Functional Ecology 2012
doi: 10.1111/j.1365-2435.2012.02024.x
Sensory constraints on prey detection performance in an ensemble of vespertilionid understorey rain forest bats Daniela A. Schmieder1, Tigga Kingston*,2, Rosli Hashim3 and Björn M. Siemers1 1
Sensory Ecology Group, Max Planck Institute for Ornithology, 82319, Seewiesen, Germany; 2Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409-3131, USA; and 3Faculty of Science, Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia
Summary 1. Bats evolved different strategies to find prey close to vegetation. Previous studies on European bats of the genus Myotis (Vespertilionidae) revealed an association between echolocation call bandwidth and the ability to find and capture prey close to vegetation. Here, we investigated whether the role of call bandwidth in prey detection is a more general principle in bat sensory ecology. We focused on eight palaeotropical species of the vespertilionid subfamilies Kerivoulinae and Murininae, as they also achieve very broad bandwidths with the first harmonic of their echolocation calls. 2. All species emitted calls of bandwidths broader than 90 kHz with extremely high start frequencies (max. 230 kHz), and all of five experimentally tested species were able to catch prey closer than 6 cm, occasionally even closer than 2·5 cm, to a standardized vegetation-like background. The performance and call data corroborate the hypothesis that bats with very broadband calls and high-frequency components have access to prey very close to vegetation and establish this as a more general principle in bat sensory ecology. 3. In a second experiment, we questioned whether echolocation is the only sensory cue used by the bats to find prey. Echo-acoustic prey dummies that did not smell or taste like arthropods and did not produce any sounds or movement were presented to all five species. In 80 of 83 cases, the bats caught or attempted to catch the dummy, indicating that the bats used only echo-acoustic information for prey detection and recognition in our experiments. 4. We then tested whether the sensory difficulty in finding prey close to clutter constrains the bats’ attacks on prey – or whether flight manoeuvrability may be limiting – by manipulating the echo reflection properties of the background. The bats were able to find prey very slightly, but significantly closer to a background with lower echo reflection (an easier sensory task), which corroborates the limiting role of sensory performance. 5. While silent, motionless prey close to and in vegetation will be accessible to these specialists, it will go undetected by other bats. This scenario supports the idea that sensory specialization mediates resource access and niche separation (‘sensory niche partitioning’). Key-words: call bandwidth, clutter, community ecology, echolocation, foraging, Kerivoula, Malaysia, Murina, Phoniscus, sensory niche partitioning
Introduction Detecting prey close to vegetation is a difficult task for bats as they must contend with the effects of both forThis paper is dedicated to the memory of Bjo¨rn M. Siemers, a great friend, mentor and colleague, who passed away in May 2012. *Correspondence author. E-mail:
[email protected]
ward masking (overlap of the outgoing call and returning echo) and backward masking (when echoes from the vegetation background overlap the prey echoes) (Schnitzler & Kalko 2001). Bats have evolved different strategies to solve this problem (Schnitzler, Moss & Denzinger 2003; Jones & Teeling 2006). Many species within the families Vespertilionidae, Phyllostomidae and Megadermatidae find
© 2012 The Authors. Functional Ecology © 2012 British Ecological Society
2 D. A. Schmieder et al. arthropods in echo-cluttering vegetation by eavesdropping on prey-generated locomotion or communication sounds, a strategy sometimes termed ‘passive listening’ (Kulzer et al. 1984; Arlettaz, Jones & Racey 2001; Page & Ryan 2005; Siemers & Swift 2006; Russo, Jones & Arlettaz 2007; Goerlitz, Greif & Siemers 2008; Jones et al. 2011). Bats in the families Rhinolophidae and Hipposideridae detect fluttering prey close to vegetation by evaluating ‘acoustic glints’ imprinted by insect wing beats onto the echoes of the bats’ constant frequency echolocation calls (Emde & Menne 1989; Emde & Schnitzler 1990; Lazure & Fenton 2011). Other species within the family Vespertilionidae have evolved another sophisticated echolocation behaviour to detect prey close to vegetation, using broadband, frequency-modulated (FM) calls of short duration (Siemers & Schnitzler 2000, 2004). These large signal bandwidths are believed to activate more neuronal filters than smaller bandwidths, improving the accuracy of range and angle determination (Kick 1982; Schnitzler & Kalko 2001), and may deliver spectral cues that can be used for target classification and target–background discrimination (Schumm, Krull & Neuweiler 1991; Schmidt, Hanke & Pillat 2000; Siemers & Schnitzler 2004). The short call duration reduces overlap of target and background echoes. Previous flight tent studies on sympatric and potentially competing bats of the genus Myotis (Vespertilionidae) revealed that species emitting calls of a broader bandwidth had greater success in finding and capturing prey close to vegetation-like background than did species calling with narrower bandwidth (Siemers & Schnitzler 2004). All five tested species tolerated some overlap of prey echoes and background echoes. The best performing species, Myotis nattereri, detected prey as close as 2 cm to echo-cluttering background by echolocation and produced call bandwidths spanning more than three octaves with only the first harmonic (Siemers & Schnitzler 2000, 2004). In the present study, we investigated whether the role of call bandwidth in prey detection performance holds beyond the genus Myotis and is thus a more general principle in bat sensory ecology. Promising candidates are the bats of the palaeotropical subfamilies Kerivoulinae and Murininae, as they also achieve very broad bandwidths with the first harmonic of their echolocation calls (Kingston et al. 1999; Schmieder et al. 2010). The few available field observations suggest that these bats hunt in and around clutter-producing vegetation (Payne & Francis 1985; Kingston, Lim & Akbar 2006). Here we experimentally tested the sensory basis of prey detection performance of five of these species from an assemblage of Malaysian rain forest bats. In the experiments, we used artificial vegetation, which consisted of a screen that reflected many strong echoes mimicking the effect of vegetative clutter. We also recorded echolocation calls of these and three additional species and checked for correlation of call bandwidth with prey detection performance. The aim of this first set of experiments was to test the hypothesis that bats with very broadband calls have sensory access to prey very close to vegetation.
In a second experiment, we tested whether other sensory cues – specifically smell, movement and sound – play a role in prey detection and location, and presented the bats with mealworm dummies. Additionally, we sought to determine whether it is indeed the sensory difficulty of finding prey close to clutter that constrains the bats’ attacks on prey or the motor difficulty of flying and manoeuvring very close to clutter. In such situations, bats have to fly very slowly or even hover, which is a challenging task and species differ in their ability to do so (Aldridge 1986; Alridge & Rautenbach 1987; Norberg & Rayner 1987; Stockwell 2001; Voigt et al. 2010). In an attempt to answer this question, we tested in a third experiment the detection behaviour of bats for prey close to two different backgrounds: the clutter screen from the first experiment and a foam screen that reflected fewer and weaker background echoes. While the challenge for the bats’ flight manoeuvres remained unchanged between treatments, the sensory difficulty did not. If sensory constraints indeed limit prey detection close to background, we predicted that the bats find prey closer to the low-echo background than to the clutter screen. If, however, motor constraints prevail, we predicted the same prey detection performance for both backgrounds.
Materials and methods CAPTURE AND HUSBANDRY OF BATS
Fieldwork was conducted from February until May 2009 in Malaysian lowland rain forest at Kuala Lompat Research Station, Krau Wildlife Reserve, Pahang, Peninsular Malaysia (3°43′N, 102°10′E), with permission of the Economic Planning Unit Malaysia (UPE: 40/200/19/2359) and the Director General of the Department of Wildlife and National Parks. Capture of bats, their husbandry and our behavioural experiments were specifically licensed by this permit. See Kingston et al. (1999) for details on the field site. Bats were caught in four-bank harp traps positioned across trails in the forest understorey, and species were identified following Kingston, Lim & Akbar (2006). Only adult bats were used for experiments. Animals were kept individually or in pairs for a number of days in round mesh cages (30 cm diameter, height 40 cm) under a natural light regime. Bats received food during the experiments and were handfed additional mealworms (larvae of Tenebrio molitor) to sustain their capture weight if necessary. Water was available ad libitum, and up to three times per week, the bats received a vitamin supplement (Nutri-Cal, Albrecht, Germany). After completion of the experiments, all bats were released at the site of capture.
SPECIES
We recorded echolocation calls of 33 individuals from the following eight species: Kerivoula intermedia (one female, five males), K. krauensis (one male), K. papillosa (4, 3), K. pellucida (1, 2), Phoniscus atrox (six males), P. jagorii (one male), Murina cyclotis (four males) and M. suilla (1, 4). For the tests of prey detection performance, only those individuals that readily captured mealworms from strings during pre-tests were used: Kerivoula intermedia (one male), K. papillosa (four females, two males), Phoniscus atrox (one male), Murina cyclotis (two males) and M. suilla (one male).
© 2012 The Authors. Functional Ecology © 2012 British Ecological Society, Functional Ecology
Prey detection performance in rain forest bats ECHOLOCATION CALLS
Bats were flown singly in a large screen tent (Eureka, Breezeway; ground area 3·5 9 3·5 m, 2·5 m central height) during their natural activity period. Recordings were made when the bat passed close (
