J Comp Physiol A DOI 10.1007/s00359-011-0630-0 ORIGINAL PAPER Frequency alternation and an offbeat rhythm indicate foraging behavior in the echolocating bat, Saccopteryx bilineata John M. Ratcliffe • Lasse Jakobsen • Elisabeth K. V. Kalko • Annemarie Surlykke Received: 22 December 2010 / Revised: 28 January 2011 / Accepted: 30 January 2011 Ó Springer-Verlag 2011 Abstract The greater sac-winged bat, Saccopteryx bi- Keywords Sensory ecology Á Foraging Á Behavioral lineata (Emballonuridae), uses two distinct echolocation flexibility Á Source level Á Detection distance call sequences: a ‘monotonous’ sequence, where bats emit *48 kHz calls at a relatively stable rate, and a frequency- Abbreviations alternating sequence, where bats emit calls at *45 kHz dB SPL RMS Decibel sound pressure level re. 20 lPa (low-note call) and *48 kHz (high-note call). The fre- root mean square quencies of these low–high-note pairs remain stable within PF Peak frequency sequences. In Panama, we recorded echolocation calls from S. bilineata with a multi-microphone array at two sites: one a known roosting site, the other a known foraging site. Our results indicate that this species (1) only produces mono- Introduction tonous sequences in non-foraging contexts and, at times, directly after emitting a feeding buzz and (2) produces The greater sac-winged bat, Saccopteryx bilineata, belongs frequency-alternating sequences when actively foraging. to the family of sheath-tailed bats (Emballonuridae), a pan- These latter sequences are also characterized by an unu- tropical group comprising approximately 90 extant species sual, offbeat emission rhythm. We found significant posi- the origins of which date back to the Eocene (Teeling et al. tive relationships between (1) call intensity and call 2005). Found from Mexico to Brazil and on the islands of duration and (2) call intensity and distance from clutter. Trinidad and Tobago (Yancey et al. 1998), S. bilineata However, these relationships were weaker than those weighs *10 g and forages in a variety of habitats (Brad- reported for bats from other families. We speculate on how bury and Vehrenkamp 1976; Kalko 1995; Jung et al. 2007) call frequency alternation and an offbeat emission rhythm on wings well suited to edge habitats and semi-open spaces might reflect a novel strategy for prey detection at the edge (Norberg and Rayner 1987). S. bilineata is insectivorous of complex habitat in this ancient family of bats. and takes a wide range of small to medium sized prey (Bradbury and Vehrenkamp 1976; Yancey et al. 1998). Unlike the more recently derived molossids and vesperti- J. M. Ratcliffe (&) Á L. Jakobsen Á A. Surlykke lionids, most emballonurids, including S. bilineata, Institute of Biology, University of Southern Denmark, emphasize the second, rather than first, harmonic in their Campusvej 55, 5230 Odense M, Denmark echolocation calls. We note that over some of its range, S. e-mail: [email protected] bilineata uses slightly lower call frequencies (e.g. Biscardi E. K. V. Kalko et al. 2004) than those we report below. Institute of Experimental Ecology, University of Ulm, S. bilineata is unusual among echolocating bats in that it Albert-Einstein Allee 11, 89069 Ulm, Germany uses two distinct call sequences. One is a remarkable fre- quency-alternating sequence, where bats emit pairs of calls: E. K. V. Kalko Smithsonian Tropical Research Institute, a first call at *45 kHz followed by a second call at P.O. Box 0843-03092, Balboa, Ancon, Republic of Panama *48 kHz. Call intervals between pairs are roughly 123 J Comp Physiol A 1.5 times longer than intra-pair intervals (Pye 1980;Bar- sequences with 55 kHz calls, the acoustic channels used by clay 1983; Jung et al. 2007). Peak frequencies (maximum congeneric S. leptura are brought closer to those frequen- energy) of the first and the second call remain stable within cies used by S. bilineata. Typical interpretations predict a sequence. The second sequence type is monotonous, sister species should instead select channels further apart characterized by calls with frequencies *48 kHz emitted from one another if acoustic partitioning was a driving at a relatively steady rate (Pye 1980; Jung et al. 2007). force in their evolution (Kingston and Rossiter 2004). Monotonous sequences are regarded as typical of many Whereas S. bilineata’s unusual frequency-alternating echolocating bats while they are in transit or prior to sequences have garnered much attention from researchers detecting prey (Simmons et al. 1979; Surlykke and Moss in the context of foraging behavior, the function of the 2000). Greater sac-winged bats are more often observed monotonous sequences have not, to our knowledge, been as emitting frequency-alternating sequences than they are thoroughly considered. As the monotonous sequences are monotonous sequences (Barclay 1983; Kalko 1995; typically associated with bats flying near to the roost (e.g. O’Farrell and Miller 1997; Jung et al. 2007). Pye 1980; Jung et al. 2007) their relative simplicity may Several hypotheses have been proposed to explain the reflect a greater reliance on spatial memory (Ratcliffe et al. existence and predominance of the frequency-alternating 2005), reduced demand for prey-background resolution echolocation call sequences, none of which is necessarily and/or serve an as yet unknown secondary social function mutually exclusive (Jung et al. 2007). Here, we divide when flying in familiar space in the presence of familiar them into two classes: (1) sensory hypotheses with a individuals (Fenton et al. 2002). functional explanation for alternating sequences pertaining In this study, we used a multi-microphone array to to echolocation itself, and (2) social hypotheses, suggesting record flying S. bilineata at two locations, one close to a a secondary social function. We consider monotonous known roost where bats flew close to vegetation and the sequences under roughly these same classes. ground, and one nearby a known foraging patch where bats With respect to sensory hypotheses, call frequency flew slightly higher and further away from background alternation may help bats avoid ambiguity in call-echo (E. K. V. Kalko, unpublished data). Our purpose was plain: matching, because returning echoes are effectively to document the differences, if any, between the (1) ‘marked’ as echoes originating from either 45 or 48 kHz echolocation call designs and (2) call emission patterns calls. For example, echoes returning from a 45 kHz call used at the two sites with respect to the following param- should be recognizable to a bat even if a 48 kHz has been eters: (1) call frequency, duration, and intensity and (2) call emitted in the intervening period (Behr and von Helversen interval, pattern and flight speed. We then input call 2004; Jung et al. 2007). In contrast, bats using monotonous intensity data to a simple acoustic model and estimated the sequences are not expected to be able to reliably match intensity of echoes returning to a bat based on the bat’s echo to call if an audible echo returns after a subsequent estimated distance from (1) the array (as proxy for fore- call has already been emitted (Schnitzler and Kalko 2001). most background), (2) virtual insects in front of the array Another hypothesis, which has been proposed in only the and outside of the call-echo-overlap zone (Schnitzler and most general of terms, is that S. bilineata produces fre- Kalko 2001), (3) virtual background from which echoes quency-alternating sequences when hunting for prey and would return as the call window closes and (4) virtual monotonous sequences when in transit between roosts and insects from which echoes would return at this same point foraging sites (Pye 1980). Other sensory hypotheses have in time (Holderied and von Helversen 2003). We discuss been put forward [e.g. two closely spaced calls of different our results, paying particular attention to measured call peak frequency (PF) increase effective bandwidth] but intensities and those estimated for echoes, within the have since been refuted (see Barclay 1983; Jung et al. 2007 context of the hypotheses outlined above. and references therein). Possible social functions for alternating sequences include acoustic partitioning (Jung et al. 2007). However, Materials and methods adding a 45 kHz call for the purpose of partitioning acoustic channels seems unlikely. On the one hand, no Study site sympatric emballonurid’s echolocation calls in Central America typically produce calls with peak frequencies Our study was conducted in March 2008 during one of the around 48 kHz (see Jung et al. 2007). On the other hand, a biannual dry seasons on Barro Colorado Island (BCI), 45 kHz call is close to those used in the monotonous Panama; a field station of the Smithsonian Tropical sequences of Balantiopteryx plicata (*43 kHz) and Research Institute (STRI) near the Panama Canal (9°110N, Centronycteris centralis (*41 kHz) (Jung et al. 2007). 79°500W). BCI is characterized by semi-deciduous, moist Furthermore, by adding, for example, 51 kHz calls to tropical lowland forest and home to over 70 species of 123 J Comp Physiol A echolocating bats representing several families (Jung et al. horizontal axis of the cross (x plane). Two Avisoft CM16 2007; Kalko et al. 2008). Recordings of free-flying Sac- condenser microphones were positioned perpendicular to copteryx bilineata were made at two locations: one site and at an equal distance from the horizontal axis, above and close to a known day roost; the other, a volume of airspace below the fourth G.R.A.S. microphone; together these three commonly used for foraging by this and other insectivorous microphones comprised the shorter vertical axis of the cross bat species (e.g. Myotis nigricans (Vespertilionidae), Sie- (z plane). At the roost site, the seven microphones were set mers et al. 2001). 50 cm apart, the two Avisoft microphones 75 cm above and The known roost was the vertical exterior wall of a below.