Treefrog Dendropsophus Ebraccatus Research Articles

Correction to: Effects of multiple-speaker playbacks on aggressive calling behavior in the treefrog Dendropsophus ebraccatus

Correction to: Effects of multiple-speaker playbacks on aggressive calling behavior in the treefrog Dendropsophus ebraccatus

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

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

Patterns of variability are consistent across signal types in the treefrogDendropsophus ebraccatus

Animal signal characteristics vary at multiple levels, and this variation can be related to the selective forces acting on signal structure. However, the effectiveness of selection acting on any one signal type may depend on selective forces acting on the same characteristics in other signal types, particularly if the signals share a common physical production mechanism. In anurans, signal variability has been related to the potential for various forms of selection by female choice on the characteristics of male advertisement calls. The significance of variability in the characteristics of another vocalization type, the aggressive call, is less well understood. In the present stiudy, within- and between-male variability was measured in several characteristics of both advertisement and aggressive calls in the treefrog Dendropsophus ebraccatus. Many characteristics of both call types were repeatable within males. Fine-temporal and spectral characteristics generally had low variation within males, whereas gross-temporal characteristics were more variable. Unexpectedly, there were strong correlations between both measures of variability and mean values of the call characteristics of advertisement and aggressive calls. Thus, despite potentially conflicting selection pressures acting on advertisement and aggressive calls, the characteristics of individuals' calls were consistent across these two signal types. The potential forces responsible for consistency across call types are discussed, including morphological constraints and behavioural syndromes that act across different signalling contexts. In general, it is argued that measurements of variability made across multiple signal types, as in the present study, can provide important insights into the evolution of signal structure in organisms with complex signal repertoires. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 131–145.

A Treefrog with Reproductive Mode Plasticity Reveals a Changing Balance of Selection for Nonaquatic Egg Laying

Nonaquatic reproduction has evolved repeatedly, but the factors that select for laying eggs on land are not well understood. The treefrog Dendropsophus ebraccatus has plasticity in its reproductive mode, laying eggs that successfully develop in or out of water. This permits the first experimental comparison of the selective agents that shape adult oviposition behavior and embryo developmental capacity. I quantified the sources and strengths of arboreal and aquatic egg mortality and how mortality varies with weather patterns, and I assessed 39 years of daily rainfall patterns to infer historic levels of egg mortality and effects of climate change on the selective balance between aquatic and nonaquatic egg deposition. Aquatic predators and desiccation were the strongest selective agents in water and air, respectively. Egg mortality varied with weather such that aquatic oviposition was advantageous when rainfall was low but laying eggs out of water increased survival when rainfall was high. Additionally, I found that since 1972 there have been significant changes in the rainfall patterns in central Panama, and this has altered the selective landscape acting on egg-laying behavior. This work provides insight into the evolution and maintenance of adaptive phenotypic plasticity as well as historic and current selection on reproduction.

Call timing is determined by response call type, but not by stimulus properties, in the treefrog Dendropsophus ebraccatus

A common form of signal competition in acoustically chorusing animals involves the precise timing of calls relative to those of other nearby individuals. In this study, I present a detailed description of nonrandom timing of both advertisement and aggressive calls in males of the Neotropical treefrog Dendropsophus ebraccatus. I used playback tests to measure call delays for both advertisement and aggressive calls given in response to synthetic advertisement and aggressive call stimuli presented with either a fixed or random timing arrangement. Call delays for a given response call type were nonrandomly distributed and did not differ depending on the fixed or random periodicity of stimulus presentation or on the stimulus call type. In general, advertisement call responses overlapped the playback stimuli, while aggressive calls were given with a much longer delay and did not overlap the playback stimuli. A second test involved the presentation of low pulse number advertisement and aggressive call stimuli to determine if males were capable of nonrandom timing to truncated stimuli. These playbacks also assessed whether they responded more aggressively to truncated aggressive call stimuli. Males usually showed synchrony in response to truncated calls of both types, more commonly in response to truncated advertisement calls. There were no differences in aggressive responses to truncated advertisement or aggressive calls. Call delays appear to be a property solely of the type of call that the male produces, regardless of the kind of stimulus. Thus, there may be a conflict between the ability to discriminate between signals and the ability to rapidly respond to these signals with an appropriate call delay.

Effects of multiple-speaker playbacks on aggressive calling behavior in the treefrog Dendropsophus ebraccatus

In addition to producing signals, males of chorusing species also act as receivers by adjusting properties of their vocalizations in response to those of other nearby individuals. Although it is likely that males are responsive to more than one other individual, most playback studies investigating male response have involved dyads in which vocal responses are measured to stimuli presented from a single speaker. In this study, I explored changes in both the propensity to give aggressive calls and the temporal properties of those calls in response to the playback of multiple aggressive call stimuli in the treefrog Dendropsophus ebraccatus. I found that males were sensitive to both the number of simulated aggressive callers and their specific call characteristics. Males generally gave a highly aggressive response to the first stimulus presented, but their response to the modification of this stimulus by the addition or subtraction of a simulated competitor depended on the degree of aggressiveness of the stimuli. Males tended to decrease their aggressive responses when either a more aggressive call was silenced or a less aggressive call was added and to increase their aggressive responses in the opposite situation. Aggressive calling in this species is clearly affected by complex changes in the social environment and I suggest that future studies explore these issues in other species to improve the understanding of communication interactions.

Aggressive calls improve leading callers’ attractiveness in the treefrog Dendropsophus ebraccatus

In complex acoustic choruses, competitive call timing interactions are often important in female mate choice. In the treefrog Dendropsophus ebraccatus, neighboring males’ advertisement calls tend to overlap and females prefer lagging calls. Males that produce leading advertisement calls are thus at a disadvantage relative to lagging males. In this study, I propose a novel strategy by which leading males may overcome this problem: the production of aggressive calls. Aggressive calls are longer than advertisement calls. Therefore, if a lagging male responds with an advertisement call to a leading aggressive call, the leading aggressive call may end after the lagging call. If females prefer calls that end last, then leading aggressive calls may be more attractive. I compared female preferences for advertisement and aggressive calls when they either overlapped, with the aggressive call leading, or alternated. Females preferred the advertisement call in alternation, but this preference was abolished when it overlapped with the aggressive call. I recorded interactions between pairs of males to determine whether leading males utilized aggressive calls as predicted. Among leading calls, aggressive calls were more likely to end after lagging calls than were advertisement calls. When switches to aggressive calling occurred after a bout of overlapping advertisement calls, it was more likely that the male that switched to aggressive calling had been in the leading position previously. These experiments suggest a strategy for leading males to reduce their disadvantage in call timing interactions and provide an explanation for this species’ high levels of

Habitat-specific constraints on induced hatching in a treefrog with reproductive mode plasticity

Many organisms show adaptive phenotypic plasticity in response to environmental variation. Some environmental factors may, however, impose constraints on the ability of organisms to respond to other factors. The neotropical treefrog Dendropsophus ebraccatus lays eggs both above water on leaves and directly in water, thereby exposing embryos to different abiotic conditions and predator communities. Rising pond levels can also flood arboreal clutches after rainstorms. We tested for predator-induced hatching in submerged and arboreal D. ebraccatus egg masses and assessed effects of prior hydration or desiccation on escape success in attacks by a terrestrial predator, Azteca ants, and an aquatic predator, large conspecific tadpoles. Embryos responded to both aquatic and terrestrial predator attacks by hatching prematurely, as much as 67% earlier than the peak of hatching in undisturbed clutches. Desiccation reduced the hatching response of terrestrial embryos, resulting in substantially lower escape rates. This desiccation effect disappeared rapidly with flooding; all embryos showed high escape hatching success underwater. The occurrence of predator-induced escape hatching in response to 2 different predators, in 2 different physical environments, suggests that this is a general response of D. ebraccatus to egg predator attack. Both ant attack and sublethal desiccation are common in nature, thus the inhibition of escape hatching in this context likely impacts tadpole recruitment. More generally, we demonstrate that an adaptive plastic response to risk is contingent on additional environmental variables and suggest that many instances of plasticity may similarly be modified by environmental constraints. Key words: abiotic‐biotic environmental variation, adaptive phenotypic plasticity, anura, complex life cycle, Hyla ebraccata, interaction modification, predator-facilitated hatching. [Behav Ecol]

Thermally contingent plasticity: temperature alters expression of predator-induced colour and morphology in a Neotropical treefrog tadpole

1. Behavioural, morphological and coloration plasticity are common responses of prey to predation risk. Theory predicts that prey should respond to the relative magnitude of risk, rather than a single level of response to any risk level. In addition to conspecific and predator densities, prey growth and differentiation rates affect the duration of vulnerability to size- and stage-limited predators and therefore the relative value of defences. 2. We reared tadpoles of the Neotropical treefrog Dendropsophus ebraccatus with or without cues from a predator (Belostoma sp.) in ecologically relevant warm or cool temperatures. To track phenotypic changes, we measured morphology, tail coloration and developmental stage at three points during the larval period. 3. Cues from predators interacted with growth conditions causing tadpoles to alter their phenotype, changing only tail colour in response to predators in warm water, but both morphology and colour in cool growth conditions. Tadpoles with predators in warm water altered coloration early but converged on the morphology of predator-free controls. Water temperature alone had no effect on tadpole phenotype. 4. We demonstrate that seemingly small variation in abiotic environmental conditions can alter the expression of phenotypic plasticity, consistent with predictions about how growth rate affects risk. Predator-induced tadpole phenotypes depended on temperature, with strong expression only in temperatures that slow development. Thermal modulation of plastic responses to predators may be broadly relevant to poikilotherm development. It is important to include a range of realistic growth conditions in experiments to more fully understand the ecological and evolutionary significance of plasticity.

Short‐ and long‐term effects of the abiotic egg environment on viability, development and vulnerability to predators of a Neotropical anuran

Summary 1. Environmental variation during development is common and often has long‐lasting effects on phenotypes and survival. In organisms with complex life cycles, such effects may carry over from one life stage into the subsequent stages, affecting reproductive success and survival in both direct and indirect manners. Much research has focused on the transition from the larval to adult stages, but fewer studies have addressed how egg‐stage variation may affect the larval stage, development to metamorphosis, and adult fitness. 2. We assessed the short‐ and long‐term consequences of abiotic environmental variation during egg development of the Neotropical treefrog Dendropsophus ebraccatus. Typically, D. ebraccatus eggs are oviposited terrestrially on leaves above water and hydrated by rainfall. However, at our field site in Panama ∼25% of terrestrial eggs become desiccated during development and ∼19% become submerged underwater. In addition, in unshaded ponds D. ebraccatus lays eggs directly in water. We assessed immediate and carryover effects of egg development under hydrated, desiccated and submerged conditions. We measured morphology and vulnerability to predators at hatching and at three time points during the larval period. We also measured morphology at metamorphosis. 3. Submerged eggs hatched less developed and later and had higher baseline mortality after hatching than either hydrated or desiccated terrestrial eggs. By 10 days after hatching, the morphology of tadpoles from the three egg environments was indistinguishable. Nonetheless, the egg environment affected predation, with tadpoles from submerged eggs being least vulnerable; later in development egg environment ceased to affect vulnerability. Tadpoles from all egg environments grew to a size refuge from dragonfly nymphs, whereas vulnerability to water bugs remained constant throughout development. At metamorphosis, froglets from submerged eggs were the largest and those from hydrated eggs were the smallest. 4. With anticipated climate change in the Neotropics, rainstorms are predicted to become more sporadic but larger when they do occur, potentially increasing the chances of both egg desiccation and flooding. The incidence of different egg environments may therefore change, potentially affecting amphibian phenotypes, interactions with predators, and survival across multiple life stages.

Aggressive thresholds in Dendropsophus ebraccatus: habituation and sensitization to different call types

Males in many chorusing anuran species use aggressive calls during defense of calling spaces from other males. The minimal intensity of another male’s vocalizations that elicits an aggressive call response has been termed the aggressive threshold. Previous studies of aggressive thresholds have shown that they are plastic: males habituated (increased their aggressive thresholds) in response to repeated presentation of stimuli above initial threshold levels. Habituation likely contributes to the stable chorus structure of these species, in which aggressive calling is rare compared to advertisement calls. I have observed high levels of aggressive calling in the treefrog Dendropsophus ebraccatus, suggesting that males of this species do not habituate. In this study, I investigated the plasticity of aggressive thresholds in D. ebraccatus. I measured the aggressive thresholds of males before and after suprathreshold stimulation by both advertisement and aggressive calls. I found that the different call types had different effects: males habituated to advertisement calls but lowered their aggressive thresholds in response to aggressive calls. I consider the latter response to be an example of sensitization, a behavior that has been documented infrequently in vocalizing anurans. Sensitization is a plausible mechanism responsible for the high levels of aggressive calling observed in this species. Given the high costs of aggressive calling, however, it is unclear why a mechanism that increases aggressive call output would be maintained.

Negative synergism of rainfall patterns and predators affects frog egg survival

1. The importance of rainfall is recognized in arid habitats, but has rarely been explored in ecosystems not viewed as rainfall limited. In addition, most attempts to study how rainfall affects organismal survival have focused on long-term rainfall metrics (e.g. monthly or seasonal patterns) instead of short-term measures. For organisms that are short lived or are sensitive to desiccation, short-term patterns of rainfall may provide insight to understanding what determines survival in particular habitats. 2. We monitored daily rainfall and survival of arboreal eggs of the treefrog Dendropsophus ebraccatus at two ponds during the rainy season in central Panama. Desiccation and predation were the primary sources of egg mortality and their effects were not independent. Rainfall directly reduced desiccation mortality by hydrating and thickening the jelly surrounding eggs. In addition, rainfall reduced predation on egg clutches. 3. To elucidate the mechanism by which rainfall alters predation, we exposed experimentally hydrated and dehydrated egg clutches to the two D. ebraccatus egg predators most common at our site, ants and social wasps. Ants and wasps preferentially preyed on dehydrated clutches and ants consumed dehydrated eggs three times faster than hydrated eggs. 4. Rainfall patterns are expected to change and the responses of organisms that use rainfall as a reliable cue to reproduce may prove maladaptive. If rainfall becomes more sporadic, as is predicted to happen during this century, it may have negative consequences for desiccation-sensitive organisms.

Reproductive mode plasticity: Aquatic and terrestrial oviposition in a treefrog

Diversification of reproductive mode is a major theme in animal evolution. Vertebrate reproduction began in water, and terrestrial eggs evolved multiple times in fishes and amphibians and in the amniote ancestor. Because oxygen uptake from water conflicts with water retention in air, egg adaptations to one environment typically preclude development in the other. Few animals have variable reproductive modes, and no vertebrates are known to lay eggs both in water and on land. We report phenotypic plasticity of reproduction with aquatic and terrestrial egg deposition by a frog. The treefrog Dendropsophus ebraccatus, known to lay eggs terrestrially, also lays eggs in water, both at the surface and fully submerged, and chooses its reproductive mode based on the shade above a pond. Under unshaded conditions, in a disturbed habitat and in experimental mesocosms, these frogs lay most of their egg masses aquatically. The same pairs also can lay eggs terrestrially, on vegetation over water, even during a single night. Eggs can survive in both aquatic and terrestrial environments, and variable mortality risks in each may make oviposition plasticity adaptive. Phylogenetically, D. ebraccatus branches from the basal node in a clade of terrestrially breeding species, nested within a larger lineage of aquatic-breeding frogs. Reproductive plasticity in D. ebraccatus may represent a retained ancestral state intermediate in the evolution of terrestrial reproduction.

Fish and dragonfly nymph predators induce opposite shifts in color and morphology of tadpoles

Many prey species, including amphibian larvae, can adaptively alter coloration and morphology to become more or less conspicuous to predators. Despite abundant research on predator‐induced plasticity in tadpoles, the combination of color and morphological responses to predators remains largely unexplored. We measured predator‐induced morphological and color plasticity in tadpoles. We reared tadpoles of the neotropical treefrog Dendropsophus ebraccatus with dragonfly nymph or fish predators, or in a predator‐free control. After 10 days, we digitally photographed tadpoles and measured eight morphometric variables and five tail color variables. Tadpoles reared with nymphs developed the largest and reddest tails, but incurred a developmental cost, being the smallest overall. Cues from fish induced an opposite tail phenotype in tadpoles, causing shallow achromatic tails. Control tadpoles developed intermediate tail phenotypes. This provides the first experimental evidence that tadpoles can shift both color and morphology in opposite, predator‐specific directions in response to a fish and an odonate predator. Despite mean differences, however, there was substantial variation in the degree of phenotype induction across treatments. Tail redness was correlated with tail spot size, but not perfectly, indicating that color and morphology may be partially decoupled in D. ebraccatus. Balancing selection from multiple conflicting predators may result in genetic variation for developmental plasticity.

Balancing sexual selection through opposing mate choice and male competition

Male–male competition and female mate choice act contemporaneously in the cockroach Nauphoeta cinerea and the social pheromone of males influences the outcome of both forms of sexual selection. We therefore examined the joint and separate effects of male–male competition and female mate choice to determine if the selective optima for the pheromone were the same or different. Dominant males in a newly established hierarchy mated more frequently, but not exclusively. Manipulations of the multi-component social pheromone produced by males of N. cinerea showed that both long- and close-range attraction of females by males were influenced by the quantity and composition of the pheromone. The most attractive composition, however, differed from that which was most likely to confer high status to males. Since the outcome of male–male competition can conflict with mating preferences exhibited by females, there is balancing sexual selection on the social pheromone of N. cinerea. Such balancing selection might act to maintain genetic variation in sexually selected traits. We suggest that the different forms of sexual selection conflict in N. cinerea because females prefer a blend different to that which is most effective in male–male competition in order to avoid mating with overly aggressive males.