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Acoustic Identification of Mormoopid Bats: a Survey During the Evening Exodus

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Acoustic Identification of Mormoopid Bats: a Survey During the Evening Exodus Journal of Mammalogy, 87(2):324–330, 2006 ACOUSTIC IDENTIFICATION OF MORMOOPID BATS: A SURVEY DURING THE EVENING EXODUS SILVIO MACI´AS,* EMANUEL C. MORA, AND ADIANEZ GARCI´A Department of Human and Animal Biology, Faculty of Biology, Havana University, CP 10 400, Ciudad de La Habana, Cuba (SM, ECM, AG) Department of Basic Formation, Faculty of Psychology, Havana University, Calle San Rafael No. 1168 entre Mazo´n y Basarrate, Centro Habana, Ciudad de La Habana, Cuba (SM) Echolocation calls emitted by the 4 species of Cuban mormoopid bats were compared to determine vocal signatures that enable identification of each species in the field during their evening exodus. Echolocation calls produced by Mormoops blainvilli are downward frequency-modulated (FM) signals in the range of 68.4– 52.5 kHz. Echolocation calls emitted by Pteronotus macleayii and P. quadridens have a similar design consisting of a short constant-frequency (CF) segment followed by a downward FM segment. The CF segment was at 70.0 kHz in calls from P. macleayii, and at 83.3 kHz in calls from P. quadridens. Echolocation calls from P. parnellii consist of a long CF segment, which is preceded by a short initial upward sweep and followed by a downward FM terminal sweep. The CF value of the 2nd harmonic was a good parameter for species identification. The features of the echolocation calls of each of the species were used to identify them during the evening exodus from 2 Cuban caves. Key words: echolocation, evening exodus, identification, mormoopid bats Effective monitoring of echolocation calls is vital in many families, such as Mormoopidae, should make it possible to use studies of the ecology and conservation of bats (Fenton 1997). acoustic methods for species identification (Iban˜ez et al. 1999; Ultrasonic microphones, ‘‘bat detectors,’’ have been developed Macı´as and Mora 2003; Mora et al. 2002; O’Farrell and Miller to allow investigators to hear, ‘‘visualize,’’ or both, the ultra- 1997; Schnitzler et al. 1987, in litt.). sonic echolocation calls of bats (Hayes 1997; O’Farrell and Echolocation signals of mormoopid bats can readily be Miller 1999; Sherwin et al. 2000). The use of acoustic detection distinguished from calls of members of other families (Fenton has been shown to be a powerful supplement to standard cap- 1994; Iban˜ez et al. 1999, 2000; Koessl et al. 1999; Macı´as and ture methods to identify many insectivorous bats that are gen- Mora 2003; O’Farrell and Miller 1999). However, interspecific erally underrepresented in field inventories (O’Farrell and identification of sympatric mormoopids has not been well Miller 1999; O’Farrell et al. 1999). studied. It is argued that most bats could be identified by the Here, we describe the echolocation calls produced by the frequency–time structure of their echolocation calls, with the 4 species of Cuban mormoopids: Pteronotus quadridens, exception of a number of species known to use low-intensity, P. macleayii, P. parnellii, and Mormoops blainvillei in an en- short-duration calls that seem to differ little among species closed space, showing that calls of these species are reliably (e.g., phyllostomids—Griffin 1958; Hayes 2000; Jones et al. identifiable. The usefulness of acoustic identification of Cuban 2000; Kalko et al. 1996). Some authors have criticized the species of this family was proved in an acoustic survey con- qualitative approach for acoustic identification of species of ducted during the evening exodus from their diurnal roost. bats because of intraspecific variation resulting from geogra- phy, habitat, and species-assemblage factors (Barclay 1999; MATERIALS AND METHODS Barclay et al. 1999; Guille´n et al. 2000). However, the low within-species variability in the echolocation calls of some Echolocation calls from single individuals.—We captured 8 M. blainvillei,4P. macleayii,5P. parnellii, and 14 P. quadridens to characterize their echolocation calls while they were flying in cluttered space. Bats were captured using mist nets. After capture, each bat was * Correspondent: [email protected], [email protected] released from the hand and allowed to fly in circles until several passes of echolocation calls were recorded in a bat-free, enclosed sector of Ó 2006 American Society of Mammalogists a cave, measuring 4 Â 3 Â 3 m. Species identification was based on www.mammalogy.org a key of external characters given by Silva (1979). 324 April 2006 MACI´AS ET AL.—ACOUSTIC IDENTIFICATION OF MORMOOPIDS 325 FIG.1.—Representative oscillograms (above), spectrograms (middle), and power spectra (below) of the echolocation calls emitted by each of the 4 species of Cuban mormoopid bats while flying in a confined space. A) Mormoops blainvillei,B)Pteronotus macleayii,C)P. parnellii, and D) P. quadridens. M. blainvillei emits frequency-modulated signals, whereas P. macleayii, P. quadridens, and P. parnellii produce constant- frequency–frequency-modulated signals. Sonograms of P. macleayii and P. quadridens always show 3 harmonics, whereas M. blainvillei and P. parnellii vary their harmonic composition and sonograms show 2 or 3, or 1 or 3, harmonics, respectively. Recording equipment and sound analysis.—Echolocation calls were as spectrograms and temporal digitized recordings (oscillograms) with recorded using an ultrasonic detector (U30 Ultra Sound Advice, BatSound 2.1. Spectrograms were made of consecutive fast-Fourier London, United Kingdom) with flat sensitivity (6 2 dB) between transforms with a 99% overlap. Usually, a 512-point fast-Fourier 20 and 200 kHz. The detector’s high-frequency output was fed to an transform was chosen to get a good compromise between frequency analog–digital input port of a digital signal-processing board (model and time resolution. On oscillograms and spectrograms, time resolu- PCM-DAS 16S/330, Plug-In Electronic, Eichenau, Germany). The tion was 0.1 ms. On spectrograms the frequency resolution was board was controlled with the commercial software BatSound 2.1 610 Hz. To obtain power spectra, fast-Fourier transforms were cal- (Pettersson Elektronik AB, Uppsala, Sweden). Sampling frequency culated with 256–2,048 data points. Spectrograms and power spectra was set at 312 kHz. Echolocation calls were displayed simultaneously were made using a Hanning window. The length of the fast-Fourier 326 JOURNAL OF MAMMALOGY Vol. 87, No. 2 TABLE 1.—Mean values 6 SD of acoustic parameters measured in the echolocation calls emitted by each of the studied mormoopid species (Mormoops blainvillei, Pteronotus parnellii, P. macleayii, and P. quadridens) while flying in a confined space. A comparison of the species calls was done with an analysis of variance for each of the parameters. n is the number of individuals. P shows very significant differences (P , 0.01) among the species. Lowercase letters represent the results of a Student–Newman–Keuls test (P , 0.05) applied to each parameter (a different from b; b different from c; c different from d). 1st, 2nd, and 3rd refer to 1st, 2nd, and 3rd harmonics of a call. Acoustic parameters are defined in the text. M. blainvillei (n ¼ 8) P. parnellii (n ¼ 5) P. macleayii (n ¼ 4) P. quadridens (n ¼ 14) P DUR (ms) 2.42 6 0.17 c 21.23 6 0.87 a 4.03 6 0.07 b 3.79 6 0.14 b ,0.01 1.8a 25À27a 2.9a 3.1a 30.4b CF 1st (kHz) 29.90 6 0.46 c 35.51 6 0.36 b 41.71 6 0.37 a ,0.01 CF 2nd (kHz) 60.60 6 0.08 c 70.69 6 0.43 b 83.40 6 0.36 a ,0.01 61.3a 71.2a 77À83a DurCF 2nd (ms) 16.19 6 0.11 a 1.22 6 0.09 b 1.24 6 0.08 b ,0.01 1a 1.2a CF 3rd (kHz) 90.26 6 0.15 c 105.18 6 0.69 b 124.00 6 0.60 a ,0.01 IF 1st (kHz) 33.33 6 0.16 c 29.90 6 0.46 d 35.51 6 0.36 b 41.90 6 0.22 a ,0.01 FF 1st (kHz) 25.76 6 0.84 c 24.40 6 0.53 c 28.17 6 0.18 b 31.49 6 0.19 a ,0.01 IF 2nd (kHz) 67.05 6 0.45 c 60.60 6 0.08 d 70.69 6 0.43 b 83.40 6 0.36 a ,0.01 FF 2nd (kHz) 48.14 6 0.74 c 48.05 6 0.61 c 54.94 6 0.97 b 61.22 6 0.38 a ,0.01 IF 3rd (kHz) 98.67 6 0.42 c 90.26 6 0.15 d 105.11 6 0.74 b 124.00 6 0.06 a ,0.01 FF 3rd (kHz) 78.45 6 1.45 c 73.28 6 1.07 d 83.73 6 0.92 b 93.83 6 0.47 a ,0.01 PF 1st (kHz) 30.94 6 0.22 c 30.00 6 0.08 c 34.92 6 0.26 b 41.00 6 0.19 a ,0.01 MINF 1st (kHz) 27.20 6 0.26 c 29.73 6 0.08 b 29.41 6 0.04 b 30.15 6 0.21 a ,0.01 MAXF 1st (kHz) 34.24 6 0.18 c 30.21 6 0.07 d 36.11 6 0.29 b 42.05 6 0.20 a ,0.01 BW 1st (kHz) 7.16 6 0.30 ab 0.48 6 0.03 c 6.66 6 0.31 b 7.91 6 0.22 a ,0.01 PF 2nd (kHz) 61.03 6 0.44 c 60.00 6 0.17 c 69.02 6 0.55 b 80.92 6 0.59 a ,0.01 MINF 2nd (kHz) 51.59 6 1.07 c 59.61 6 0.16 b 58.69 6 0.65 b 69.97 6 0.59 a ,0.01 49a 54.5b 55.2a MAXF 2nd (kHz) 67.26 6 0.51 c 60.23 6 0.16 d 71.07 6 0.44 b 83.21 6 0.39 a ,0.01 68a 63.5b BW 2nd (kHz) 15.67 6 1.23 a 0.62 6 0.05 b 12.37 6 0.38 a 15.24 6 0.51 a ,0.01 PF 3rd (kHz) 90.46 6 0.78 c 90.01 6 0.25 c 100.62 6 1.25 b 113.24 6 1.62 a ,0.01 MINF 3rd (kHz) 78.20 6 0.76 c 89.57 6 0.25 b 88.03 6 2.37 b 100.42 6 0.65 a ,0.01 MAXF 3rd (kHz) 99.00 6 0.43 c 90.24 6 0.25 d 106.21 6 0.79 b 123.71 6 0.57 a ,0.01 BW 3rd (kHz) 19.79 6 0.63 b 0.67 6 0.02 c 18.47 6 1.55 b 23.28 6 0.67 a ,0.01 a Schnitzler et al.
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