Courtship Calls Research Articles

Vocalisation in wild-living mountain gazelles (Gazella gazella): structure and context of acoustical signals

Abstract Describing vocalisations of species in the wild is an important step to understanding their function. A wild-living population of mountain gazelles (Gazella gazella) was monitored in Israel, using camera traps, thereby providing a first detailed description of the acoustic repertoire. We described six acoustical signals that were either reported by previous authors or that were hitherto not reported. Acoustic signals were categorised according to behavioural context as alarm calls, courtship calls or threat calls and — if possible — characterised by four acoustic variables, i.e., duration, maximum amplitude frequency, three power quartiles and fundamental frequency. Vocalisations were illustrated as spectrograms supplemented by full video sequences to show the acoustical signal in its environmental, social, and behavioural context. Given the rather inconspicuous character of many acoustic signals, we proposed further in-depth studies of vocalisation in mountain gazelles and other Antilopine species to unravel new insights into their behaviour and social organisation.

Characteristics of courtship calls that could provide clues to physiological state or genetics of the emperor penguin, Aptenodytes forsteri: A case study of analysis using the Teager-Kaiser energy operator

Vocal behavior can be an indicator of physiological state or genetic make-up, but has not been developed as a diagnostic tool in seabirds. Aptenodytes penguins lack external sexual dimorphism, but the sexes have dimorphic courtship calls. We present a case study in which unique call structure of an emperor penguin (Aptenodytes forsteri) was associated with a same-sex bonded pair. Typical males produce lower frequency calls with proportionally more long bursts, while typical females produce slightly higher frequency calls with proportionally more short bursts. We recorded two male emperor penguins (E-79 and E-81) at SeaWorld San Diego that behaved as a bonded pair. E-79 produced a call that was qualitatively different from the male type to human listeners. Using the Teager-Kaiser Energy Operator to visualize bursts, we calculated and compared burst rates of E-79 and E-81 to other emperor penguins in the SeaWorld colony and a colony at Cape Crozier, Antarctica. Analysis showed E-79’s calls had a unique burst rate structure that was intermediate between typical male and female patterns. Our results suggest that while emperor courtship calls are usually strongly sexually dimorphic, it is not always the case. The exceptions could provide interesting insights into call development, physiology, and/or genetics.

Midbrain neurons important for the production of mouse ultrasonic vocalizations are not required for distress calls

A fundamental feature of vocal communication is that animals produce vocalizations with different acoustic features in different behavioral contexts (contact calls, territorial calls, courtship calls, etc.). The midbrain periaqueductal gray (PAG) is a key region that regulates vocal production, and artificial activation of the PAG can elicit the production of multiple species-typical vocalization types.1,2,3,4,5,6,7,8,9 How PAG circuits are organized to regulate the production of different vocalization types remains unknown. On the one hand, studies have found that partial PAG lesions abolish the production of some vocalization types while leaving others intact,3,8,10,11 suggesting that different populations of PAG neurons might control the production of different vocalization types. On the other hand, electrophysiological recordings have revealed individual PAG neurons that increase their activity during the production of multiple vocalization types,12,13,14 suggesting that some PAG neurons may regulate the production of more than one vocalization type. To test whether a single population of midbrain neurons regulates the production of different vocalization types, we applied intersectional methods to selectively ablate a population of midbrain neurons important for the production of ultrasonic vocalizations (USVs) in mice. We find that, although ablation of these PAG-USV neurons blocks USV production in both males and females, these neurons are not required for the production of distress calls. Our findings suggest that distinct populations of midbrain neurons control the production of different vocalization types.

Midbrain node for context-specific vocalisation in fish

Vocalizations communicate information indicative of behavioural state across divergent social contexts. Yet, how brain regions actively pattern the acoustic features of context-specific vocal signals remains largely unexplored. The midbrain periaqueductal gray (PAG) is a major site for initiating vocalization among mammals, including primates. We show that PAG neurons in a highly vocal fish species (Porichthys notatus) are activated in distinct patterns during agonistic versus courtship calling by males, with few co-activated during a non-vocal behaviour, foraging. Pharmacological manipulations within vocally active PAG, but not hindbrain, sites evoke vocal network output to sonic muscles matching the temporal features of courtship and agonistic calls, showing that a balance of inhibitory and excitatory dynamics is likely necessary for patterning different call types. Collectively, these findings support the hypothesis that vocal species of fish and mammals share functionally comparable PAG nodes that in some species can influence the acoustic structure of social context-specific vocal signals.

Linking courtship calls and observed behaviours of Epinephelus marginatus in the wild offers new insights into its reproduction and conservation

Abstract Groupers are marine fishes particularly vulnerable to overexploitation owing to their reproduction‐related traits. The dusky grouper Epinephelus marginatus is classified as ‘Endangered’ in the Mediterranean Sea, where protection measures have proven critical for allowing population recovery and persistence of the species. However, knowledge gaps remain regarding its reproductive behaviours and spawning sites. As with other grouper species, the dusky grouper is known to produce courtship‐associated sounds, which were validated in captivity, but no study has ever established a link between sound production and observed behaviours in the wild. This study aims to characterize, both visually and acoustically, the behavioural patterns of wild dusky grouper, thus specifically linking visual courtship behaviours to the associated sound production. Visual as well as passive acoustic methods were employed at two presumptive spawning sites within a Mediterranean Marine Protected Area (MPA) in the north‐western Mediterranean Sea over two consecutive summer seasons (2017 and 2018). The temporal patterns of sound production showed site specificity over the month in which reproductive activity was most intense. Courtship calls were mostly recorded around sunset at both study sites and were significantly associated with visual reproductive behaviours. Results also indicated a temporal partitioning in the acoustic activity of the species, with different sound types being recorded at distinct times of the day, likely corresponding to the occurrence of various behaviours during those periods. These findings have important implications for identifying and monitoring dusky grouper spawning sites using passive acoustic methods, therefore providing valuable information for the development, implementation, and/or enforcement of effective conservation measures therein.

Two conserved vocal central pattern generators broadly tuned for fast and slow rates generate species-specific vocalizations in Xenopus clawed frogs.

Across phyla, males often produce species-specific vocalizations to attract females. Although understanding the neural mechanisms underlying behavior has been challenging in vertebrates, we previously identified two anatomically distinct central pattern generators (CPGs) that drive the fast and slow clicks of male Xenopus laevis, using an ex vivo preparation that produces fictive vocalizations. Here, we extended this approach to four additional species, X. amieti, X. cliivi, X. petersii, and X. tropicalis, by developing ex vivo brain preparation from which fictive vocalizations are elicited in response to a chemical or electrical stimulus. We found that even though the courtship calls are species-specific, the CPGs used to generate clicks are conserved across species. The fast CPGs, which critically rely on reciprocal connections between the parabrachial nucleus and the nucleus ambiguus, are conserved among fast-click species, and slow CPGs are shared among slow-click species. In addition, our results suggest that testosterone plays a role in organizing fast CPGs in fast-click species, but not in slow-click species. Moreover, fast CPGs are not inherited by all species but monopolized by fast-click species. The results suggest that species-specific calls of the genus Xenopus have evolved by utilizing conserved slow and/or fast CPGs inherited by each species.

Evolution of acoustic signals associated with cooperative parental behavior in a poison frog

The emergence of complex social interactions is predicted to be an important selective force in the diversification of communication systems. Parental care presents a key social context in which to study the evolution of novel signals, as care often requires communication and behavioral coordination between parents and is an evolutionary stepping-stone toward increasingly complex social systems. Anuran amphibians (frogs and toads) are a classic model of acoustic communication and the vocal repertoires of many species have been characterized in the contexts of advertisement, courtship, and aggression, yet quantitative descriptions of calls elicited in the context of parental care are lacking. The biparental poison frog, Ranitomeya imitator, exhibits a remarkable parenting behavior in which females, cued by the calls of their male partners, feed tadpoles unfertilized eggs. Here, we characterized and compared calls across three social contexts, for the first time including a parental care context. We found that egg-feeding calls share some properties with both advertisement and courtship calls but also had unique properties. Multivariate analysis revealed high classification success for advertisement and courtship calls but misclassified nearly half of egg feeding calls as either advertisement or courtship calls. Egg feeding and courtship calls both contained less identity information than advertisement calls, as expected for signals used in close-range communication where uncertainty about identity is low and additional signal modalities may be used. Taken together, egg-feeding calls likely borrowed and recombined elements of both ancestral call types to solicit a novel, context-dependent parenting response.

A new glassfrog species of the genus Centrolene (Amphibia, Anura, Centrolenidae) from Cordillera del Cóndor, southern Ecuador.

Based on an integrative taxonomical approach, using molecular, morphological, and bioacoustics data, a new species of glassfrog of the genus Centrolene is described from Refugio de Vida Silvestre El Zarza, southern Ecuador. Centrolenezarzasp. nov. is a medium sized species, easily distinguished from all other glassfrogs by its unique combination of characters, such as a shagreen dorsum with elevated warts corresponding to white spots, an evident tympanum, half or more than half of the upper parietal peritoneum covered by iridophores, iridophores absent on all visceral peritonea, including the pericardium, a lobed liver lacking iridophores, males with small projecting humeral spines, the outer edges of forearms and tarsus with a row of enameled warts that often continue into the external edges of Finger IV and/or Toe V, and white or yellowish white iris with thick black reticulations. The new species is closely related to a currently undescribed species and superficially resembles C.condor, C.pipilata, C.solitaria, C.altitudinalis, and C.daidalea. The tadpole and advertisement and courtship calls are described, and the threats to the species survival, mainly represented by habitat loss and contamination due to mining activities, are briefly discussed.

Nathusius’ bats, Pipistrellus nathusii, bypass mating opportunities of their own species, but respond to foraging heterospecifics on migratory transit flights

In late summer, migratory bats of the temperate zone face the challenge of accomplishing two energy-demanding tasks almost at the same time: migration and mating. Both require information and involve search efforts, such as localizing prey or finding potential mates. In non-migrating bat species, playback studies showed that listening to vocalizations of other bats, both con-and heterospecifics, may help a recipient bat to find foraging patches and mating sites. However, we are still unaware of the degree to which migrating bats depend on con-or heterospecific vocalizations for identifying potential feeding or mating opportunities during nightly transit flights. Here, we investigated the vocal responses of Nathusius’ pipistrelle bats, Pipistrellus nathusii, to simulated feeding and courtship aggregations at a coastal migration corridor. We presented migrating bats either feeding buzzes or courtship calls of their own or a heterospecific migratory species, the common noctule, Nyctalus noctula. We expected that during migratory transit flights, simulated feeding opportunities would be particularly attractive to bats, as well as simulated mating opportunities which may indicate suitable roosts for a stopover. However, we found that when compared to the natural silence of both pre-and post-playback phases, bats called indifferently during the playback of conspecific feeding sounds, whereas P. nathusii echolocation call activity increased during simulated feeding of N. noctula. In contrast, the call activity of P. nathusii decreased during the playback of conspecific courtship calls, while no response could be detected when heterospecific call types were broadcasted. Our results suggest that while on migratory transits, P. nathusii circumnavigate conspecific mating aggregations, possibly to save time or to reduce the risks associated with social interactions where aggression due to territoriality might be expected. This avoidance behavior could be a result of optimization strategies by P. nathusii when performing long-distance migratory flights, and it could also explain the lack of a response to simulated conspecific feeding. However, the observed increase of activity in response to simulated feeding of N. noctula, suggests that P. nathusii individuals may be eavesdropping on other aerial hawking insectivorous species during migration, especially if these occupy a slightly different foraging niche.

A new species of rain frog (Anura: Strabomantidae: Pristimantis) from the Guiana Shield and amended diagnosis of P. ockendeni (Boulenger, 1912)

Pristimantis is already the most speciose genus among vertebrates, yet the current number of species remains largely underestimated. A member of the P. unistrigatus species group from the Guiana Shield has been historically misidentified as P. ockendeni, a species described from southern Peru. We combined mitochondrial (16S and COI) and nuclear (RAG1) loci, external morphology, skull osteology (μ-CT scan), vocalization (advertisement and courtship calls), geographic distribution and natural history data to differentiate the Guiana Shield populations from P. ockendeni, and describe them as a new species. The new species is crepuscular and nocturnal and inhabits the understory of unflooded (terra firme) forests in Brazil, Guyana and Suriname. It is phylogenetically related to P. arda­lonychus, P. martiae and undescribed species from Brazilian Amazonia. The new species notably differs from P. ockendeni and its congeners in the P. unistrigatus species group occurring in the Guiana Shield by the combination of the following characters: absence of dentigerous processes of vomers, presence of vocal slits in males, body size (SVL 16.2–20.7 mm in males and 21.4–25.7 mm in females), advertisement call (call with 4–6 notes, call duration of 158–371 ms and dominant frequency of 3,466–4,521 Hz) and translucent groin coloration in life. To facilitate the recognition and description of cryptic species previously hidden under the name P. ockendeni, we provide an amended diagnosis of this taxon based on external morphology and advertisement call of specimens recently collected nearby the type locality and additional localities in southwestern Amazonia.

Male antiphonal calls and phonotaxis evoked by female courtship calls in the large odorous frog (Odorrana graminea).

Acoustic communication plays a vital role in frog reproduction. In most anuran species, long-distance sound communication is one-way from males to females; during the reproductive season, males produce species-specific advertisement calls to attract gravid females, and females are generally silent but perform phonotactic movements that lead to amplexus. One exception is the concave-eared torrent frog (Odorrana tormota). In this species, females produce courtship calls that elicit antiphonal vocalizations by males, followed by precise phonotactic movements. The large odorous frog O. graminea (previously Odorrana livida) in southern China is subject to the same environmental constraints as O. tormota, with which it is sympatric; it is unclear whether their sound communication is one-way or bidirectional. Here, we provide the first data on female O. graminea vocalizations and their functions. Using playbacks of female calls, we conducted acoustic behavioral experiments in the laboratory in response to which males emitted single- or multi-note antiphonal calls with a varying fundamental frequency. Moreover, they were attracted to female call playbacks, exhibiting precise phonotaxis. The female courtship call-male response interaction thus forms a duet between partners of a receptive pair. These results demonstrate that this unique communication system likely reflects an adaptation to an environment in which short-distance communication is at a premium given the high levels of ambient noise.

The courtship call of <i>Bokermannohyla ibitiguara</i> (Anura: Hylidae) and details of its mating behavior

Complex courtships have been described for neotropical frogs, but detailed quantifications of calls emitted during this behavior are still rare. Herein, we describe the courtship call of Bokermannohyla ibitiguara, a gladiator tree frog from the Brazilian Cerrado, as well as the female behavior during courtship, and the clutch characteristics. Moreover, we statistically compare the acoustic parameters of the advertisement and courtship calls. We observed that the female also touches the male during courtship and that the courtship call is overall similar to the long note of the advertisement call. However, we uncovered significant differences in frequencies and pulses between these two call types emitted by the same male. This ability to modify call parameters is consistent with previous results in aggressive contexts and reinforces sexual selection as a strong mechanism shaping call variation in this species. This is the third courtship call described for the genus and we emphasize that the description of rare behaviors, even in artificial conditions, is important to advance the field of behavioral ecology across taxa.

Cross-modal facilitation of auditory discrimination in a frog.

Stimulation in one sensory modality can affect perception in a separate modality, resulting in diverse effects including illusions in humans. This can also result in cross-modal facilitation, a process where sensory performance in one modality is improved by stimulation in another modality. For instance, a simple sound can improve performance in a visual task in both humans and cats. However, the range of contexts and underlying mechanisms that evoke such facilitation effects remain poorly understood. Here, we demonstrated cross-modal stimulation in wild-caught túngara frogs, a species with well-studied acoustic preferences in females. We first identified that a combined visual and seismic cue (vocal sac movement and water ripple) was behaviourally relevant for females choosing between two courtship calls in a phonotaxis assay. We then found that this combined cross-modal stimulus rescued a species-typical acoustic preference in the presence of background noise that otherwise abolished the preference. These results highlight how cross-modal stimulation can prime attention in receivers to improve performance during decision-making. With this, we provide the foundation for future work uncovering the processes and conditions that promote cross-modal facilitation effects.

Octopamine affects courtship call structure in male Acheta domesticus crickets

Secondary sexual displays vary considerably in both type and structure both within and across animal species. Although such variation is of keen interest to evolutionary biologists, the functional factors driving variation in male displays are poorly understood. In crickets, acoustic calls are produced by muscular contractions via stridulation of file and scraper wing components. We tested the effect of varying octopamine, an important biogenic amine neurohormone in invertebrates, on call production in male Acheta domesticus house crickets by blocking the octopamine receptors that influence skeletal muscle function with epinastine, a synthetic octopamine antagonist. We then measured male courtship calls and analyzed the call structure to quantify the differences in call structure based on the changes in carrier frequency, and whether chirps or ticks are a more prevalently expressed frequency in treated vs untreated males. Males treated with epinastine exhibited clear differences in call structure compared to untreated controls, such that epinastine-treated males were more likely to produce simpler calls and to exhibit their carrier frequencies as ticks rather than chirps. Thus, we were able to directly modify male courtship calling performance during mating interactions by altering the neuropharmacological milieu, demonstrating the potential role of biogenic amines in contributing to the diversity of call types in nature.

Acoustic modulation of reproductive hormones in the blacktail shiner, Cyprinella venusta, a soniferous cyprinid

Animal communication networks consist of multisensory signals and often include an acoustic element. Many freshwater fishes, including the blacktail shiner, Cyprinella venusta , produce specific vocalizations during courtship and agonistic behaviours. Similar to other vocal taxa, fish communication networks are vulnerable to noise pollution. The dominant frequencies of anthropogenic noise often overlap spectrally with animal acoustic signals. To investigate the role of acoustic signalling in breeding soniferous fishes in a physiological context, we conducted a series of acoustic playback trials. We measured waterborne levels of oestradiol (E2) and prostaglandin F2 α (PGF2 α ) in gravid females exposed to courtship calls, and levels of 11-ketotestosterone (11KT) in males exposed to agonistic calls. In a separate series of trials, we exposed individuals to calls masked with bridge traffic noise. Hormone levels were quantified using enzyme-linked immunosorbent assays (ELISA) and analysed using repeated measures ANOVAs. Gravid females exhibited a significant drop in E2 ( P = 0.023) and an increase in PGF2 α during courtship calls ( P = 0.01). Our research suggests that growl signals contribute to the onset of spawning behaviours in female C. venusta and this response may be dampened by anthropogenic noise pollution. • We examined effects of anthropogenic noise on acoustic signalling in C. venusta. • Males produce growls (courtship/spawning) and knocks (male–male aggression). • Unmasked growls modulated levels of reproductive hormones in gravid females. • Males did not respond hormonally to unimodal stimuli. • Fish exposed to masked vocalizations did not exhibit hormonal changes.

The advertisement and courtship calls of Phyllobates bicolor (Anura: Dendrobatidae) from a natural population in the Colombian pacific cloud forests.

The advertisement and courtship calls of Phyllobates bicolor (Anura: Dendrobatidae) from a natural population in the Colombian pacific cloud forests.

Female large odorous frogs (Odorrana graminea) prefer males with higher nonlinear vocal components.

In anurans, the complexity of courtship calls may affect female mate choice. The current study suggests that nonlinear phenomena (NLP) components can contribute to increasing complexity in courtship calls and attracting female attention. The results of a recent study showed that calls of large odorous frog (Odorrana graminea) contained NLP components. However, whether the nonlinear components of courtship calls in O. graminea improve male attractiveness remains unknown. We hypothesized that female O. graminea would prefer males producing calls with a higher proportion of NLP components (P‐NLP‐C). To test this hypothesis, we recorded the advertisement calls of 28 males and confirmed that the P‐NLP‐C was significantly positively related to body size. We also measured the body size of natural amplectant males and non‐amplectant males in the field and found that amplectant males had larger body sizes than non‐amplectant males, and the results of two‐choice amplexus experiments similarly revealed a female preference for males with larger body sizes. Additionally, phonotaxis experiments also revealed that females preferred male calls with a high P‐NLP‐C. The results suggest that a higher P‐NLP‐C in calls can enhance male attractiveness, and the P‐NLP‐C may provide key information about male body conditions for female O. graminea. Our study provides a new insight for better understanding the role of NLP in anuran mate selection.

Individuality, species-specific features, and female discrimination of male southern white rhinoceros courtship calls.

Male vocalizations associated with courtship can play a key role in mate selection. They may help females obtain information about males' quality and identity and/or may contain species-specific properties that help prevent interspecies breeding. Despite vocalizations being a prominent part of the courtship of white rhinos, the role that they play in white rhino breeding behaviour has not been extensively studied. Both southern (SWR) and critically endangered northern white rhino (NWR) males intensively vocalize during courtship with hic calls. We examined these calls and found that call properties differed between NWR and SWR males. In addition, we found that individual SWR males could be identified with a high degree of accuracy using their hic calls and that the signature information capacity in hic calls would allow females to individually recognize about 11 adult males living in or moving through their home-ranges, which may help with mate selection. Then, we conducted playback experiments with wild anoestrus SWR females. The females discriminated between the NWR and SWR hic calls and between the SWR hic and SWR pant calls. However, we only found differences in the latency of observed behaviours, not in their duration or in the intensity of females' reaction. This might suggest that females which are not in oestrus are not highly responsive to a male's motivation (i.e., seeking contact or mating), but are more interested in assessing his dominance status or familiarity. Ultimately, our results indicate that courtship hic calls encode information which might help females choose mating partners.

Male Barn Swallows Tolerate Nestling-Like Courtship Calls of Rival Males

Animals often exhibit conspicuous, and sometimes curious, courtship traits, such as nestling-like courtship display in birds, though modern studies of nestling-like courtship display (and calls) are virtually lacking. An exception is previous experiments on the barn swallowHirundo rustica, demonstrating that females are equally attracted to playback of two structurally similar calls, nestling-like male courtship calls and nestling food-begging calls. The experiments support the sensory trap hypothesis, i.e., that male signals mimic nestling stimuli to exploit female parental care for nestlings. However, female attraction might not be the sole function of nestling-like traits, and males might also have a sensory bias toward nestling-like traits, in which males would be less aggressive toward characteristics typical of immature individuals. Here, I conducted playback experiments to study the function of nestling-like male courtship calls in the context of male–male interactions. Playback of male courtship songs induced frequent approaches by neighbouring males, while nestling-like male courtship calls or nestling food-begging calls induced fewer approaches, though male responses to the latter two vocalisations increased when approaching the nestling period. The observed pattern indicates that, by mimicking immature individuals, males attract intended signal receivers (i.e., females) while avoiding interference from eavesdroppers (i.e., neighbouring males). This unique function can explain why species with parental care exhibit immature-like behaviour.

The potential role of reproductive interference in the decline of native green treefrogs following Cuban treefrog invasions

Reproductive interference is increasingly implicated in the decline of native taxa following alien species invasions. We examined reproductive interference in the context of acoustic modulation of hormone levels and declines in native green treefrogs (Hyla cinerea) following invasions of Cuban treefrogs (Osteopilus septentrionalis) in the southeastern United States. The motivation for our study stemmed from similarities in spectro-temporal properties of Cuban treefrog courtship calls and green treefrog aggressive calls. The aggressive calls of green treefrogs stimulate glucocorticoid production in rival conspecific males, which suppresses androgen production and reproductive behavior. We thus hypothesized that native male green treefrogs exposed to advertisement calls of this invasive species exhibit increased levels of circulating glucocorticoids. We found that broadcast aggressive calls of green treefrogs stimulated glucocorticoid production in conspecific males but that Cuban treefrog vocalizations did not increase glucocorticoid levels in green treefrogs. In natural choruses, the density of calling male green treefrogs and the proportion of non-calling males were positively correlated with glucocorticoid levels and negatively correlated with androgens, whereas body size was positively correlated with androgens. After controlling for these variables, there was no evidence that hormone levels or behavior differed in choruses of green treefrogs in the presence and absence of Cuban treefrogs. Together, our results suggest that interactions among male green treefrogs modulate hormone levels but that the presence of Cuban treefrogs, calling or not, is not altering levels of glucocorticoids or androgens in breeding male green treefrogs.