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Relyea, R.A. (2008) A cocktail of contaminants: How pesticide mixtures at low concentrations affect aquatic communities. Oecologia :In Press The ubiquity of anthropogenic chemicals in nature poses a challenge to understand how ecological communities are impacted. While we are rapidly gaining an understanding of how individual contaminants affect communities, communities are exposed to suites of contaminants yet investigations of the effects of diverse contaminant mixtures in aquatic communities are rare. I examined how a single application of five insecticides (malathion, carbaryl, chlorpyrifos, diazinon, and endosulfan) and five herbicides (glyphosate, atrazine, acetochlor, metolachlor, and 2,4-D) at low concentrations (2 to 16 ppb) affected aquatic communities composed of zooplankton, phytoplankton, periphyton, and larval amphibians (gray tree frogs, Hyla versicolor, and leopard frogs, Rana pipiens). Using outdoor mesocosms, I examined each pesticide alone, a mix of insecticides, a mix of herbicides, and a mix of all 10 pesticides. Individual pesticides had a wide range of direct and indirect effects on all trophic groups. For some taxa (i.e. zooplankton and algae), the impact of pesticide mixtures could largely be predicted from the impacts of individual pesticides; for other taxa (i.e. amphibians) it could not. For amphibians, there was an apparent direct toxic effect of endosulfan that caused 84% mortality of leopard frogs and an indirect effect induced by diazinon that caused 24% mortality of leopard frogs. When pesticides were combined, the mix of herbicides had no negative effects on the survival and metamorphosis of amphibians, but the mix of insecticides and the mix of all 10 pesticides eliminated 99% of leopard frogs. Interestingly, these mixtures did not cause mortality in the gray tree frogs and, as a result, the gray tree frogs grew nearly twice as large due to reduced competition with leopard frogs. In short, wetland communities can be dramatically impacted by low concentrations of pesticides (both separate and combined) and these results offer important insights for the conservation of wetland communities. Relyea, R.A., and J.T. Hoverman (2008) Interactive effects of pesticides and predators on aquatic communities. Oikos :In Press Chemical contaminants are ubiquitous in nature and a major goal of ecologists has been to understand and predict their impacts on natural communities. While direct toxic effects can be garnered from single-species laboratory studies, the full suite of possible effects can only be observed when organisms are embedded within a community. In this study, we manipulated the concentration of malathion (a broad-spectrum insecticide) to determine the impacts on aquatic communities containing phytoplankton, periphyton, and 27 species of animals (16 zooplankton, 5 snails, 3 tadpoles, and 3 predatory insects). Using relatively low concentrations (0.13 to 0.46 mg/L), we found important direct (and interactive) effects of predators and malathion on the food web as well as a number of apparent density- and trait-mediated indirect effects. Malathion initiated an indirect effect by decreasing zooplankton diversity and abundance, which propagated an increase in phytoplankton, a decrease in periphyton, and a subsequent decrease in the growth of leopard frog tadpoles. There also was an apparent trait-mediated indirect effect whereby increased amounts of the pesticide reduced predation rates on amphibians without affecting the survival of the primary amphibian predator (larval Anax dragonflies). In contrast, snail survival and growth was unaffected by the pesticide but there were strong, species-specific effects from their primary predator (adult Belostoma water bugs). This is one of few studies to examine the impacts of malathion on aquatic communities across a range of concentrations, despite the fact that it is currently the most commonly applied insecticide in the United States, it is applied around the world, and it can be legally directly sprayed over aquatic habitats to control the mosquitoes that carry malaria and West Nile virus. Our results suggest several mechanisms by which a wide variety of pesticides with similar modes of action might impact aquatic communities. McCauley, S.J., C.J. Davis, R.A. Relyea, K.L. Yurewicz, D.K. Skelly, and E.E. Werner (2008) Metacommunity patterns in larval odonates. Oecologia :In Press The growth of metacommunity ecology as a sub-discipline has increased interest in how processes at different spatial scales structure communities. However, a significant gap remains relating the action of niche- and dispersal-assembly mechanisms to observed species distributions across gradients. Surveys of the larval dragonfly community (Odonata: Anisoptera) in 57 lakes and ponds in southeast Michigan were used to evaluate hypotheses about the processes regulating community structure in this system. We considered the roles of both niche- and dispersal-assembly processes in determining patterns of species richness and composition across a habitat gradient involving changes in the extent of habitat permanence, canopy cover, area, and top predator type. We compared observed richness patterns and species distributions in this system to patterns predicted by four general community models: species sorting related to adaptive trade-offs, a developmental constraints hypothesis, dispersal-assembly, and a neutral community assemblage. Our results supported neither the developmental constraints nor the neutral-assemblage models. Observed patterns of richness and species distributions were consistent with patterns expected when adaptive trade-offs and dispersal-assembly mechanisms affect community structure. Adaptive trade-offs appeared to be important in limiting the distributions of species which segregate across the habitat gradient. However, dispersal was important in shaping the distributions of species that utilize habitats with a broad range of hydroperiods and alternative top predator types. Our results also suggest that the relative importance of these mechanisms may change across this habitat gradient and that a metacommunity perspective which incorporates both niche- and dispersal-assembly processes is necessary to understand how communities are organized. Auld, J.R., and R.A. Relyea (2008) Are there interactive effects of mate availability and predation risk on life history and defense in a simultaneous hermaphrodite? J. Evol. Biol. :In Press Encountering mates and avoiding predators are ubiquitous challenges faced by many organisms and they can affect the expression of many traits including growth, timing of maturity, and resource allocation to reproduction. However, these two factors are commonly considered in isolation rather than simultaneously. We examined whether predation risk and mate availability interact to affect morphology and life-history traits (including lifetime fecundity) of a hermaphroditic snail (Physa acuta). We found that mate availability reduced juvenile growth rate and final size. Predator cues from crayfish induced delayed reproduction, but there were no reduced-fecundity costs associated with predator induction. While there were interactive effects on longevity, lifetime fecundity was determined by the number of reproductive days. Therefore, our results indicate a resource-allocation trade-off among growth, longevity, and reproduction. Future consideration of this interaction will be important for understanding how resource-allocation plasticity affects the integration of defensive, life-history and mating-system traits. Relyea, R.A., and N. Diecks (2008) An unforeseen chain of events for amphibians: Lethal effects of pesticides at sublethal concentrations. Ecol. Appl. :In Press The field of toxicology has traditionally assessed the risk of contaminants by using laboratory experiments and a range of pesticide concentrations that are held constant for short periods of time (1 to 4 d). From these experiments, one can estimate the concentration that causes no effect on survival. However, organisms in nature frequently experience multiple applications of pesticides over time rather than a single constant concentration. In addition, organisms are embedded in ecological communities which can propagate indirect effects through a food web. Using outdoor mesocosms, we examined how low concentrations (10 to 250 g/L) of a globally common insecticide (malathion) applied at various amounts, times, and frequencies affected aquatic communities containing zooplankton, phytoplankton, periphyton, and larval amphibians (reared at two densities) for 79 d. All application regimes caused a decline in zooplankton which initiated a trophic cascade in which there was a bloom in phytoplankton and, in several treatments, a subsequent decline in the competing periphyton. The reduced periphyton had little effect on wood frogs (Rana sylvatica) which have a short time to metamorphosis. However, leopard frogs (R. pipiens) have a longer time to metamorphosis and they experienced large reductions in growth and development which led to subsequent mortality as the environment dried. Hence, malathion (which rapidly breaks down) did not directly kill amphibians, but initiated a trophic cascade that indirectly resulted in substantial amphibian mortality. Importantly, repeated applications of the lowest concentration ( a "press treatment" consisting of seven weekly applications of 10 g/L) caused larger impacts on many of the response variables than single "pulse" applications that were 25 times greater in concentration. These results are not only important because malathion is the most commonly applied insecticide and is found in wetlands, but also because the mechanism underlying the trophic cascade is common to a wide range of insecticides, offering the possibility of general predictions for how many insecticides impact aquatic communities and the populations of larval amphibians. Relyea, R.A. (2008) Multiple stressors and indirect food web effects of contaminants on herptofauna. Pp In Press in Ecotoxicology of Amphibians and Reptiles, 2nd edition, Sparling, D., Ed. CRC Press, New York Schoeppner, N.M., and R.A. Relyea (2008) Detecting small environmental differences: Risk-response curves for predator-induced behavior and morphology. Oecologia 154:743-754 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.
Hoverman, J.T., and R.A. Relyea (2008) Temporal variation in predation risk: Phenotypes, fitness, and trait-mediated interactions. Oikos 117:23-32 Understanding the role of history in the formation of communities has been a major challenge in community ecology. Here, we explore the role of phenotypic plasticity and its associated trait-mediated indirect interactions as a mechanism behind priority effects. Using organisms with inducible defenses as a model system, we examine how aquatic communities initially containing different predator environments are affected at the individual and community level by the colonization of a second predator. Snails and tadpoles were established in four different caged-predator environments (no predator, fish, crayfish, or water bugs). These four communities were then crossed with three predator colonization treatments (no colonization, early colonization, or late colonization) using lethal water bugs as the predator. The snails responded to the caged predator environments with predator-specific behavioral and morphological defenses. In the colonization treatments, snails possessing the wrong phenotype attempted to induce phenotypic changes to defend themselves against the new risk. However, snails initially induced by a different predator environment often suffered high predation rates. Hence, temporal variation in predation risk not only challenged the snail prey to try to track this environmental variation through time by adjusting their defensive phenotypes, but also caused trait-mediated interactions between snails and the colonizing predator. For tadpoles within these communities, there was little evidence that the morphological responses of snails indirectly effected tadpole predation rates by colonizing water bugs. Unexpectedly, predation rates on tadpoles by colonizing water bugs were generally higher in the three caged-predator treatments, suggesting that water bugs elevated their foraging activity in response to potentially competiting predators. In summary, we demonstrate an important priority effect in which the initial occurrence of one species of predator can facilitate predation by a second predator that colonizes at a later date (i.e. a TMII) suggesting that phenotypic plasticity can be an important driver behind priority effects (i.e. historical exposure to predators).
Relyea, R.A. (2008) The effects of pesticides on amphibians. Pp 48-49 in Threatened Amphibians of the World, Stuart, S.N., M. Hoffman, J.S. Chanson, N.A. Cox, R.J. Berridge, P. Ramini, and B.E. Young, Ed. Lynx Ediciones, Barcelona Hoverman, J.T., and R.A. Relyea (2007) The rules of engagement: How prey respond to multiple predators. Oecologia 154:551-560 Studies of inducible defenses have traditionally examined prey responses to one predator at a time. However, prey in nature encounter combinations of predators that should force them to produce phenotypic compromises. We examined how snails (Helisoma trivolvis) alter their phenotype with three different predator species that were present alone and in pairwise combinations. When snails were exposed to each predator alone, they formed predator-specific defenses that reflected the differences in each predator#s foraging mode. When snails were exposed to pairwise combinations of predators, their phenotype was dependent on the their ability to detect each predator, the risk posed by each predator, and the effectiveness of a given defense against each predator. Consequently, responses to combined predators were typically biased towards one of the predators in the pair. This suggests that prey facing combined predators do not form simple intermediate defenses and, as a result, may experience enhanced mortality risk when they encounter natural predator regimes.
Werner, E.E., D.K. Skelly, R.A. Relyea, and K.L. Yurewicz (2007) Amphibian species richness across environmental gradients. Oikos 116:1697-1712 Large-scale field patterns are a fundamental source of inferences on processes responsible for variation in species richness among habitats. We examined species richness of larval amphibian communities in 37 ponds over 7 yrs on the University of Michigan#s E. S. George Reserve. Ordination of the community incidence matrix indicated a strong major axis of variation in species associations that was correlated with pond hydroperiod, surface area and forest canopy cover. Communities were significantly nested with those species found in ponds with high canopy cover, small area and short hydroperiod being nested subsets of those found in ponds with contrasting characteristics. Presence of fish had strong negative effects on species richness; relaxation of this effect also was apparent when fish were extirpated from ponds by drought. We employed a model selection analysis to identify the most appropriate statistical model for predicting the long-term average species richness of these ponds from local abiotic and biotic (predator and competitor density) factors. A model including only the abiotic factors was overwhelmingly superior for the anurans; hierarchical partitioning indicated that area and canopy cover alone accounted for over 70% of the independent effects of predictor variables. The global model including both abiotic and biotic factors was the best supported model for the caudates, and correspondingly hierarchical partitioning suggested that area, hydroperiod, invertebrate predators and caudate biomass all accounted for 9 - 16% of the independent effects. Overall, biotic factors accounted for much less of the variation in species richness than abiotic factors. The patterns in larger, open-canopy ponds provided little evidence of competitive effects on species richness, though there were patterns consistent with competitive effects in small, closed-canopy ponds. The unusual temporal and spatial extent of these data enabled us to critically evaluate ideas regarding patterns in larval amphibian communities, and the effects of area, disturbance (hydroperiod) and productivity (canopy cover) on species richness of these communities. These results have important implications to the conservation of amphibian species richness in freshwater wetlands, which are among the most threatened ecosystems worldwide.
Werner, E.E., K.L. Yurewicz, D.K. Skelly, and R.A. Relyea (2007) Turnover in an amphibian metacommunity: the role of local and regional factors. Oikos 116:1713-1725 Ecologists have long realized that stable species richness values can mask rapid turnover in species composition. Because turnover occurs as a consequence of both local and regional processes, understanding the responsible factors provides insight on processes influencing community structure at different scales. Despite the insights to be gained from data on species turnover, they remain relatively uncommon. We present data on the interannual turnover in species composition of larval amphibian communities in 37 ponds over 7 yrs. Species composition of a given pond community was highly dynamic; about half of the species that could be found breeding in a particular pond were actually present in a given year. All species participated in this community turnover, but to different degrees. Using a model selection approach, we show that a statistical model including local environmental factors (pond area, hydroperiod, and canopy cover) and pond connectivity on the landscape provided the best predictions of turnover. Averaged parameter estimates were significant for area, hydroperiod, and connectivity and these same variables were identified by hierarchical partitioning as having significant independent effects on turnover. Area and hydroperiod were negatively related to turnover, whereas connectivity was positively related to turnover. Additionally, the average fraction of years a species was present in a pond was positively correlated with average local population size, but even more strongly correlated with regional population size, suggesting both local and regional influences on turnover. Of the measured biotic factors (biomass of fish, invertebrate predators, anuran and caudate larvae), presence of fish was the only factor that significantly affected rates of turnover. Several mechanism could be responsible for changes in species composition (species extinctions, skipped breeding and movement of choruses), but extinctions appear to be the major cause of turnover. These results have important implications to understanding long-term persistence of species on landscapes and the causes of patterns in species richness on environmental gradients.
Relyea, R.A. (2007) Getting out alive: How predators affect metamorphic decisions. Oecologia 152:389-400 Metamorphosis has intrigued biologists for a long time as an extreme form of complex life cycles that are ubiquitous in animals. While investigated from a variety of perspectives, the ecological focus has been on identifying and understanding the ecological factors that affect an individual's decision on when, and at what size, to metamorphose. Predation is a major factor that affects metamorphic decisions and a recent review (Benard 2004) documented how predator cues induce metamorphic changes relative to model predictions. Importantly, however, real predators affect larval prey via several mechanisms beyond simple induction. In this article, I contrast the leading models of metamorphosis, provide an overview of the multiple ways that predators can directly and indirectly affect larval growth and development (via induction, thinning, and selection), and identify how each process should affect the time to and size at metamorphosis. With this mechanistic foundation established, I then turn to the well studied model system of larval amphibians to synthesize studies on 1) caged predators (which cause only induction) and 2) lethal predators (which cause induction, thinning, and selection). Among the caged predator studies, the chemical cues emitted by predators rarely induce a smaller size at metamorphosis or a shorter time to metamorphosis, which is in direct contrast to theoretical predictions but in agreement with Benard's (2004) review based on a considerably smaller dataset. Among the lethal predator studies, there is a diversity of outcomes depending upon the relative importance of induction versus thinning with the relative importance of the two processes appearing to change with larval density. Finally, I review the persistent effects of larval predators after metamorphosis including both phenotypic and fitness effects. At the end, I outline a number of future directions to allow researchers to continue gaining insight into how predators affect the metamorphic decisions of their prey.
Hoverman, J.T., and R.A. Relyea (2007) How flexible is phenotypic plasticity? Developmental windows for trait induction and reversal. Ecology 88:693-705 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.
Relyea, R.A., and J.T. Hoverman (2006) Assessing the ecology in ecotoxicology: A review and synthesis in freshwater systems. Ecol. Lett. 9:1157-1171 The field of ecotoxicology is experiencing a surge in attention among ecologists as we gain a deeper appreciation for how contaminants can impact natural ecosystems. This interest is particularly strong in aquatic systems where many non-target organisms experience pesticides. In this article, we assess how pesticides affect freshwater systems by applying the conceptual framework of density- and trait-mediated indirect effects from the field of basic ecology. We demonstrate the utility of this framework for understanding the conditions under which pesticides affect species interactions, communities, and ecosystems. Through the integration of laboratory toxicity tests and this ecological framework, ecotoxicologists should be better able to identify the mechanisms through which pesticides affect communities and ecosystems. We also identify several areas of research that are in critical need of empirical attention including synergistic effects between pesticides and natural stressors, the importance of pesticides on community assembly via habitat preferences and oviposition effects, the timing and frequency of pesticide applications, pesticide effects on population dynamics, the evolution of pesticide resistance in non-target organisms, and ecosystem recovery. With this knowledge, one can improve upon management decisions and help protect non-target species that are of conservation concern.
Relyea, R.A. (2006) The impact of insecticides and herbicide on the biodiversity and productivity of aquatic communities: Response. Ecol. Appl. 16:2027-2034 Assessing how hundreds of pesticides affect thousands of non-target organisms in nature is certainly a daunting challenge. When it comes to glyphosate-based products (including Roundup), Thompson et al. (2006) have taken exception to the conclusions of Relyea (2005a). To support this position, they discuss application rates, environmental concentrations, possible methodological flaws, and prior risk assessments. Here, I provide evidence to demonstrate that application rates are wider ranging than the authors suggest, that environmental concentrations cited by Thompson et al. (2006) are a highly biased subset of existing data, that the suspected flaws reflect a lack of knowledge of aquatic ecology, and that previous risk assessments are largely irrelevant to assessing Roundup's risk to tadpoles. Finally, I assess the current weight of the evidence as to whether Roundup (in its many formulations containing the surfactant POEA) is likely to be lethal to amphibians under environmentally relevant concentrations.
Relyea, R.A. (2006) The effects of pesticides, pH and predatory stress in amphibians under mesocosm conditions. Exotoxicol. 15:503-511 Pesticides are applied throughout the world often with unintended consequences on ecological communities. In some regions, pesticides are associated with declining amphibians, but we have a poor understanding of the underlying mechanisms. Pesticides break down more slowly under low pH conditions and become more lethal to amphibians when combined with predatory stress, but these phenomena have not been tested outside of the laboratory. I examined how pH, predatory stress, and a single application of an insecticide (carbaryl) affected the survival and growth of larval bullfrogs (Rana catesbeiana) and green frogs (R. clamitans) in outdoor mesocosms. Decreased pH had no effect on survival, but caused greater tadpole growth. Low concentrations of carbaryl had no effect on either species, but high concentrations caused lower survival and greater growth in bullfrogs. Predatory stress and reduced pH did not make carbaryl more lethal likely due to the rapid breakdown rate of carbaryl in outdoor mesocosms. Thus whereas the stress of pH and predators can make carbaryl (and other pesticides) more lethal under laboratory conditions using repeated applications of carbaryl, these stressors did not interact under mesocosm conditions using a single application of carbaryl.
Clausen, J.C., I.M. Ortega, C.M. Glaude, R.A. Relyea, G. Garay, and O. Guineo (2006) Classification of wetlands in a Patagonian National Park, Chile. Wetlands 26:217-229 Wetlands in Torres del Paine National Park in Patagonia, Chile were studied to determine their variety and type because resident wetlands had not been previously described. In 2001, 88 wetlands were sampled for vegetation, water chemistry, water depth, substrate type, and hydroperiod to develop a classification system using a combination of factor, discriminant, and cluster techniques. In 2002-2003 the classification system was applied to an additional 323 wetlands. Types were named for floristic characteristics but were cross-typed with NWI and Ramsar classifications. Types described include Carex-Nothofagus, Juncus-Glyceria, Hippuris-Myriophyllum, Ranunculus, and Schoenoplectus marshes; peatlands; and vegas. Lake/ponds and mudflats were also identified. Wetlands were found in basins, slopes, and channels and have water regimes varying from saturated to permanently flooded. Differences were found in the chemical characteristics of water among wetland types and regions of the Park. Torres del Paine National Park is rich in its diversity of wetland types.
Miner, B.G., S.E. Sultan, S.G. Morgan, D.K. Padilla, and R.A. Relyea (2005) Ecological consequences of phenotypic plasticity. Trends Ecol. Evol. 20:685-692 Phenotypic plasticity is widespread in nature, and often involves ecologically relevant phenotypic traits. As a result, plasticity alters numerous interactions between organisms and their abiotic and biotic environments. Although much work on plasticity has focused on its patterns of expression and evolution, researchers are increasingly interested to understand how plasticity can affect ecological patterns and processes at various levels. Here we highlight a growing body of work examining how plasticity can affect all levels of ecological organization, from individuals and populations to communities and ecosystems, through effects on demographic parameters, direct and indirect species interactions such as competition, predation, and coexistence, and ultimately carbon and nutrient cycles.
Relyea, R.A. (2005) The lethal impact of Roundup® on aquatic and terrestrial amphibians. Ecol. Appl. 15:1118-1124 The global decline in amphibian diversity has become an international environmental problem with a multitude of possible causes. There is evidence that pesticides may play a role, yet few pesticides have been tested on amphibians. For example, Roundup® is a globally-common herbicide that is conventionally thought to be nonlethal to amphibians. However, Roundup® has been tested on few amphibian species, with existing tests conducted mostly under laboratory conditions and on larval amphibians. Recent laboratory studies have indicated that Roundup® may be highly lethal to North American tadpoles, but we need to determine whether this effect occurs under more natural conditions and in post-metamorphic amphibians. I assembled communities of three species of North American tadpoles in outdoor pond mesocosms that contained different types of soil (which can absorb the pesticide) and I applied Roundup® as a direct overspray. After 3 wks, Roundup® killed 96-100% of larval amphibians (regardless of soil presence). I then exposed three species of juvenile (post-metamorphic) anurans to a direct overspray of Roundup in laboratory containers. After 1 d, Roundup killed 68-86% of juvenile amphibians. These results suggest that Roundup®, a compound designed to kill plants, can cause extremely high rates of mortality to amphibians that could lead to population declines.
Hoverman, J.T., J.R. Auld, and R.A. Relyea (2005) Putting prey back together again: Integrating predator-induced behavior, morphology, and life history. Oecologia 144:481-491 The last decade has seen an explosion in the number of studies exploring predator-induced plasticity. Recently, there has been a call for more comprehensive approaches that can identify functional relationships between traits, constraints on phenotypic responses, and the cost and benefits of alternative phenotypes. In this study, we exposed Helisoma trivolvis, a freshwater snail, to a factorial combination of three resource levels and five predator environments (no predator, 1 or 2 water bugs, and 1 or 2 crayfish) and examined 10 traits including behavior, morphology, and life history. Each predator induced a unique suite of behavioral and morphological responses. Snails increased near-surface habitat use with crayfish but not with water bugs. Further, crayfish induced narrow and high shells whereas water bugs induced wide shells and wide apertures. In terms of life history, both predators induced delayed reproduction and greater mass at reproduction. However, crayfish induced a greater delay in reproduction that resulted in reduced fecundity whereas water bugs did not induce differences in fecundity. Resource levels impacted the morphology of Helisoma; snails reared with greater resource levels produced higher shells, narrower shells, and wider apertures. Resource levels also impacted snail life history; lower resources caused longer times to reproduction and reduced fecundity. Based on an analysis of phenotypic correlations, the morphological responses to each predator most likely represent phenotypic trade-offs. Snails could either produce invasion-resistant shells for defense against water bugs or crush-resistant shells for defense against crayfish, but not both. Our use of a comprehensive approach to examine the responses of Helisoma has provided important information regarding the complexity of phenotypic responses to different environments, the patterns of phenotypic integration across environments, and the potential costs and benefits associated with plastic traits.
Relyea, R.A., and J.R. Auld (2005) Predator- and competitor-induced plasticity: How changes in foraging morphology affect phenotypic trade-offs. Ecology 86:1723-1729 Studies of phenotypic plasticity frequently demonstrate functional trade-offs between alternative phenotypes by documenting environment-specific costs and benefits. However, the functional mechanisms underlying these trade-offs are often unknown. For example, predator-induced traits typically provide superior predator resistance but slower growth while competitor-induced traits provide better growth but inferior predator resistance. While the mechanisms underlying predator resistance have been identified, the mechanisms underlying differential growth have remained elusive. To determine whether competitor and predator environments affect individual growth by induced changes in foraging morphology, we raised wood frog tadpoles (Rana sylvatica) under a factorial combination of competitors and predators. In general, competitors induced relatively larger oral discs, wider beaks, and longer tooth rows while predators induced relatively smaller oral discs, narrower beaks, and shorter tooth rows. These effects were interactive; the largest competitor-induced responses occurred under high predator density and the largest predator-induced responses occurred under low competition. Further, one of the tooth rows that commonly appeared under low predation risk was frequently absent under high predation risk. These discoveries suggests that predator and competitor environments can have profound effects on prey foraging structures and that these effects set up growth tradeoffs between phenotypes that favor the evolution of phenotypically plastic responses.
Schoeppner, N.M., and R.A. Relyea (2005) Damage, digestion, and defense: The roles of alarm cues and kairomones for inducing prey defenses. Ecol. Lett. 8:505-512 Inducible defenses are widely used for studying phenotypic plasticity, yet frequently we know little about the cues that induce these defenses. For aquatic prey, defenses 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 predator diets. We examined how tadpoles (Hyla versicolor) altered their defenses when ten different predator diets were either crushed by hand or consumed by predators. Across all diets, crushing induced only a subset of the defenses induced by consumption. Consuming versus crushing produced additive responses for behavior but synergistic responses for morphology and growth. Moreover, we discovered the first extensive evidence that prey responses to different predator diets depends on diet phylogeny. These results suggest that the amount of information available to the prey affects both the quantitative and qualitative nature of the defended phenotype.
Relyea, R.A., N.M. Schoeppner, and J.T. Hoverman (2005) Pesticides and amphibians: The importance of community context. Ecol. Appl. 15:1125-1134 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.
Relyea, R.A. (2005) The heritability of inducible defenses in tadpoles. J. Evol. Biol. 18:856-866 The evolution of plastic traits requires phenotypic trade-offs and heritable traits, yet the latter requirement has received little attention, especially for predator-induced traits. Using a half-sib design, I examined the narrow-sense heritability of predator-induced behavior, morphology, and life history in larval wood frogs (Rana sylvatica). Many of the traits had significant additive genetic variation in predator (caged Anax longipes) and no-predator environments. Whereas most traits had moderate to high heritability across environments, tail depth exhibited high heritability with predators but low heritability without predators. In addition, several traits had significant heritability for plasticity, suggesting a potential for selection to act on plasticity per se. Genetic correlations confirmed known phenotypic relationships across environments and identified novel relationships within each environment. This appears to be the first investigation of narrow-sense heritabilities for predator-induced traits and confirms that inducible traits previously shown to be under selection also have a genetic basis and should be capable of exhibiting evolutionary responses.
Relyea, R.A. (2005) The lethal impacts of Roundup and predatory stress on six species of North American tadpoles. Arch. Environ. Contam. Toxicol. 48:351-357 The decline in amphibians across the globe has sparked a search for the causes and recent evidence suggests a connection with pesticides. However, for most pesticides, tests on amphibians are rare, conducted for short durations (1-4 d), and without natural stressors. Recent studies have discovered that the stress of predator cues in the water can make insecticides much more lethal to larval amphibians, but it is unknown whether this phenomenon can be generalized to other types of pesticides. Using six species of North American amphibian larvae (Rana sylvatica, R. pipiens, R. clamitans, R. catesbeiana, Bufo americanus and Hyla versicolor), I examined the impact of a globally-common herbicide (Roundup) on the survival of tadpoles for 16 d with and without the chemical cues emitted by predatory newts (Notophthalmus viridescens). LC5016-d estimates varied from 0.55 to 2.52 mg of active ingredient (AI)/L, considerably lower than the few previous studies using Roundup (1.5 to 15.5 mg AI/L). Moreover, in one of the six species tested (R. sylvatica), the addition of predatory stress made Roundup twice as lethal. This discovery suggests that synergistic interactions between predatory stress and pesticides may indeed be a generalizable phenomenon in amphibians that occurs with a wide variety of pesticides.
Relyea, R.A. (2005) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol. Appl. 15:618-627 Pesticides constitute a major anthropogenic addition to natural communities. In aquatic communities, a great majority of pesticide impacts are determined from single species experiments conducted under laboratory conditions. While this is an essential protocol to rapidly identify the direct impacts of pesticides on organisms, it prevents an assessment of direct and indirect pesticide effects on organisms embedded in their natural ecological contexts. In this study, I examined the impact of four globally-common pesticides (two insecticides: carbaryl (Sevin™) and malathion; two herbicides: glyphosate (Roundup™ and 2,4-D) on the biodiversity of aquatic communities containing algae and 25 species of animals. Species richness was reduced by 15% with Sevin, 30% with malathion, and 22% with Roundup while 2,4-D had no effect. Both insecticides reduced zooplankton diversity by eliminating cladocerans but not copepods (the latter increased in abundance). The insecticides also reduced the diversity and biomass of predatory insects, had an apparent indirect positive effect on several species of tadpoles, but had no effect on snails. The two herbicides had no effects on zooplankton, insect predators, or snails. Moreover, the herbicide 2,4-D had no effect on tadpoles. However, Roundup completely eliminated two species of tadpoles and nearly exterminated a third species, resulting in a 70% decline in the species richness of tadpoles. This study represents one of the most extensive experimental investigations of pesticide effects on aquatic communities and offers a comprehensive perspective on the impacts of pesticides when non-target organisms are examined under ecologically relevant conditions.
Relyea, R.A. (2005) Constraints on inducible defenses: Phylogeny, ontogeny, and phenotypic trade-offs. Pp 189-207 in Ecology of Predator-Prey Interactions, Barbarosa, P., and I. Castellanos, Ed. Oxford University Press, Oxford Anti-predator defenses are widespread in the animal kingdom and include an overwhelming mélange of traits. Hundreds of studies have examined the inducible defenses of multiple prey taxa and documented a wide range of anti-predator defenses. Most studies have focused on a single species of prey, observed prey responses at a single ontogenetic stage, and conducted the experiments under a single set of environmental conditions. While this approach is useful in establishing which prey taxa respond to predators, the approach is limited because it makes it difficult to identify potential contraints. By taking a more comprehensive approach that includes multiple species, multiple ontogenetic stages, and multiple environmental conditions, one can identify a series of potential constraints that may prevent prey from exhibiting predator-induced plasticity. Such constraints are multi-faceted and include historical constraints of phylogeny, the existence of restrictive developmental windows through ontogeny, and the presence of phenotypic trade-offs that occur when prey face conflicting pressures from two different predators, predators versus parasites, or predators versus competitors. In this chapter, I review what we know about these three potential constraints on inducible defenses and identify how these insights will likely change how we conduct our experiments, interpret our empirical results, and design future research programs.
Lawrence, R.K., S. Demarais, R.A. Relyea, S.P. Haskell, W.B. Ballard, and T.L. Clark (2004) Desert mule deer survival in southwest Texas. J. Wildlife Manage. 68:561-569 We studied population structure and limiting factors within a desert mule deer (Odocoileus hemionus eremicus) population in Brewster County of the Trans-Pecos Region in Texas, USA. We estimated and compared annual survival and pregnancy rates from March 1990-February 1993 for 121 adult (>33 months old) male and female, 61 subadult (21-33 months old), and 77 young (8-20 months old) deer. Variation in weather patterns (i.e., drought) was associated with-if not causative of-annual variation in survival patterns. Adult female and young survival had the strongest correlation with drought. Pregnancy status of young (less than or equal to 1.5 yr) and old (greater than or equal to 6.5 yr) deer appeared most affected by drought. Seasonal periods of natural stress differed for adult sex classes, with most female mortalities occurring during months associated with parturition and lactation, and most male natural stress losses occurring during late winter and early spring. The major mortality sources were hunting and natural stressors for adult males, natural stressors and predation for adult females, and predation and natural stressors for young. Subadult mortalities were too few to identify significant mortality agents. The significance of natural stress-related survival and fecundity impacting herd productivity and stability warrants further consideration of poorly understood causative mechanisms. Ideally, replicated treatment areas would be used to address compensatory and additive mortality issues relative to predator abundance, harvest, and natural-stress losses. Sih, A., J. Kerby, A. Bell., and R.A. Relyea (2004) Response to Schmidt. Pesticides, mortality and population growth rate. Trends Ecol. Evol. 19:460-461
Relyea, R.A., and J.R. Auld (2004) Having the guts to compete: How intestinal plasticity explains costs of inducible defenses. Ecol. Lett. 7:869-875 Predators commonly induce phenotypic changes that make prey better at surviving predation at the cost of reduced growth. While we have a good understanding of how trait changes affect predation risk, we lack a mechanistic understanding of why predator-induced phenotypes differ in growth. Using two mesocosm experiments, we combined phenotypic plasticity theory with predictions from optimal digestion theory to demonstrate that intra- and interspecific competition induced relatively long guts while predators induced relatively short guts. The longer guts induced by competition appear to be an adaptive response that allows more efficient digestion and more rapid growth whereas the shorter guts induced by predators appear to result from a tradeoff of building larger tails in predator environments at the cost of smaller bodies. By combining these two bodies of theory, we now have a much better understanding of the mechanisms that cause the phenotypic trade-offs that select for inducible defenses.
Relyea, R.A. (2004) The growth and survival of five amphibian species exposed to combinations of pesticides. Environ. Toxicol. Chem. 23:1737-1742 The global decline of amphibians has sparked interest in the role that pesticides may play. Pesticides in nature typically exist in combinations, but given the vast number of chemicals used, most toxicological experiments have necessarily examined one pesticide at a time. I examined how four commercial formulations of pesticides (diazinon, carbaryl, malathion, and glyphosate) affected the survival and growth of five larval amphibian species (Rana pipiens, R. clamitans, R. catesbeiana, Bufo americanus, and Hyla versicolor) when alone (at 1 or 2 mg/L of active ingredient) and in pairwise combinations (1 mg/L of each pesticide). At 1 mg/L, the pesticides reduced survival in 5% of the 20 species-pesticide comparisons and reduced growth in 35% of the comparisons. At 2 mg/L, the pesticides had more widespread effects, reducing survival in 35% of the 20 species-pesticide comparisons and reducing growth in 70% of comparisons. Combined pesticides occasionally caused lower survival and growth than either pesticide alone, but the effects were never larger than the more deadly of the two pesticides alone at 2 mg/L. This suggests that the impact of combining these four pesticides is similar to that predicted by the total concentration of pesticides in the system.
Relyea, R.A. (2004) Synergistic impacts of malathion and predatory stress on six species of North American tadpoles. Environ. Toxicol. Chem. 23:1080-1084 The decline of many amphibian populations is associated with pesticides, but for most pesticides we know little about their toxicity to amphibians. Malathion is a classic example; it is sprayed over aquatic habitats to control mosquitoes that carry malaria and the West Nile virus, yet we know little about its effect on amphibians. I examined the survival of six species of tadpoles (wood frogs, Rana sylvatica; leopard frogs, R. pipiens; green frogs, R. clamitans; bullfrogs, R. catesbeiana; American toads, Bufo americanus; and gray tree frogs, Hyla versicolor) for 16 d in the presence or absence of predatory stress and six concentrations of malathion. Malathion was moderately toxic to all species of tadpoles (LC50 values, the concentration estimated to kill 50% of a test population, ranged from 1.25 # 5.9 mg/L). These values are within the range of values reported for the few amphibians that have been tested (0.2 - 42 mg/L). In one of the six species, malathion became twice as lethal when combined with predatory stress. Similar synergistic interactions have been found with the insecticide carbaryl, suggesting that the synergy may occur in many carbamate and organophosphate insecticides. While malathion has the potential to kill amphibians and it's presence is correlated with habitats containing declining populations, its actual role in amphibian declines is uncertain given the relatively low concentration in aquatic habitats.
Relyea, R.A. (2004) Fine-tuned phenotypes: Tadpole plasticity under 16 combinations of predators and competitors. Ecology 85:172-179 It is now well appreciated that most organisms can alter their phenotypes when faced with environmental variation. Decades of empirical investigations have documented hundreds of examples of phenotypic plasticity, yet most studies have focused on the presence or absence of a single environmental factor. As a result, we know little about how organisms respond to gradients of environmental factors (i.e. threshold responses versus continuous responses) nor do we understand how organisms respond to combinations of environmental variables. I examined how larval wood frogs (Rana sylvatica) altered their behavior, morphology, and growth in response to combined gradients of predation and competition. Increased predation risk induced lower activity, deeper tails, and shorter bodies which collectively caused slower growth. Increased competition caused slower growth which induced higher activity, shallower tails, and longer bodies. For both environmental gradients, the responses were frequently continuous rather than threshold responses. Moreover, predation and competition had interactive effects. Responses to predators were always larger under low competition than under high competition. Responses to competition were larger under low predation risk when predation and competition induced traits in the same direction, but larger under high predation risk when predation and competition induced traits in opposite directions. The results demonstrate that responses to phenotypically plastic traits can be fine-tuned to a wide variety of environmental combinations.
Relyea, R.A. (2004) Integrating phenotypic plasticity when death is on the line: Insights from predator-prey systems. Pp 176-194 in The Evolutionary Biology of Complex Phenotypes, Pigliucci, M., and K. Preston, Ed. Oxford University Press, Oxford, U.K. : Environmental heterogeneity is the norm of nature. As a result, many organisms have evolved the ability to alter their phenotypes to track changing environments and improve their fitness. During the past century, investigators have studied phenotypic plasticity with a primary focus on single traits. This has provided us with an excellent collection of case studies that have documented the species that possess plastic traits, the types of traits that are plastic, and the types of environments that induce the trait changes. However, it is becoming increasingly clear that we need to examine multiple traits and determine how they work together in producing an integrated organism. In animal systems, one of the most extensively studied types of reactions to the environment is predator-induced plasticity. Thus, it can serve as a good system from which to draw examples of the importance of integrating multiple plastic traits. In a review of 125 studies, more than one-third examined only one trait, and 73% examined three or fewer traits. There have been similar emphases on behavioral traits (26%), morphological traits (41%), and life historical traits (32%), but little attention to physiological traits (1%). Most studies examined only one type of trait (67%); nearly all studies examined two or fewer trait types (97%). The central question is whether we can actually learn more about predator-induced plasticity (and phenotypic plasticity in general) if we were to take a more integrated approach that incorporated more traits and more types of traits. In this chapter, I argue that while it requires more time, money, and energy to examine multiple traits, it is imperative that we do so if we wish to understand the evolution and ecology of phenotypic plasticity.
Relyea, R.A. (2003) Predator cues and pesticides: A double dose of danger for amphibians. Ecol. Appl. 13:1515-1521 Amphibians are declining globally and biologists have struggled to identify the causes. Pesticides may play a role in these declines, but pesticide concentrations in nature often are low and considered sublethal. Past research has found that the globally-common pesticide carbaryl can become more lethal under different environmental conditions including differences in temperature and competition. A recent study has found that predatory stress, a situation common for most amphibians, can make carbaryl two to four times more deadly to gray tree frogs (Hyla versicolor). To determine whether this is a general phenomenon in amphibians, I examined how carbaryl affected the survival of six amphibian species in the presence and absence of predatory stress. Higher concentrations of carbaryl caused higher mortality. In two of the six species, carbaryl became even more lethal when combined with predatory stress (up to 46 times more lethal). This suggests that apparently safe concentrations of carbaryl (and perhaps other pesticides with similar modes of action), can become more deadly to some amphibian species when combined with predator cues.
Relyea, R.A. (2003) Predators come and predators go: The reversibility of predator-induced traits. Ecology 84:1840-1848 While numerous studies have been conducted on the ecology and evolution of phenotypic plasticity, to really understand plasticity we need to expose organisms to different environments over several ontogenetic stages. In this way, we can examine whether organisms change their phenotypic strategy over ontogeny, whether there are developmental windows that constrain the development of plastic traits, and whether behavior is more reversible than morphology if the environment reverts back to its original state. I addressed these questions by examining predator-induced plasticity in gray treefrog tadpoles (Hyla versicolor). Using aquatic mesocosms, I reared tadpoles with a constant absence of predators, a constant presence of predators, and the addition or removal of predators at three different times during their larval period. Tadpoles changed their phenotypic strategy over ontogeny; early in ontogeny they responded to predators by hiding, reducing their activity, and developing relatively deep tails fins. Later in ontogeny the tadpoles no longer employed behavioral defenses but relied on a combination of greater mass, deeper tails and shorter bodies. The phenotypic changes were inducible throughout most of ontogeny, suggesting that there were few developmental windows. Activity, tail depth, and body depth were highly reversible early in ontogeny but less reversible later in ontogeny; because hiding was only used early in ontogeny, I could not assess its reversibility. This reversibility should affect not only the induced species, but will likely transmit the effects throughout the larger ecological community.
Relyea, R.A. (2003) How prey respond to combined predators: A review and an empirical test. Ecology 84:1827-1839 Studies of phenotypic plasticity frequently ask how organisms respond to a change in their environment, but most organisms do not experience single environmental changes. Therefore, we need to move to the next step and understand how organisms respond to combinations of environmental changes. Recent studies of predator-induced plasticity have addressed how prey respond to different combinations of predators. I briefly review 22 studies of combined predator effects on prey phenotypes and identify four factors that make it difficult to interpret the results of these studies: 1) uncontrolled prey consumption, 2) a low number of prey traits, 3) a low number of predator combinations, and 4) confounded predator composition and total predator density. I address these challenges in an experiment that examined how wood frog tadpoles (Rana sylvatica) altered 12 behavioral, morphological and life historical traits in response to four different caged predators (Erythemis, Belostoma, Dytiscus, and Anax). The predators were present alone at low density, alone at high density (2X), or combined into six pairwise combinations. When each predator was alone (at either low or high density), tadpoles discriminated among different predators and produced predator-specific phenotypes. The doubling of predator density rarely induced more extreme prey phenotypes. When predators were combined, the tadpoles generally developed phenotypes that were similar to those induced by the more-risky predator alone (90% of all traits examined, at either low or high density). These results suggest that tadpoles perceive the risk of combined predators as being similar to the risk of the most dangerous predator in the pair, and not as a summed or averaged predation risk. The actual risk from these predator combinations remains to be tested. This appears to be the first study to take a comprehensive approach that controls prey consumption, examines a large number of prey traits, uses a large number of predator combinations, and separate the effects of predator composition and predator density. There is a clear need for more such studies to determine whether these results can be generalized to other taxa.
Relyea, R.A., and J.T. Hoverman (2003) The impact of larval predators and competitors on the morphology and fitness of juvenile tree frogs. Oecologia 134:596-604 Studies of phenotypic plasticity typically focus on traits in single ontogenetic stages. However, plastic responses can be induced in multiple ontogenetic stages and traits induced early in ontogeny may have lasting effects. We examined how gray treefrog larvae altered their morphology in four different larval environments and whether different larval environments affected the survival, growth, development, and morphology of juvenile frogs at metamorphosis. We then reared these juveniles in terrestrial environments under high and low intraspecific competition to determine whether the initial differences in traits at metamorphosis affected subsequent survival and growth, whether the initial phenotypic differences converged over time, and whether competition in the terrestrial environment induced further phenotypic changes. Larval and juvenile environments both affected treefrog traits. Larval predators induced relatively deep tail fins and short bodies, but there was no impact on larval development. In contrast, larval competitors induced relatively short tails and long bodies, reduced larval growth, and slowed larval development. At metamorphosis, larval predators had no effect on juvenile growth or relative morphology while larval competitors produced juveniles that were smaller and possessed relatively shorter limbs and shorter bodies. After one month of terrestrial competition among the juvenile frogs, the initial differences in juvenile morphology did not converge. There were no differences in growth due to larval treatment but there were differences in survival. Individuals that experienced low competition as tadpoles experienced near perfect survival as juvenile frogs but individuals that experienced high competition as tadpoles suffered an 18% decrease in survival as juvenile frogs. There were also morphological responses to juvenile competition, but these changes appear to be due, at least in part, to allometric effects. Collectively, these results demonstrate that larval environments can have profound impacts on the traits and fitness of organisms later in ontogeny.
Skelly, D.K, K.L. Yurewicz, E.E. Werner, and R.A. Relyea (2003) Quantifying decline and distributional change in amphibians. Conserv. Biol. 17:744-751 Concern over species declines has prompted researchers to use historical data as a basis for comparison with present day information from the same sites to assess changes in presence/absence distributions. A review of the literature reveals that these resurveys typically have lasted for one or two years, and many have been based on museum records or other data relying on known historical presences. Using data on 9 amphibian species from a set of 32 ponds at the E. S. George Reserve (ESGR) in Michigan, we evaluated the importance of the duration of a resurvey, and the type of historical data used (information on historical presences and absences vs. historical presences only). We compared data we collected between 1996 and 2000 with information from the same ponds collected between 1967 and 1974. By systematically degrading the 1996 - 2000 data, we determined that a resurvey lasting one year would yield an estimated 45% decline in the number of presences, where a resurvey lasting 2 years yielded an estimate of 28% decline. By contrast, a 5-year resurvey yielded an estimate of 3% decline in the number of presences. In addition, we found that when our historical data were limited to known presences in the past, even a 5-year resurvey yielded an estimated 30% decline in the number of presences. Our results suggest that estimates of decline and distributional change can be extremely sensitive to the duration of resurvey effort and the type of historical data used. The pattern found in analyses of ESGR data is echoed in published studies where multiple year resurveys tend to yield smaller estimates of decline compared to single year resurveys. Based on our findings, we suggest that future resurveys extend for long enough to estimate the value of additional data and that geographic scales of inference be chosen based on the amount and quality of historical information.
Relyea, R.A., and K.L. Yurewicz (2002) Predicting community outcomes from pairwise interactions: Integrating density- and trait-mediated effects. Oecologia 131:569-579 Understanding how species interactions shape the structure of ecological communities based on pairwise comparisons has been a difficult undertaking for ecologists because effects in reassembled communities can be different than simple density-mediated interactions would suggest. Part of this complexity occurs because many species change their behavior and morphology with different predators and competitors and, thus, change their per-capita interaction rates (i.e. trait-mediated interactions). Our objective was to use a simple experimental community of two predators (larval dragonflies, Anax longipes, and larval salamanders, Ambystoma tigrinum), two prey (larval green frogs, Rana clamitans, and larval bullfrogs, R. catesbeiana), and a shared prey resource to determine whether we can predict interactions in a reassembled community by combining our knowledge of density- and trait-mediated interactions. We combined pairwise laboratory experiments on predation rates and predator-induced behaviors with a mesocosm experiment to examine density- and trait-mediated effects. We used a factorial combination of no predators, caged Anax (to induce anti-predator traits without changing prey density), and lethal Anax crossed with no predators, caged Ambystoma, and lethal Ambystoma. The species interactions in the reassembled community were qualitatively predictable based on the pairwise experiments. Lethal Anax preyed upon Ambystoma and green frogs while lethal Ambystoma only preyed upon green frogs. Anax also reduced the activity of the green frogs; this caused a decrease in salamander predation on green frogs, a decrease in green frog acquisition of resources, and an increase in bullfrog acquisition of resources. Ambystoma had no effect on green frog activity, no effect on resource acquisition by green frogs, and no effect on resource acquisition by bullfrogs. These results suggest that we can better understand how species interact in natural communities if we have a more detailed understanding of trait-mediated mechanisms. However, if predicting the structure of large communities requires identifying how each species alters its traits in the presence of all other species along with altering density, improving our predictive ability may be a prohibitively large undertaking.
Relyea, R.A. (2002) The many faces of predation: How induction, selection, and thinning combine to alter prey phenotypes. Ecology 83:1953-1964 Populations in nature face a number of factors that can alter their traits and subsequent performance. Predation is one factor that can have widespread effects on the mean trait value in a prey population because predators can impact prey traits through a number of processes. Predators can directly induce prey phenotypes through visual and chemical cues, predators can indirectly alter prey phenotypes by thinning the prey population (thereby reducing competition), and predators can cause selection on prey phenotypes through non-random killing. Ecologists are beginning to understand each of these three processes in isolation, but these processes act on prey phenotypes simultaneously and we lack information on the relative importance of these processes in determining the final phenotype of prey. I used a system of gray treefrog tadpoles (Hyla versicolor) and dragonfly predators (Anax longipes) to determine the separate and combined impacts of induction, thinning, and selection on the behavior, morphology, and growth of tadpoles reared in aquatic mesocosms. Using combinations of hand thinning, cues emitted from caged predators, and lethal predators, I demonstrated that the impact of lethal predators on growth was mediated primarily through thinning, the impact on morphology was primarily through induction, and the impact on behavior was affected similarly through thinning and induction. Surprisingly, while we know from numerous studies that the dragonflies kill tadpoles nonrandomly, selection did not have a significant impact on the final phenotypes of the tadpoles. This work appears to be the first study that identifies the relative magnitudes of the three predatory processes on a suite of prey phenotypes. The three processes can have opposing or supporting effects, the relative magnitudes of which likely differ among systems, illustrating why we often observe contradictory results when we examine the impact of lethal predators on prey phenotypes. Thus, it is important that we identify the mechanisms underlying the outcomes of predation rather than simply observing the outcomes and then inferring which processes are responsible.
Relyea, R.A. (2002) Costs of phenotypic plasticity. Am. Nat. 159:273-282 Phenotypically plastic organisms display alternative phenotypes in different environments. It is widely appreciated that possessing alternative phenotypes can affect fitness. However, some investigators have suggested that simply carrying the ability to be plastic also could affect fitness . Evolutionary models suggest that high costs of plasticity could constrain the evolution of optimal phenotypes. However, costs (and limits) of plasticity are primarily hypothetical. Little empirical evidence exists that increased plasticity leads to reduced growth and development, increased developmental instability, or that it limits the ability of organisms to produce more extreme phenotypes. I used half-sib families of larval wood frogs (Rana sylvatica) reared in outdoor mesocosms to examine how tadpoles altered behavioral, morphological, and life historical traits in response to larval dragonfly predators (Anax longipes). The predators induced wood frogs to have lower activity and develop relatively large tails and small bodies. As a result, wood frogs experienced reduced growth and development. I then examined whether tadpole sibships with higher plasticity experienced fitness costs (above and beyond the costs of expressing a particular phenotype) and whether they were limited in producing extreme phenotypes. Fitness effects of plasticity were widespread. Depending on the trait examined and the environment experienced, increased plasticity had either positive effects, negative effects, or no effects on tadpole mass, development, and survivorship. I found no relationship between increased plasticity and greater developmental instability. There also was no evidence that sibships with increased plasticity produced less extreme phenotypes; the most extreme trait states always were produced by the most plastic genotypes. This work suggests that costs of plasticity may be pervasive in nature and may substantially impact the evolution of optimal phenotypes in organisms that live in heterogeneous environments.
Relyea, R.A. (2002) Local population differences in phenotypic plasticity: Predator-induced changes in wood frog tadpoles. Ecol. Monogr. 72:77-93 Taxa that are divided into separate populations with low levels of interpopulation dispersal have the potential to evolve genetically-based differences in their phenotypes and the plasticity of those phenotypes. These differences can be due to random processes including genetic drift and founder effects or they can be the result of different selection pressures among populations. I investigated population-level differences in predator-induced phenotypic plasticity in eight populations of larval wood frogs (Rana sylvatica) over a small geographic scale (interpopulation distances of 0.3-8 km). Using a common-garden experiment containing predator and no-predator environments, I found population differences in behavior, morphology, and life history. These responses exhibited a habitat-related pattern; larvae from the four populations from closed-canopy ponds did not differ from each other in all of their phenotypes whereas the four populations from open-canopy ponds did differ from each other in these traits. This phenotypic matches the pattern of competitors and predators found in these two types of ponds; based on two years of pond surveys, the four closed-canopy ponds contained very similar competitor and predator assemblages while the assemblages of the four open-canopy ponds were more diverse and highly variable among open-canopy ponds. When combined with past studies, which demonstrate that predators and competitors select for alternative behavioral and morphological traits, these patterns suggest that the population differences may have arisen via natural se! lection and not via random mutation or drift. In a second experiment, I cross-transplanted two of the populations into each others' ponds to determine if the populations were locally adapted to the conditions of their native pond (using low and high competition crossed with the presence or absence of a lethal predator). The populations continued to exhibit phenotypic differences and one of the two populations tested exhibited superior growth in its native pond. This suggests that some wood frog populations are adapted to the local conditions of their natal pond and that localized selection by predation and competition may be the underlying mechanism. Collectively, these experiments indicate that taxa that are divided into discrete populations and face different predator and competitor environments can evolve different phenotypically plastic responses.
Relyea, R.A. (2002) Competitor-induced plasticity in tadpoles: consequences, cues, and connections to predator-induced plasticity. Ecol. Monogr. 72:523-540 Phenotypically plastic responses to environmental change are typically compartmentalized by the type of environmental cues that cause the induction (e.g., temperature, light), but different types of environmentally-induced responses might very well be related to each other. I used a number of experiments to document competitor-induced behavior and morphology in wood frog tadpoles (Rana sylvatica), to quantify how competitor-induced changes affected subsequent competitive ability, and to investigate the cues responsible for the competitor-induced response. Competitors induced wood frogs to increase their activity and generally develop larger bodies and smaller tails. Further, wood frogs were able to discriminate between intraspecific and interspecific competitors. Whereas behavioral responses to competitors are well documented, the widespread morphological responses are a new discovery; these responses are particularly intriguing because they are in the opposite direction of predator-induced responses in tadpoles. The competitor-induced phenotypes are not simply an allometric effect, but appear to be adaptive responses to competitors; competitor-induced wood frogs experienced higher relative growth rates than non-induced wood frogs in subsequent performance trials but past studies suggest that the competitor-induced phenotype should experience higher predation risk. When responding to competition, wood frogs were not responding to reduced food. They were able to sense changes in both the per-capita food levels and changes in density (per-unit-volume) that were independent of per-capita food level. Thus, these animals have an amazing ability to sense changes in their environments and respond in very precise ways. When we consider competitor-induced responses in light of past studies on predator-induced phenotypes in larval anurans, we see that predator-induced traits provide individuals with increased predator resistance but decreased competitive ability whereas competitor-induced traits provide individuals with increased competitive ability but decreased predator resistance. This suggests that predator- and competitor-induced plasticity have evolved an intricate link that presents a tradeoff between competitive ability and predator resistance ability. This tradeoff is common across species and makes sense in light of the environments in which wood frogs live, ranging from ponds with high densities of predators and few tadpoles competing to ponds with few predators and extremely high densities of tadpoles competing. Further, there is evidence that this type of plasticity tradeoff might be quite common in other phenotypically plastic taxa.
Relyea, R.A., and N. Mills (2001) Predator-induced stress makes the pesticide carbaryl more deadly to grey treefrog tadpoles (Hyla versicolor). Proc. Natl. Acad. Sci., USA 98:2491-2496 Global declines in amphibians likely have multiple causes including widespread pesticide use. Our knowledge of pesticide effects on amphibians is largely limited to short-term (4 d) toxicity tests conducted under highly artificial conditions to determine lethal concentrations (LC50). We found that if we used slightly longer exposure times (10-16 d), low concentrations of the pesticide carbaryl (3-4% of LC504-d) killed 10-60% of gray treefrog (Hyla versicolor) tadpoles. If predatory cues also were present, the pesticide became 2-4 times more lethal, killing 60-98% of tadpoles. Thus, under more realistic conditions of increased exposure times and predatory stress, current application rates for carbaryl can potentially devastate gray treefrog populations. Further, because predator-induced stress is ubiquitous in animals and carbaryl's mode of action is common to many pesticides, these negative impacts may be widespread in nature.
Relyea, R.A. (2001) The lasting effects of adaptive plasticity: Predator-induced tadpoles become long-legged frogs. Ecology 82:1947-1955 Changes in environmental conditions often alter the traits of individuals but we have a poor understanding of how changes in phenotypically plastic traits early in development subsequently affect traits later in development when the environments are no longer present. To address this phenomenon, one must first understand how early and late traits are related to each other and then use these relationships to interpret how different early environments affect traits expressed later in development. In this study, I examine how differences in the mass, morphology, and larval period of aquatic tadpoles (Rana sylvatica) subsequently affects the mass and morphology of terrestrial metamorphs. I found three major patterns: 1) larval mass and larval period were positively related to metamorphic mass; 2) larval period was positively related to metamorph hindlimb and forelimb size and negatively related to metamorph body width; and 3) larval body length was negatively related to metamorph forelimb size, reflecting a possible constraint on forelimbs, which completely develop within the body. I then used these correlations to interpret the connection between the morphology of tadpoles reared either in the presence or absence of caged predators. Caged predators (aeshnid dragonflies) induce tadpoles to develop deep tail fins, short bodies, low mass, and long larval periods. Metamorphs produced from larval predator environments exhibited larger hindlimbs and forelimbs and narrower bodies than metamorphs produced in predator-free larval environments. Based on the relationships developed from the correlation analysis, it appears that these differences between the two groups of metamorphs arose primarily due to the effect of predators on larval period and not due to the striking effects of the predators on tadpole morphology. By examining a wide range of both larval and metamorphic traits, we can now generate mechanistic hypotheses for the developmental pathways connecting early and late traits in organisms and also make testable predictions about how a variety of environmental changes early in development should alter traits later in development.
Relyea, R.A. (2001) The relationship between predation risk and antipredator responses in larval anurans. Ecology 82:523-540 Organisms that produce alternative, nondiscrete phenotypes in response to environmental conditions are expected to alter their phenotypes in relation to the degree of environmental change. This idea has been applied to the evolution of antipredator responses by prey, in which it has been hypothesized that prey should respond more strongly to predators that pose greater mortality risk. In a companion paper, I quantified predator-induced behavioral and morphological responses in six species of larval anurans across five different predator environments and found that these responses were prey- and predator-specific. In the present study, I addressed whether the responses were related to the level of predation risk posed by each of the predators. Within each prey species, I found that different predators posed different levels of predation risk; within each predator species, different prey species experienced different levels of risk. The differences in predation risk could be understood mechanistically after I quantified differences among predators in their ability to capture, handle, and consume prey and differences among prey in behavior and morphology. Using multivariate analyses, I found that predation risk had no significant effect on how a given prey responds to predators, although there were significant univariate behavioral effects; higher predation risk was related to greater decreases in activity and greater spatial avoidance. I also examined the relationship between risk and response across the six prey species within a predator treatment and found that higher predation risk across species leads to greater decreases in activity in the presence of Umbra and greater increases in tail depth in the presence of Anax. Thus, while previous studies have found relationships between predation risk and prey response when focusing on relatively few species, few predators, and a single trait, this more powerful test using 30 predator-prey combinations and nine traits suggests that the relationship is not well supported. This finding arises from the fact that larval anurans, as well as many other taxa, exhibit predator- and prey-specific behavioral and morphological changes in response to predator- and prey-specific risk.
Relyea, R.A. (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:541-554 Many organisms can adjust to a changing environment by developing alternative phenotypes that improve their fitness. Our understanding of phenotypic plasticity is largely based upon observations from single species responding to two different environments and measuring a single plastic trait. In this study, I examine predator-induced phenotypic plasticity in tadpoles by observing how six species of larval anurans respond to five different predator environments in 11 different traits (seven morphological traits, two behavioral traits, growth, and development). The results demonstrated that behavioral and morphological plasticity may be ubiquitous in larval anurans. The six prey species exhibited different responses to the same predator species and each prey exhibited different responses to different predator species. This suggests that responses to a particular predator may not serve as general defense against all predators; rather, prey express predator-specific suites of responses. I also compared relative differences in plasticity among species and among traits. In contrast to earlier findings using only two predator environments, I found that different anurans possess similar degrees of plasticity for most of their traits when reared in a large number of environments. In addition, behavioral traits were always more plastic than morphological traits. Finally, I examined trait integration to address whether there were apparent tradeoffs among traits and limits imposed by the abiotic environment. Trait integration, or the degree of correlated responses among traits across predator environments within a prey species, was very low. This further suggests that the suites of responses are predator-specific and may be under independent directions of selection in different predator environments. Trait correlations across prey species indicated that there is an apparent tradeoff between tail fin depth and body size. This relationship is supported by selection studies within prey species. Relating the responses to the pond permanence habitat gradient over which the amphibians exist, I found that species that can inhabit more temporary ponds possess higher general activity levels, shallower tail fins, and larger bodies; these traits are known to result in more rapid growth. In a companion paper (Relyea, in review), I quantified the predation risk of the 30 predator-prey combinations and examined the relationships between prey response and predation risk.
Relyea, R.A., R.K. Lawrence, and S. Demarais (2000) Home range of desert mule deer: testing the body-size and habitat productivity hypotheses. J. Wildlife Manage. 64:146-153 The body-size hypothesis of home range predicts that, given constant home range productivity, larger animals with higher absolute metabolic requirements use larger home ranges to meet their metabolic needs. This relationship is well supported across a wide range of mammals and often has been invoked to explain differences in home range size between sexes that differ in body size. However, the body-size hypothesis has rarely been tested within a species. A corollary to this hypothesis states that for a given mass, animals in areas of low habitat productivity should have home ranges larger than those in productive habitat. To test these 2 hypotheses, we radiomonitored desert mule deer (Odocoileus hemionus crooki) for 2 years in southwest Texas to determine the effects of sex, mass and habitat productivity on annual home range size. Although male mule deer had more massive bodies than females (P < 0.001) and used consistently larger annual home ranges than females (P < 0.01), we found little support for the body-size hypothesis. In contrast, we found sex-specific support for the habitat-productivity hypothesis. Male and female mule deer had home ranges of similar size in areas of high habitat productivity but males used larger home ranges than females when habitat productivity was low. Our results suggest that differential sex responses to productivity may be the mechanism underlying the frequent observation that male cervids have larger home ranges than female cervids.
Relyea, R.A. (2000) Trait-mediated indirect effects in larval anurans: Reversing competitive outcomes with the threat of predation. Ecology 81:2278-2289 Ecologists recently have been focusing on the role that trait-mediated indirect effects can have on community structure and composition. To date, this work has primarily focused on the effects of predator-induced behavioral plasticity on communities. However, predator-induced morphological plasticity, which has been documented in many taxa, might also lead to trait-mediated indirect effects. Here, I examined how predators altered the behavior and morphology of larval wood frogs (Rana sylvatica) and leopard frogs (R. pipiens) and how these phenotypic changes altered the outcome of competition between the two species. Competition in the absence of caged predators was asymmetric; when reared separately, leopard frogs grew more than wood frogs but when competing (without predators), wood frogs grew faster than leopard frogs. The presence of caged predators reversed the outcome of competition between the two anuran prey. In the presence of larval dragonflies (Anax spp.) or caged mudminnows (Umbra limi), leopard frogs grew faster than wood frogs while total tadpole biomass production remained unchanged. Thus, there was a predator-mediated indirect effect. Because predators alter both the behavior and morphology of larval anurans and both of these traits are known to affect resource consumption and growth, both are potential mechanisms to explain the change in competitive outcome. Changes in behavior were not related to changes in growth but changes in morphology (specifically mouth width and tail length) were related to changes in growth. When competitors were added (without predators) wood frogs increased their mouth width by 10% and their tail length by 3% while leopard frogs increased their mouth width by 5% and did not change their tail length. The greater increase in mouth width for wood frogs should increase their forage intake since tadpoles feed by scraping periphyton; the importance of a 3% longer tail in competitive ability is unknown. The presence of the predator threat (via chemical cues from the caged predators) reduced both the mouth width and tail length in the two prey species to pre-competition levels. This response corresponded with the reduced competitive ability of the wood frogs. This work demonstrates that both competitors and predators can alter prey morphology and suggests that changes in morphology can cause trait-mediated indirect effects.
Relyea, R.A., and E.E. Werner (2000) Morphological plasticity of four larval anurans distributed along an environmental gradient. Copeia 2000:178-190 We investigated morphological plasticity to the presence of predators in the tadpoles of four ranid frog species distributed along a pond hydroperiod gradient in southeast Michigan. We first reared all four species (wood frog, Rana sylvatica; leopard frog R. pipiens; green frog, R. clamitans; and bullfrog, R. catesbeiana) under identical laboratory conditions in the presence and absence of caged larval dragonflies (Anax spp.). We then reared wood frog and leopard frog in outdoor mesocosms to examine the predator-induced responses during ontogeny. Finally, we reared leopard frog with predators fed either leopard frog or wood frog larvae to determine whether prey responses depended upon predators consuming conspecific prey. All four ranids exhibited some degree of morphological change in the presence of Anax; these differences were species-specific and fairly robust to different experimental conditions. The responses over ontogeny indicated that the changes were direct responses to the predator's presence and not an indirect result of the predator slowing anuran growth or development. Finally, larval leopard frog responded similarly to predators feeding on conspecifics and congenerics. Taken together, these results suggest that morphological responses to predators may be relatively common in larval anurans. Further, because many of the responses are known to be adaptive antipredator strategies, predator-induced morphological plasticity has important evolutionary and ecological implications.
Relyea, R.A., and E.E. Werner (1999) Quantifying the relation between predator-induced behavior and growth performance in larval anurans. Ecology 80:2117-2124 Because the nature and magnitude of species interactions are functions of the traits that species possess, understanding how individual traits affect performance is important to our understanding of community structure. To examine the relation between species traits and performance, we first assessed behavioral responses of two larval anurans to three predator species in the laboratory. We then correlated these responses with growth performance of the two anurans when they competed in the field. In the laboratory experiment, larval bullfrogs (Rana catesbeiana) and green frogs (R. clamitans) exhibited no reduction in activity or spatial avoidance to bluegill sunfish (Lepomis macrochirus), moderate reductions in activity and spatial avoidance of mudminnows (Umbra limi), and large reductions in activity and spatial avoidance of larval dragonflies (Anax spp.). In the field experiment, these behavioral responses were directly related to corresponding reductions in growth of the anuran larvae. Thus, for both species, changes in growth in the field could be correlated to the behavioral responses observed in the laboratory. Further, proportional changes in behavior in the presence of the different predators appeared to be related to changes in competitive relations in the field.
Van Buskirk, J., and R.A. Relyea (1998) Natural selection for phenotypic plasticity: Predator-induced morphological responses in tadpoles. Biol. J. Linn. Soc. 65:301-328 The hypothesis that phenotypic plasticity is an adaptation to environmental variation rests on the two assumptions that plasticity improves the performance of individuals that possess it, and that it evolved in response to selection imposed in heterogeneous environments. The first assumption has been upheld by studies showing the beneficial nature of plasticity. The second assumption is difficult to test since it requires knowing about selection acting in the past. However, it can be tested in its general form, by asking whether natural selection currently acts to maintain phenotypic plasticity. We adopted this approach in a study of plastic morphological traits in larvae of the wood frog, Rana sylvatica. First we reared tadpoles in artificial ponds for 18 days, in either the presence or absence of Anax dragonfly larvae (confined within cages to prevent them from killing the tadpoles). These conditioning treatments produced dramatic differences in size and shape: tadpoles from ponds with predators were smaller and had relatively short bodies and deep tail fins. We estimated selection by Anax on the two kinds of tadpoles by testing for non-random mortality in overnight predation trials. Dragonflies imposed strong selection by preferentially killing individuals with relatively large bodies, shallow and short tail fins, and narrow tail muscles. The same traits that exhibited the strongest plasticity were under the strongest selection, except that tail muscle width exhibited no plasticity but experienced strong increasing selection. A laboratory competition experiment, testing for selection in the absence of predators, showed that tadpoles with deep tail fins grew relatively slowly. In the cattle tanks, where there were also no free predators, the predator-induced phenotype survived more poorly and developed slowly, but this cost was apparently not associated with particular morphological traits. These results show that selection is currently promoting morphological plasticity in R. sylvatica, and support the hypothesis that plasticity represents an adaptation to variable predator environments.
Relyea, R.A., and S. Demarais (1994) Activity monitoring in mule deer: Assessing telemetry accuracy. Wildlife Soc. B. 22:656-661 We evaluated a new, automated, telemetry system for monitoring activity in desert mule deer. The system quantified the amount of time between pulses using a perpendicularly-oriented activity sensor. The increased automation brought increased monitoring efficiency, but the system could not accurately discriminate specific activities (bedded, standing, walking, and feeding). At a lower resolution, bedded activities could be discriminated from nonbedded activities 73-77% of the time and less active behaviors (bedded and standing) could be discriminated from more active behaviors (walking and feeding) 74-81% of the time using 1-, 2- , 3-, 4-, and 5-minute sample intervals. We recommend incorporating the automation technology with more accurate, parallel-oriented, tip-switch collars. Relyea, R.A., and S. Demarais (1994) Desert mule deer activity during the breeding season. J. Mammal. 75:940-949 Motion-sensitive radio collars and an automated telemetry system were used to quantify relative activity levels of desert mule deer (Odocoileus hemionus crooki) in southwest Texas during the 1990-1991 breeding season. Activity data were divided into prerut, peak rut, and postrut periods and analyzed for gender and period effects. Gender did not affect relative activity level and activity increased from prerut to peak rut to postrut. Of 4 possible explanations for the increased activity from prerut to postrut (day length, mate searching, increased feeding, and shifted breeding season), mate searching was supported best by the results. |
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