Doris Preininger

Multimodal Communication in a Noisy Environment: A Case Study of the Bornean Rock Frog Staurois parvus

High background noise is an impediment to signal detection and perception. We report the use of multiple solutions to improve signal perception in the acoustic and visual modality by the Bornean rock frog, Staurois parvus. We discovered that vocal communication was not impaired by continuous abiotic background noise characterised by fast-flowing water. Males modified amplitude, pitch, repetition rate and duration of notes within their advertisement call. The difference in sound pressure between advertisement calls and background noise at the call dominant frequency of 5578 Hz was 8 dB, a difference sufficient for receiver detection. In addition, males used several visual signals to communicate with conspecifics with foot flagging and foot flashing being the most common and conspicuous visual displays, followed by arm waving, upright posture, crouching, and an open-mouth display. We used acoustic playback experiments to test the efficacy-based alerting signal hypothesis of multimodal communication. In support of the alerting hypothesis, we found that acoustic signals and foot flagging are functionally linked with advertisement calling preceding foot flagging. We conclude that S. parvus has solved the problem of continuous broadband low-frequency noise by both modifying its advertisement call in multiple ways and by using numerous visual signals. This is the first example of a frog using multiple acoustic and visual solutions to communicate in an environment characterised by continuous noise.

Multimodal signaling in the Small Torrent Frog (Micrixalus saxicola) in a complex acoustic environment

Many animals use multimodal (both visual and acoustic) components in courtship signals. The acoustic communication of anuran amphibians can be masked by the presence of environmental background noise, and multimodal displays may enhance receiver detection in complex acoustic environments. In the present study, we measured sound pressure levels of concurrently calling males of the Small Torrent Frog (Micrixalus saxicola) and used acoustic playbacks and an inflatable balloon mimicking a vocal sac to investigate male responses to controlled unimodal (acoustic) and multimodal (acoustic and visual) dynamic stimuli in the frogs’ natural habitat. Our results suggest that abiotic noise of the stream does not constrain signal detection, but males are faced with acoustic interference and masking from conspecific chorus noise. Multimodal stimuli elicited greater response from males and triggered significantly more visual signal responses than unimodal stimuli. We suggest that the vocal sac acts as a visual cue and improves detection and discrimination of acoustic signals by making them more salient to receivers amidst complex biotic background noise.

Communication in Noisy Environments i: Acoustic Signals of Staurois Latopalmatus Boulenger 1887

Abstract Physical aspects of anurans constrain sound production, and noisy habitats pose a challenge to signal recognition and detection. Habitat acoustics impose selection on anuran calls within the phylogenetic and morphological constraints of the vocal apparatus of senders and the auditory system of receivers. Visual displays and alerting calls can be used as alternative or additional signal strategies to overcome these problems. In this study, we investigated sound pressure levels and spectral features of calls of the ranid rock-skipper frog Staurois latopalmatus, exclusively found at waterfalls of Bornean streams. A total of 176 calls and waterfall recordings were analyzed to characterize acoustic signals and environmental noise. To obtain information on possible signal adaptations, dominant frequency and snout–vent length of 75 ranid species were collected from the literature and compared to our findings. Distributions along acoustically characterized rapids and waterfalls within a 1-km long river transect showed that S. latopalmatus exclusively occurs in noisy habitats. Two different call types could be distinguished in S. latopalmatus: a short, single-note call and a long, multi-note call. Both calls had a lower sound pressure than the noise produced by waterfalls. The dominant frequency analyses revealed that the signal-to-noise ratio can be maximized within high frequency bands around 5 kHz. Correlations of frequency versus body size in ranids indicated that S. latopalmatus has higher call frequencies than predicted by body size, suggesting acoustic adaptation to environmental noise. We conclude that acoustic signal efficiency in environments with low-frequency dominated noise can only be attained through high frequency calls. The single-note call is interpreted as an alerting signal directing the receivers attention to a subsequent visual signal. The multi-note call is interpreted as a graded aggressive call. We suggest that microhabitat characteristics represent strong selective pressures on the form of acoustic signals. Short calls with a narrow frequency band could reflect a trade-off among detectabilty, sound propagation and discrimination between individuals.

Communication in Noisy Environments Ii: Visual Signaling Behavior of Male Foot-flagging Frogs staurois Latopalmatus

Abstract Acoustic signals are constrained by background noise. Visual signals are an alternative or complementary communication mode in noisy habitats and play a fundamental role in anuran communication. The Bornean rock-skipper frog, Staurois latopalmatus, is a diurnal species living along fast-flowing streams and waterfalls. Males perform foot-flagging displays with either one or two legs to advertise their readiness to defend their territories. In quantitative video analyses of visual displays during 14 male-male agonistic interactions, totaling 106 minutes, foot flagging performed in the direction of the interacting male was the most common display and was performed at a higher rate than advertisement calls. According to a dyadic transition matrix, foot flagging was preceded by foot-flagging displays of interacting males. Advertisement calls were temporally coupled with foot flaggings and act as introductory components to direct the receivers attention to the subsequent visual display. We conclude that foot flagging acts as a spacing mechanism and may have resulted from the ritualization of agonistic male behavior to minimize physical attacks.

Don’t get the blues: conspicuous nuptial colouration of male moor frogs (Rana arvalis) supports visual mate recognition during scramble competition in large breeding aggregations

Conspicuous male colouration is expected to have evolved primarily through selection by female choice. In what way conspicuous colours could be advantageous to males scrambling for mates remains largely unknown. The moor frog (Rana arvalis) belongs to the so-called explosive breeders in which spawning period is short; intrasexual competition is strong, and males actively search and scramble for females. During breeding, male body colouration changes from a dull brown (similar to females) to a conspicuous blue, and we wanted to test if male blueness influences mating success or facilitates male mate recognition. To do so, we first measured the colour of mated and non-mated males using a spectrophotometer. In an experiment, we then analysed interactions of actual male moor frogs in natural spawning aggregations with a brown (resembling a female or a non-breeding male) and a blue model frog. Mated and non-mated males did not differ in colouration, suggesting that female choice based on colour traits was unlikely. In our behavioural experiment, male moor frogs spent significantly more time in contact and in amplexus with the brown model than with the blue model. Our results suggest that the nuptial colouration in moor frogs can act as a new type of visual signal in anurans evolved to promote instantaneous mate recognition allowing males to quickly move between rivals while scrambling for females.

The anuran vocal sac: a tool for multimodal signalling

Although in anurans the predominant mode of intra- and intersexual communication is vocalization, modalities used in addition to or instead of acoustic signals range from seismic and visual to chemical. In some cases, signals of more than one modality are produced through or by the anuran vocal sac. However, its role beyond acoustics has been neglected for some time and nonacoustic cues such as vocal sac movement have traditionally been seen as an epiphenomenon of sound production. The diversity in vocal sac coloration and shape found in different species is striking and recently its visual properties have been given a more important role in signalling. Chemosignals seem to be the dominant communication mode in newts, salamanders and caecilians and certainly play a role in the aquatic life phase of anurans, but airborne chemical signalling has received less attention. There is, however, increasing evidence that at least some terrestrial anuran species integrate acoustic, visual and chemical cues in species recognition and mate choice and a few secondarily mute anuran species seem to fully rely on volatile chemical cues produced in glands on the vocal sac. Within vertebrates, frogs in particular are suitable organisms for investigating multimodal communication by means of experiments, since they are tolerant of disturbance by observers and can be easily manipulated under natural conditions. Thus, the anuran vocal sac might be of great interest not only to herpetologists, but also to behavioural biologists studying communication systems.

Divergent receiver responses to components of multimodal signals in two foot-flagging frog species.

Multimodal communication of acoustic and visual signals serves a vital role in the mating system of anuran amphibians. To understand signal evolution and function in multimodal signal design it is critical to test receiver responses to unimodal signal components versus multimodal composite signals. We investigated two anuran species displaying a conspicuous foot-flagging behavior in addition to or in combination with advertisement calls while announcing their signaling sites to conspecifics. To investigate the conspicuousness of the foot-flagging signals, we measured and compared spectral reflectance of foot webbings of Micrixalus saxicola and Staurois parvus using a spectrophotometer. We performed behavioral field experiments using a model frog including an extendable leg combined with acoustic playbacks to test receiver responses to acoustic, visual and combined audio-visual stimuli. Our results indicated that the foot webbings of S. parvus achieved a 13 times higher contrast against their visual background than feet of M. saxicola. The main response to all experimental stimuli in S. parvus was foot flagging, whereas M. saxicola responded primarily with calls but never foot flagged. Together these across-species differences suggest that in S. parvus foot-flagging behavior is applied as a salient and frequently used communicative signal during agonistic behavior, whereas we propose it constitutes an evolutionary nascent state in ritualization of the current fighting behavior in M. saxicola.

Increased androgenic sensitivity in the hind limb muscular system marks the evolution of a derived gestural display

Significance Diverse species signal using limb gestures, but little is known about how selection incorporates such movements into display routines. We study this issue in a tropical frog that produces complex waving displays with its hind limbs. We find not only that androgenic hormones activate such signaling behavior, but also that the signal’s recent evolution is marked by a dramatic increase in androgenic sensitivity of the thigh muscles that control hind limb maneuvering. Moreover, we demonstrate that this muscular phenotype mirrors that which is found in the larynx of other frogs that primarily produce androgen-dependent vocalizations as social signals. We therefore uncover strong coevolution between the emergence of complex sexual gestural signals and enhanced androgenic signaling mechanisms in the muscular system. Physical gestures are prominent features of many species’ multimodal displays, yet how evolution incorporates body and leg movements into animal signaling repertoires is unclear. Androgenic hormones modulate the production of reproductive signals and sexual motor skills in many vertebrates; therefore, one possibility is that selection for physical signals drives the evolution of androgenic sensitivity in select neuromotor pathways. We examined this issue in the Bornean rock frog (Staurois parvus, family: Ranidae). Males court females and compete with rivals by performing both vocalizations and hind limb gestural signals, called “foot flags.” Foot flagging is a derived display that emerged in the ranids after vocal signaling. Here, we show that administration of testosterone (T) increases foot flagging behavior under seminatural conditions. Moreover, using quantitative PCR, we also find that adult male S. parvus maintain a unique androgenic phenotype, in which androgen receptor (AR) in the hind limb musculature is expressed at levels ∼10× greater than in two other anuran species, which do not produce foot flags (Rana pipiens and Xenopus laevis). Finally, because males of all three of these species solicit mates with calls, we accordingly detect no differences in AR expression in the vocal apparatus (larynx) among taxa. The results show that foot flagging is an androgen-dependent gestural signal, and its emergence is associated with increased androgenic sensitivity within the hind limb musculature. Selection for this novel gestural signal may therefore drive the evolution of increased AR expression in key muscles that control signal production to support adaptive motor performance.

Ontogenetic Change of Signal Brightness in the Foot-Flagging Frog Species Staurois parvus and Staurois guttatus

Abstract:  Adult individuals of several anuran species exhibit conspicuous visual displays during intraspecific communication. While signal properties in adults have been subject to an increasing number of studies, little is known about the variation of visual signals in juveniles and during ontogenetic changes. Foot-flagging signals of the Bornean frogs Staurois guttatus and S. parvus were observed in juveniles a few days after metamorphosis. We investigated color parameters of foot webbings and body coloration of individuals bred at the Vienna Zoo, and their relation to age and body size using spectrophotometry. Our results indicate that the brightness of foot webbings of S. guttatus and S. parvus increased with increasing age. Additionally, we compared the results with measurements of adult individuals from a population in Brunei and discuss possible differences related to diet and age as well as the habitat use of juveniles and adults. We suggest that the ontogenetic increase in foot-webbing brightness enhances visual conspicuousness and the signal-to-noise ratio of the visual signal with sexual maturity and potentially functions as cue to the age of the signaler.

Multimodal Signal Testing Reveals Gestural Tapping Behavior in Spotted Reed Frogs

Abstract In the majority of anuran species, acoustic signals are the dominant mode of inter- and intrasexual communication. Male calls are always accompanied by the movement of a more or less conspicuous vocal sac—a potential visual cue. Reed frogs possess a striking vocal sac with a colorful patch of gland tissue clearly visible once the vocal sac is inflated during acoustic signaling. To investigate the visual signal function of vocal sac and gular gland, we presented male Spotted Reed Frogs (Hyperolius puncticulatus) with unimodal and multimodal signal playbacks of conspecific rivals in their natural habitat and recorded their behavioral responses. We found no difference in receiver response to unimodal advertisement call stimuli and to multimodal stimulus presentations of calls combined with visual signals of an artificial vocal sac with or without a gular patch, moving synchronously or asynchronously with the call playback. The inflations of a vocal sac with a colorful gular patch did not alter receiver response and neither increase nor decrease signal salience during male–male communication. Interestingly, males frequently displayed a novel hind and front foot-tapping behavior in response to all playbacks. Comparison of male responses to advertisement and aggressive call playbacks showed that Spotted Reed Frogs approached the sound source less during aggressive call presentations. Tapping behavior was not influenced by either call playback. We suggest that the gestural tapping behavior might act as vibrational signal and discuss its potential signal function in male contests and courtship for females.