Inducible defences are widely used for studying phenotypic plasticity, yet frequently we know little about the cues that induce these defences. For aquatic prey, defences are induced by chemical cues from predators (kairomones) and injured prey (alarm cues). Rarely has anyone determined the separate and combined effects of these cues, particularly across phylogenetically diverse prey types. We examined how tadpoles (Hyla versicolor) altered their defences when 10 different prey were either crushed by hand or consumed by predators. Across all prey types, crushing induced only a subset of the defences induced by consumption. Consuming vs. crushing produced additive responses for behaviour but synergistic responses for morphology and growth. Moreover, we discovered the first extensive evidence that prey responses to different alarm cues depends on prey phylogeny. These results suggest that the amount of information available to the prey affects both the quantitative and qualitative nature of the defended phenotype.
Summary1. For phenotypically plastic organisms to produce phenotypes that are well matched to their environment, they must acquire information about their environment. For inducible defences, cues from damaged prey and cues from predators both have the potential to provide important information, yet we know little about the relative importance of these separate sources of information for behavioural and morphological defences. We also do not know the point during a predation event at which kairomones are produced, i.e. whether they are produced constitutively, during prey attack or during prey digestion. 2. We exposed leopard frog tadpoles (Rana pipiens) to nine predator cue treatments involving several combinations of cues from damaged conspecifics or heterospecifics, starved predators, predators only chewing prey, predators only digesting prey or predators chewing and digesting prey. 3. We quantified two behavioural defences. Tadpole hiding behaviour was induced only by cues from crushed tadpoles. Reduced tadpole activity was induced only by cues from predators digesting tadpoles or predators chewing + digesting tadpoles. 4. We also quantified tadpole mass and two size-adjusted morphological traits that are known to be phenotypically plastic. Mass was unaffected by the cue treatments. Relative body length was affected (i.e. there were differences among some treatments), but none of the treatments significantly differed from the no-predator control. Relative tail depth was affected by the treatments and deeper tails were induced only when tadpoles were exposed to cues from predators digesting tadpoles or cues from predators chewing + digesting tadpoles.5. These results demonstrate that some prey species can discriminate among a diverse set of potential cues from heterospecific prey, conspecific prey and predators. Moreover, the results illustrate that the cues responsible for the full suite of behavioural and morphological defences are not induced by tadpole crushing nor can they be induced by generalized digestive chemicals produced when predators digest their prey. Instead, both prey damage and predator digestion of conspecific tissues appear to be important for communicating predatory risk to phenotypically plastic anuran prey. Importantly, the production of chemical cues by predators may be unavoidable and prey have evolved the ability to eavesdrop on these signals.
The widespread application of pesticides has attracted the attention of ecologists as we struggle to understand the impacts of these chemicals on natural communities. While we have a large number of laboratory-based, single-species studies of pesticides, such studies can only examine direct effects. However, in natural communities, species can experience both direct and indirect effects. We conducted an outdoor mesocosm experiment on aquatic communities containing three tadpole species (Hyla versicolor, Bufo americanus, and Rana pipiens), zooplankton, and algae. We then manipulated a factorial combination of predators (no predators; newts, Notophthalmus viridescens; and larval beetles, Dytiscus sp.) and pesticides (no pesticides, the insecticide malathion, and the herbicide Roundup). We found that Roundup (1.3 mg of active ingredient/L) had substantial direct negative effects on the tadpoles, reducing total tadpole survival and biomass by 40%. However, Roundup had no indirect effects on the amphibian community via predator survival or algal abundance. Malathion (0.3 mg/L) had few direct effects on the tadpoles. Malathion caused no indirect effects with one of the predators (red-spotted newts) but caused substantial positive effects on amphibians (a five-fold increase in total tadpole survival and biomass) due to the sensitivity of the predatory beetles to the insecticide. Thus, while high concentrations of malathion can directly kill larval anurans, more ecologically relevant concentrations can have large positive effects in mesocosms by removing predatory insects. These results make it clear that pesticides can have both direct and indirect effects in natural communities and that these effects critically depend upon the composition of the community.
Most organisms possess traits that are sensitive to changes in the environment (i.e., plastic traits) which results in the expression of environmentally induced polymorphisms. While most phenotypically plastic traits have traditionally been treated as threshold switches between induced and uninduced states, there is growing evidence that many traits can respond in a continuous fashion. In this experiment we exposed larval anurans (wood frog tadpoles, Rana sylvatica) to an increasing gradient of predation risk to determine how organisms respond to small environmental changes. We manipulated predation risk in two ways: by altering the amount of prey consumed by a constant number of predators (Dytiscus sp.) and by altering the number of predators that consume a constant amount of prey. We then quantified the expression of predator-induced behavior, morphology, and mass to determine the level of risk that induced each trait, the level of risk that induced the maximal phenotypic response for each trait, whether the different traits exhibited a plateauing response, and whether increasing risk via increasing predator number or via increasing prey consumption induced similar phenotypic changes. We found that all of the traits exhibited fine-tuned, graded responses and most of them exhibited a plateauing response with increased predation risk, suggesting either a limit to plasticity or the reflection of high costs of the defensive phenotype. For many traits, a large proportion of the maximum induction occurred at low levels of risk, suggesting that the chemical cues of predation are effective at extremely low concentrations. In contrast to earlier work, we found that behavioral and morphological responses to increased predator number were simply a response to increased total prey consumption. These results have important implications for models of plasticity evolution, models of optimal phenotypic design, expectations for how organisms respond to fine-grained changes (i.e., within generation) in their environment, and impacts on ecological communities via trait-mediated indirect effects.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.