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the effects of spatially separated call components on phonotaxis in túngara frogs: evidence for auditory grouping.numerous animals across disparate taxa must identify and locate complex acoustic signals imbedded in multiple overlapping signals and ambient noise. a requirement of this task is the ability to group sounds into auditory streams in which sounds are perceived as emanating from the same source. although numerous studies over the past 50 years have examined aspects of auditory grouping in humans, surprisingly few assays have demonstrated auditory stream formation or the assignment of multicomponent ...200212417822
mosaic evolution of neural development in anurans: acceleration of spinal cord development in the direct developing frog eleutherodactylus coqui.previous studies have shown that spinal cord development in direct developing frogs of the genus eleutherodactylus, which have evolutionarily lost the tadpole stage, differs from that in biphasically developing anurans (with the larval and the adult stage separated by metamorphosis). the present study of spinal cord development in eleutherodactylus coqui provides additional information about neurogenesis, neuronal differentiation and growth analyzed by immunostaining for proliferating cell nucle ...200312592573
morphometric relationships of take-off speed in anuran amphibians.locomotory speed correlates with muscle mass (determining force and stride rate), limb length (stride rate and distance), and laterally compressed body trunk (force and stride distance). to delineate generalization of the locomotory-morphometric relationships specifically in anuran amphibians, we investigated take-off speed and the three morphological variables from seven species, rana nigromaculata, r. rugosa, and bombina orientalis, eleuthrodectilus fitzingeri, e. diastema, bufo typhonius, col ...200312975797
hormonal state influences aspects of female mate choice in the túngara frog (physalaemus pustulosus).females alter their mate choices as they transition through different reproductive stages; however, the proximal mechanisms for such behavioral fluctuation are unclear. in many taxa, as females transition through different reproductive stages, there is an associated change in hormone levels; therefore, we examined whether fluctuation in hormone levels serves as a proximal mechanism for within-individual variation in mate choice in female túngara frogs (physalaemus pustulosus). we manipulated hor ...200616277986
development of the retinotectal system in the direct-developing frog eleutherodactylus coqui in comparison with other anurans.abstract:200818573199
estradiol induces sexual behavior in female túngara frogs.steroid hormones play an important role in regulating vertebrate sexual behavior. in frogs and toads, injections of exogenous gonadotropins, which stimulate steroid hormone production, are often used to induce reproductive behavior, but steroid hormones alone are not always sufficient. to determine which hormonal conditions promote sexual behavior in female túngara frogs, we assessed the effect of hormone manipulation on the probability of phonotaxis behavior toward conspecific calls in post-rep ...200918840446
sexual differences in prevalence of a new species of trypanosome infecting túngara frogs.trypanosomes are a diverse group of protozoan parasites of vertebrates transmitted by a variety of hematophagous invertebrate vectors. anuran trypanosomes and their vectors have received relatively little attention even though these parasites have been reported from frog and toad species worldwide. blood samples collected from túngara frogs (engystomops pustulosus), a neotropical anuran species heavily preyed upon by eavesdropping frog-biting midges (corethrella spp.), were examined for trypanos ...201626977404
major histocompatibility complex selection dynamics in pathogen-infected túngara frog (physalaemus pustulosus) populations.pathogen-driven selection can favour major histocompatibility complex (mhc) alleles that confer immunological resistance to specific diseases. however, strong directional selection should deplete genetic variation necessary for robust immune function in the absence of balancing selection or challenges presented by other pathogens. we examined selection dynamics at one mhc class ii (mhc-ii) locus across panamanian populations of the túngara frog, physalaemus pustulosus, infected by the amphibian ...201627531158
spread of amphibian chytrid fungus across lowland populations of túngara frogs in panamá.chytridiomycosis, caused by the fungal pathogen batrachochytrium dendrobatidis (bd), is an emergent infectious disease partially responsible for worldwide amphibian population declines. the spread of bd along highland habitats (> 500 meters above sea level, m a.s.l.) of costa rica and panamá is well documented and has been linked to amphibian population collapses. in contrast, data are scarce on the prevalence and dispersal of bd in lowland habitats where amphibians may be infected but asymptoma ...201627176629
acute toxicity and sublethal effects of the mixture glyphosate (roundup active) and cosmo-flux 411f to anuran embryos and tadpoles of four colombian species.glyphosate is the most widely used herbicide in the world with application in agriculture, forestry, industrial weed control, garden and aquatic environments. however, its use is highly controversial for the possible impact on not-target organisms, such as amphibians, which are vanishing at an alarming and rapid rate. due to the high solubility in water and ionic nature, the glyphosate requires of surfactants to increase activity. in addition, for the control of coca (erythroxylum coca) and agri ...201526299127
toxicity of formulated glyphosate (glyphos) and cosmo-flux to larval colombian frogs 1. laboratory acute toxicity.the spraying of coca (erythroxylum coca) with glyphosate in colombia has raised concerns about possible impacts on amphibians. there are few toxicity data for species other than those from temperate regions, and these have not been generated with the combination of formulated glyphosate (glyphos) and the adjuvant, cosmo-flux (coca mix) as used in coca control in colombia. in order to characterize toxicity of the spray mixture to frogs from colombia, gosner stage-25 tadpoles of scinax ruber, dend ...200919672764
collateral damage or a shadow of safety? the effects of signalling heterospecific neighbours on the risks of parasitism and predation.although males often display from mixed-species aggregations, the influence of nearby heterospecifics on risks associated with sexual signalling has not been previously examined. we tested whether predation and parasitism risks depend on proximity to heterospecific signallers. using field playback experiments with calls of two species that often display from the same ponds, túngara frogs and hourglass treefrogs, we tested two hypotheses: (1) calling near heterospecific signallers attractive to e ...201627194694
multimodal cues improve prey localization under complex environmental conditions.predators often eavesdrop on sexual displays of their prey. these displays can provide multimodal cues that aid predators, but the benefits in attending to them should depend on the environmental sensory conditions under which they forage. we assessed whether bats hunting for frogs use multimodal cues to locate their prey and whether their use varies with ambient conditions. we used a robotic set-up mimicking the sexual display of a male túngara frog (physalaemus pustulosus) to test prey assessm ...201526336176
risks of multimodal signaling: bat predators attend to dynamic motion in frog sexual displays.many sexual displays contain multiple components that are received through a variety of sensory modalities. primary and secondary signal components can interact to induce novel receiver responses and become targets of sexual selection as complex signals. however, predators can also use these complex signals for prey assessment, which may limit the evolution of elaborate sexual signals. we tested whether a multimodal sexual display of the male túngara frog (physalaemus pustulosus) increases preda ...201425165134
risky ripples allow bats and frogs to eavesdrop on a multisensory sexual display.animal displays are often perceived by intended and unintended receivers in more than one sensory system. in addition, cues that are an incidental consequence of signal production can also be perceived by different receivers, even when the receivers use different sensory systems to perceive them. here we show that the vocal responses of male túngara frogs (physalaemus pustulosus) increase twofold when call-induced water ripples are added to the acoustic component of a rival's call. hunting bats ...201424458640
do frog-eating bats perceptually bind the complex components of frog calls?the mating calls of male túngara frogs, physalaemus pustulosus, attract intended (conspecific females) and unintended (eavesdropping predators and parasites) receivers. the calls are complex, having two components: a frequency-modulated "whine" followed by 0-7 harmonic bursts or "chucks". the whine is necessary and sufficient to elicit phonotaxis from females and the chuck enhances call attractiveness when it follows a whine. although chucks are never made alone, females perceptually bind the wh ...201323322446
sequential assessment of prey through the use of multiple sensory cues by an eavesdropping bat.predators are often confronted with a broad diversity of potential prey. they rely on cues associated with prey quality and palatability to optimize their hunting success and to avoid consuming toxic prey. here, we investigate a predator's ability to assess prey cues during capture, handling, and consumption when confronted with conflicting information about prey quality. we used advertisement calls of a preferred prey item (the túngara frog) to attract fringe-lipped bats, trachops cirrhosus, th ...201222592417
signal perception in frogs and bats and the evolution of mating signals.psychophysics measures the relationship between a stimulus's physical magnitude and its perceived magnitude. because decisions are based on perception of stimuli, this relationship is critical to understanding decision-making. we tested whether psychophysical laws explain how female túngara frogs (physalaemus pustulosus) and frog-eating bats (trachops cirrhosus) compare male frog calls, and how this imposes selection on call evolution. although both frogs and bats prefer more elaborate calls, th ...201121817052
evaluating the diversity of neotropical anurans using dna barcodes.this study tested the effectiveness of coi barcodes for the discrimination of anuran species from the amazon basin and other neotropical regions. barcodes were determined for a total of 59 species, with a further 58 species being included from genbank. in most cases, distinguishing species using the barcodes was straightforward. each species had a distinct coi barcode or codes, with intraspecific distances ranging from 0% to 9.9%. however, relatively high intraspecific divergence (11.4-19.4%) wa ...201628138277
evolution of nerve development in frogs. ii. modified development of the peripheral nervous system in the direct-developing frog eleutherodactylus coqui (leptodactylidae).we use whole-mount immunohistochemistry to describe the pattern of development of cranial nerves and muscles in the direct-developing leptodactylid frog eleutherodactylus coqui. comparison with nerve development in the biphasically developing frogs physalaemus pustulosus (leptodactylidae) and discoglossus pictus (discoglossidae; described in a companion paper) allows us to infer the ancestral leptodactylid ontogenetic pattern and the extent to which it has been modified during the evolution of d ...19979261555
embryogenesis and laboratory maintenance of the foam-nesting túngara frogs, genus engystomops (= physalaemus).the vast majority of embryological research on amphibians focuses on just a single genus of frogs, xenopus. to attain a more comprehensive understanding of amphibian development, experimentation on non-model frogs will be essential. here, we report on the early development, rearing, and embryological analysis of túngara frogs (genus engystomops, also called physalaemus). the frogs engystomops pustulosus, engystomops coloradorum, and engystomops randi construct floating foam-nests with small eggs ...200919384855
environmental conditions limit attractiveness of a complex sexual signal in the túngara frog.animals choosing particular display sites often balance sexual and natural selection pressures. here we assess how physical properties of display sites can alter this balance by influencing signal production and attractiveness of the túngara frog (physalaemus pustulosus). males that call from very shallow water bodies (few mm depth) benefit from reduced predation risk, but by manipulating water levels, we show that this comes at a cost of reduced attractiveness to females. our data show that cal ...201729192162
neurobiology of female mate choice in frogs: auditory filtering and valuation.mate choice is a decision making process with profound implication for the reproductive success of both the sender and the chooser. preferences for conspecific over heterospecific males and for some conspecifics over others are typically mediated by a female's response to signals produced by males. and although one can experimentally describe a female's preference function, there is relatively little understood about the neural mechanisms mediating these preferences. in anurans, mating preferenc ...201729048536
modeling sexual selection in túngara frog and rationality of mate choice.the males of the species of frogs engystomops pustulosus produce simple and complex calls to lure females, as a way of intersexual selection. complex calls lead males to a greater reproductive success than what simple calls do. however, the complex calls are also more attractive to their main predator, the bat trachops cirrhosus. therefore, as m. ryan suggests in (the túngara frog: a study in sexual selection and communication. university of chicago press, chicago, 1985), the complexity of the c ...201728983864
perceived synchrony of frog multimodal signal components is influenced by content and order.multimodal signaling is common in communication systems. depending on the species, individual signal components may be produced synchronously as a result of physiological constraint (fixed) or each component may be produced independently (fluid) in time. for animals that rely on fixed signals, a basic prediction is that asynchrony between the components should degrade the perception of signal salience, reducing receiver response. male túngara frogs, physalaemus pustulosus, produce a fixed multis ...201728582535
low temperature tolerance, cold hardening and acclimation in tadpoles of the neotropical túngara frog (engystomops pustulosus).many frogs from temperate climates can tolerate low temperatures and increase their thermal tolerance through hardening and acclimation. most tropical frogs, on the other hand, fail to acclimate to low temperatures. this lack of acclimation ability is potentially due to lack of selection pressure for acclimation because cold weather is less common in the tropics. we tested the generality of this pattern by characterizing the critical temperature minimum (ctmin), hardening, and acclimation respon ...201728477909
adsorption of the natural protein surfactant rsn-2 onto liquid interfaces.to stabilize foams, droplets and films at liquid interfaces a range of protein biosurfactants have evolved in nature. compared to synthetic surfactants, these combine surface activity with biocompatibility and low solution aggregation. one recently studied example is rsn-2, a component of the foam nest of the frog engystomops pustulosus, which has been predicted to undergo a clamshell-like opening transition at the air-water interface. using atomistic molecular dynamics simulations and surface t ...201728289744
vasotocin induces sexually dimorphic effects on acoustically-guided behavior in a tropical frog.the neuropeptide arginine vasotocin (avt) promotes sexual advertisement and influences vocalization structure in male anuran amphibians. in the present study, we used wild túngara frogs (physalaemus pustulosus) to investigate the effects of avt on phonotaxis in males and females-thereby controlling for potential task differences between the sexes. using a combined within- and between-subjects design, we showed that acoustic choice behavior in female frogs is not influenced by injection per se (v ...201728283755
schema vs. primitive perceptual grouping: the relative weighting of sequential vs. spatial cues during an auditory grouping task in frogs.perceptually, grouping sounds based on their sources is critical for communication. this is especially true in túngara frog breeding aggregations, where multiple males produce overlapping calls that consist of an fm 'whine' followed by harmonic bursts called 'chucks'. phonotactic females use at least two cues to group whines and chucks: whine-chuck spatial separation and sequence. spatial separation is a primitive cue, whereas sequence is schema-based, as chuck production is morphologically cons ...201728197725
light and noise pollution interact to disrupt interspecific interactions.studies on the consequences of urbanization often examine the effects of light, noise, and heat pollution independently on isolated species providing a limited understanding of how these combined stressors affect species interactions. here, we investigate how these factors interact to affect parasitic frog-biting midges (corethrella spp.) and their túngara frog (engystomops pustulosus) hosts. a survey of túngara frog calling sites revealed that frog abundance was not significantly correlated wit ...201728170099
the conformation of interfacially adsorbed ranaspumin-2 is an arrested state on the unfolding pathway.ranaspumin-2 (rsn-2) is a surfactant protein found in the foam nests of the túngara frog. previous experimental work has led to a proposed model of adsorption that involves an unusual clam-shell-like unhinging of the protein at an interface. interestingly, there is no concomitant denaturation of the secondary structural elements of rsn-2 with the large-scale transformation of its tertiary structure. in this work we use both experiment and simulation to better understand the driving forces underp ...201627558717
wind- and rain-induced vibrations impose different selection pressures on multimodal signaling.the world is a noisy place, and animals have evolved a myriad of strategies to communicate in it. animal communication signals are, however, often multimodal; their components can be processed by multiple sensory systems, and noise can thus affect signal components across different modalities. we studied the effect of environmental noise on multimodal communication in the túngara frog (physalaemus pustulosus). males communicate with rivals using airborne sounds combined with call-induced water r ...201627501086
mixed sex effects on the second-to-fourth digit ratio of túngara frogs (engystomops pustulosus) and cane toads (rhinella marina).sexual dimorphism in the ratio of digit lengths has been correlated to behavioral, physiological, and morphological traits in a variety of taxa. while sexual dimorphism in the second-to-fourth digit length ratio (2d:4d) is a well-established indicator of prenatal androgen exposure in mammals, investigations into the patterns of 2d:4d and the drivers of such variation in other taxa are lacking. we used linear mixed effects models to gain a mechanistic understanding of the factors that drive varia ...201626815928
female túngara frogs do not experience the continuity illusion.in humans and some nonhuman vertebrates, a sound containing brief silent gaps can be rendered perceptually continuous by inserting noise into the gaps. this so-called "continuity illusion" arises from a phenomenon known as "auditory induction" and results in the perception of complete auditory objects despite fragmentary or incomplete acoustic information. previous studies of auditory induction in gray treefrogs (hyla versicolor and h. chrysoscelis) have demonstrated an absence of this phenomeno ...201626692450
effects of estradiol on neural responses to social signals in female túngara frogs.estradiol plays an important role in mediating changes in female sexual behavior across reproductive cycles. in the túngara frog [physalaemus (=engystomops) pustulosus], the relationship between gonadal activity and female sexual behavior, as expressed by phonotaxis, is mediated primarily by estradiol. estradiol receptors are expressed in auditory and motivational brain areas and the hormone could serve as an important modulator of neural responses to conspecific calls. to better understand how ...201526449971
consequences of life history switch point plasticity for juvenile morphology and locomotion in the túngara frog.many animals with complex life cycles can cope with environmental uncertainty by altering the timing of life history switch points through plasticity. pond hydroperiod has important consequences for the fitness of aquatic organisms and many taxa alter the timing of life history switch points in response to habitat desiccation. for example, larval amphibians can metamorphose early to escape drying ponds. such plasticity may induce variation in size and morphology of juveniles which can result in ...201526417546
sexual selection. irrationality in mate choice revealed by túngara frogs.mate choice models derive from traditional microeconomic decision theory and assume that individuals maximize their darwinian fitness by making economically rational decisions. rational choices exhibit regularity, whereby the relative strength of preferences between options remains stable when additional options are presented. we tested female frogs with three simulated males who differed in relative call attractiveness and call rate. in binary choice tests, females' preferences favored stimulus ...201526315434
ultrastructural evidence of serous gland polymorphism in the skin of the tungara frog engystomops pustulosus (anura leptodactylidae).three types of serous products were detected in the syncytial cutaneous glands of the leptodactylid tungara frog, engystomops pustulosus: type ia, granules with wide halos and variable density cores; type ib, high density granules without halos; and type ii, vesicles containing a finely dispersed product. ultrastructural evidence revealed that these products were manufactured by different serous gland types and excluded that they represented different steps in the secretory cycle of a single gla ...201526080618
danger comes from all fronts: predator-dependent escape tactics of túngara frogs.the escape response of an organism is generally its last line of defense against a predator. because the effectiveness of an escape varies with the approach behaviour of the predator, it should be advantageous for prey to alter their escape trajectories depending on the mode of predator attack. to test this hypothesis we examined the escape responses of a single prey species, the ground-dwelling túngara frog (engystomops pustulosus), to disparate predators approaching from different spatial plan ...201525874798
crossmodal comparisons of signal components allow for relative-distance assessment.animals have multiple senses through which they detect their surroundings and often integrate sensory information across different modalities to generate perceptions. animal communication, likewise, often consists of signals containing stimuli processed by different senses. stimuli with different physical forms (i.e., from different sensory modalities) travel at different speeds. as a consequence, multimodal stimuli simultaneously emitted at a source can arrive at a receiver at different times. ...201425042586
the mechanism of sound production in túngara frogs and its role in sexual selection and speciation.sexual communication can evolve in response to sexual selection, and it can also cause behavioral reproductive isolation between populations and thus drive speciation. anurans are an excellent system to investigate these links between behavior and evolution because we have detailed knowledge of how neural mechanisms generate behavioral preferences for calls and how these preferences then generate selection on call variation. but we know far less about the physical mechanisms of call production, ...201425033110
harmonic calls and indifferent females: no preference for human consonance in an anuran.the human music faculty might have evolved from rudimentary components that occur in non-human animals. the evolutionary history of these rudimentary perceptual features is not well understood and rarely extends beyond a consideration of vertebrates that possess a cochlea. one such antecedent is a preferential response to what humans perceive as consonant harmonic sounds, which are common in many animal vocal repertoires. we tested the phonotactic response of female túngara frogs (physalaemus pu ...201424990679
interactions of multisensory components perceptually rescue túngara frog mating signals.sexual signals are often complex and perceived by multiple senses. how animals integrate signal components across sensory modalities can influence signal evolution. here we show that two relatively unattractive signals that are perceived acoustically and visually can be combined in a pattern to form a signal that is attractive to female túngara frogs. such unanticipated perceptual effects suggest that the evolution of complex signals can occur by alteration of the relationships among already-exi ...201323744778
robots in the service of animal behavior.as reading fiction can challenge us to better understand fact, using fake animals can sometimes serve as our best solution to understanding the behavior of real animals. the use of dummies, doppelgangers, fakes, and physical models have served to elicit behaviors in animal experiments since the early history of behavior studies, and, more recently, robotic animals have been employed by researchers to further coax behaviors from their study subjects. here, we review the use of robots in the servi ...201223181162
development of communication behaviour: receiver ontogeny in túngara frogs and a prospectus for a behavioural evolutionary development.most studies addressing the development of animal communication have focused on signal production rather than receiver decoding, and similar emphasis has been given to learning over nonlearning. but receivers are an integral part of a communication network, and nonlearned mechanisms appear to be more ubiquitous than learned ones in the communication systems of most animals. here we review the results of recent experiments and outline future directions for integrative studies on the development o ...201222649307
developmental expression of sex steroid- and thyroid hormone-related genes and their regulation by triiodothyronine in the gonad-mesonephros of a neotropical frog, physalaemus pustulosus.gonadal differentiation in frogs is affected by sex steroids and thyroid hormones (ths); however, the genes controlling differentiation and the molecular effects of ths in the gonad are not clear and have only been investigated in a few anuran species. in this study, we established developmental profiles and th regulation of sex steroid- and th-related genes in the gonad-mesonephros complex (gmc) of the túngara frog (physalaemus pustulosus), and compared the results to our previous research in a ...201222487252
developmental profiles and thyroid hormone regulation of brain transcripts in frogs: a species comparison with emphasis on physalaemus pustulosus.in amphibians, thyroid hormones (ths) are considered key regulators of brain remodeling during metamorphosis, while sex steroids (estrogens and androgens) control sexual differentiation and gonadal development. however, these two endocrine axes can interact during tadpole brain development. previously, we demonstrated that ths affect sex steroid-related gene expression in the developing brain of silurana tropicalis and rana pipiens; however, the gene expression changes differed between species. ...201222142812
auditory selectivity for acoustic features that confer species recognition in the tungara frog.in anurans, recognition of species-specific acoustic signals is essential to finding a mate. in many species, behavioral tests have elucidated which acoustic features contribute to species recognition, but the mechanisms by which the brain encodes these species-specific signal components are less well understood. the túngara frog produces a `whine' mating call that is characterized by a descending frequency sweep. however, much of the signal is unnecessary for recognition, as recognition behavio ...201121832134
relative comparisons of call parameters enable auditory grouping in frogs.whereas many studies on mate choice have measured the relative attractiveness of acoustic sexual signals, there is little understanding of another critical process: grouping and assigning the signals to their sources. for female túngara frogs, assigning the distinct components of male calls to the correct source is a challenge because males sing in aggregations, producing overlapping calls that lead to perceptual errors analogous to those of the 'cocktail party problem'. here we show that for pr ...201121811239
the brain as a source of selection on the social niche: examples from the psychophysics of mate choice in túngara frogs.the main premise of this article is that various cognitive functions involved in signal analysis, memory, and decision making, all modulated by the animal's internal milieu, can generate selection for the forms of signals used in social interactions. thus, just as an animal's view of its world, its umwelt, determines how it interacts with its ecological niche, it can influence the evolution of its social niche. thus, the brain is not only a landscape on which selection can act, but also it is a ...201121771854
multimodal signal variation in space and time: how important is matching a signal with its signaler?multimodal signals (acoustic+visual) are known to be used by many anuran amphibians during courtship displays. the relative degree to which each signal component influences female mate choice, however, remains poorly understood. in this study we used a robotic frog with an inflating vocal sac and acoustic playbacks to document responses of female túngara frogs to unimodal signal components (acoustic and visual). we then tested female responses to a synchronous multimodal signal. finally, we test ...201121307068
neural distribution of the nuclear progesterone receptor in the túngara frog, physalaemus pustulosus.the gonadal steroid hormone progesterone plays an important role across all vertebrates in mediating female reproductive physiology and behavior. many effects of progesterone are mediated by a nuclear progesterone receptor (pr), which is crucial for integration of external signals and internal physiological cues in the brain to produce an appropriate behavioral output. the túngara frog, physalaemus pustulosus, is an excellent model system for the study of mechanisms by which sensory signals, suc ...201121256209
characterization of the dopamine system in the brain of the túngara frog, physalaemus pustulosus.dopamine is an evolutionarily ancient neurotransmitter that plays an essential role in mediating behavior. in vertebrates, dopamine is central to the mesolimbic reward system, a neural network concerned with the valuation of stimulus salience, and to the nigrostriatal motor system and hypothalamic nuclei involved in the regulation of locomotion and social behavior. in amphibians, dopaminergic neurons have been mapped out in several species, yet the distribution of dopaminoreceptive cells is unkn ...201021099197
sexually dimorphic sensory gating drives behavioral differences in tungara frogs.males and females can differ both in the social behaviors they perform and in the contexts in which they engage in these behaviors. one possible mechanism of sex differences in behavior is a sexual dimorphism in the relay of sensory information to motor areas, but no studies have examined the role of such a relay in vertebrate sexually dimorphic behaviors. we used egr-1 expression as a marker of neural activation in frogs exposed to conspecific and heterospecific acoustic signals to compare acti ...201020889827
neural activity patterns in response to interspecific and intraspecific variation in mating calls in the túngara frog.during mate choice, individuals must classify potential mates according to species identity and relative attractiveness. in many species, females do so by evaluating variation in the signals produced by males. male túngara frogs (physalaemus pustulosus) can produce single note calls (whines) and multi-note calls (whine-chucks). while the whine alone is sufficient for species recognition, females greatly prefer the whine-chuck when given a choice.201020877560
characterization of the plasticity-related gene, arc, in the frog brain.in mammals, expression of the immediate early gene arc/arg3.1 in the brain is induced by exposure to novel environments, reception of sensory stimuli, and production of learned behaviors, suggesting a potentially important role in neural and behavioral plasticity. to date, arc has only been characterized in a few species of mammals and birds, which limits our ability to understand its role in modifying behavior. to begin to address this gap, we identified arc in two frog species, xenopus tropica ...201020602363
sexually dimorphic androgen and estrogen receptor mrna expression in the brain of túngara frogs.sex steroid hormones are potent regulators of behavior and they exert their effects through influences on sensory, motor, and motivational systems. to elucidate where androgens and estrogens can act to regulate sex-typical behaviors in the túngara frog (physalaemus pustulosus), we quantified expression of the androgen receptor (ar), estrogen receptor alpha (eralpha), and estrogen receptor beta (erbeta) genes in the brains of male and females. to do so, we cloned túngara-specific sequences for ar ...201020600046
ecological and genetic divergence between two lineages of middle american túngara frogs physalaemus (= engystomops) pustulosus.uncovering how populations of a species differ genetically and ecologically is important for understanding evolutionary processes. here we combine population genetic methods (microsatellites) with phylogenetic information (mtdna) to define genetic population clusters of the wide-spread neotropical túngara frog (physalaemus pustulosus). we measure gene flow and migration within and between population clusters and compare genetic diversity between population clusters. by applying ecological niche ...201020482771
complexity increases working memory for mating signals.females often prefer to mate with males who produce complex signals. it is not clear why they do so. females might prefer complexity if it predicts mate quality, or signals might evolve complexity to exploit females' sensory or cognitive biases. we tested whether complexity increases active time, the period over which a signal influences a receiver's response to that signal. mating signals are often ephemeral, yet their active time has largely been ignored. here we demonstrate that signal comple ...201020206525
artificial photosynthesis in ranaspumin-2 based foam.we present a cell-free artificial photosynthesis platform that couples the requisite enzymes of the calvin cycle with a nanoscale photophosphorylation system engineered into a foam architecture using the tungara frog surfactant protein ranaspumin-2. this unique protein surfactant allowed lipid vesicles and coupled enzyme activity to be concentrated to the microscale plateau channels of the foam, directing photoderived chemical energy to the singular purpose of carbon fixation and sugar synthesis ...201020205454
the development of sexual behavior in túngara frogs (physalaemus pustulosus).we examined the emergence of a critical component of sex, response to sexual signals-phonotaxis-in male and female túngara frogs (physalaemus pustulosus). we determined the ontogenetic trajectories of phonotactic responses as animals developed from metamorphic froglets to reproductive adults. the results demonstrated that species-typical phonotaxis emerges quite early during postmetamorphic development, well before sexual maturity, suggesting that a developmentally early bias in the auditory sys ...201020175598
building a home from foam--túngara frog foam nest architecture and three-phase construction process.frogs that build foam nests floating on water face the problems of over-dispersion of the secretions used and eggs being dangerously exposed at the foam : air interface. nest construction behaviour of túngara frogs, engystomops pustulosus, has features that may circumvent these problems. pairs build nests in periodic bursts of foam production and egg deposition, three discrete phases being discernible. the first is characterized by a bubble raft without egg deposition and an approximately linear ...201020106853
acoustic radiation patterns of mating calls of the tungara frog (physalaemus pustuosus): implications for multiple receivers.in order for a signal to be transmitted from a sender to a receiver, the receiver must be within the active space of the signal. if patterns of sound radiation are not omnidirectional, the position as well as the distance of the receiver relative to the sender is critical. in previous measurements of the horizontal directivity of mating calls of frogs, the signals were analyzed using peak or root-mean-square analysis and resulted in broadband directivities that ranged from negligible to a maximu ...200919894851
treatment with arginine vasotocin alters mating calls and decreases call attractiveness in male túngara frogs.the peptide hormone arginine vasotocin (avt) and its mammalian homolog arginine vasopressin modulate a variety of social behaviors in vertebrates. in anurans, avt influences the production of advertisement calls, the acoustic signals that males use to attract females and repel rival males. in this study, we investigate the effects of avt on call characteristics in the túngara frog (physalaemus pustulosus). túngara frogs produce a "whine" that is important for species recognition; they may also p ...201019576218
changes in localization and expression levels of shroom2 and spectrin contribute to variation in amphibian egg pigmentation patterns.one contributing factor in the worldwide decline in amphibian populations is thought to be the exposure of eggs to uv light. enrichment of pigment in the animal hemisphere of eggs laid in the sunlight defends against uv damage, but little is known about the cell biological mechanisms controlling such polarized pigment patterns. even less is known about how such mechanisms were modified during evolution to achieve the array of amphibian egg pigment patterns. here, we show that ectopic expression ...200919554350
ranaspumin-2: structure and function of a surfactant protein from the foam nests of a tropical frog.ranaspumin-2 (rsn-2) is a monomeric, 11 kda surfactant protein identified as one of the major foam nest components of the túngara frog (engystomops pustulosus), with an amino acid sequence unlike any other protein described so far. we report here on its structure in solution as determined by high-resolution nmr analysis, together with investigations of its conformation and packing at the air-water interface using a combination of infrared and neutron reflectivity techniques. despite the lack of ...200919527658
foam nest components of the túngara frog: a cocktail of proteins conferring physical and biological resilience.the foam nests of the túngara frog (engystomops pustulosus) form a biocompatible incubation medium for eggs and sperm while resisting considerable environmental and microbiological assault. we have shown that much of this behaviour can be attributed to a cocktail of six proteins, designated ranaspumins (rsn-1 to rsn-6), which predominate in the foam. these fall into two discernable classes based on sequence analysis and biophysical properties. rsn-2, with an amphiphilic amino acid sequence unlik ...200919324764
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 cont ...200919141428
acoustically evoked immediate early gene expression in the pallium of female túngara frogs.in anurans, much is known about the role of the auditory midbrain in processing conspecific calls, but comparatively little is known about the role of the pallium. to address this deficiency, we investigated the induction of the immediate early gene egr-1 by natural mate chorus in the medial, dorsal, lateral, and ventral pallium of female túngara frogs. we found strong acoustically evoked egr-1 expression in the dorsal medial pallium (p < 0.01) and ventral pallium (p = 0.02), with a weaker effec ...200818997464
categorical perception of a natural, multivariate signal: mating call recognition in túngara frogs.categorical perception is common in humans, but it is not known whether animals perceive continuous variation in their own multidimensional social signals categorically. there are two components to categorical perception: labeling and discrimination. in the first, continuously variable stimuli on each side of a category boundary are labeled. in the second, there is strong discrimination between stimuli from opposite sides of the boundary, whereas stimuli on the same side of the boundary are not ...200818577592
visual sensitivity to a conspicuous male cue varies by reproductive state in physalaemus pustulosus females.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-i ...200818375844
functional coupling between substantia nigra and basal ganglia homologues in amphibians.neuroanatomical and pharmacological experiments support the existence of a homologue of the mammalian substantia nigra-basal ganglia circuit in the amphibian brain. demarcation of borders between the striatum and pallidum in frogs, however, has been contentious, and direct evidence of functional coupling between the putative nigral and striatal homologues is lacking. to clarify basal ganglia function in anurans, the authors used expression of immediate-early gene egr-1 as a marker of neural acti ...200718085893
acoustic modulation of immediate early gene expression in the auditory midbrain of female túngara frogs.to better understand the molecular consequences of auditory processing in frogs, we investigated the acoustic modulation of two immediate early genes (iegs), egr-1 and fos, in the auditory midbrain of female túngara frogs. since túngara frog egr-1 had already been identified, we first isolated a túngara-specific fos clone using degenerate pcr followed by rapid amplification of cdna ends. in order to examine the temporal kinetics of acoustically modulated ieg mrna expression, we first acousticall ...200818061149
reproductive hormones modify reception of species-typical communication signals in a female anuran.in many vertebrates, the production and reception of species-typical courtship signals occurs when gonadotropin and gonadal hormone levels are elevated. these hormones may modify sensory processing in the signal receiver in a way that enhances behavioral responses to the signal. we examined this possibility in female túngara frogs (physalaemus pustulosus) by treating them with either gonadotropin (which elevated estradiol) or saline and exposing them to either mate choruses or silence. expressio ...200818032889
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 distan ...200717956386
arginine vasotocin promotes calling behavior and call changes in male túngara frogs.in the túngara frog, physalaemus pustulosus, males alter calling behavior with changes in their social environment, adding 'chucks' to their advertisement calls in response to the calls of conspecific males. other studies demonstrate that adding chucks increases the attractiveness of calls to females but also increases the risk of bat predation. in the current study, subcutaneous injections of the neuropeptide hormone arginine vasotocin (avt) significantly increased chuck production in male túng ...200717299257
integration of sensory and motor processing underlying social behaviour in túngara frogs.social decision making involves the perception and processing of social stimuli, the subsequent evaluation of that information in the context of the individual's internal and external milieus to produce a decision, and then culminates in behavioural output informed by that decision. we examined brain networks in an anuran communication system that relies on acoustic signals to guide simple, stereotyped motor output. we used egr-1 mrna expression to measure neural activation in male túngara frogs ...200717254988
cues for eavesdroppers: do frog calls indicate prey density and quality?predators and parasites that eavesdrop on the mating signals of their prey often preferentially select individuals within a prey/host species that produce specific cues. mechanisms driving such signal preferences are poorly understood. in the tungara frog physalaemus pustulosus, conspecific females, frog-eating bats, and blood-sucking flies all prefer complex to simple mating calls. in this study we assess the natural signal variation in choruses in the wild and test two hypotheses for why eaves ...200717230403
túngara frogs. 200617141600
geographic variation of genetic and behavioral traits in northern and southern tüngara frogs.we use a combination of microsatellite marker analysis and mate-choice behavior experiments to assess patterns of reproductive isolation of the túngara frog physalaemus pustulosus along a 550-km transect of 25 populations in costa rica and panama. earlier studies using allozymes and mitochondrial dna defined two genetic groups of túngara frogs, one ranging from mexico to northern costa rica (northern group), the second ranging from panama to northern south america (southern group). our more fine ...200617017067
the vocal sac increases call rate in the tungara 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 tungara frogs. ...200616826497
animal communication: complex call production in the túngara frog.animals' sound-producing organs often act as an integrated whole--particular vocal structure are not directly associated with the creation of discrete syllables. but here we show that the 'chuck' of the 'whine-chuck' mating call of the túngara frog, physalaemus pustulosus, is caused by a fibrous mass attached to the vocal folds; the chuck is eliminated by removal of this structure, although the frog still tries to produce the sound. sexual selection affects the acoustic complexity of the frog's ...200616672962
social regulation of plasma estradiol concentration in a female anuran.the behavior of an individual within a social aggregation profoundly influences behavior and physiology of other animals within the aggregation in such a way that these social interactions can enhance reproductive success, survival and fitness. this phenomenon is particularly important during the breeding season when males and female must synchronize their reproductive efforts. we examined whether exposure to conspecific social cues can elevate sex steroid levels, specifically estradiol and andr ...200616545384
a cognitive framework for mate choice and species recognition.mating decisions contribute to both the fitness of individuals and the emergence of evolutionary diversity, yet little is known about their cognitive architecture. we propose a simple model that describes how preferences are translated into decisions and how seemingly disparate patterns of preference can emerge from a single perceptual process. the model proposes that females use error-prone estimates of attractiveness to select mates based on a simple decision rule: choose the most attractive a ...200616475097
phylogeny of the túngara frog genus engystomops (= physalaemus pustulosus species group; anura: leptodactylidae).we present a phylogeny of the neotropical genus engystomops (= physalaemus pustulosus species group) based on sequences of approximately 2.4 kb of mtdna, (12s rrna, valine-trna, and 16s rrna) and propose a phylogenetic nomenclature. the phylogeny includes all described taxa and two unnamed species. all analyses indicate that engystomops is monophyletic and contains two basal allopatric clades. clade i (edentulus) includes e. pustulosus and the amazonian e. petersi + e. cf. freibergi. clade ii (d ...200616446105
biogeography of the túngara frog, physalaemus pustulosus: a molecular perspective.physalaemus pustulosus, a small leptodactylid frog with south american affinities, ranges across northern south america through middle america to southern mexico. to investigate its geographic variation and evolutionary origins, we analysed the presumptive gene products of 14 allozyme loci and sequenced a portion of the mitochondrial coi gene from individuals sampled throughout the distribution. generally, allozyme dissimilarities and sequence divergences are correlated with each other and with ...200516202101
the effects of time, space and spectrum on auditory grouping in túngara frogs.male túngara frogs (physalaemus pustulosus) produce complex calls consisting of two components, a approximately 350 ms fm sweep called the "whine" followed by up to seven approximately 40 ms harmonic bursts called "chucks". in order to choose and locate a calling male, females attending to choruses must group call components into auditory streams to correctly assign calls to their sources. previously we showed that spatial cues play a limited role in grouping: calls with normal spectra and tempo ...200516088388
gonadal steroids vary with reproductive stage in a tropically breeding female anuran.tropically breeding anurans that require heavy rainfall in order to reproduce are subject to favorable breeding conditions that are sporadic. although there is an increased probability of rain during the rainy season, the probability of local rainfall is unpredictable and this may influence female anuran reproductive strategies. the female túngara frog, a neotropical frog that requires standing water to breed, maintains readiness to breed at any time via asynchronous oogenesis. although females ...200515993104
adsorption of frog foam nest proteins at the air-water interface.the surfactant properties of aqueous protein mixtures (ranaspumins) from the foam nests of the tropical frog physalaemus pustulosus have been investigated by surface tension, two-photon excitation fluorescence microscopy, specular neutron reflection, and related biophysical techniques. ranaspumins lower the surface tension of water more rapidly and more effectively than standard globular proteins under similar conditions. two-photon excitation fluorescence microscopy of nest foams treated with f ...200515626715
functional mapping of the auditory midbrain during mate call reception.we examined patterns of neural activity as assayed by changes in gene expression to localize representation of acoustic mating signals in the auditory midbrain of frogs. we exposed wild-caught male physalaemus pustulosus to conspecific mating calls that vary in their behavioral salience, nonsalient mating calls, or no sound. we measured expression of the immediate early gene egr-1 (also called zenk, zif268, ngfi-a, and krox-24) throughout the torus semicircularis, the auditory midbrain homolog o ...200415601932
sexual selection in female perceptual space: how female túngara frogs perceive and respond to complex population variation in acoustic mating signals.female preferences for male mating signals are often evaluated on single parameters in isolation or small suites of characters. most signals, however, are composites of many individual parameters. in this study we quantified multivariate traits in the advertisement call of the túngara frog, physalaemus pustulosus. we represented the calls in multidimensional scaling space and chose nine test calls to represent the range of population variation. we then tested females for phonotactic preference b ...200314686535
fine-scale genetic pattern and evidence for sex-biased dispersal in the túngara frog, physalaemus pustulosus.túngara frogs (physalaemus pustulosus) are a model system for sexual selection and communication. population dynamics and gene flow are of major interest in this species because they influence speciation processes and microevolution, and could consequently provide a deeper understanding of the evolutionary processes involved in mate recognition. although earlier studies have documented genetic variation across the species' range, attempts to investigate dispersal on a local level have been limit ...200314629349
generalization in response to mate recognition signals.females usually exhibit strong and unequivocal recognition of conspecific mating signals and reject those of other sympatric heterospecifics. however, most species are allopatric with one another, and the degree to which females recognize mating signals of allopatric species is more varied. such mating signals are often rejected but are sometimes falsely recognized as conspecific. we studied the dynamics of mate recognition in female túngara frogs (physalaemus pustulosus) in response to a series ...200312699219
phylogeny of frogs of the physalaemus pustulosus species group, with an examination of data incongruence.characters derived from advertisement calls, morphology, allozymes, and the sequences of the small subunit of the mitochondrial ribosomal gene (12s) and the cytochrome oxidase i (coi) mitochondrial gene were used to estimate the phylogeny of frogs of the physalaemus pustulosus group (leptodactylidae). the combinability of these data partitions was assessed in several ways: measures of phylogenetic signal, character support for trees, congruence of tree topologies, compatibility of data partition ...199812064230
evolution of calls and auditory tuning in the physalaemus pustulosus species group.in species within the physalaemus pustulosus species group, male frogs produce a whine-like advertisement call consisting of a frequency sweep typically descending from 1,000 to 400 hz (depending on the species). one species, physalaemus pustulosus, the túngara frog, has evolved a second call syllable, the chuck, which males place after their whine. most energy in the chuck is above 1,500 hz and peaks at 2,400 hz. we investigated whether the evolution of this new call component in p. pustulosus ...200111910171
vestigial preference functions in neural networks and túngara frogs.although there is a growing interest in understanding how perceptual mechanisms influence behavioral evolution, few studies have addressed how perception itself is shaped by evolutionary forces. we used a combination of artificial neural network models and behavioral experiments to investigate how evolutionary history influenced the perceptual processes used in mate choice by female túngara frogs. we manipulated the evolutionary history of artificial neural network models and observed an emergen ...200111698682
history influences signal recognition: neural network models of túngara frogs.animals often attend to only a few of the cues provided by the complex displays of conspecifics. we suggest that these perceptual biases are influenced by mechanisms of signal recognition inherited from antecedent species. we tested this hypothesis by manipulating the evolutionary history of artificial neural networks, observing how the resulting networks respond to many novel stimuli and comparing these responses to the behaviour of females in phonotaxis experiments. networks with different evo ...200011467426
how evolutionary history shapes recognition mechanisms.evolutionary psychologists have emphasized the importance of natural selection in shaping cognitive functions, but historical contingency has not received direct study. this is crucial because in response to selection, complex traits tend to be fine-tuned or jury-rigged rather than totally reconstructed. we hypothesize that the neural and cognitive strategies an animal employs in signal recognition are influenced by the strategies used by its ancestors. the responses of female túngara frogs to a ...200111287267
a sense of history.mating preferences for specific traits increase the fertility, fecundity or offspring fitness of choosy individuals. however, current fitness benefits offer an incomplete account of the relative influence of different signals on mate choice. the history of selection on sensory systems in a broader ecological context can provide many missing details. recent innovative use of neural networks by phelps and ryan shows that modelling the chronological order in which past selective forces have acted p ...200111179568
effects of inter-pond distance on the breeding ecology of tungara frogs.habitat and resource distributions can influence the movement and aggregation of individuals and thus have important effects on breeding behavior and ecology. though amphibians have been model systems for the study of breeding behavior and sexual selection, most studies have examined breeding behavior within a single pond. as a result, little is known about how inter-pond distance affects breeding amphibians. we studied the effects of inter-pond distance on the breeding ecology of the tungara fr ...200028308343
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