When the optimal phenotype differs among environments, adaptive phenotypic plasticity can evolve unless constraints impede such evolution. Costs and limits of plasticity have been proposed as important constraints on the evolution of plasticity, yet confusion exists over their distinction. We attempt to clarify these concepts by reviewing their categorization and measurement, highlighting how costs and limits are defined in different currencies (and may describe the same phenomenon). Conclusions from studies that measure the costs of plasticity have been equivocal, but we caution that these conclusions may be premature owing to a potentially common correlation between environment-specific trait values and the magnitude of trait plasticities (i.e. multi-collinearity) that results in imprecise and/or biased estimates of the costs. Meanwhile, our understanding of the limits of plasticity, and how they may be underlain by the costs of plasticity, is still in its infancy. Based on our re-evaluation of these constraints, we discuss areas for future research.
Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity's key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.
Pesticides constitute a major anthropogenic addition to natural communities. In aquatic communities, a great majority of pesticide impacts are determined from singlespecies experiments conducted under laboratory conditions. Although 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, whereas 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 and 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 nontarget organisms are examined under ecologically relevant conditions.
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 nontarget species that are of conservation concern. Keywords Biodiversity, density-mediated indirect effects, ecosystem function, fungicide, herbicide, insecticide, trait-mediated indirect effects.Ecology Letters (2006) 9: 1157-1171 I N T R O D U C T I O NThe fields of ecology and toxicology have largely evolved as separate disciplines over the past century with unique journals, unique tools and a distinct jargon that has reinforced an allopatric evolution of ideas. While ecologists have focused on how biotic and abiotic factors affect species distribution and species interactions, toxicologists have traditionally focused on single-species toxicity tests. There is, however, the growing field of ecotoxicology, a name that naturally implies a hybrid of ideas and approaches from ecology and toxicology. Given that the number of ecotoxicological studies has experienced tremendous growth in the past decade, it is an excellent time to evaluate what we have learned. In this essay, we evaluate the study of ecotoxicology in freshwater systems, an arena that has received a great deal of research focus. In doing so, we examine how one can use general ecological theory to integrate ecology and ecotoxicology to better understand and conserve the ecology of aquatic systems.
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 LC50 4-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.
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 vs. 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.
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