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Auditory Communication Processing in Bats: What We Know and Where to Go

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Auditory Communication Processing in Bats: What We Know and Where to Go Behavioral Neuroscience © 2019 American Psychological Association 2019, Vol. 133, No. 3, 305–319 0735-7044/19/$12.00 http://dx.doi.org/10.1037/bne0000308 Auditory Communication Processing in Bats: What We Know and Where to Go Angeles Salles, Kirsten M. Bohn, and Cynthia F. Moss Johns Hopkins University Bats are the second largest mammalian order, with over 1,300 species. These animals show diverse behaviors, diets, and habitats. Most bats produce ultrasonic vocalizations and perceive their environment by processing information carried by returning echoes of their calls. Echolocation is achieved through a sophisticated audio-vocal system that allows bats to emit and detect frequencies that can range from ten to hundreds of kilohertz. In addition, most bat species are gregarious, and produce social communication calls that vary in complexity, form, and function across species. In this article, we (a) highlight the value of bats as model species for research on social communication, (b) review behavioral and neurophysi- ological studies of bat acoustic communication signal production and processing, and (c) discuss important directions for future research in this field. We propose that comparative studies of bat acoustic communication can provide new insights into sound processing and vocal learning across the animal kingdom. Keywords: bats, Chiroptera, communication, auditory processing Understanding how the brain processes communication sounds particular, we aim to (a) discuss the relevance of bats as model is a key topic in neuroscience. Researchers have used a variety of species to broaden our understanding of acoustic communication animal models to tackle this problem, such as mice, birds, and in mammals, (b) review what is currently known about neural primates, yet our understanding of vocal communication process- activity evoked by social calls at different levels of the bat auditory ing, particularly when it comes to complex, functionally charac- pathway, and (c) discuss new questions and techniques that we terized signals, remains rudimentary. Although extensive research believe will be fundamental to advancing knowledge of the mech- has been directed at the production and processing of echolocation anisms of acoustic communication in bats and other animals. signals in bats, comparably fewer studies have investigated social communication signals. Here, we discuss how and why research on bat models can add fundamental insight to a broader under- What We Know standing of vocal communication in the animal kingdom. Past literature reviews have considered a variety of aspects of bat social Bats Are Social Animals With Diverse Adaptations communication, such as call diversity, evolution, and ecology (Altringham, McOwat, & Hammond, 2011; Chaverri, Ancillotto, Bats, mammals belonging to the order Chiroptera, are a group of & Russo, 2018; Gillam & Fenton, 2016). Our aim here is to focus over 1,300 species with the common characteristic that their fore- on what is known about the production and processing of vocal limbs are adapted as wings to support powered flight (Neuweiler & communication signals and to discuss future steps and challenges Covey, 2006). Chiroptera is the second largest order of mammals to unraveling acoustic communication mechanisms in bats. In (the largest order being rodents), comprising about 20% of all known mammalian species (Tsang, Cirranello, Bates, & Simmons, 2016). The majority of bat species use echolocation to orient and This document is copyrighted by the American Psychological Association or one of its allied publishers. navigate in the environment, even in complete darkness. Bats are This article is intended solely for the personal use of the individual user and is not to be disseminated broadly. This article was published Online First May 2, 2019. adapted to diverse niches, showing tremendous variety in diet and Angeles Salles, Kirsten M. Bohn, and Cynthia F. Moss, Department of habitat complexity, which, in turn, coevolves with neural struc- Psychological and Brain Sciences, Johns Hopkins University. tures that support auditory processing and spatial memory (Safi & We thank the following funding agencies for the resources that allowed Dechmann, 2005). Bats stand out among mammals not only as us to prepare this review: Human Frontiers Science Program Fellowship flying echolocators but also for their gregariousness. By far, the awarded to Angeles Salles (LT000220/2018), Brain Initiative (NSF-FO majority of bats live in social groups (Bradbury & Vehrencamp, 1734744, Air Force Office of Scientific Research (FA9550-14–1- 1977; Kerth, 2008; McCracken & Wilkinson, 2000), from small 0398NIFTI), and Office of Naval Research (N00014-17–1-2736). Cynthia tight-knit clusters (e.g., Phyllostomus hastatus [McCracken & F. Moss acknowledges the support of a Sabbatical Award from the James McKeen Cattell Fund. Bradbury, 1981]) to colonies comprising millions of individuals Correspondence concerning this article should be addressed to Angeles (e.g., Tadarida brasiliensis [Betke et al., 2008; Hristov, Betke, Salles, Department of Psychological and Brain Sciences, Johns Hopkins Theriault, Bagchi, & Kunz, 2010; McFarlane, Rentergem, Ruina, University, 3400 North Charles Street, Ames Hall, Suite 232, Baltimore, Lundberg, & Christenson, 2015; McCracken, 2003]). Their social MD 21218. E-mail: [email protected] systems vary greatly from fission–fusion societies to highly stable 305 306 SALLES, BOHN, AND MOSS social groups that remain cohesive over many years (e.g., Chav- of calls. In this article, we propose that the same organization erri, 2010; McCracken & Bradbury, 1981; Wilkinson, 1985; see principle may hold for echolocation and communication call pro- also Wilkinson et al., 2019). Given their sociality, tendency to rely cessing. That is, we hypothesize that early stages of auditory less on vision than hearing, and sophisticated audio-vocal system processing of echolocation and social communication signals are for echolocation, it is not surprising that bats use a broad array of largely shared, but at higher stages of the auditory pathway, the vocal communication signals (Altringham et al., 2011; Chaverri et neural circuitry for processing functionally distinct vocalizations al., 2018; Dechmann & Safi, 2005; Gillam & Fenton, 2016). Some diverges. species demonstrate vocal learning (Boughman, 1998; Knörn- schild, 2014; Knörnschild, Nagy, Metz, Mayer, & von Helversen, Bat Communication Calls Serve Diverse Functions 2010; Prat, Azoulay, Dor, & Yovel, 2017; Prat, Taub, & Yovel, 2015, 2016) and highly complex vocalizations (Smotherman, As noted in the previous section, bats use their sophisticated Knörnschild, Smarsh, & Bohn, 2016); however, our understanding audio-vocal systems to localize objects in their surroundings (Grif- of the perception and processing of these signals is yet in its fin, 1958). The bat’s auditory scene may not only include its own infancy. sonar vocalizations and echoes but also the echolocation sounds emitted by conspecifics and their echo returns. Some reports also Bats Have Specialized Audio-Vocal Systems suggest that bats use conspecific echolocation vocalizations for social communication (Rhinolophus spp.[Kobayasi, Hiryu, Shi- Laryngeal echolocators have specialized audio-vocal systems mozawa, & Riquimaroux, 2012]; Noctilio albiventris [Dechmann, that allow them to adapt echolocation calls in response to acoustic Wikelski, van Noordwijk, Voigt, & Voigt-Heucke, 2013]; Eptesi- information carried by echoes, which they use to localize objects cus fuscus [Grilliot, Burnett, & Mendonça, 2009]; Saccopteryx in the dark with very high accuracy (Busnel, 1980; Fenton & bilineata [Knörnschild, Feifel, & Kalko, 2013]; Myotis myotis Ratcliffe, 2017; Griffin, 1958; Nachtigall & Moore, 1988; [Yovel, Melcon, Franz, Denzinger, & Schnitzler, 2009]; Myotis Thomas, Vater, & Moss, 2003); this sophisticated audio-vocal capaccinii [Dorado-Correa, Goerlitz, & Siemers, 2013]; see Bohn system also supports the production of a wide array of communi- & Gillam, 2018, for a review), as these signals can convey infor- cation calls. Specializations for echolocation include large middle- mation about foraging activity to conspecifics. For many social ear muscles that are activated in coordination with laryngeal signal functions, bats produce specialized vocalizations that relay entirely production to attenuate direct reception of emitted echolocation different types of information, often with acoustic properties dis- vocalizations and modulate hearing sensitivity to weak returning tinct from echolocation signals. The chiropteran auditory and echoes (Suga & Jen, 1975). The larynx of echolocating bats has nervous system is tasked with processing these signals, extracting superfast muscles that permit the production of over 100 calls per relevant information, and coordinating appropriate behavioral re- second (Elemans, Mead, Jakobsen, & Ratcliffe, 2011). This kind sponses. of superfast muscle in vertebrates has thus far only been associated The majority, if not all, of bat species (including nonecholoca- with vocal communication, for example, in the songbird syrinx tors) produce a common set of social communication calls: dis- (Elemans, Mead, Rome, & Goller, 2008), though in bats it may be tress, agonistic, and infant isolation vocalizations (see Table 1). key for echolocation (Elemans et al., 2011). Distress calls are common across the animal kingdom and have Superfast laryngeal muscles in bats seem to be necessary
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