Behavior Of Anurans Research Articles

The effects of anthropogenic noise on frogs housed on exhibit at a public aquarium.

Anuran behavior and reproduction are dominated by vocalizations, rendering them vulnerable to the effects of signal masking. For anurans on display in zoos and aquaria, a major source of ambient noise is visitors, which pose a unique source of potential anthropogenic signal masking. Call characteristics (total call duration, and minimum and maximum call frequencies) of three populations of dendrobatids (Dendrobates leucomelas, Epipedobates tricolor, and Ranitomeya imitator) on public display were investigated at time periods of increasing visitor-related noise (closed, off-peak, and peak aquarium visiting hours) to determine if there were changes in call characteristics that correlated with changes in visitor noise levels. The data revealed that call length increased with more visitor noise for D. leucomelas and E. tricolor, with their longest calls during peak hours, and all three species had their shortest calls during closed hours. Both minimum and maximum call frequencies increased with more visitor noise for E. tricolor and R. imitator, with their highest frequencies during peak hours, and lowest frequencies during closed hours. This study found evidence that anurans on public display adjust their vocalizations in the presence of visitor noise. These findings support expanded monitoring of ambient noise for animals on public display to determine if noise poses significant effects that might influence well-being or reproduction.

Seasonal Pattern of Advertisement Calling and Physiology in Prolonged Breeding Anurans, Japanese Tree Frog (Dryophytes japonicus).

The calling behavior of anurans should be studied in detail as it greatly influences their physiology and immunity, particularly in prolonged breeding species. The effect can be further complicated by the emergence timing in the breeding season. We conducted a study comparing the physiology and calling behavior of the Japanese tree frog (Dryophytes japonicus), a prolonged breeder species, according to the breeding timing. During the middle of the breeding season, a high chorus size appeared, indicating a breeding peak. However, chorus size did not dominate physiology and calling behavior. In the early breeding season, frogs had a high energy storage state and immunity. In the middle of the breeding season, individuals from the early breeding season were considered to have exhausted their energy stores and had low immunity. Towards the end of the breeding season, frogs appeared to have newly introduced, at which time energy stores and immunity were as high as in the beginning. However, unlike the physiology, the pattern of calling constantly varied as the breeding season progressed. Frogs from the early season conserved energy used for calling, and frogs from the late season showed a breeding spurt for mating. Our results can help in understanding the energy metabolism of calling behavior, physiology, and disease epidemiology in prolonged breeder species. They also suggest that individuals coordinate their participation in the breeding season and that the timing of their appearance at breeding sites may not be random.

An investigation of toe‐tapping behaviour in anurans by analysis of online video resources

AbstractToe‐tapping is a widespread anuran behaviour commonly associated with feeding where the anurans move the middle toes of their hind legs up and down. Previous studies have interpreted it as a pedal lure, a prey localization method and a stimulus used to transfix prey. A database of online videos was constructed in order to study this behaviour across species, with a particular focus on arrow poison frogs (Dendrobatidae); tapping occurrence, prey characteristics and environmental factors were recorded. The data collected include 19 species that have, as of yet, not been recorded to tap, 16 of which exhibit feeding‐related tapping, while in the three other species, tapping seemed to be related to courtship. Across dendrobatid species, a significant correlation was found between prey activity and the occurrence of tapping, which supports a prey localization hypothesis. The database proved to be a valid method of research as it provided a sample size large enough for detailed data analysis across the Dendrobatidae. The utility of the data was partially limited by the available number of observations per species and the inconsistency in video quality, however.

Neotropical dancing frog: the rich repertoire of visual displays in a hylodine species

During reproductive season, males usually must defend their territory against competitor males and attract females for reproduction. Acoustic signals evolved as an alternative to physical attacks, thus reducing injuries to both opponents during a territorial dispute, but they are also the primarily trait used by female frogs to select males. However, there is some recent evidence that visual signalling also can be important during social interactions in frogs. Here, for the first time, we describe the sophisticated visual behaviour of Hylodes meridionalis, a diurnal species that is endemic to the southern Atlantic Forest, where it inhabits fast streams. We submitted resident males to mirror self-image presentations to simulate the presence of an intruder male in their territories. Furthermore, we collected observations from close-range interactions between individuals of this very shy species. We observed seven types of visual displays: toe flagging (slow up-and-down movements of one or more toes), arm lifting (rapid up-and-down movements of one arm), leg lifting (rapid up-and-down movements of one leg), arm waving (lifting an arm and waving it in an arc), both legs kicking (rapidly stretching both hind limbs towards the back), foot flagging (slowly raising one hind limb in a semi-arch movement) and throat display (pulsation of one or both paired lateral vocal sacs without sound production). Only the kicking of both legs was displayed exclusively by females; toe flagging and foot flagging were displayed by males only during agonistic interactions. The frequency of visual displays (7 types, 117 events) was much greater than that of acoustic signals (3 types, 66 events). Our data demonstrate that the visual repertoire of the genus Hylodes is richer than previously noted and that visual display behaviour in anurans could be more common than previously believed. Therefore, this characterisation study aids our understanding of the function of the rich repertoire of visual displays in frog species and highlights that ethologists should be directing more of their attention towards this poorly explored anuran behaviour.

Ancestral state, phylogenetic signal and convergence among anuran distress calls

Past interactions between predators and prey have resulted in the emergence of numerous defensive mechanisms in the animal kingdom. Commonly reported in anurans (frogs and toads) are distress calls, which are vocalizations emitted while under attack that theoretically reduce predation risk by surprising or frightening the predator. Therefore, we would expect that the distress call is effective against a wide range of predators. In order to be effective against different predators, distress calls from different species must share common acoustic properties, and differ from advertisement calls, which are influenced by divergent selective pressures, safeguarding species recognition. Our hypothesis is that distress calls are more similar among related species than advertisement calls. In addition, distress calls are lacking in several unrelated phylogenetic groups or species. Therefore, it is unclear whether this attribute has been lost or evolved several times in the phylogeny of Anura. In order to test our hypothesis and to evaluate the evolution of distress calls, we used a combination of literature review, personal communications, and audio database assessment. Based on ancestral character estimation, we found that distress calls are an ancestral behavior in anurans, which carry phylogenetic signal. We also found more similarity comparing distress calls among species when we compared advertisement calls of the same group of species, suggesting that distress calls did not face divergent selective pressures. On the contrary, this attribute seems to have experienced convergent selection or neutral evolution. Finally, we found that body size determines the occurrence of distress calls in anurans, with smaller species lacking this behavior. We hypothesize that this may be because small body size may not allow for the production of long or loud enough calls to be effective against predators.

Do Bufonids Employ Different Anti-Predator Behaviors Than Ranids? Comparison among Three European Anurans

European anurans are prey for a variety of predators, against which they have evolved a range of defense behaviors. We investigated defensive behaviors of three European anurans: the Common Toad (Bufo bufo), the Common Frog (Rana temporaria), and the Edible Frog (Pelophylax esculentus) during interactions with a predator (hedgehog) and a control stimulus (rabbit). We hypothesized that (H1) due to small capacity to flee quickly from a predator, B. bufo has evolved a more diverse repertoire of behavioral defenses than the ranids, R. temporaria and P. esculentus. We also hypothesized that (H2) B. bufo can minimize the secretion of metabolically costly poison through behavioral control. According to our predictions, the repertoire of defensive behaviors was more complex in B. bufo than in the ranids. Also, the number of threatening behaviors was higher in toads than in both frog species. Fleeing was the most common response employed by all tested anurans. We report a new anti-predator behavior in the Common Toad: head hitting. As B. bufo released the poison only after squeezing of parotoid macroglands by the predator, we conclude that the Common Toad can minimize poison release through behavioral control. Our data suggest that length of hind-legs and, related to this, mode of locomotion (jumping vs. hopping) can affect anti-predator behavior in anurans.

Sound source localization and segregation with internally coupled ears: the treefrog model.

Acoustic signaling plays key roles in mediating many of the reproductive and social behaviors of anurans (frogs and toads). Moreover, acoustic signaling often occurs at night, in structurally complex habitats, such as densely vegetated ponds, and in dense breeding choruses characterized by high levels of background noise and acoustic clutter. Fundamental to anuran behavior is the ability of the auditory system to determine accurately the location from where sounds originate in space (sound source localization) and to assign specific sounds in the complex acoustic milieu of a chorus to their correct sources (sound source segregation). Here, we review anatomical, biophysical, neurophysiological, and behavioral studies aimed at identifying how the internally coupled ears of frogs contribute to sound source localization and segregation. Our review focuses on treefrogs in the genus Hyla, as they are the most thoroughly studied frogs in terms of sound source localization and segregation. They also represent promising model systems for future work aimed at understanding better how internally coupled ears contribute to sound source localization and segregation. We conclude our review by enumerating directions for future research on these animals that will require the collaborative efforts of biologists, physicists, and roboticists.

Lateralized Turning Biases in Two Neotropical Tadpoles

AbstractLateralized turning behavior in startle responses and upon descent after surfacing for a breath of air has been documented for tadpoles in several anuran species. A left‐handed preference is most common and was previously thought to be linked to the asymmetry in spiracle location. Here, we investigate the presence of behavioral asymmetries in tadpoles of Agalychnis callidryas and Leptodactylus melanonotus in explosive turns after air‐breathing. Data were also collected on lateralized posture in the orientation of tails of embryonic A. callidryas within the egg case, as well as the startle response of free‐swimming tadpoles exposed to mechanical stimulation. A left‐curled tail bias was found among several clutches from Costa Rica, but this was not the case among clutches examined from Panama. Free‐living tadpoles of L. melanonotus displayed a distinct right‐handed preference during explosive turns. While some tadpoles of A. callidryas were at stages too early to detect any explosive turns when breathing, later‐staged individuals did display a left‐handed bias in startle response to mechanical stimulation. Additionally, it appears that the expression of behavioral lateralization of larvae (but not embryos) may predict whether or not the adults exhibit similar lateralization. Findings herein provide insight into the ontogeny and evolutionary origins of lateralized behavior in anurans.

Acute changes in whole body corticosterone in response to perceived predation risk: A mechanism for anti-predator behavior in anurans?

Anuran larvae exhibit behavioral and morphological plasticity in response to perceived predation risk, although response type and magnitude varies through ontogeny. Increased baseline corticosterone is related to morphological response to predation risk, whereas the mechanism behind behavioral plasticity remains enigmatic. Since tadpoles alter behavioral responses to risk immediately upon exposure to predator cues, we characterized changes in whole body corticosterone at an acute (<1h post-exposure) timescale. Tadpoles (Lithobates sylvaticus) at Gosner stage (GS) 25 (free-swimming, feeding larvae) increased corticosterone levels to a peak at 10–20min post-exposure to predator cues, paralleling the acute stress response observed among other taxa. Tadpoles reared for 3weeks (mean GS29) with predation risk (caged, fed Aeshnid dragonfly nymph) had lower corticosterone levels at 10–20min post-exposure to dragonfly cues than predator-naïve controls, suggesting habituation, although the magnitude of increase was markedly diminished when compared to younger tadpoles (GS25). These experiments represent the first assessment of tadpole hormonal responses to predation risk at the acute timescale. Further research is required to establish causality between hormonal responses and behavioral changes, and to examine how and why responsiveness changes over ontogeny and with chronic exposure to risk.

How do males of Hypsiboas goianus (Hylidae: Anura) respond to conspecific acoustic stimuli?

Acoustic communication plays an important role in the social behavior of anurans. Acoustic signals, which can be used in different contexts such as mate attraction and territory defense, may mediate social interactions among individuals. Herein, we used playback experiments to test whether males of Hypsiboas goianus (Lutz, 1968) change their vocal behavior in response to conspecific advertisement calls. Specifically, we used different field playback experiments in which we modified the time interval between advertisement calls to simulate males with distinct states of motivation (Sequence A and B). We did not observe differences in the acoustic response of males of H. goianus between the two types of field playback experiments. On the other hand, we observed that H. goianus males reduce the dominant frequency of the advertisement call and increase the rate of aggressive calls in response to a conspecific competitor. Our results suggest that the acoustic plasticity observed in males of H. goianus represents an aggressive response that allows repelling conspecific individuals.

Gray tree frogs, Hyla versicolor, give lower-frequency aggressive calls in more escalated contests

As animal contests escalate, variation in the performance of aggressive signaling behaviors can give important insights into contest dynamics. In anuran amphibians, males of numerous species utilize distinctive aggressive vocalizations during disputes over calling spaces. Little is known, however, about the causes and consequences of variation in aggressive-call characteristics. We analyzed recordings of calls made during staged aggressive interactions between male gray tree frogs, Hyla versicolor, to determine how variation in a key aggressive-call characteristic, dominant frequency, was affected by increasing contest escalation. We found that dominant frequencies of aggressive calls were lower than those of advertisement calls used to attract females. Furthermore, we found that males lowered their aggressive-call frequencies with increases in escalation. Winners tended to have lower-frequency aggressive calls than losers. We conclude that aggressive calls in H. versicolor are similar to the graded aggressive calls that have been described in several other species. This gradation may allow males to balance the energetic costs of producing lower-frequency calls with the benefits of efficiently repelling rival males. Other processes related to motivation and the physiological effects of participating in contests may also be responsible for the observed variation in aggressive-call frequency with contest escalation. Our results demonstrate that detailed experimental studies of aggressive calling behavior in anurans, which to this point have rarely been performed, are feasible and generate important insights relating to general problems in animal contest behavior and animal communication.

Ultrasonic frogs show extraordinary sex differences in auditory frequency sensitivity

AbstractAcoustic communication plays an important role in the reproductive behavior of anurans. Males of concave-eared torrent frog (_Odorrana tormota_) have ultrasonic communication capacity 1, 2, but it is unknown whether females communicate with ultrasound. Here we show that O. tormota exhibits great sex differences in the auditory frequency sensitivity. Acoustic playback experiments demonstrated that the male's advertisement calls evoke gravid females' positive phonotaxis and vocal responses, whereas ultrasonic components of the male's calls (frequencies above 20 kHz) do not elicit female phonotaxis or vocalization. The behavioral study was complemented by electrophysiological recordings from the auditory midbrain and by laser Doppler vibrometer measurements of the tympanic membrane's response to acoustic stimuli. These measurements revealed that females have an upper frequency limit up to 16 kHz (threshold 107 dB SPL) and no ultrasound sensitivity, unlike males which have an upper frequency limit of up to 35 kHz (87 dB SPL). Single units in the female auditory midbrain have the best excitatory frequencies (BEFs) peaked around 5 kHz, corresponding to the fundamental frequency (F0) of male's most calls, whereas the male auditory midbrain units have BEFs mostly above 8 kHz, largely consistent with the F0 of female courtship calls. Females have a frequency sensitive bandwidth (10 dB above threshold) ranged from 2 to 6 kHz, narrower than that males have (5-20 kHz). The velocity amplitude of the tympanic membranes peaked around 5 kHz in females, whereas 7 kHz in males. The results suggest that the frog species O. tormota is an example of a vertebrate, which demonstrates well phonotaxis and extraordinary sex differences in hearing.

Lack of phylogenetic signal in the variation in anuran microhabitat use in southeastern Brazil

Microhabitat use is an important component of anuran behavior in both the tadpole and the adult stages. It is potentially influenced by phylogeny and extant ecological factors acting as selective pressures, such as predation, competition, or physical habitat properties. We aimed to test whether patterns of microhabitat use vary among species, habitats and sites, and how much of this variation can be explained by phylogenetic relatedness. We collected data on microhabitat use at five different sites, where we obtained a total of 4,230 records of individual tadpoles of 34 species in 15 genera and 7 families, and a total of 1,163 records of adult individuals of 39 species in 16 genera and 8 families. Mantel tests conducted to relate species dissimilarities in microhabitat use and phylogenetic relatedness indicated a weak but significant relationship for adult anurans, and no relationship for tadpoles. Our results suggest that microhabitat use is a plastic and variable trait, overcoming phylogenetic signal in tadpoles. In adult anurans, very little of the variation in microhabitat use can be explained by phylogenetic relatedness. Microhabitat use is not a good predictor of phylogeny, but it may be a very interesting subject to study natural selection and adaptation.

Conservation management implications of substrate choice in recently metamorphosed American toads (Bufo americanus)

We experimentally examined the choice of three substrate types by American toad (Bufo americanus) metamorphs. Metamorphs clearly preferred deciduous leaf litter over coniferous leaf litter and bare soil, and coniferous leaf litter over bare soil. These results emphasize that modification of terrestrial habitats surrounding breeding ponds can impact anuran behavior and populations.

A Prey Catching and Predator Avoidance Neural-Schema Architecture for Single and Multiple Robots

The paper presents a biologically inspired multi-level neural-schema architecture for prey catching and predator avoidance in single and multiple autonomous robotic systems. The architecture is inspired on anuran (frogs and toads) neuroethological studies and wolf pack group behaviors. The single robot architecture exploits visuomotor coordination models developed to explain anuran behavior in the presence of preys and predators. The multiple robot architecture extends the individual prey catching and predator avoidance model to experiment with group behavior. The robotic modeling architecture distinguishes between higher-level schemas representing behavior and lower-level neural structures representing brain regions. We present results from single and multiple robot experiments developed using the NSL/ASL/MIRO system and Sony AIBO ERS-210 robots.

Externally Attached Radio-Transmitters Have Limited Effects on the Antipredator Behavior and Vagility of Rana Pipiens and Rana Sylvatica

Anurans display a variety of antipredator behaviors from flight and crypsis to defensive postures. External attachment of a radio-transmitter is a commonly used technique that could potentially interfere with the antipredator behavior of anurans. We investigated the effect of an externally attached radio-transmitter on the antipredator behavior and vagility of adult Northern Leopard Frogs (Rana pipiens) and adult Wood Frogs (Rana sylvatica). We simulated attacks by birds and snakes and used fluorescent powder to follow the path of individuals through natural habitats. Both species displayed a different frequency of behaviors in response to each predator, but the presence of a transmitter did not affect the frequency of antipredator behaviors. When carrying a transmitter, R. pipiens exhibited a different escape angle during attacks by simulated aerial predators and exhibited a change in the mean turn angle over 4-h movement paths. Rana sylvatica's escape behavior and vagility were unaffected by a transmitter during simulated attacks, although frogs with a transmitter did take more jumps per 4-h movement paths and followed straighter paths than did frogs without a transmitter. The body mass of the individual did not affect any of our behavior or movement metrics. Although most of our metrics did not change markedly in response to the presence of a transmitter, the subtle changes in vagility and escape behavior are analogous to the negative effects of externally attached transmitters seen in birds and mammals. These results suggest that transmitters may have consequences for the energetics, survival, and reproduction of anurans.

DC electrical stimulation of the pretectal thalamus and its effects on the feeding behavior of the toad (Bufo bufo)

The feeding motivation of the common European common toad (Bufo bufo) can be quantified by the feeding sequence of arousal-orientation-approach-fixate-snap. Previous work has found that the optic tectum is an important structure responsible for the mediation of feeding behaviors, and combined electrical and visual stimulation of the optic tectum was found to increase the animals feeding behaviors. However, the pretectal thalamus has an inhibitory influence upon the optic tectum and its lesion results in disinhibited feeding behaviors. This suggests that feeding behavior of anurans is also subject to influence from the pretectal thalamus. Previous studies involving the application of DC stimulation to brain tissue has generated slow potential shifts and these shifts have been implicated in the modulation of the neural mechanisms associated with behavior. The current study investigated the application of DC stimulation to the diencephalon surface dorsal to the lateral posterodorsal pretectal thalamic nucleus in Bufo bufo, in order to assess effects on feeding motivation. The application of DC stimulation increased the incidence of avoidance behaviors to a visual prey stimulus while reducing the prey catching behavior component of approach, suggesting that the DC current applied to the pretectum increased the inhibition upon the feeding elements of the optic tectum. This can be explained by the generation of slow potential shifts.

A GENERAL CLASS OF MULTINOMIAL MIXTURE MODELS FOR ANURAN CALLING SURVEY DATA

We propose a general framework for modeling anuran abundance using data collected from commonly used calling surveys. The data generated from calling surveys are indices of calling intensity (vocalization of males) that do not have a precise link to actual population size and are sensitive to factors that influence anuran behavior. We formulate a model for calling-index data in terms of the maximum potential calling index that could be observed at a site (the “latent abundance class”), given its underlying breeding population, and we focus attention on estimating the distribution of this latent abundance class. A critical consideration in estimating the latent structure is imperfect detection, which causes the observed abundance index to be less than or equal to the latent abundance class. We specify a multinomial sampling model for the observed abundance index that is conditional on the latent abundance class. Estimation of the latent abundance class distribution is based on the marginal likelihood of the index data, having integrated over the latent class distribution. We apply the proposed modeling framework to data collected as part of the North American Amphibian Monitoring Program (NAAMP).

6-hydroxydopamine lesions in anuran amphibians: a new model system for Parkinson's disease?

We investigated the effects of dopamine depletion on acoustically guided behavior of anurans by conducting phonotaxis experiments with female gray treefrogs (Hyla versicolor) before and 90 min after bilateral injections of 3, 6, or 12 microg 6-hydroxydopamine (6-OHDA) into the telencephalic ventricles. In experiments with one loudspeaker playing back a standard artificial mating call, we analyzed the effects of 6-OHDA on phonotactic response time. In choice tests we measured the degree of distraction from the standard call (20 pulses/s) by three different variants with altered pulse-rate (30/s, 40/s, 60/s). Five days after experiments, brains were immunostained for tyrosine hydroxylase. Labeled neurons were counted in the suprachiasmatic nucleus, posterior tuberculum, interpeduncular nucleus, and locus coeruleus, and correlation between neuronal numbers and behavioral scores was tested. Response times increased together with 6-OHDA concentrations, which was mainly due to longer immobile periods before the animals started movement. In choice tests the most irrelevant stimulus (60/s) distracted 6-OHDA injected females from the standard stimulus, while sham injected controls were undistracted. The number of catecholaminergic neurons decreased with increasing 6-OHDA concentration in the suprachiasmatic nucleus, posterior tuberculum, and interpeduncular nucleus. The normalized number of immunoreactive neurons in the posterior tuberculum was positively correlated with phonotaxis scores in the one-speaker test, demonstrating that motor deficits are a function of tubercular cell loss. We conclude that bilateral 6-OHDA lesions in anuran amphibians cause motor (difficulty to start movements) as well as cognitive symptoms (higher distraction by irrelevant stimuli) that have also been described for human Parkinson patients.

Steroid hormone profiles and relative body condition of calling and satellite toads: implications for proximate regulation of behavior in anurans

Males of most anuran species (frogs and toads) vocalize to attract mates. However, individuals of many vocal species may also adopt alternative noncalling ‘‘satellite’’ tactics. Satellite males characteristically remain in close proximity to calling conspecifics and attempt to intercept incoming females attracted to advertising males. Emerson proposed that alternation between calling and noncalling behavior in anurans is mediated by a reciprocal interaction between circulating levels of corticosterone and androgens that is driven by depletion of energy reserves during vocalization. We tested this hypothesis by examining steroid hormone profiles and the relative body condition of calling and satellite Woodhouse’s toads (Bufo woodhousii) and Great Plains toads (B. cognatus). Consistent with Emerson’s hypothesis, callers had significantly higher circulating corticosterone levels and were in better condition than satellites. However, levels of testosterone and dihydrotestosterone did not differ significantly between satellites and callers, and we found no evidence that high levels of corticosterone had an inhibitory effect on androgen production in either species. These data thus support a relationship between corticosterone levels and depletion of energy reserves during bouts of vocalization but suggest that alternation between calling and satellite behavior may be associated with direct effects of corticosterone on brain vocal control centers. We propose a model that incorporates relationships among energy reserves, androgens, corticosterone, and arginine vasotocin-producing neurons in the telencephalon to explain transitions between calling and satellite tactics in toads. Key words: alternative mating tactics, anurans, body condition, hormones, satellite behavior, steroids. [Behav Ecol 15:313–320 (2004)]