Effects of behavioral and morphological plasticity on risk of predation in a Neotropical tadpole

Predator-induced phenotypic plasticity is widespread among aquatic animals, however the relative contributions of behavioral and morphological shifts to reducing risk of predation remain uncertain. We tested the phenotypic plasticity of a Neotropical tadpole (Rana palmipes) in response to chemical cues from predatory Belostoma water bugs, and how phenotype affects risk of predation. Behavior, morphology, and pigmentation all were plastic, resulting in a predator-induced phenotype with lower activity, deeper tail fin and muscle, and darker pigmentation. Tadpoles in the predator cue treatment also grew more rapidly, possibly as a result of the nutrient subsidy from feeding the caged predator. For comparison to phenotypes induced in the experiment, we quantified the phenotype of tadpoles from a natural pool. Wild-caught tadpoles did not match either experimentally induced phenotype; their morphology was more similar to that produced in the control treatment, but their low swimming activity was similar to that induced by predator cues. Exposure of tadpoles from both experimental treatments and the natural pool to a free-ranging predator confirmed that predator-induced phenotypic plasticity reduces risk of predation. Risk of predation was comparable among wild-caught and predator-induced tadpoles, indicating that behavioral shifts can substantially alleviate risk in tadpoles that lack the typical suite of predator-induced morphological traits. The morphology observed in wild-caught tadpoles is associated with rapid growth and high competition in other tadpole species, suggesting that tadpoles may profitably combine a morphology suited to competition for food with behaviors that minimize risk of predation.     

Costs and limits of phenotypic plasticity: Tests with predator-induced morphology and life history in a freshwater snail

Potential constraints on the evolution of phenotypic plasticity were tested using data from a previous study on predator-induced morphology and life history in the freshwater snail Physa heterostropha. The benefit of plasticity can be reduced if facultative development is associated with energetic costs, developmental instability, or an impaired developmental range. I examined plasticity in two traits for 29 families of P. heterostropha to see if it was associated with growth rate or fecundity, within-family phenotypic variance, or the potential to produce extreme phenotypes. Support was found for only one of the potential constraints. There was a strong negative selection gradient for growth rate associated with plasticity in shell shape (β = ?0.3, P < 0.0001). This result was attributed to a genetic correlation between morphological plasticity and an antipredator behavior that restricts feeding. Thus, reduced growth associated with morphological plasticity may have had unmeasured fitness benefits. The growth reduction, therefore, is equivocal as a cost of plasticity. Using different fitness components (e.g., survival, fecundity, growth) to seek constraints on plasticity will yield different results in selection gradient analyses. Procedural and conceptual issues related to tests for costs and limits of plasticity are discussed, such as whether constraints on plasticity will be evolutionarily ephemeral and difficult to detect in nature.     

Clutch identity and predator-induced hatching affect behavior and development in a leaf-breeding treefrog

For species with complex life cycles, transitions between life stages result in niche shifts that are often associated with evolutionary trade-offs. When conditions across life stages are unpredictable, plasticity in niche shift timing may be adaptive; however, factors associated with clutch identity (e.g., genetic or maternal) may influence the effects of such plasticity. The red-eyed treefrog (Agalychnis callidryas) is an ideal organism for investigating the effects of genetics and life stage switch point timing because embryos exhibit adaptive phenotypic plasticity in hatching time. In this study, we evaluated the effects of experimentally manipulated hatching time and clutch identity on antipredator behavior of tadpoles and on developmental traits of metamorphs, including larval period, mass, SVL, and jumping ability. We found that in the presence of dragonfly nymph predator cues at 21 days post-oviposition, tadpoles reduced both their activity level and height in the water column. Furthermore, early-hatched tadpoles were less active than late-hatched tadpoles of the same age. This difference in behavior patterns of early- and late-hatched tadpoles may represent an adaptive response due to a longer period of susceptibility to odonate predators for early-hatched tadpoles, or it may be a carry-over effect mediated by early exposure to an environmental stressor (i.e., induction of early hatching). We also found that hatching time affected both behavioral traits and developmental traits, but its effect on developmental traits varied significantly among clutches. This study shows that a single early-life event may influence a suite of factors during subsequent life stages and that some of these effects appear to be dependent on clutch identity. This interaction may represent an evolutionary response to a complex life cycle and unpredictable environments, regardless of whether the clutch differences are due to additive genetic variance or maternal effects.     

Phenotypic lability and the evolution of predator-induced plasticity in tadpoles

The hypothesis that predator-induced defenses in anuran larvae are maintained by divergent selection across multiple predation environments has not been fully supported by empirical results. One reason may be that traits that respond slowly to environmental variation experience a fitness cost not incorporated in the standard adaptive model, due to a time lag between detecting the state of the environment and expressing the phenotypic response. I measured the rate at which behavior and morphology of Rana temporaria tadpoles change when confronted with a switch in the predation environment at two points in development. Hatchling tadpoles that had been exposed during the egg stage to Aeshna dragonfly larvae were not phenotypically different from those exposed as eggs to predator-free conditions, and both responded similarly to post-hatching predator treatments. When 25-day-old tadpoles from treatments with and without dragonflies were subjected to a switch in the environment, their activity budgets reversed completely within 24-36 h, and their body and tail shape began changing significantly within 4 days. The behavioral response was conservative: Tadpoles switched from high-risk to predator-free treatments were slower to adjust their activity. The study confirmed that behavioral traits are relatively labile and exhibit strong plasticity, but it did not reveal such a pattern at the level of individual traits: Morphological traits that developed slowly did not show the least plasticity. Thus, I found that differences in lability of traits were useful for predicting the magnitude of plasticity only for fundamentally different kinds of characters.     

The ecological role of chemical stimuli for the zooplankton: predator-induced morphology in Daphnia

Summary Numerous adaptive predator-induced responses occurred when eight clones representing seven Daphnia (Crustacea: Cladocera) species were tested against three common predators: fourth instar larval phantom midge Chaoborus americanus, adult backswimmer Notonecta undulata, and small sunfish Lepomis macrochirus. The predators were confined within small mesh bags, suggesting that the signal for induction is chemical. The induced responses included longer tail spines, longer heads, smaller bodies, increased egg clutches, and decreased lipid reserves. Each Daphnia species responded to each of the three predators in a unique manner. Induced responses in the above characters showed no significant association. The induced morphological changes are generally consistent with current theories of what is an adaptive response for the various sizes of Daphnia exposed to tactile and visual predators. The abundance of induced responses in these experiments suggests that predator-induced responses are a widespread and ecologically important phenomenon of the freshwater zooplankton.     

Temperature- and predator-induced phenotypic plasticity in Bosmina cornuta and B. pellucida (Crustacea: Cladocera)

SUMMARY 1. Clones of Bosmina cornuta and B. pellucida (B. longirostris species complex) were derived from samples collected from Scheuermühlenteich and Lake Windsborn(westernGermany). Experimental temperature change (to 10 °C and 20 °C) and exposure to Acanthocyclops vernalis copepods (12 L^?1) significantly altered external morphology in laboratory cultures of the two species. Morphological traits were derived from eight log₁₀‐transformed and standardised morphometric distances by factorial analysis: factor 1 represented body size, factor 2, size of appendages and factor 3, the head size. 2. Acclimation of clones to cold water (10 °C, >14 days) led to an increase in body, antennule and mucrone size in B. cornuta and B. pellucida. Moreover, at 10 °C, B. cornuta cultures usually collapsed within a few weeks. Compared to the trials at 10 °C, acclimation to 20 °C (the two species) and to 15 °C (B. pellucida only) left the size of body appendages unchanged. Individuals were unequivocally assigned to each species by discriminant functions. Conspecific individuals that were acclimated to different temperatures between 10 and 20 °C also differed in external morphology, but discriminant analysis yielded misclassification rates of 5.3–23.3%. 3. Morphological response to the presence of copepod predators was weaker than that caused by temperature change. Long‐term exposure of clones to copepod predators induced a significant increase in size of appendages in the two species but left body size unaffected. Again, species identification by discriminant functions could be made without any error, whereas conspecific controls and experimentals were misclassified at rates between 19.4 and 29.5%. 4. It is suggested that temperature is the main proximal cue for Bosmina cyclomorphosis. The distinct response to temperature of B. pellucida and B. cornuta may also account for seasonal differences in abundance observed in field.     

Adaptive plasticity in predator-induced defenses in a common freshwater snail: altered selection and mode of predation due to prey phenotype

Studies of putatively adaptive plasticity, such as inducible defenses, frequently explore the fitness consequences of expressing alternative phenotypes in alternative environments, but few studies examine how and why the pattern of selection changes in relation to trait induction. We induced snails in the presence/absence of nonlethal predatory crayfish, exposed both phenotypes (alone and combined) to selection by lethal crayfish, and quantified linear and nonlinear selection differentials. Crayfish induced an increase in mass, shell thickness, and absolute (but not relative) shell dimensions. Crayfish predation on uninduced snails was rapid, accomplished via shell-crushing and revealed strong selection for increased size (i.e., mass and shell dimensions). Conversely, crayfish predation on predator-induced snails was slower, often accomplished using an alternative mode of predation (shell-crushing 70% of the time, but shell-extraction 30% of the time), and revealed selection for wide apertures and thick shells. Crayfish selection on uninduced snails in the presence of predator-induced snails was stronger than predation on uninduced snails alone demonstrating that selection can be frequency dependent. Therefore, predator-induced changes in size and shell thickness appear to be adaptive and, along with reciprocal adjustments in the mode of predation, result in altered patterns of selection.     

Initial versus longer‐term effects of tadpole declines on algae in a Neotropical stream

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Agricultural intensification alters bat assemblage composition and abundance in a dynamic Neotropical landscape

The recent trend of agricultural intensification in tropical landscapes poses a new threat to biodiversity conservation. Conversion of previously heterogeneous agricultural landscapes to intensive plantation agriculture simplifies and homogenizes the landscape, reducing availability, and connectivity of natural habitat for native species. To assess the impact of agricultural intensification on bats, we characterized the bat assemblage in the Sarapiquí region of Costa Rica, where heterogeneous land uses are being converted to intensive, large‐scale pineapple plantations. In 2012 and 2013, we sampled bats in 20 remnant forest patches surrounded by varying proportions of pasture, mature forest, and pineapple and captured 1821 individual bats representing 39 species. We used ordination analyses to evaluate changes in species composition, where pineapple is the main component of the agricultural matrix. We identified landscape metrics specifically correlated with pineapple and used multiple linear regression to test their effects on bat species richness, diversity, and guild‐specific relative abundance. Results suggest pineapple expansion is driving changes in assemblage composition in remnant forest patches, resulting in new assemblages with higher proportions of frugivorous bats and lower proportions of insectivorous bats than in continuous mature forests. In addition, while pineapple does not diminish total bat species richness and diversity, the reduced forest cover and increased distance between forest patches in pineapple plantations has a significant negative impact on the relative abundance of insectivores. We also identify a potential threshold effect whereby patches surrounded by more than 50 percent forest can retain assemblage composition similar to that found in continuous mature forest.     

Phenotypic plasticity and local adaptation favor range expansion of a Neotropical palm

One of the most intriguing questions in plant ecology is which evolutionary strategy allows widely distributed species to increase their ecological range and grow in changing environmental conditions. Phenotypic plasticity and local adaptations are major processes governing species range margins, but little is known about their relative contribution for tree species distribution in tropical forest regions. We investigated the relative role of phenotypic plasticity and local adaptation in the ecological distribution of the widespread palm Euterpe edulis in the Brazilian Atlantic Forest. Genetic sampling and experiments were performed in old‐growth remnants of two forest types with higher (Seasonal Semideciduous Forests vs. Submontane Rainforest) and lower biogeographic association and environmental similarities (Submontane Rainforest vs. Restinga Forest). We first assessed the molecular genetic differentiation among populations, focusing on the group of loci potentially under selection in each forest, using single‐nucleotide polymorphism (SNPs) outliers. Further, we looked for potential adaptive divergence among populations in a common garden experiment and in reciprocal transplants for two plant development phases: seedling establishment and sapling growth. Analysis with outlier loci indicated that all individuals from the Semideciduous Forest formed a single group, while another group was formed by overlapping individuals from Submontane Rainforest and Restinga Forest. Molecular differentiation was corroborated by reciprocal transplants, which yielded strong evidence of local adaptations for seedling establishment in the biogeographically divergent Rainforest and Semideciduous Forest, but not for Restinga Forest and Submontane Rainforest. Phenotypic plasticity for palm seedling establishment favors range expansion to biogeographically related or recently colonized forest types, while persistence in the newly colonized ecosystem may be favored by local adaptations if climatic conditions diverge over time, reducing gene flow between populations. SNPs obtained by next‐generation sequencing can help exploring adaptive genetic variation in tropical trees, which impose several challenges to the use of reciprocal transplants.     

Associated evolution of fruit size,fruit colour and spines in Neotropical palms

Understanding how ecological interactions have shaped the evolutionary dynamics of species traits remains a challenge in evolutionary ecology. Combining trait evolution models and phylogenies, we analysed the evolution of characters associated with seed dispersal (fruit size and colour) and herbivory (spines) in Neotropical palms to infer the role of these opposing animal–plant interactions in driving evolutionary patterns. We found that the evolution of fruit colour and fruit size was associated in Neotropical palms, supporting the adaptive interpretation of seed‐dispersal syndromes and highlighting the role of frugivores in shaping plant evolution. Furthermore, we revealed a positive association between fruit size and the presence of spines on palm leaves, bracteas and stems. We hypothesize that interactions between palms and large‐bodied frugivores/herbivores may explain the evolutionary relationship between fruit size and spines. Large‐bodied frugivores, such as extinct megafauna, besides consuming the fruits and dispersing large seeds, may also have consumed the leaves or damaged the plants, thus simultaneously favouring the evolution of large fruits and defensive structures. Our findings show how current trait patterns can be understood as the result of the interplay between antagonistic and mutualistic interactions that have happened throughout the evolutionary history of a clade.     

Background noise from a natural chorus alters female discrimination of male calls in a Neotropical frog

Many animals communicate in environments with high levels of background noise. Although it is a fundamental prediction of signal detection theory that noise should reduce both detection and discrimination of signals, little is known about these effects in animal communication. Female treefrogs, Hyla ebraccata, in Costa Rica choose mates in large noisy multispecies choruses. We tested gravid females for preferences between computer-synthesized calls with carrier frequencies of 3240 and 2960 Hz (values near the mode and the fifth percentile of the population, respectively) in four levels of background noise from a natural chorus. In the absence of noise (signal/noise ratio >25 dB), females preferred the lower frequency. With moderate signal/noise ratios (6 and 9 dB), they did not discriminate between these frequencies. With low signal/noise ratios (3 dB), females preferred the frequency near the mode for the population. Similar experiments had previously demonstrated that females can detect the presence of a male's calls with signal/noise ratios of 3 dB or greater. Thus moderate levels of natural background sound reduced a female's ability to discriminate between males' calls even when she could detect them. In high levels of background sound, females abandoned discrimination for low-frequency calls and reverted to the task of detecting signals with modal properties for the population. These results justify recent theoretical analyses of the importance of receivers' errors in the evolution of communication.     

Body size,but not age-at-maturation or context,affects the expression of predator-induced behavioural plasticity in female green swordtails (Xiphophorus hellerii)

Behavioural plasticity is a form of reversible phenotypic plasticity in which a genotype can express different behavioural phenotypes under different environmental conditions. Though an interest in among-individual differences in behavioural plasticity has flourished in recent decades, few studies have considered the effects of intrinsic factors, such as life-history or morphological traits, in tandem with extrinsic factors, such as presence of conspecifics in different social contexts, on predator-induced behavioural plasticity. Here, we present a study conducted with female green swordtail fishes, Xiphophorus hellerii, designed to assess the effects of age-at-maturation and body size on the expression of predator-induced behavioural plasticity in two social contexts: (a) female-only (two females) and (b) female-and-male (two females and a male). We further examined the extent to which individual expression of behavioural plasticity is consistent across these two social contexts. We found that in the presence of a predator, focal females were more timid in response to the stimulus and more tolerant of the non-focal female, and small females expressed this change from bold/less tolerant to timid/more tolerant to a greater degree than large females, regardless of age-at-maturation. However, individuals were not consistent in the degree or direction of plasticity expressed in the behaviours of interest between the female-only and the female-and-male context. Here, we show that within- and among-individual differences in behavioural expression are common but inconsistent. How intrinsic and extrinsic factors independently or together drive expression of plasticity in antipredator and agonistic behaviours is varied and warrants further study.     

Tadpole transport logistics in a Neotropical poison frog: indications for strategic planning and adaptive plasticity in anuran parental care

Introduction

Individuals should aim to adjust their parental behaviours in order to maximize the success of their offspring but minimize associated costs. Plasticity in parental care is well documented from various bird, mammal and fish species, whereas amphibians were traditionally assumed as being highly instinct-bound. Therefore, little is known about ‘higher’ cognitive abilities of amphibians, such as strategic planning and behavioural flexibility. Dendrobatid frogs have evolved a remarkable diversity of parental behaviours. The most noticeable of these behaviours is tadpole transport, which is obligatory in almost all species. Nonetheless, there is limited knowledge about spatial and temporal patterns of tadpole transport and the possible existence of behavioural plasticity on the individual level. In this study, we investigated correlates of tadpole transport behaviour in a natural population of the dendrobatid frog Allobates femoralis during five years.

Results

Tadpole transport was predominantly observed during morning hours. Although tadpoles were carried almost exclusively by males (N?=?119), we also observed ten females performing this task. The parentage analysis revealed that in all cases females transported their own offspring. In contrast, four tadpole-carrying males were not the genetic fathers of the larvae they were transporting. The average clutch size of 20 eggs and our observation of an average of 8 tadpoles on the back of transporting individuals indicate that frogs do not carry entire clutches at once, and/or that they distribute their larvae across several water bodies. Contrary to the predictions from a hypothetical random search for deposition sites, the number of transported tadpoles was higher in males that travelled over longer distances.

Conclusions

Our results suggest a strong selective pressure on males to shift the time invested in tadpole transport to periods of low intra-specific competition. The number of tadpoles on the back of the males significantly correlated with displacement distance from the respective home territories, indicating a strategic non-random tadpole transport rather than random search for suitable tadpole deposition sites during tadpole transport. The observation of females who occasionally transported larvae supports the prevalence of adaptive plasticity in parental behaviours even in a species with a rather low level of parental care.

     

Antisense expression of a cell wall-associated protein kinase, WAK4, inhibits cell elongation and alters morphology

The Arabidopsis cell wall-associated receptor-like kinase (WAK) gene family contains five highly related members whose products are suited for exchanging signals between the intracellular and extracellular compartments. WAK members are expressed in specific organs and regulated differentially by various biotic and abiotic factors. To gain further insight into how WAKs function during development, we used a glucocorticoid-inducible system to express ectopically the WAK4 antisense gene. The induced expression of the WAK4 antisense gene resulted in a significant decrease of WAK proteins. Ninety-six hours after the induction of WAK4 antisense expression, WAK proteins became undetectable. Cell elongation was impaired, and lateral root development was blocked. The level of WAK protein could be controlled by the concentration of the applied inducer, dexamethasone, and was correlated with the severity of the cell elongation inhibition phenotype. These results suggest that the WAKs serve a vital role in cell elongation and are required for plant development.     

The heritable basis and cost of colour plasticity in coastrange sculpins

Both genetic and plastic traits contribute to adaptation in novel environments. Phenotypic plasticity can facilitate adaptation by allowing for existence in a wider range of conditions and a faster response to environmental change than gene‐based selection. Coastrange sculpins (Cottus aleuticus) colonize new and variable streams arising in the wake of receding glaciers in south‐east Alaska, and substrate‐matching plasticity may enhance colonization success by reducing detection by visual predators. As part of a long‐term study of the fitness consequences of colour plasticity and its capacity to respond to both positive and negative selection, we investigated whether it is heritable and costly. We raised full‐sib broods of sculpins in the laboratory: one half of each brood was raised in white containers, the other half in black. After 4 months, we digitally analysed their colour and found significant but weak heritability in both baseline colour and colour plasticity. To investigate the cost of colour plasticity, we compared the growth and mortality rates of juvenile sculpins reared under constant substrate colours to those reared on substrates that changed colour frequently, and compared growth rates among sculpin that differed in their colour change ability. We found evidence of small costs of plasticity, consistent with other studies of natural populations. Evidence of heritable genetic variation for plasticity and small costs to its maintenance and expression contributes to explanations of how plasticity is variable and persistent among wild populations and underscores its ability to respond both positively and negatively to selection in variable habitats.