Ximena E. Bernal

Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females

SUMMARY The vocal sac is a visually conspicuous attribute of most male frogs, but its role in visual communication has only been demonstrated recently in diurnally displaying frogs. Here we characterized the spectral properties of the inflated vocal sac of male túngara frogs (Physalaemus pustulosus), a nocturnal species, and túngara visual sensitivity to this cue across reproductive state and sex. We measured the spectral and total reflectance of different male body regions, including inflated and non-inflated vocal sacs, along with samples of the visual background against which males are perceived. Inflated vocal sacs were the most reflective of all body parts, being one log unit more reflective than background materials. We utilized an optomotor drum with black stripes and stripes that mimicked the spectral reflectance of the inflated vocal sacs with various nocturnal light intensities to measure the visual sensitivity thresholds of males, non-reproductive females and reproductive females. All three groups exhibited visual sensitivities corresponding to intensities below moonless conditions in open habitats or at the edge of secondary tropical forests. Reproductive females exhibited the greatest visual sensitivity of all groups, and were significantly more sensitive than non-reproductive females. Though the mechanism for this physiological difference between reproductive and non-reproductive females is unknown, it is consistent with previously observed patterns of light-dependent phonotaxic behavior in túngaras. We suggest that the visual ecology of the vocal sac, especially in nocturnal frogs, offers a rich source for investigations of visual ecology and physiological regulation of vision.

The Vocal Sac Increases Call Rate in the Túngara Frog Physalaemus pustulosus

In most anurans, the production of advertisement calls is accompanied by the inflation of a vocal sac. Current functions of the vocal sac, however, are not fully understood, although several hypotheses have been proposed. One hypothesis suggests that the vocal sac decreases the intercall interval (i.e., increases call rate) by reinflating the lungs more rapidly than is possible with the buccal pump. We investigate this hypothesis by analyzing audio and video recordings of calling túngara frogs. We compare the first two call bouts emitted by an originally uninflated male. The first call bout requires lung inflation via buccal pumping, but in the second, the male is already inflated because of capture of air and reinflation of the lungs by the vocal sac. Lung inflation to typical field levels requires 26–51 buccal pumps, which takes at least 4.4 s. This estimate is more than 2.5 times the typical intercall interval with lung reinflation via a vocal sac (ca. 1.7 s). Evidence from phonotaxis tests demonstrates that these differences in intercall intervals are salient to females and that female Physalaemus pustulosus prefer the shorter intercall interval/higher call rate. Acoustic analyses demonstrate that the first call of bout 1, which requires buccal pumping, is usually shorter, of lower amplitude, and spans a smaller frequency range than the first call of bout 2, which does not require buccal pumping. Because females prefer longer, more intense calls, these results suggest that the vocal sac not only increases call rate but also allows males to produce more calls of increased attractiveness to females.

GEOGRAPHIC VARIATION IN ADVERTISEMENT CALL AND GENETIC STRUCTURE OF COLOSTETHUS PALMATUS (ANURA, DENDROBATIDAE) FROM THE COLOMBIAN ANDES

Among frogs endemic to the Colombian Andes, the dendrobatid Colostethus palmatus has an exceptionally wide geographic distribution. We examined the patterns of variation in calls and genetic properties to determine whether this variation is associated with geographic barriers and distances between populations. We analyzed variation in advertisement calls and RAPD products in seven populations along a 346-km transect from south to north throughout the Cordillera Oriental covering an extensive part of the geographical range of C. palmatus. Populations of this species inhabit both slopes of the Cordillera Oriental, and are separated by a continuous ridge along these mountains. We found more inter- than intrapopulational variation. Four call variables and male snout–vent length exhibited clinal variation, generating a predictable geographic pattern which coincided with a climatic gradient of increasing moisture and seasonality. The genetic relations between populations are explained by their location on the Andes, particularly by the side of the slope. Differences between populations in four call characteristics and genetic distance were significantly correlated with linear geographic distances between populations on the same slope. We found evidence for genetic and bioacoustic differentiation between populations living on opposite slopes.

Female and male behavioral response to advertisement calls of graded complexity in túngara frogs, Physalaemus pustulosus

We investigated the natural dynamics in a sexual signal that combines different call components and explored the role of call complexity in sexual selection using a neotropical frog. Male túngara frogs, Physalaemus pustulosus, facultatively add up to seven short, multi-harmonic components (chucks) to the simple form of their calls (whines). Female túngara frogs are preferentially attracted to whines with chucks over whines without chucks, and males also call more in response to calls containing chucks. Because acoustic predators prefer complex calls, in the context of simple (no chucks) versus complex (any number of chucks) calls, the variably complex call appears to have evolved in response to the opposing selective forces of natural and sexual selection. There is no evidence, however, for the function of increasing the number of chucks within complex calls. We tested two aspects of increasing call complexity: natural patterns of use of call types in males and how both sexes respond to variation in multi-chuck calls. Males incrementally change call complexity by the addition or subtraction of a single chuck and usually do not produce more than two chucks. Variation in call complexity, for calls with at least one chuck, does not influence response calling in males or phonotaxis in females. Our results suggest that one reason for not increasing call complexity beyond a single chuck is the diminishing effectiveness on the responses of both sexes.

Sex differences in response to nonconspecific advertisement calls: receiver permissiveness in male and female túngara frogs

In many species, males advertise to both male and female audiences. Given the asymmetry in fitness costs of recognition errors in response to mating signals for the sexes, usually higher for females than males, males are expected to be more permissive than females in their responses to signals. Few studies, however, have investigated such differences and there is no consensus on which sex is more permissive to signal variation. We examined the evoked vocal responses of male tungara frogs, Physalaemus pustulosus, to 14 species of heterospecific and ancestral male mating calls to evaluate the influence of call similarity and phylogenetic distance on their responses. We also compared male calling responses to female phonotactic responses to examine the propensity of response errors between the sexes. Recognition errors were higher for males than females, as predicted by the different costs associated with recognition errors for each sex. Males responded to the calls of most species with mating calls, and produced aggressive calls in response to two other heterospecific/ancestral calls. The responses of males were explained by phylogenetic distance but not by overall call similarity. Similarly, females were more likely to show phonotaxis to calls of species and ancestors that were more closely related. Therefore, evolutionary history has left a perceptual footprint on the brain of both sexes but the details seem to differ. We discuss proximate reasons underlying sexual differences in receiver permissiveness in tungara frogs and potential factors leading to their evolution.

Patterns of mating call preferences in túngara frogs, Physalaemus pustulosus

We examine acoustic mating preferences of a focal population at four different scales of divergence: within the population, between populations in the same genetic group, between populations in different genetic groups and between different species. At all scales there is substantial genetic divergence, variation in mating signals and preferences are influenced by signal variation. There is, however, no support for the hypothesis that mating preferences accumulate predictably with genetic distance. Females preferred the local conspecific call to the foreign conspecific call in about one‐third of the experiments, and preferred the local call to all of the heterospecific calls tested. But there was no significant relationship between the variation in the strength of preference and genetic distance either among conspecific populations, or among heterospecific species. Thus, in this study macroevolutionary patterns are not apparent at the microevolutionary scale.

Task differences confound sex differences in receiver permissiveness in túngara frogs

In many mating systems, both sexes respond to the same sexual signal. In frogs, males typically call in response to advertisement calls, while females approach male calls in choosing a mate. The costs of signal detection errors are expected to differ between the sexes. Missed opportunities are costly for males because ignoring a signal results in failing to compete with rivals for mates, while their cost for misidentification is lower (time and energy displaying to the incorrect target). By contrast, for females, the cost of misidentification is high (mating with incorrect species or low-quality partner), while their cost for missed opportunity is lower because the operational sex ratio puts females at a premium. Consequently, females should be more selective in their response to signal variation than males. We report that presumed sexual differences in selectivity in túngara frogs (Physalaemus pustulosus) are task-specific rather than sex-specific. As predicted, male túngara frogs are less selective in their vocal responses than are females in their phonotactic responses. Males exhibiting phonotaxis to the same calls, however, are as selective as females, and are significantly more selective than when they respond vocally to the same calls. Our study shows that apparent differences between the sexes emerge from differences in the behaviours themselves and are not intrinsic to each sex. Analogous behavioural differences might confound sex differences in other systems; thus, we suggest consideration of the behavioural plasticity of sex as well as its stereotypy.

No evidence for female mate choice based on genetic similarity in the túngara frog Physalaemus pustulosus

In most sexually reproducing animals, the behavior of one or both sexes during courtship critically influences the success at mating of the opposite sex. This behavior is often interpreted as “mate choice,” and there is great interest in why such choices are exercised. The explanation for the evolution of mate choice that has received the most attention and generated the most controversy is based on assumed genetic effects. In this study, we investigated whether female túngara frogs, which choose mates based on acoustic cues, have a preference for genetically less related males. Specifically, we determine if there is disassortive mating based on microsatellite markers, if there is information in the advertisement call that could be used to assess genetic similarity, and if females exhibit acoustic-based mating preferences that would promote choice for genetic diversity. Using seven microsatellite markers, we found no correlation of male call similarity and male genetic relatedness. Female choice experiments showed no female preference for calls of less related males, and there was no evidence for inbreeding avoidance in the field. Our results do not support the hypothesis of mate choice based on information about genetic relatedness conveyed by acoustic signals in túngara frogs.

First report of mite parasitization in frog-biting midges (Corethrella species)

Water mites (Acari: Hydrachnidiae) were collected from males of frog-biting midges (Corethrellidae) in Gamboa, Panama. All Corethrella squamifemora males collected were parasitized with water mites. The mites were attached to the soft tissues of the thoracic region of the midges. No mites were found on female frog-biting midges of the same species. This study is the first report of mite parasitization in frog-biting midges.