Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance

Anthropogenic sensory pollution is affecting ecosystems worldwide. Human actions generate acoustic noise, emanate artificial light and emit chemical substances. All of these pollutants are known to affect animals. Most studies on anthropogenic pollution address the impact of pollutants in unimodal sensory domains. High levels of anthropogenic noise, for example, have been shown to interfere with acoustic signals and cues. However, animals rely on multiple senses, and pollutants often co-occur. Thus, a full ecological assessment of the impact of anthropogenic activities requires a multimodal approach. We describe how sensory pollutants can co-occur and how covariance among pollutants may differ from natural situations. We review how animals combine information that arrives at their sensory systems through different modalities and outline how sensory conditions can interfere with multimodal perception. Finally, we describe how sensory pollutants can affect the perception, behaviour and endocrinology of animals within and across sensory modalities. We conclude that sensory pollution can affect animals in complex ways due to interactions among sensory stimuli, neural processing and behavioural and endocrinal feedback. We call for more empirical data on covariance among sensory conditions, for instance, data on correlated levels in noise and light pollution. Furthermore, we encourage researchers to test animal responses to a full-factorial set of sensory pollutants in the presence or the absence of ecologically important signals and cues. We realize that such approach is often time and energy consuming, but we think this is the only way to fully understand the multimodal impact of sensory pollution on animal performance and perception.     

Differential Evolution of Advertisement Call Traits in Dart-Poison Frogs (Anura: Dendrobatidae)

The ability to recognise and discriminate between heterospecific and conspecific individuals plays an essential role in mate choice, reproductive isolation and thus species diversification. Many animals discriminate based on advertisement calls, whose evolution may be driven by a variety of forces such as natural selection, sexual selection or stochastic processes. The relative importance of stochastic processes acting on a given trait is usually correlated with its phylogenetic signal. Mate-recognition signals are complex traits composed of multiple features that could potentially respond independently to evolutionary forces. The advertisement call of anurans is used in species recognition and mate choice. In this study, we estimate the phylogenetic signal for body size and a suite of traits describing the male advertisement call from dart-poison frogs (Anura: Dendrobatidae). We found a surprisingly high phylogenetic signal for all call traits. In addition, call traits varied in their degree of phylogenetic signal, suggesting that evolutionary forces have been acting differently on different traits. Pulse duration showed the strongest phylogenetic signal. Peak frequency and body size were correlated and presented high phylogenetic signal indicating that the evolution of one trait may be driving or constraining the other. Since most variation in call traits can be explained by the phylogenetic history of the species, we cannot reject the hypothesis that stochastic processes account for significant evolutionary divergence in frog calls.     

Anuran occupancy of created wetlands in the Central Appalachians

Evaluating the adequacy of created wetlands to replace the functions of lost natural wetlands is important because wetland mitigation is a major tool used to offset wetland losses. However, measurements such as vegetative cover and presence of wildlife may not provide sufficient evidence that created wetlands are functioning properly and thus examining the ecology of wetland biota such as that of amphibians may be a more useful surrogate for function. The objectives of this study were to compare the occupancy and detection of calling anurans in created wetlands relative to beaver-created wetlands. Five-, 10-min, and broadcast call surveys were performed at 24 wetlands throughout the Central Appalachians once every month from March through August of 2009 and 2010. Occupancy modeling was used to estimate the occupancy and detection of individual species, incorporating relevant environmental variables. The occupancy of anurans did not differ between human-created and beaver (Castor canadensis)-created wetlands. Detection of anurans was largely unaffected by call survey type, but several environmental covariates had a significant effect on the detectability of calling anurans. Our results suggest that the function of providing adequate chorusing habitat for adult anurans is being fulfilled by the created wetlands that we examined.     

Mate sampling by female barking treefrogs (Hyla gratiosa)

Despite intense interest in mate choice, relatively little isknown about how individuals sample prospective mates. Indeed,a key issue is whether females sample males or simply matewith the first male encountered. We investigated mate samplingby female barking treefrogs (Hyla gratiosa). Females choosingmates in natural choruses did not move between males but insteadmated with the first male they approached closely. Most femalesmated with the male closest to them at the start of their mate-choiceprocess, and females were more likely to mate with the closest male when the distance to other males was large. These observationsare consistent with the hypothesis that females do not samplepotential mates but instead mate with the first male they distinguishfrom the rest of the chorus. To test this initial detectionhypothesis, we conducted a playback experiment in which weoffered females a choice between two calls, one of which was detectable above the background chorus sound at the female'srelease point, and one of which became detectable only as femalesmoved toward the initially detectable call. Females did notprefer the initially detectable call, thus ruling out the initialdetection hypothesis and implicating sampling of potentialmates by females. Based on the behavior of females in natural choruses, we hypothesize that females approach the chorus, moveto locations where they are able to detect the calls of severalmales simultaneously, and choose a mate from among these malesat some distance from the males. Such simultaneous samplingmay be common in lekking and chorusing species, which havebeen the subjects of many studies of sexual selection.     

Moonlighting? - Consequences of lunar cues on anuran reproductive activity

While the influence of environmental variables, particularly temperature and rainfall, on the breeding behavior of amphibians is widely recognized, relatively few studies have addressed how the moon affects amphibian behavior. Yet, the lunar cycle provides several rhythmic temporal cues that animals could use to time important group events such as spawning, and the substantial changes in light levels associated with the different moon phases may also affect the behavior of nocturnal frogs. Using seven years of field observation data, we tested for lunar effects on the reproductive activity of male and female Eastern Gray Treefrogs (Hyla versicolor). We found that chorusing and breeding activity was statistically more likely to occur around the first quarter of the moon and during intermediately bright nights, but that reproductive activity also occurred during various other times during the lunar cycle. We discuss these findings in relation to the two main hypotheses of lunar effects on animals: predator avoidance and temporal synchronization of breeding.     

Frequency modulated calls and species recognition in a neotropical frog

Summary The neotropical frogPhysalaemus pustulosus (Leptodactylidae) has a complex advertisement call and different call components perform different functions. The whine is a necessary and sufficient stimulus for species recognition. The chuck provides information about male body size that is used by females in mate choice (Ryan 1980, 1983), but the chuck must be combined with the species-identifying whine to elicit maximum behavioral responses from males and females. One of the important features of the whine in eliciting behavioral responses from both sexes is the direction of frequency modulation. This suggests that current models of species recognition in anurans based on a frequency filtering mechanism of the peripheral auditory system and selective responses to combinations of frequencies in the central nervous system are not sufficient to explain species recognition inP. pustulosus. Recent neurophysiological studies of the anuran torus semicircularis are discussed in terms of a mechanism for decoding frequency sweeps.     

Elevated stress hormone diminishes the strength of female preferences for acoustic signals in the green treefrog

Mate selection can be stressful; time spent searching for mates can increase predation risk and/or decrease food consumption, resulting in elevated stress hormone levels. Both high predation risk and low food availability are often associated with increased variation in mate choice by females, but it is not clear whether stress hormone levels contribute to such variation in female behavior. We examined how the stress hormone corticosterone (CORT) affects female preferences for acoustic signals in the green treefrog, Hyla cinerea. Specifically, we assessed whether CORT administration affects female preferences for call rate — an acoustic feature that is typically under directional selection via mate choice by females in most anurans and other species that communicate using acoustic signals. Using a dual speaker playback paradigm, we show that females that were administered higher doses of CORT were less likely to choose male advertisement calls broadcast at high rates. Neither CORT dose nor level was related to the latency of female phonotactic responses, suggesting that elevated CORT does not influence the motivation to mate. Results were also not related to circulating sex steroids (i.e., progesterone, androgens or estradiol) that have traditionally been the focus of studies examining the hormonal basis for variation in female mate choice. Our results thus indicate that elevated CORT levels decrease the strength of female preferences for acoustic signals.     

Does artificial light pollution impair problem‐solving success in peafowl?

Behavioral innovations allow animals to adjust their behavior to solve novel problems. While innovative behavior can be important for animals living in new environments, anthropogenic pollution may limit their ability to adapt by impairing cognition or motivation. In particular, exposure to light pollution at night can cause sleep deprivation and may, therefore, hinder innovative behavior. To test this hypothesis, we examined experimentally whether exposure to acute light pollution impacts problem‐solving success in peafowl (Pavo cristatus). After peafowl were exposed to artificial light pollution for one night, they were presented with a problem‐solving task in which they could extract food by piercing the lid of an unfamiliar food bowl. Their problem‐solving success was unrelated to short‐term light pollution exposure. Other factors, including persistence, sex of the bird, and moon illumination, influenced their success in solving the task. The results suggest that short‐term exposure to light pollution does not limit behavioral innovation, but long‐term studies are necessary to further probe this question.     

How long do females really listen? Assessment time for female mate choice in the grey treefrog, Hyla versicolor

A satisfactory understanding of the process of mate choice in many species of anurans requires that we know how sensitive females are to the variation in male calls under natural conditions and what is the timescale or ‘window’ over which females compare potential mates. In natural choruses, grey treefrog females may sit near calling males for many minutes before approaching a particular individual to mate, whereas in laboratory-based phonotaxis tests, they may approach a speaker within 30 s of exposure to broadcast calls. Females prefer long versus short calls. To estimate ‘assessment time’ of females in nature, we broadcast calls from four pairs of 360-degree speakers suspended within screen cages at four locations at the edge of a pond. One speaker per pair presented calls of constant duration while the other speaker shifted between broadcasts of calls that were longer or shorter than the constant duration call. The time period over which this change in call duration occurred differed between the four venues. Laboratory-based choice tests indicated that females preferred call sources with variable numbers of pulses to those with constant numbers of pulses when the former had more total pulses per time window. Accordingly, we assigned the probabilities of field captures at the different speakers based on the summed pulses from the constant and cycling speakers within the possible assessment windows. These probabilities, together with the numbers of females captured at the speaker array over the breeding season, indicated that the most likely assessment time is close to 2 min.     

Fitness Benefits of Mate Choice for Compatibility in a Socially Monogamous Species

Research on mate choice has primarily focused on preferences for quality indicators, assuming that all individuals show consensus about who is the most attractive. However, in some species, mating preferences seem largely individual-specific, suggesting that they might target genetic or behavioral compatibility. Few studies have quantified the fitness consequences of allowing versus preventing such idiosyncratic mate choice. Here, we report on an experiment that controls for variation in overall partner quality and show that zebra finch (Taeniopygia guttata) pairs that resulted from free mate choice achieved a 37% higher reproductive success than pairs that were forced to mate. Cross-fostering of freshly laid eggs showed that embryo mortality (before hatching) primarily depended on the identity of the genetic parents, whereas offspring mortality during the rearing period depended on foster-parent identity. Therefore, preventing mate choice should lead to an increase in embryo mortality if mate choice targets genetic compatibility (for embryo viability), and to an increase in offspring mortality if mate choice targets behavioral compatibility (for better rearing). We found that pairs from both treatments showed equal rates of embryo mortality, but chosen pairs were better at raising offspring. These results thus support the behavioral, but not the genetic, compatibility hypothesis. Further exploratory analyses reveal several differences in behavior and fitness components between “free-choice” and “forced” pairs.     

Variation in Male Calling Behaviour and Relation to Male Mating Success in the Strawberry Poison Frog (Dendrobates pumilio)

Calling behaviour and the characteristics of the males’ call are important for mate attraction, female mate choice and male mating success in anurans. In this study I investigated the variation in calling activity and the variation in one spectral (dominant frequency) and four temporal properties (call rate, call duration, duty cycle and pulse rate) of the advertisement call of strawberry poison frogs, Dendrobates pumilio, in two Costa Rican populations during two study periods. Regarding all call properties, no differences were found between populations or years, but between‐male variation was significantly higher than within‐recording and within‐male variation. Dominant frequency was less variable within and among males than temporal call properties and I classified the former as static and the latter as intermediate properties of the call. No call property seemed to be strongly affected by body length or weight. Moreover, I used behavioural observations to relate male calling behaviour to mating success. Calling activity was more variable between males and accounted for more variability in mating success in multiple regression models than any call property. Some call properties (call rate, dominant frequency and pulse rate) were also related to male mating success in one or two study periods. These call properties are probably important for females during courtship to assess their prospective mate and/or for competitive male–male interactions. Furthermore, I compared call properties and mating success of some males for which data were available for both study periods. Pulse rate was lower in the second than in the first year, suggesting age‐related changes in this call property. Moreover, male D. pumilio increased their relative mating success from the first to the second study year. Together with other studies, the data of this study suggest that, in anurans, endurance rivalry contributes more to variation in male mating success than does female choice based on male characteristics.     

Non‐visual cues and indirect strategies that enable discrimination of asymmetric mates

The postulates of developmental instability–sexual selection hypothesis is intensely debated among evolutionary biologists, wherein despite a large amount of empirical data, evidence for or against it has been largely inconclusive. A key assumption of this hypothesis is that animals assess symmetry in potential mates as an indicator of genetic quality (developmental stability), and consequently use this information to discriminate against those with higher asymmetries while choosing mates. However, the perceptional basis that must underlie such discriminatory behavior (is symmetry a signal or is symmetry signaled) is not clearly defined. It is also argued that since asymmetry levels in natural populations are very low, the low signal‐to‐noise ratio would make accurate assessment of symmetry both difficult and costly. Rather than attempting to validate this hypothesis or even as to whether animals assess mate symmetry, this review simply aims to examine the plausibility that animals perceive symmetry (directly or indirectly) and consequently discriminate against asymmetric mates in response to perceived irregularities during courtship. For this, we review mate choice and courtship literature to identify potential sensory cues that might advertise asymmetry or lead to discrimination of asymmetric individuals. Although signaling associated with mate choice is commonly multimodal, previous studies on asymmetry have mainly focused on visual perception. In the light of a recent study (Vijendravarma et al., 2022, Proceedings of the National Academy of Sciences of the United States of America, 119, e2116136119), this review attempts to balance this bias by emphasizing on non‐visual perception of asymmetry. In conclusion, we discuss the methodological challenges associated with testing the role of multimodal cues in detecting mate asymmetry, and highlight the importance of considering ecological, behavioral, and evolutionary aspects of animals while interpreting empirical data that test such hypothesis.     

Changes in the Frequency Structure of a Mating Call Decrease Its Attractiveness to Females in the Cricket Frog Acris crepitans blanchardi

In many species, females often prefer male signals that are more complex than in nature or beyond the range of calls naturally produced by conspecific males in spectral, temporal and amplitude features. In this study we examined both the ability of females to recognize signals outside the normal range of spectral frequency variation seen in male advertisement calls, and the influence of increasing call complexity by adding spectral components to enhance the attractiveness of a male advertisement call in the cricket frog Acris crepitans blanchardi, while keeping its amplitude constant. We used two different natural male call groups and created the following synthetic call groups: with a dominant frequency at 3500 Hz, i.e. at the normal dominant frequency with a frequency band within the sensitivity range of the inner ear basilar papilla; with a dominant frequency at 700 Hz, i.e. outside the normal range of variation and with a frequency band outside the sensitivity range of the basilar papilla but within the range of the amphibian papilla; with two dominant frequencies, one at 700 Hz and another at 3500 Hz, stimulating the basilar and amphibian papilla simultaneously. In double choice experiments we tested all combinations of the three call groups, and we tested the 3500 Hz call groups against the same natural call groups. Additionally, we tested the 700 Hz call groups against white noise to see whether these signals are meaningful in mate choice. Females preferred 3500 Hz call groups over all other call groups. The synthetic call group was as attractive to females as the same natural call group. The 700 Hz call group was not meaningful in mate choice. The combined (700 Hz + 3500 Hz) call group was significantly less attractive to females than the 3500 Hz call group. Thus, making a call more spectrally complex without increasing its overall amplitude decreases its attractiveness to cricket frog females.     

Toxic,invasive treefrog creates evolutionary trap for native gartersnakes

Possession of unique defensive toxins by nonindigenous species may increase the likelihood of creating evolutionary traps for native predators. We tested the hypothesis that nonindigenous, toxic Cuban Treefrogs (Osteopilus septentrionalis) have created an evolutionary trap for native, generalist snakes. Additionally, we explored the possibility that populations of snakes that co-occur with Cuban Treefrogs have responded in ways that allow them to escape potential trap dynamics. To evaluate a potential fitness cost of consuming Cuban Treefrogs, we monitored growth of 61 wild-caught Common Gartersnakes (Thamnophis sirtalis) fed exclusive diets of either Cuban Treefrogs, native Green Treefrogs (Hyla cinerea), or native Golden Shiners (Notemigonus crysoleucas). Snakes in the Cuban Treefrog diet treatment gained less than half the mass of those consuming native prey, and Cuban Treefrogs were significantly less digestible than native prey. There was no difference in the response of gartersnakes to prey scent cues of Cuban Treefrogs and Green Treefrogs. Our results indicate that Cuban Treefrogs likely represent an evolutionary trap for snakes because consumption of these frogs carries fitness costs, yet snakes fail to recognize this prey as being costly. We found no difference in growth or response to prey cues between snakes from invaded and non-invaded regions, suggesting snakes have not responded to escape trap dynamics. Interactions of native snakes and Cuban Treefrogs support the idea that introduced species with novel toxins may increase the likelihood of evolutionary trap formation.     

Taxonomic and sensory biases in the mate-choice literature: there are far too few studies of chemical and multimodal communication

The sexual selection literature has grown rapidly in recent years. In an effort to elucidate biases in the focus of current mate-choice research here, I review 297 studies among 230 species. Among taxa, studies of birds were most common (40% of all studies), with insects, fishes, and anurans less well represented (20%, 18%, 14%, respectively). All other taxa were poorly represented in the literature (<3%). Across sensory modalities, studies of visual and acoustic signals were most common (46%, 30%, respectively), with relatively few studies investigating chemical, tactile, and electrical signals in mate choice (3%, 3%, <1%, respectively). Most mate-choice studies of birds and fishes investigated visual signals, while the majority of insect and anuran studies investigated acoustic signals. While these associations may reflect biological realities—birds and anurans tend not to emphasize chemical cues in mate choice; electric communication may indeed be quite uncommon—they may also be grossly misleading: chemical cues are likely critical for mate choice in millions of insect species. Moreover, I suggest that the particularly high vulnerability of chemical communication networks to anthropogenic fouling should provide immediate motivation for many more studies of chemical signals in mate choice. Finally, I find that despite widespread acceptance that male displays are often comprised of multiple elements produced across sensory modalities, studies simultaneously investigating the use of multiple cues in mate choice are rare. While not exhaustive, this review identifies biases in the focus of mate-choice studies, and should serve to identify fruitful directions for future mate-choice research.     

Opportunity for sexual selection arises at moderate densities in the frog Rana chensinensis: an experimental approach

Heavily male-biased operational sex ratio and high male density characterizing explosively breeding anurans are expected to enhance the opportunity for sexual selection through large-male mating advantage brought about by severe male–male competition. However, our previous study on the temperate frog Rana chensinensis suggested that these two factors might restrict the opportunity under natural conditions for females to be grasped by any male they meet first, and scramble competition between males occurred less frequently because amplectant pairs hid on the bottom of ponds. In the present experimental study, in which the operational sex ratios and male densities were much lower and individual interactions were sufficiently longer than in natural population, we found a large-male pairing advantage in female mate choice, multiple mate choice, and male displacement experiments. These findings lend circumstantial support for the predication, although there was no evidence of large-female mating advantage in a male mate choice experiment.     

Behavioral models of hydrothermal regulation in anurans: A field study in the Atlantic Forest,Brazil

Anurans rely on different microhabitats and microclimates for hydro-thermoregulation, which is an important physiological property for locomotor performance, body temperature, water flux, and pathogen defense. We ask whether microhabitat scouting is related to physiological states, specifically if microhabitat choice benefits the production of behavioral fever (e.g., increasing body temperature by selecting warmer places) or sickness behavior (e.g., inactivity and anorexia). We investigated how thermoregulatory behaviors affect hydro-thermoregulation in anurans, using agar models as a sampling unit, simulating four behaviors related to behavioral fever and sickness behavior. We compared the models' hydro-thermal balance in two different environments (wet and transitional forests). We showed that the wet forest was warmer and more stable than transitional forest and the agar models in the wet forest were warmer. Still, the four behavioral simulations exhibited similar average temperatures during the five-day study period in both forests. However, the apathetic behavior models had the lowest daily temperatures. The percentage hydration across models was higher in the wet forest, and daily variation in water loss for each behavioral simulation was higher in the transitional forest. Nevertheless, when limiting the analysis to the warmest times (1000–1600 h), apathetic behavior models lost less water than the others in both forests. We showed that different forests provide microclimatic variation for understory anurans, but different thermoregulatory behaviors may lead to similar body temperatures. Therefore, the Atlantic Forest offers different microclimates and thermoregulation options for anurans, as some species could develop behavioral fever while others demonstrate sickness behavior. Abstract in Portuguese is available with online material.     

Melodic males and flashy females: Geographic variation in male and female reproductive behavior in red‐eyed treefrogs (Agalychnis callidryas)

Geographic variation in courtship behavior can affect reproductive success of divergent phenotypes via mate choice. Over time, this can lead to reproductive isolation and ultimately to speciation. The Neotropical red‐eyed treefrog (Agalychnis callidryas) exhibits high levels of phenotypic variation among populations in Costa Rica and Panama, including differences in color pattern, body size, and skin peptides. To test the extent of behavioral premating isolation among differentiated populations, we quantified male advertisement calls from six sites and female responses to male stimuli (acoustic and visual signals) from four sites. Our results show that both male advertisement calls and female behavior vary among populations: Discriminant function analyses can predict the population of origin for 99.3% ± 0.7 of males based on male call (dominant frequency and bandwidth) and 76.1% ± 6.6 of females based on female response behavior (frequency and duration of visual displays). Further, female mate choice trials (n = 69) showed that population divergence in male signals is coupled with female preference for local male stimuli. Combined, these results suggest that evolved differences among populations in male call properties and female response signals could have consequences for reproductive isolation. Finally, population variation in male and female behavior was not well explained by geographic or genetic distance, indicating a role for localized selection and/or drift. The interplay between male courtship and female responses may facilitate the evolution of local variants in courtship style, thus accelerating premating isolation via assortative mating.     

Pattern recognition and call preferences in treefrogs (Anura: Hylidae): a quantitative analysis using a no-choice paradigm

Studies of mate attraction have traditionally employed one of two experimental methods: choice tests in which female preferences from among two or more signals are tabulated, or single-stimulus tests in which the female response to one signal is quantified. Choice tests have long been preferred for examining mate attraction in anurans. Inspired by Wagner's (1998, Animal Behaviour,55, 1029-1042) discussion of the strengths and weaknesses of the two experimental approaches, we used a single-stimulus design to examine mate attraction in two sibling species of treefrogs (Hyla versicolor and H. chrysoscelis). We quantified female responses based upon the relative time required to approach signals varying in pulse rate, pulse rise time and pulse number. The data were used to generate response functions providing a quantitative measure of female attraction to the stimuli. Comparisons with data from choice experiments reveal broad similarities, as well as properties of female responses that had not been detected with choice tests. The results are discussed with regard to female selectivity for call parameters that are likely to mediate sexual selection and homospecific pairing.     

Spatio-Temporal Dynamics of Field Cricket Calling Behaviour: Implications for Female Mate Search and Mate Choice

Amount of calling activity (calling effort) is a strong determinant of male mating success in species such as orthopterans and anurans that use acoustic communication in the context of mating behaviour. While many studies in crickets have investigated the determinants of calling effort, patterns of variability in male calling effort in natural choruses remain largely unexplored. Within-individual variability in calling activity across multiple nights of calling can influence female mate search and mate choice strategies. Moreover, calling site fidelity across multiple nights of calling can also affect the female mate sampling strategy. We therefore investigated the spatio-temporal dynamics of acoustic signaling behaviour in a wild population of the field cricket species Plebeiogryllus guttiventris. We first studied the consistency of calling activity by quantifying variation in male calling effort across multiple nights of calling using repeatability analysis. Callers were inconsistent in their calling effort across nights and did not optimize nightly calling effort to increase their total number of nights spent calling. We also estimated calling site fidelity of males across multiple nights by quantifying movement of callers. Callers frequently changed their calling sites across calling nights with substantial displacement but without any significant directionality. Finally, we investigated trade-offs between within-night calling effort and energetically expensive calling song features such as call intensity and chirp rate. Calling effort was not correlated with any of the calling song features, suggesting that energetically expensive song features do not constrain male calling effort. The two key features of signaling behaviour, calling effort and call intensity, which determine the duration and spatial coverage of the sexual signal, are therefore uncorrelated and function independently.