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Underwater acoustic communication in the African pipid frog Xenopus borealis
Abstract
The totally aquatic African pipid frog Xenopus borealis produces a range of acoustic signals underwater at night.The repertoire of males in heightened reproductive condition consists of three call types. All of the calls are composed of the same impulsive, click-like components. The clicks have a rise-time of 0.5 msec, a duration of 2–5 msec, and most of their energy concentrated at 2600 Hz with a secondary peak at 1100 Hz. The sound pressure levels average 109 dB SPL at 1 meter. The advertisement call is characterized by interclick intervals of 300–600 msec (depending on temperature) and very low coefficients of variation—3%-10%. Phonotaxis experiments confirm that it is effective in attracting females. The approach call, produced when swimming toward or clasping another frog, has interclick intervals averaging 105 msec. Males show pronounced agonistic behavior accompanied by series of clicks with interclick intervals averaging 43 msec.Unreceptive females sometimes produce a very weak release call when clasped, but are otherwise silent.Comparison of this underwater acoustic communication system with terrestrial anuran systems shows surprisingly few differences, given the strong contrast in acoustic environments. The structure of the male's clicks, however, suggests that a major adaptation to underwater signalling may involve the sound production mechanism itself.
... Each call consists of trains of brief sound pulses, with the specific rate and temporal pattern of pulses defining each call. Full repertoires have been described for two species, X. laevis and Xenopus borealis (Fig. 1;Yager 1992;Tobias et al. 1998;Tobias et al. 2004). As in all described Xenopus species, X. laevis and X. borealis males produce advertisement calls in isolation or in the presence of conspecifics to advertise their sexual state to potential mates (Tobias et al. 2011). ...
... Neuromodulators regulate behavioral dynamics 855 laevis males produce three agonistic calls, while X. borealis males produce one. When clasping a conspecific, male X. laevis produce an "amplectant" call (Tobias et al. 2004), while X. borealis produce an "approach" call (Yager 1992). Xenopus borealis males switch regularly and rapidly between advertisement calling and approach calling as they interact with and clasp females. ...
... Sexually unreceptive female X. laevis produce a "release" call when clasped by a male, and gravid females produce an advertisement call ("rapping") when they are unable to locate a calling male. In contrast, X. borealis females are only known to produce release calls when clasped by a conspecific while sexually unreceptive (Yager 1992). Regardless of species differences in vocal repertoires, individual frogs integrate a wide range of information about their own internal states with social sensory signals from nearby conspecifics to produce appropriate vocal responses. ...
Synopsis
Across the animal kingdom, the ability to produce communication signals appropriate to social encounters is essential, but how these behaviors are selected and adjusted in a context-dependent manner are poorly understood. This question can be addressed on many levels, including sensory processing by peripheral organs and the central nervous system, sensorimotor integration in decision-making brain regions, and motor circuit activation and modulation. Because neuromodulator systems act at each of these levels, they are a useful lens through which to explore the mechanisms underlying complex patterns of communication. It has been clear for decades that understanding the logic of input–output decision making by the nervous system requires far more than simply identifying the connections linking sensory organs to motor circuits; this is due in part to the fact that neuromodulators can promote distinct and temporally dynamic responses to similar signals. We focus on the vocal circuit dynamics of Xenopus frogs, and describe complementary examples from diverse vertebrate communication systems. While much remains to be discovered about how neuromodulators direct flexibility in communication behaviors, these examples illustrate that several neuromodulators can act upon the same circuit at multiple levels of control, and that the functional consequence of neuromodulation can depend on species-specific factors as well as dynamic organismal characteristics like internal state.
... Hence, the ecology and behaviour of such species in natural conditions is usually poorly known due to the difficulty of recording behaviour and the subsequent lack of knowledge about the environmental factors that influence the expression pattern of activities like breeding and foraging. This is the case for pipid frogs, which are aquatic, call underwater (Yager, 1992;Tobias et al., 2010), feed within the water column (Carreño and Nishikawa, 2010), and move overland only to reach the next water body (Measey, 2016). Xenopus laevis is a particularly prominent example of the difficulty of studying aquatic anurans. ...
... Our approach is useful for an aquatic species that can occur in turbid (Lobos et al., 2013), vegetated (Courant et al., 2018a), or deep ponds (Tinsley et al., 2015). It could also be used for other pipid species (Yager, 1992;Tobias et al., 2010), or other aquatic anurans (Narins and Feng, 2006). Our study provides insight into the influence of the lunar cycle on the regulation of time partitioning in these secretive amphibians, but should be taken with caution, as it was conducted on one single year at one breeding site. ...
Aquatic anuran species are difficult to detect and observe and this is a major limit to the study of their behaviour and ecology. This habit limits the direct monitoring of sexual and foraging activity, and the investigation of how environmental factors influence their expression as well as how individuals allocate time between competing activities. We investigated this issue in Xenopus laevis , a mostly aquatic frog that forages and emits calls underwater. This model species in biology has been extensively studied in the lab but its behaviour in nature remains poorly described. We carried out a study in a pond during the breeding season in the French invasive range. We recorded underwater vocal activity as a proxy for sexual activity using a hydrophone, set food-baited traps to quantify foraging activity, and recorded environmental conditions (moonlight intensity, temperature and rainfall) over two lunar cycles. We found that individuals engage in these two activities during the breeding season. At the peak of the breeding period, vocal activity was expressed during the day. The investment in reproduction (calling activity) may reduce the time allocated to foraging on a circadian scale. The two activities seem to be partitioned depending on moonlight intensity, with a stronger effect on males. Foraging activity decreased and vocal activity increased when moonlight intensity increased. We also observed a negative effect of temperature and a positive effect of rainfall on vocal activity only. Our method is promising to monitor the activity of other aquatic anurans.
... Resonant vs. non-resonant clicks. Pressure waveforms were particularly susceptible to resonance artifacts, a common phenomenon in small tanks (Parvulescu, 1964(Parvulescu, , 1967Yager, 1992;Akamatsu et al., 2002). Clicks were judged as resonant if a series of high amplitude, high frequency waveforms occurred during or immediately after the rise of the click in the time domain (Figure 3-10). ...
... The resonance artifacts I documented in sound pressure among clicks are typical of problems of sound distortion in small tanks, that have been known for some time (Parvulescu, 1964(Parvulescu, , 1967. Yager (1992) also documented resonance artifacts when recording clicks from the African Pipid frog (Xenopus borealis) in small tanks; showing a broad band of high-amplitude energy between 5-40 kHz that is not present when clicks are recorded in a pond. However, my tests showed no significant differences among the frequency components of the clicks in the 0-1000 Hz frequency band, that is within the range of hearing of H. erectus and other hearing generalists. ...
Loud noise in aquaria represents a cacophonous environment for captive fishes. I tested the effects of loud noise on acoustic communication, feeding behavior, courtship behavior, and the stress response of the lined seahorse, Hippocampus erectus. Total Root Mean Square (RMS) power of ambient noise to which seahorses are exposed in captivity varies widely but averages 126.1 +/- 0.8 deciBels with reference to one micropascal (dB re: 1 μPa) at the middle of the water column and 133.7 +/- 1.1 dB at the tank bottom, whereas ambient noise in the wild averages 119.6 +/- 3.5 dB. Hearing sensitivity of H. erectus, measured from auditory evoked potentials, demonstrated maximum spectrum-level sensitivities of 105.0 +/- 1.5 dB and 3.5 X 10-3 + 7.6 X 10-4 m/s2 at 200 Hz; which is characteristic of hearing generalists. H. erectus produces acoustic clicks with mean peak spectrum-level amplitudes of 94.3 +/- 0.9 dB at 232 +/- 16 Hz and 1.5 X 10-3 +/- 1.9 X 10-4 m/s2 at 265 +/- 22 Hz. Frequency matching of clicks to best hearing sensitivity, and estimates of audition of broadband signals suggest that seahorses may hear conspecific clicks, especially in terms of particle motion.
Behavioral investigations revealed that clicking did not improve prey capture proficiency. However, animals clicked more often as time progressed in a courtship sequence, and mates performed more courtship behaviors with control animals than with muted animals, lending additional evidence to the role of clicking as an acoustic signal during courtship. Despite loud noise and the role of clicking in communication, masking of the acoustic signal was not demonstrated.
Seahorses exposed to loud noise in aquaria for one month demonstrated physiological, chronic stress responses: reduced weight and body condition, and increased heterophil to lymphocyte ratio. Behavioral alterations were characterized by greater mean and variance of activity among animals housed in loud tanks in the first week, followed by habituation. By week four, animals in loud tanks demonstrated variable performance of clicking and piping, putative distress behaviors. Despite the physiological stress response, animals in loud tanks did not reduce feeding response or courtship behavior, suggesting allostasis.
... . Tinsley et al., 1996, The Biology of Xenopus 114. Evans et al., 2004, "A Mitochondrial DNA Phylogeny of African Clawed Frogs" niches and breeding conditions: 16-22°C, 19-23°C, and 22-30°C for Xl, Xb, and Xt respectively.(115,116). Hence, microtubule dynamic instability-a ...
... These signals are mostly transmitted by air but also by using other material as carrier substrates (e.g. water or soil ;Yager 1992;Platz 1993;Christensen-Dalsgaard and Elepfandt 1995;Seidel 1999;Lewis et al. 2001;Seidel et al. 2001;Bradbury and Vehrencamp 2011;Irisarri et al. 2011;Zheng et al. 2011). The main functions of intra-specific acoustic communication are attraction, detection and selection of mates, territoriality, and / or exchange of other information (e.g. ...
Zoologists have widely acknowledged the utility of classification systems for characterising variation in anuran egg and clutch types, tadpole morphotypes, embryonic and tadpole development, amplexus types and reproductive modes. These classification systems have facilitated unambiguous communication between researchers, often working in completely different fields (e.g. taxonomy, ecology , behaviour), as well as comparisons among studies. A syntactic system, classifying anuran call guilds, is so far lacking. Based on examination of the calls of 1253 anuran species we present a simple, easy to use dichotomous key and guild system for classifying anuran advertisement calls-the call type most frequently emitted by anurans and studied by researchers. The use of only three call elements, namely clearly-defined calls, notes, and pulses, plus presence or absence of frequency modulation, allows assigning all currently known anuran advertisement calls to one of eight distinct call guilds defined here. This novel toolkit will facilitate comparative studies across the many thousand anuran species, and may help to unravel drivers of anuran call evolution, and to identify ecological patterns at the level of acoustic communities.
... Furthermore, these studies focused on a single species: the African clawed frog, Xenopus laevis (e.g., Hayes et al. 2002;Smith et al. 2005;Qin et al. 2007). Although Xenopus laevis is a model organism in development and genetics, its laryngeal morphology is atypical for anurans (Sassoon and Kelley 1986;Colafrancesco and Gridi-Papp 2016) as this species is fully aquatic and calls underwater (Yager 1992). It is also unclear how similar the physiological responses to endocrine disruptors are among Xenopus and other anuran taxa (Pattersson and Berg 2007;Tamschick et al. 2016). ...
Anthropogenic factors, including the spread of endocrine-disrupting chemicals, have been linked to alterations in the reproductive physiology, morphology, and behavior of wildlife. Few studies of endocrine disruption, however, focus on secondary sexual traits that affect mating signals, despite their importance for reproductive success. The larynx of many anurans (frogs and toads), for example, is larger in males than in females and is crucial for producing mating calls. We aim to determine if wild populations of cane toads (Rhinella marina) near sugarcane fields in Florida have demasculinized larynges when compared to populations near urban areas. We find evidence of demasculinization in both primary and secondary sexual traits in male toads living near sugarcane. Relative to body size, the laryngeal mass, vocal cord length, and dilator muscle width are all reduced in males from sugarcane regions compared to their urban counterparts. Strong correlations between primary and secondary male sexual traits indicate that demasculinization occurs in concert both within and across diverse organs, including the testes, larynx, and skin. Our results show that anurans near sugarcane fields have demasculinized reproductive systems, that this disruption extends to secondary sexual traits like the larynx, and that it is likely due to anthropogenic causes.
... These studies revealed an extensive vocal repertoire in X. laevis. The existence of several calls has also been shown in X. borealis (Yager 1992), and it has been suggested that most species of Xenopus will probably have 3-6 different call types (Yager 1996). ...
We studied the acoustic and reproductive behaviour of the clawed frog, Xenopus laevis, in a pond with clear water in South Africa over a period of two months. It contained 21 adult males and females. Each was marked with a transponder so that the behaviour of individuals could be tracked. The animals inhabited the bottom of the pond. They were active from dusk to midnight. Series of nights in which several males called alternated with series without calling. Simultaneous calls were not synchronised. On nights when males called, several of them established territories on the bottom of the pond that they defended against other males. They delineated the territory by calling along its borders. When meeting a male intruder they emitted an encounter call, followed by a fighting call if they fought. At the end of a fight the loser emitted a release call. Territories could remain constant over several weeks. They were abandoned on nights without calling, but re-established by the same individuals at the same locations on nights with calling. When a female entered a territory, the male approached, started the courtship call and attempted amplexus. The female usually rejected the male while emitting a release call. Females spawned synchronously on one or two nights, with weeks without oviposition in-between. Eggs were laid individually or in small groups on hard structures all over the pond. The adults preyed upon the tadpoles and only a few single tadpoles remained after two weeks. Raising the water level stimulated calling activity.
... Completely aquatic pipid frogs communicate acoustically in shallow ponds using broadband clicks with main energies from 1 to 5 kHz. This seems to be an adaptation to shallow-water habitats, which facilitate the propagation of high-frequency sounds (see Introduction). Yager (1992b), however, pointed out that secondarily aquatic anurans largely retained the terrestrial anuran communication pattern. The frequency band used is not shifted upward, and coding of species specificity using temporal patterns has also been documented in tree frogs and toads. ...
Sound propagates much faster and over larger distances in water than in air, mainly because of differences in the density of these media. This raises the question of whether terrestrial (land mammals, birds) and (semi-)aquatic animals (frogs, fishes, cetaceans) differ fundamentally in the way they communicate acoustically. Terrestrial vertebrates primarily produce sounds by vibrating vocal tissue (folds) directly in an airflow. This mechanism has been modified in frogs and cetaceans, whereas fishes generate sounds in quite different ways mainly by utilizing the swimbladder or pectoral fins. On land, vertebrates pick up sounds with light tympana, whereas other mechanisms have had to evolve underwater. Furthermore, fishes differ from all other vertebrates by not having an inner ear end organ devoted exclusively to hearing. Comparing acoustic communication within and between aquatic and terrestrial vertebrates reveals that there is no 'aquatic way' of sound communication, as compared witha more uniform terrestrial one. Birds and mammals display rich acoustic communication behaviour, which reflects their highly developed cognitive and social capabilities. In contrast, acoustic signaling seems to be the exception in fishes, and is obviously limited to short distances and to substrate-breeding species, whereas all cetaceans communicate acoustically and, because of their predominantly pelagic lifestyle, exploit the benefits of sound propagation in a dense, obstacle-free medium that provides fast and almost lossless signal transmission.
The anurans—frogs and toads—are highly speciose and widely distributed throughout the world. Most species are known to use acoustic signals to communicate a range of information across many social contexts. Vocal behaviors coordinate courtship and reproduction, and are thus subject to both intrasexual and intersexual selection. The sexes differ dramatically in their vocalizations, and these behaviors are therefore strongly influenced by gonadal steroid hormones. Because of their energetic costs and roles in coordinating social interactions, other hormones such as corticosterone and arginine vasotocin are also known to regulate vocalizations. In this chapter, we begin by describing well-understood relationships between hormones and anuran vocalizations. We then discuss the known peripheral and central mechanisms of vocal production, and describe how many of these processes are established or maintained by hormones. We summarize the relatively small number of experiments that address how endocrine disrupting chemical pollutants can adversely affect anuran vocal pathways. While anuran vocal behaviors are described for a great number of species, the mechanisms and hormonal regulation are only described for a relatively small subset of species. In this chapter, we focus our attention on these best understood groups, with one goal of promoting similar efforts across the anuran phylogeny. Future studies into the roles of hormones, and the detrimental impacts of endocrine disrupting pollutants, across distantly related anurans will help to identify conserved endocrine regulatory processes and discern traits that make anurans more, or less, susceptible to endocrine disruption.
The patterns of geographical distribution shown by the species of Xenopus (Anura Pipidae) are briefly reviewed; some areas of sympatry are identified and various implications are discussed.
The potential exchange of parasite infections between host species is facilitated in areas of sympatry. However, evidence from the host specificity of monogenean, cestode and nematode parasites shows that, despite the sharing of habitats, several Xenopus may maintain species-specific infections. The disjunctions in the host distribution of these parasites corresponds with genome duplication in the series of Xenopus species.
Sympatry facilitates hybridisation. In South Africa, interbreeding of X. gilli Rose & Hewitt and X. laevis (Daudin) gives rise to gene introgression and, potentially, to polyploidisation. In Central Africa, hybridisation and polyploidisation have been important factors in evolution; the genus contains an allopolyploid series with species possessing 2n = 20, 36, 72 and 108 chromosomes.
There is evidence of a major change in species distributions in one area of sympatry. X. laevis bunyoniensis Loveridge was abundant in lakes of SW Uganda in 1913–1939, but apparently has since been totally replaced by X. vestitus Laurent and X. wittei Tinsley et al., species which were previously absent from the lakes. The replaced bunyoniensis is unknown outside this area and may now be near to extinction.
The mating system of hormonally stimulated Xenopus laevis laevis has been examined. The mating call of the male can be divided into two parts, one displaying a greater pulse repetition rate. These two components follow one another in calling bouts without intervals of silence between them. Temporal characteristics of the call are presented. The mating call has a complex frequency structure. Up to five energetic frequency bands are present, and individual frogs from the same population emphasize different bands. Female Xenopus laevis respond to the mating call with a positive phonotactic response. This has been quantified, and the associated behaviour described. Females, when clasped by males, produce a release call which rarely resulted in the release of the female, the result of overstimulation of the male with sex hormone. Males give a soft ‘amplectant call’ while clasping. Clasped males produce a release call which effects their release. Of all modes of ° communication, the mating call is considered to convey the a highest information content for mate recognition. Other communication relates to the physiological condition of the clasped frog.Die paringsstelsel van hormoongestimuleerde Xenopus laevis laevis was ondersoek. Die paringsroep van die mannetjie word in twee dele verdeel waarvan die een 'n groterw trilherhalingstempotoon. Hierdie twee komponente volg mekaar sonder stiltes tussen die roepbeurte op. Temporele a eienskappe van die paringsroep is beskryf. Die paringsroep a het 'n ingewikkelde frekwensiestruktuur, met tot vyf energiebande. Indiwiduele paddas van dieselfde bevolking beklemtoon verskillende bande. Die wyfie Xenopus laevis reageer positief fonotakties op die paringsroep van die mannetjie. Die is gekwantifiseer en die gepaardgaande gedrag is beskryf. Wanneer wyfies deur mannetjies vasgegryp word, produseer hulle 'n vrylatingsroep, wat as die klopgeroep beskryf kan word, maar as gevolg van die oorgestimuleerde § geslagshormone van die mannetjie het dit selde die vrylating s van die wyfie tot gevolg. Die mannetjie gee 'n sagte a ‘ampleksieroep’ terwyl hy vasgryp, maar gee 'n manlike vrylatingsroep wat vrylating tot gevolg het. Van alle soorte kommunikasie bevat die paringsroep maksimum inligtingsinhoud vir paarherkenning. Verdere kommunikasie het betrekking op diefisiologiese toestand van die vasgegrypte padda.
The last decades has seen an increasing interest in the sound communication of insects. Much information has been accumulated in “classical” fields, such as the anatomy of sound-producing and sound-receiving structures, the analysis of sounds, acoustic behavior, and hexing. This chapter concentrates on the biophysical aspects of sound communication. Both the sound-producing mechanisms and the sound-receiving structures have evolved independently in a number of insects. The main problem of bioengineering in insect sound communication is that of matching the impedances of the sound transmitter, the medium, and the sound receptor. This problem is similar to the impedance matching of electrical equipment: For the transmission to be efficient, the output impedance of the sender should be low, compared with the input impedance of the receiver. In sound emission, the mechanical impedance of the transmitter (the vibrating parts of the insect) should be low, compared with that of the air (the radiation impedance). In sound reception, the impedance of the air should be low, compared with that of the sound-receiving structure. The frequency range of insect sounds is limited, mainly by the impedance problem because the radiation impedance depends very much upon the size of the object relative to the wavelength of sound.
Of all the sensory stimuli discussed in this volume, only sound allows longrange transmission of information underwater. This is a consequence of the extraordinarily low attenuation of sound in water and the ability of sound speed gradients in the ocean to channel sound so that it can propagate without interaction with the surface or bottom.
The poorly known Telmatobius montanus was rediscovered in the high Andean mountains between Mendoza and Talca on the Argentinian-Chilean frontier. Morphological characters of the adults and tadpoles are described. There is convergence in male secondary sex characters toward the leptodactylid frogs of the genus Eupsophus (nodosus group).