran Daphnia mitsukuri to different combinations of fish predation cues and diets containing toxic Microcystis aeruginosa (0%-30%). D.mitsukuri matured at a small size and had elongated relative tail spine as adaptive responses to fish cues. Despite the comparable tail spine defense, fish cue-induced changes in growth and reproduction in the clone SH were more pronounced than those in the clone ZJ under no M.aeruginosa. Animals accumulated microcystin in the whole body with increasing abundance of M.aeruginosa. However, the inducible enhanced tail spine allometry was not affected, resulting in unchanged tail spine defense by Daphnia under all M.aeruginosa treatments. By contrast, M.aeruginosa remarkably decreased the adaptive maturation size and the offspring number in all animals. However, the inducible reproductive effort tended to increase or remain unchanged depending on clones associated with the constant or decreased responses of the somatic growth effort under increasing M.aeruginosa. Our results suggested that toxic M.aeruginosa did not alter the resource allocation to antipredator morphological defense but affected the somatic growth and reproduction in D.mitsukuri under fish cues. The present study highlights the different effects of toxic cyanobacteria on adaptive predator-induced responses in zooplankton, promoting the understanding for the morphological defense-mediated predator-prey interactions in eutrophic environments.

Effects of predator cues carry over from egg and larval stage to adult life-history traits in a damselfly

Non-consumptive predator effects experienced in early life stages of prey may result in life-history costs in later life stages. Such effects can, for example, alter the growth rate during the juvenile stage, which may carry over to size at maturity. However, we have limited knowledge of the carry-over effects starting from the egg stage through the larval stage to the adult stage. Here, we present results from a laboratory experiment in which we exposed a damselfly, Ischnura elegans, to chemical cues originating from a fish predator, perch. We used a 2 × 2-full-factorial design in which the damselflies were exposed to predator cues during either the immobile egg or the mobile larval stage. The presence of predator cues, i.e., non-consumptive predator effects, during the egg stage caused decreased survival, but only until 2 wk after larval hatching. Predator cues during the larval stage caused decreased survival until emergence and an increase in development time until emergence. However, mass at emergence was not affected by predator cues. When fish cues were present in the egg or larval stage, there was a lower growth rate until final-instar larvae than in larvae that did not receive fish cues. Our results add to the growing number of studies showing that predation-risk cues in the egg stage can carry over to the adult stage, which ultimately could have consequences for adult life-history traits, such as survival and fecundity.

Better desiccated than eaten by fish: Distribution of anurans among habitats with different risks to offspring

Abstract Freshwater species with complex life cycles face a trade‐off between the risks of offspring mortality due to desiccation in temporary habitats and due to predators common in long‐duration habitats, especially fish. In real‐world conditions, intermediate‐gradient areas that are highly suitable for some ecological specialists are often limited. I examined the relative significance of drivers of the permanence–predation gradient in habitat selection by pond‐breeding anurans. Anuran oviposition was investigated at the community level in fish pond landscapes with only three types of habitat, permanent fish‐containing ponds and highly desiccation‐prone pools, either fishless or recently emptied of fish and with fish odour (fish cue). Altogether, 65 ponds/pools, interspersed in four clusters, were examined for the presence of egg masses. Bufo bufo was the only species preferring permanent ponds. Egg masses of Rana sp. (Rana arvalis/Rana temporaria) occurred in all fishless pools, and less frequently in the ponds. Bufotes viridis and long larval period species Pelobates fuscus and Hyla orientalis oviposited almost exclusively in fishless pools. Fish‐cue pools were avoided by all species. Anuran richness was higher in fishless pools than in permanent ponds. Species distribution between the two habitats was nested, with both common and rare species occurring in fishless pools. The results indicate the primacy of offspring predation risk over hydroperiod constraints in oviposition decision‐making by fish‐intolerant anurans. The absence of some species from ponds and pools with fish or fish cues shows that non‐consumptive interactions may better explain the scarcity of anuran larvae in waters dominated by fish than actual consumption. The strict avoidance of fish habitats despite their proximity to fishless patches indicates fine‐scale assessment of predation risk. However, rigid habitat selection against fish predation on offspring may prove maladaptive if habitats with high desiccation risk are the main alternative and are indiscriminately preferred. Maintenance of fishless wetlands with a hydroperiod sufficient to allow completion of metamorphosis should be a conservation priority for anuran diversity in areas where fishless habitats are limited.

Temperature and predator cues interactively affect ontogenetic metabolic scaling of aquatic amphipods.

A common belief is that body mass scaling of metabolic rate results chiefly from intrinsic body-design constraints. However, several studies have shown that multiple ecological factors affect metabolic scaling. The mechanistic basis of these effects is largely unknown. Here, we explore whether abiotic and biotic environmental factors have interactive effects on metabolic scaling. To address this question, we studied the simultaneous effects of temperature and predator cues on the ontogenetic metabolic scaling of amphipod crustaceans inhabiting two different aquatic ecosystems, a freshwater spring and a saltwater lagoon. We assessed effects of phenotypic plasticity on metabolic scaling by exposing amphipods in the laboratory to water with and without fish cues at multiple temperatures. Temperature interacts significantly with predator cues to affect metabolic scaling. Our results suggest that metabolic scaling is highly malleable in response to short-term acclimation. The interactive effects of temperature and predators show the importance of studying effects of global warming in realistic ecological contexts.

Costs and compensation in zooplankton pigmentation under countervailing threats of ultraviolet radiation and predation

Evolutionary responses to opposing directions of natural selection include trade-offs, where the phenotype balances selective forces, and compensation, where other traits reduce the impact of one selective force. Zooplankton pigmentation protects from ultraviolet radiation (UVR) but attracts visual predators. This trade-off is understudied in the ocean where planktonic larvae in surface waters face ubiquitous UVR and visual predation threats. We tested whether crab larvae can behaviorally reduce UVR risk through downward swimming or expansion of photoprotective chromatophores. Then we examined whether more pigmented larvae are more heavily predated by silverside fish under natural sunlight in the tropics in three UVR treatments (visible light, visible + UVA, visible + UVA + UVB). Lastly, we tested the behavioral chromatophore response of larvae to predation threats in two light treatments. Armases ricordi avoided surface waters after exposure to sunlight with UVR. Armases ricordi, Armases americanum, and Eurypanopeus sp. consistently expanded chromatophores in UVR or visible light, while Mithraculus sculptus and Mithraculus coryphe showed no response. Fish preferred pigmented larvae on sunnier days in visible light lacking UVR. Lastly, both M. coryphe and M. sculptus unexpectedly expanded chromatophores in fish cues, but responses were inconsistent over trials and across light treatments. The more consistent larval responses to UVR than to predator cues and the lack of predator preferences in natural light conditions suggest that UVR may have a stronger influence on pigmentation than predation. This study improves our understanding of planktonic adaptation to countervailing selection caused by visual predation and exposure to UVR.

The impact of diel vertical migration on fatty acid patterns and allocation in Daphnia magna.

In freshwater zooplankton diel vertical migration (DVM) is a widespread predator-avoidance behavior that is induced by kairomones released from fish. Thereby zooplankton reduces predation by fish by staying in deep and dark colder strata during daytime and migrating into warmer layers during night, and thus experiences diel alterations in temperature. Constantly lower temperatures have been shown to increase the relative abundance of polyunsaturated fatty acids (PUFAs) in Daphnia sp. Furthermore, a low dietary supply of the ω3-PUFA eicosapentaenoic acid (EPA) has been shown to limit the induction of DVM in Daphnia magna and the performance of D. magna under fluctuating temperatures, as experienced during DVM. In nature DVM of D. magna in response to fish is accompanied by the presence of fish-borne kairomone and diel fluctuations of depth dependent-parameters like temperature, food, and oxygen supply. Here we investigated the effect of factors, which are differing between Daphnia that perform DVM and those which do not. We selected to examine the effect of changing temperature and light conditions and of the presence/absence of fish kairomones on D. magna. For this purpose, we conducted a full factorial experimental design in which we grew D. magna under constantly warm temperatures in a diel light-dark regime or under alternating temperatures in darkness crossed with the presence or absence of fish kairomones. We analyzed the fatty acid composition of mature animals and of their offspring in each treatment. Simulation of the light and temperature regime of migrating animals in presence of the fish kairomone resulted in an increased relative allocation of the ω3-PUFA EPA, from adult animals to their offspring, manifesting as decreased EPA concentrations in mothers and increased EPA concentrations in their offspring in response to simulated DVM (mothers). Additionally, EPA concentrations in the offspring were affected by the interaction of simulated DVM and the fish cue. The presence of the fish kairomone alone increased the EPA concentration in the offspring, that was not experiencing simulated DVM. These findings lead to the conclusion that the temperature and light regime associated with DVM alone, as well as in combination with the DVM-inducing fish kairomones, alter the allocation of fatty acids to the offspring in a manner, which is beneficial for the offspring under the decreased average temperatures, which migrating animals are exposed to. A low dietary supply of ω3-PUFAs may constrain D. magna’s amplitude of DVM, but our results suggest that the next generation of animals may be capable of regaining the full DVM amplitude due to the effect of the fish kairomone and the experienced temperature fluctuations (and darkness) on tissue fatty acid composition. These findings suggest that fatty acid limitation in DVM performing Daphnia may be more severe for the maternal than for the offspring generation.

The influence of light, substrate, and fish on the habitat preferences of the invasive bloody red shrimp, Hemimysis anomala

The invasive bloody red shrimp, Hemimysis anomala, is a novel organism in the Laurentian Great Lakes region that utilizes benthic and open-water habitat. Hemimysis is predicted to impact nearshore fish communities in the Northeastern USA where its range is expanding, either negatively through predation of shared zooplankton prey or positively as high-calorie prey. In this experimental study, we examined the factors influencing Hemimysis’ benthic habitat selection, vertical distribution, and susceptibility to fish predation. In the presence of fish cues, Hemimysis preferred cobble over other benthic substrates (Dreissena mussels, pebble, or sand) regardless of light conditions; in dark conditions without a fish present, Hemimysis preferred open waters with sand habitat. Light and fish cues also interacted to influence the vertical distribution of Hemimysis, with the majority of mysids selecting depths that minimized perceived cumulative risk. The mean feeding rates of young-of-year (YOY) alewife (Alosa pseudoharengus), adult round goby (Neogobius melanostomus), YOY yellow perch (Perca flavescens), adult pumpkinseed sunfish (Lepomis gibbosus), and YOY lake trout (Salvelinus namaycush) varied among species, prey densities, and substrate (range = 0.77–57 mysids/fish/h). In general, feeding rates were highest for alewife, a non-native species in the Great Lakes basin, and in refuge-free conditions for all species, except for non-native round goby, which fed at similar rates regardless of prey refuge availability. Collectively, our results suggest that fish feeding success is contingent upon the interaction of light and Hemimysis refuge availability due to behavioral modifications of Hemimysis in the presence of fish and adverse light conditions.

Freshwater snail responses to fish predation integrate phenotypic plasticity and local adaptation

Predators shape the phenotype of prey by means of local adaptation, within-generation plasticity, and transgenerational plasticity. Theory predicts that the influence of these three mechanisms on phenotype is determined by the number of generations exposed to the predator and the autocorrelation between parent and offspring predator environments. To test theoretical predictions about the relative effects of local adaptation, within-generation plasticity, and transgenerational plasticity on prey phenotype, we exposed two generations of freshwater snails (Physa acuta) from two populations—one from a large pond containing predatory fish and one from a set of small ponds that lacked predatory fish—to the cues from a predaceous bluegill sunfish (Lepomis macrochirus). Physa acuta exhibit both local adaptation and phenotypic plasticity in response to predation risk; thus, we predicted that snails from the population with fish and snails experimentally exposed to fish cues would produce more globose (or spherical), crush-resistant shells. In addition, given the prolonged exposure to fish predation, we predicted that snails from the population with fish would exhibit reduced phenotypic plasticity. We found evidence that snails from the population with fish were generally more globose and more crush resistant than snails from the fish-less population and exposure to fish cues led snails from both populations to develop more globose shells with increased crush resistance. However, contrary to our predictions, the offspring of snails from both populations exposed to fish cues had elongated shells and reduced crush resistance. This may reflect the negative effects of parental stress or variation in resource investment.

The non‐consumptive effects of predators and personality on prey growth and mortality

AbstractIndividual organisms vary in personality, and the ecological consequences of that variation can affect the strength of predator–prey interactions. Prey with bolder tendencies can mitigate the strength of species interactions by altering growth and initiating ontogenetic niche shifts (ONS). While the link between personality and growth has been established, recent research has highlighted the important interplay between ONS and predator cues in community ecology. The objective of this study was to evaluate the effects of prey personality and predator cues on prey growth and ONS. We predicted growth–mortality trade‐offs among personalities with higher survival, larger size, and accelerated ONS for bold individuals in comparison with shy individuals. To evaluate this objective, we conducted behavioral assays and a mesocosm experiment to test how southern leopard frog (Rana sphenocephala) tadpole personality and predatory fish (bluegill, Lepomis macrochirus) cues affects tadpole growth and metamorphosis. On average, bold tadpoles had higher mortality across all treatments in comparison with shy tadpoles. The effects of fish cues were dependent on tadpole personality with shy tadpoles metamorphosing significantly later than bold tadpoles. Bold tadpoles were larger than shy tadpoles at metamorphosis; however, that pattern reversed with fish cues as shy individuals metamorphosed larger than bold individuals. Our results suggest personality may be useful for predicting growth and life history for some prey species with predators. Specifically, the threat of predation can interact with personality to incur a benefit (earlier ONS) while also incurring a cost (size at metamorphosis). Hence by incorporating predator cues with personality, ecologists will be able to elucidate growth–mortality trade‐offs mediated by personality.

Fear and food: Effects of predator‐derived chemical cues and stoichiometric food quality onDaphnia

AbstractWhile resource quality and predator‐derived chemical cues can each have profound effects on zooplankton populations and their function in ecosystems, the strength and direction of their interactive effects remain unclear. We conducted laboratory experiments to evaluate how stoichiometric food quality (i.e., algal carbon [C] : phosphorus [P] ratios) affects responses of the zooplankter,Daphnia pulicaria,to predator‐derived chemical cues. We compared growth rates, body P content, metabolic rates, life‐history shifts, and survival of differentially P‐nourishedDaphniain the presence and absence of chemical cues derived from fish predators. We found effects of predator cues and/or stoichiometric food quality on all measured traits ofDaphnia. Exposure to fish cues led to reduced growth and increased metabolic rates but had little effect on the body %P content ofDaphnia. Elevated algal C : P ratios reduced growth and body %P and increased mass‐specific respiration rates. While most of the effects of predator cues and algal C : P ratios ofDaphniawere non‐interactive, reduced survival and relatedly reduced population growth rates that resulted from P‐poor food were amplified in the presence of predator‐derived cues. Our results demonstrate that stoichiometric food quality interacts with antipredator responses ofDaphnia, but these effects are largely trait dependent and appear connected to animal life‐history evolution. Given the ubiquity of predators and P‐poor food in lake ecosystems, our results highlight the importance of the interactive responses of animals to predator cues and poor nutrition.

Effects of urea on behavior and functional traits of Asiatic toad (Bufo gargarizans) tadpoles

As one of the important contributors of biodiversity, amphibian populations are declining worldwide. Numerous factors are involved in these declines, one of them being the use of fertilizers in agriculture. This is especially true for tadpoles which can live in the fertilizer-polluted farmland water bodies until metamorphosis. The present study aimed to assess the effects of urea (CH4N2O), as one of the most economical and effective fertilizers, on the anti-predator behavior and intraspecific functional trait variability of Asiatic toad (Bufo gargarizans) tadpoles. Based on published literatures and the field observation of urea concentrations in China, glass beakers with a gradient of urea concentrations (0, 200, 400, 600, and 1200 mg/L) were prepared, with 10 tadpoles placed in each glass beaker. Each treatment was replicated three times. Mosquito fish (Gambusia affinis) cues were used as the predator disturbance, and three main functional traits (body mass, trunk bending shape, and eye position) were selected. Our results revealed that tadpoles activity levels decreased when exposed to urea as well as to mosquito fish cues. However, urea exposure did not alter the anti-predator behaviors of tadpoles. Additionally, we found that increasing urea concentrations might modify some functional traits of tadpoles. Importantly, urea disturbance decreased tadpoles intraspecific functional trait variability. (Functional similarity increased between developmental stages.) Given that functional similarity between developmental stages could potentially increase intraspecific competition, urea could indirectly reduce tadpoles survival by decreasing intraspecific traits variability.

You cannot have it all: Heritability and constraints of predator-induced developmental plasticity in a Neotropical treefrog.

Many organisms have evolved phenotypic plasticity but examples of a heritable genetic basis or genetic constraints for plasticity across environments remain scarce. Tadpoles of the Neotropical treefrog Dendropsophus ebraccatus alter tail coloration and shape differently in response to fish or aquatic insect predators. To assess the genetic basis of plasticity we raised 1020 tadpoles from 17 maternal half-sib pairs (34 unique families) individually with chemical cues of fish or aquatic insects, or with cue-free control water. We used Bayesian animal models to estimate narrow sense heritability of morphology and cross-trait genetic correlations in all three treatments, heritability of plasticity in response to each predator, and genetic correlations between responses to fish and insects. Families showed remarkably different responses to predators and heritability was often high (0.45-0.75), as was heritability of plasticity itself (0.42-0.62). We detected strong negative genetic correlations for responses to each predator (-0.45 and -0.59), providing clear evidence of a limit to plasticity. Most importantly, we show that prey genotypes are constrained in their capacity to respond to different types of predators, which likely maintains genetic variation for plasticity in a temporally and spatially dynamic landscape where there is no single adaptive peak.

Phenotypic plasticity in specialists: How long-spined larval Sympetrum depressiusculum (Odonata: Libellulidae) responds to combined predator cues.

Phenotypic plasticity is a common defensive strategy in species experiencing variable predation risk, such as habitat generalists. Larvae of generalist dragonflies can elongate their abdominal spines in environments with fish, but long spines render larvae susceptible to invertebrate predators. Long-spined specialists adapted to fish-heavy habitats are not expected to have phenotypic plasticity in this defence trait, but no empirical studies have been undertaken. Moreover, in comparison to prey responding to multiple predators that induce similar phenotypes, relatively little is known regarding how species react to combinations of predators that favour opposing traits. We examined plasticity of larval dragonfly Sympetrum depressiusculum, a long-spined habitat specialist. In a rearing experiment, larvae were exposed to four environments: (i) no predator control, (ii) fish cues (Carassius auratus), (iii) invertebrate cues (Anax imperator), as well as (iv) a combination of (ii) and (iii). Compared with the control, fish but not invertebrate cues resulted in longer spines for two (one lateral, one dorsal) of the six spines measured. Interestingly, the combined-cue treatment led to the elongation of all four dorsal spines compared with the fish treatment alone, whereas lateral spines showed no response. Our experiment provided evidence of morphological plasticity in a long-spined specialist dragonfly. We showed that nearly all spines can elongate, but also react differently under specific predator settings. Therefore, while spine plasticity evolved in direct response to a single predator type (fish), plasticity was maintained against invertebrate predators as long as fish were also present. Selective spine induction under the combined condition suggests that S. depressiusculum can successfully survive in environments with both predators. Therefore, phenotypic plasticity may be an effective strategy for habitat generalists and specialists. Although more studies are necessary to fully understand how selection shapes the evolution of phenotypic plasticity, we demonstrated that in dragonflies, presence or absence of a specific predator is not the only factor that determines plastic defence responses.

Behaviour of freshwater snails (Radix balthica) exposed to the pharmaceutical sertraline under simulated predation risk

Due to their potential for affecting the modulation of behaviour, effects of selective serotonin reuptake inhibitors (SSRIs) in the environment are particularly interesting regarding interspecies interactions and non-consumptive effects (NCEs) induced by predator cues in prey organisms. We evaluated the effects of sertraline (0.4, 40 ng/L, 40 µg/L) over 8 days on activity and habitat choice in the freshwater snail Radix balthica, on snails’ boldness in response to mechanical stimulation (simulating predator attack), and their activity/habitat choice in response to chemical cues from predatory fish. We hypothesised that sertraline exposure would detrimentally impact NCEs elicited by predator cues, increasing predation risk. Although there were no effects of sertraline on NCEs, there were observed effects of chemical cue from predatory fish on snail behaviour independent of sertraline exposure. Snails reduced their activity in which the percentage of active snails decreased by almost 50% after exposure to fish cue. Additionally, snails changed their habitat use by moving away from open (exposed) areas. The general lack of effects of sertraline on snails’ activity and other behaviours in this study is interesting considering that other SSRIs have been shown to induce changes in gastropod behaviour. This raises questions on the modes of action of various SSRIs in gastropods, as well as the potential for a trophic “mismatch” of effects between fish predators and snail prey in aquatic systems.