Foraging Bats Avoid Noise Andrea Schaub, Joachim Ostwald and Björn M

Erratum Foraging bats avoid noise Andrea Schaub, Joachim Ostwald and Björn M. Siemers 10.1242/jeb.037283 There was an error published in J. Exp. Biol. 211, 3174-3180. In Fig. 2, the values on the x-axis (Frequency) were incorrectly labelled as scaling from 10 to 60 kHz. The correct axis scale is 0 to 50 kHz. We apologise to all authors and readers for this error. THE JOURNAL OF EXPERIMENTAL BIOLOGY 3174 The Journal of Experimental Biology 211, 3174-3180 Published by The Company of Biologists 2008 doi:10.1242/jeb.022863 Foraging bats avoid noise Andrea Schaub1, Joachim Ostwald1 and Björn M. Siemers2,* 1Zoological Institute, Department of Animal Physiology, University of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, Germany and 2Max Planck Institute for Ornithology, Sensory Ecology Group, Eberhard-Gwinner-Strasse, 82319 Seewiesen, Germany *Author for correspondence (e-mail: [email protected]) Accepted 14 August 2008 SUMMARY Ambient noise influences the availability and use of acoustic information in animals in many ways. While much research has focused on the effects of noise on acoustic communication, here, we present the first study concerned with anthropogenic noise and foraging behaviour. We chose the greater mouse-eared bat (Myotis myotis) as a model species because it represents the especially vulnerable group of gleaning bats that rely on listening for prey rustling sounds to find food (i.e. ʻpassive listeningʼ). In a choice experiment with two foraging compartments, we investigated the influence of background noise on foraging effort and foraging success. We tested the hypotheses that: (1) bats will avoid foraging areas with particularly loud background noise; and (2) the frequency–time structure of the noise will determine, in part, the degree to which it deters bats. We found a clear effect of the type of noise on the allocation of foraging effort to the compartments and on the distribution of prey capture events. When playing back silence, the bats made equal use of and were equally successful in both compartments. In the other three treatments (where a non-silent sound was played back), the bats avoided the playback compartment. The degree to which the background noise deterred bats from the compartment increased from traffic noise to vegetation movement noise to broadband computer- generated noise. Vegetation noise, set 12 dB below the traffic noise amplitude, had a larger repellent effect; presumably because of its acoustic similarity with prey sounds. Our experimental data suggest that foraging areas very close to highways and presumably also to other sources of intense, broadband noise are degraded in their suitability as foraging areas for such ʻpassive listeningʼ bats. Key words: environmental noise, anthropogenic noise, traffic noise, foraging, road ecology, Myotis myotis, gleaning bats, passive listening, echolocation, masking. INTRODUCTION to decrease the occurrence, breeding density and breeding success Ambient noise influences the availability and use of acoustic of birds (Brotons and Herrando, 2001; Fernandez-Juricic, 2001). In information in animals in many ways. In addition to noises produced marine environments, noise can affect ranging and acoustic by other animals and natural abiotic sources (e.g. wind or running behaviours of whales, porpoises and seals (Morton and Symonds, water), anthropogenic noise emissions, such as urban and traffic 2002; Koschinski et al., 2003). noise, constitute a major source of ambient noise. The main body Surprisingly, the degree to which noise can influence another of research on the effects of noise on wild animals has concentrated crucial behaviour – foraging – has been entirely neglected. Except on acoustic communication (for reviews, see Brumm and for a study on noise-increased predator vigilance, which could result Slabbekoorn, 2005; Patricelli and Blickley, 2006; Slabbekoorn and in reduced foraging efficiency in chaffinches (Quinn et al., 2006), Ripmeester, 2008) because noise can mask relevant acoustic signals the present study is the first to address the effects of noise on foraging to potential receivers. Some species of birds, amphibians and ability. It is likely that ambient noise does impact an animals’ ability dolphins shift the frequency range of their communication signals to use acoustic information for foraging because a variety of birds in an effort to avoid strong overlap with ambient noise (Slabbekoorn and mammals use sound to find their prey. For example, owls and Peet, 2003; Narins et al., 2004; Morisaka et al., 2005; Feng et (Konishi, 2003) and insect-eating primates (Goerlitz and Siemers, al., 2006; Slabbekoorn and den Boer-Visser, 2006; Bee and 2007) listen for rustling sounds produced by moving animals to Swanson, 2007). Moreover, some birds also increase their call detect and localize food. Bats represent a special case. While many amplitude when singing in noisy environments, such as a big city bats detect and intercept flying insects using echolocation (Griffin, (Brumm and Todt, 2002; Brumm, 2004), or shift singing time to 1958; Kalko, 1995; Siemers and Schnitzler, 2000), others find prey less noisy periods (Fuller et al., 2007). Such behavioural flexibility by listening for prey-produced sounds (Marimuthu and Neuweiler, and evolutionary plasticity has allowed individuals and populations, 1987; Faure and Barclay, 1992; Arlettaz et al., 2001; Siemers and respectively, to cope with natural environmental noise. Indeed, it Swift, 2006). This strategy of ‘passive listening’ is adopted by bat has enabled them to adapt their communication systems to species specialized to glean arthropods from vegetation or the ground anthropogenic noise, at least to some degree. However, there are where prey echoes are masked by overlapping, strong background clear indications that noise pollution can negatively affect wild echoes. For such ‘passive listening’ bats, it is conceivable that animals (Forman and Alexander, 1998; Forman and Deblinger, environmental noise interferes with the detection of prey. As these 2000; Jaeger et al., 2005). Roadless space is becoming scarce in bats use echolocation for spatial orientation, the reception of many places on our planet (Watts et al., 2007) and road influence relevant echoes could potentially be impaired by noise as well on wildlife is an important issue. Traffic noise has been suggested (Griffin and Grinnell, 1958; von Frenckell and Barclay, 1987; THE JOURNAL OF EXPERIMENTAL BIOLOGY Bats avoid noise 3175 Mackey and Barclay, 1989; Rydell et al., 1999; Spanjer, 2006; (hypothesis one); and (2) if the frequency–time structure of the noise Gillam and McCracken, 2007). will affect its deterring effect (hypothesis two). In the present study, we assessed the reaction of bats to both anthropogenic and natural ambient noise in a foraging context. The MATERIALS AND METHODS greater mouse-eared bat (Myotis myotis Borkhausen 1797) was used Animals and housing as a model species because it belongs to the group of bats that find Seven male greater mouse-eared bats (Myotis myotis) were used for prey by listening to their rustling sounds (Kolb, 1961; Arlettaz et experimentation. The animals were captured as juveniles in August al., 2001). This species is therefore potentially vulnerable to noise 2005 near Freiburg, Germany, for the present investigations under impact on both ‘passive listening’ and echolocation. Furthermore, licence from the responsible authority (Regierungspräsidium greater mouse-eared bats are a highly protected species (European Freiburg, licence #55-8852.44/1095). Bats were held and tested in Habitats Directive, Annex II). They are widely distributed (Güttinger specially designed facilities at the University of Tübingen, Tübingen, et al., 2001; Dietz et al., 2007) and have expansive home ranges Germany (approved by Regierungspräsidium Tübingen). They were (Audet et al., 1991; Arlettaz, 1999; Zahn et al., 2005); therefore, housed in a flight cage of 2mϫ1.5mϫ2m (lengthϫwidthϫheight) they are highly relevant in virtually all environmental impact with an inverted light regime [8h:16h (darkness:light)]. The bats assessments for larger highway or railway projects in central and received food (mealworms – larvae of Tenebrio molitor Linnaeus southern Europe. Most projected traffic routes in Europe will cross 1758), and water ad libitum during the experiments. Their diet was M. myotis foraging areas. The greater mouse-eared bat can serve as also supplemented with desert locusts (Schistocerca gregaria a model species to assess noise impact on foraging behaviour in the Forskal 1775) once a week and with vitamins and minerals once large and, from a conservation perspective, especially vulnerable every four weeks. All seven bats were in good health at the end of (Safi and Kerth, 2004) group of ‘passive listening’, gleaning bats. the experiments and remained in the Tübingen animal unit thereafter Greater mouse-eared bats roost in caves in southern Europe for further investigations of how traffic noise impacts on bat foraging and typically in large attics in central Europe (Güttinger et al., ecology. 2001; Dietz et al., 2007). Colony size ranges from a handful of reproductive females to several thousands of bats. At nightfall, Flight room and setup the colony members disperse into individual foraging areas at a Bats were tested in a large flight room with dimensions of distance of 17km or more from the communal day roost (Güttinger 13mϫ6mϫ2m (lengthϫwidthϫheight); walls and ceiling were et al., 2001). They listen for

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