J Comp Physiol A DOI 10.1007/s00359-014-0923-1 REVIEW From uni- to multimodality: towards an integrative view on anuran communication Iris Starnberger · Doris Preininger · Walter Hödl Received: 25 March 2014 / Revised: 6 June 2014 / Accepted: 8 June 2014 © The Author(s) 2014. This article is published with open access at Springerlink.com Abstract Undeniably, acoustic signals are the predomi- Introduction nant mode of communication in frogs and toads. Acousti- cally active species are found throughout the vast diversity A great diversity of signalling strategies and behaviours of anuran families. However, additional or alternative sig- can be observed during animal communication shaped nal modalities have gained increasing attention. In several by sexual selection and the environmental constraints anurans, seismic, visual and chemical communications (Narins and Zelick 1988; Endler 1992; Endler and Thery have convergently evolved due to ecological constraints 1996; Leal and Fleishman 2004; Bradbury and Vehren- such as noisy environments. The production of a visual camp 2011). In several species, not only one communi- cue, like the inevitably moving vocal sac of acoustically cation mode, but two or more are used simultaneously or advertising males, is emphasized by conspicuously col- sequentially across multiple sensory components (Partan oured throats. Limb movements accompanied by dynamic and Marler 1999; reviewed in Candolin 2003; Hebets and displays of bright colours are additional examples of strik- Papaj 2005; Otovic and Partan 2009). Multimodal commu- ing visual signals independent of vocalizations. In some nication is discussed for a wide range of species includ- multimodal anuran communication systems, the acoustic ing spiders (e.g. Uetz et al. 2009), fish (e.g.V an Staaden component acts as an alert signal, which alters the receiver and Smith 2011), reptiles (reviewed in Hews and Martins attention to the following visual display. Recent find- 2013), birds (e.g. Wiley 1973) and mammals (e.g. Bro- ings of colourful glands on vocal sacs, producing volatile Jorgensen and Dabelsteen 2008), but has been difficult to species-specific scent bouquets suggest the possibility of test until recently. Complex signalling repertoires are chal- integration of acoustic, visual and chemical cues in species lenging to investigate and valid hypotheses testing remains recognition and mate choice. The combination of signal difficult in scientific experiments (Leger 1993; Partan and components facilitates a broadened display repertoire in Marler 2005; Rosenthal 2007). However, advances in con- challenging environmental conditions. Thus, the complex- ceptual framework and technical equipment have greatly ity of the communication systems of frogs and toads may improved research in this field. In anuran amphibians, calls have been underestimated. are the predominant signals in inter- and intrasexual com- munication (Ryan 1985; Gerhardt and Huber 2002; Dor- Keywords Bioacoustics · Visual signals · Chemical cas et al. 2010). Vocalizations are the most conspicuous signals · Frogs · Toads · Signal modalities display to human observers and as a consequence other signal modalities have traditionally received less atten- tion (Waldman and Bishop 2004; Coleman 2009) or may I. Starnberger (*) · D. Preininger · W. Hödl have been misjudged, e.g. due to experimenters’ lack of Department of Integrative Zoology, University of Vienna, visual sensitivity at night (Buchanan 1993). Amphibians in Althanstraße 14, 1090 Vienna, Austria general and frogs in particular are excellent model organ- e-mail: [email protected] isms to experimentally investigate communication strate- D. Preininger gies both in the laboratory and under natural conditions, Vienna Zoo, Maxingstraße 13b, 1130 Vienna, Austria as they are hardly disturbed by observers and can be easily 1 3 J Comp Physiol A manipulated (Narins et al. 2003; Hirschmann and Hödl have evolved to match the tuning of the receiver’s auditory 2006; Taylor et al. 2007). system (Gerhardt and Schwarz 2001). This review highlights anuran signalling strategies in Any message needs to be successfully transmitted to addition to calling to promote an integrative multimodal elicit the intended response in the receiver (Shannon 1948); view on anuran communication. clear reception is a minimum requirement for a successful communication system (Shannon 1948; Endler 1993). The most basic requirement for a call is to be detectable against Anurans are born to call background noise and to minimize transmission degrada- tion and attenuation of the environment. High levels of “Frogs enjoy life and express their joy by song” (Dickerson biotic and abiotic environmental noise may mask calls and 1908). Much has changed since these lines were written, hamper accurate detection, discrimination and localiza- and due to numerous studies on acoustic signals in anu- tion (or increase response latency) by receivers (Bee 2008; rans, we have a very different albeit less romantic opinion Vélez et al. 2012, 2013; Caldwell and Bee 2014). However, on signal content and function. The male advertisement signal properties and strategies have been shaped over evo- call attracts conspecific females and signals the readiness lutionary time to enhance transmission in their respective to defend territories and calling sites to rival males; hence acoustic environments by preferences of receivers. calling behaviour plays a vital role in reproductive success To improve signalling effectiveness, anuran species and is essential for sexual selection (Narins et al. 2007). organize calling periods temporally (Klump and Ger- Many frogs and toads have more than one species-specific hardt 1992), adjust their calls to random intercall intervals call type. In addition to the prominent advertisement call (Zelick and Narins 1985) or inhibit calling heterospecif- a variety of discrete or continuous call types correspond ics (Schwartz and Wells 1983). In dense breeding aggre- to specific functions, such as the encounter call (McDiar- gations, concurrently chorusing conspecifics can achieve mid and Adler 1974), the courtship call, the territorial call, release from masking interference by spatial separation the distress call, and the release call (all reviewed in Wells from the biotic sound source (Grafe 1996; Bee 2008). In 1977). the presence of continuous background noise, the recog- nition and detection of acoustic signals can be impaired How frogs and toads get their acoustic message across dependent on the relative noise level and frequency (Feng and Schul 2006). In torrent frogs, high-frequency and in In numerous species, audio-spectral and temporal call char- some cases even ultrasonic calls enhance the signal-to- acteristics and their function as static or dynamic signal noise ratio relative to low-frequency stream noise and are properties were investigated during the last decades (Ger- suggested to be an adaptive strategy in the presence of con- hardt and Huber 2002). Robert R. Capranica was the first tinuous noise (Narins et al. 2004; Feng et al. 2006; Boeckle to combine electrophysiological analyses, behavioural data et al. 2009). For example, stream-associated species of the and synthetic playback calls to study “what the frog’s ear genus Staurois emit higher pitched calls than other ranid tells the frog’s brain” (Capranica and Moffat 1983; and see species of comparable body size (Fig. 1). Simmons 2012). As a mentor, he inspired future genera- Acoustic adaptations to overcome signalling constraints tions to study animal communication by means of integra- are limited and often opposed by morphological and phylo- tive research in the lab and also in the field and opened-up genetic constraints—but most importantly by sexual selec- a new field which likewise attracted bioacousticians and tion (e.g. Ryan and Rand 2003). In many cases, species evolutionary biologists. As a consequence, anuran vocal develop new, often spectacular ways of communication in signals and their perception are nowadays an exceptionally which the production of acoustic signals is of less impor- well-understood subject in biology. Anuran call characteris- tance or even completely abandoned (Rödel et al. 2003; tics correlate with body size and mass across species (Ryan Hirschmann and Hödl 2006; Preininger et al. 2009). 1988; Gingras et al. 2013) and within species (e.g. Narins and Smith 1986; Robertson 1990) a pattern described as the Deep croak hypothesis by Davies and Halliday (1979); When calling is not enough: from single and see Gingras et al. (2013). Furthermore, call parameters to multimodality signal species identity (e.g. Blair 1958; Hödl 1977), and in some species exhibit “individual” distinctive signatures “Compared to salamanders, olfactory cues and visual dis- (Bee and Gerhardt 2001a, b; Gasser et al. 2009), but not in plays seem to be unimportant to preamplectic courtship others (Bee 2003). Advertisement calls also regulate male in most anurans, but some tactile cues are used by certain spacing (e.g. Brenowitz 1989), increase the male’s attrac- species.” Duellman and Trueb (1986) wrote in their widely tiveness to females (e.g. Ryan and Keddy-Hector 1992) and used textbook “Biology of Amphibians” published almost 1 3 J Comp Physiol A 9500 9000 y = 8688.4+(-1650.6)*ln x 8500 r ² = 0.325 8000 SD = 1151.4 7500 7000 n = 76 6500 6000 5500 5000 4500 4000 3500 3000 2500 Dominant frequency (Hz) 2000 1500 1000 500 0 0 50 100 150 200 250 SVL (mm) Fig. 1 Logarithmic regression of call