Morphology, Echolocation Calls and Diet of Scotophilus kuhlii (Chiroptera: Vespertilionidae) on Hainan Island, South China

Author(s): Guangjian Zhu, Aleksei Chmura, and Libiao Zhang Source: Acta Chiropterologica, 14(1):175-181. 2012. Published By: Museum and Institute of Zoology, Polish Academy of Sciences DOI: http://dx.doi.org/10.3161/150811012X654394 URL: http://www.bioone.org/doi/full/10.3161/150811012X654394

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Acta Chiropterologica, 14(1): 175181, 2012

PL ISSN 1508-1109 Museum and Institute of Zoology PAS doi: 10.3161/150811012X654394

Morphology, echolocation calls and diet of Scotophilus kuhlii (Chiroptera: Vespertilionidae) on Hainan Island, south China
GUANGJIAN ZHU1, 3, ALEKSEI CHMURA2, and LIBIAO ZHANG3, 4
1Institute

of Molecular Ecology and Evolution, Institute for Advanced Interdisciplinary Research, East China Normal University, Zhongshan Bei Road, Putuo Distriction, Shanghai, 200062, China 2EcoHealth Alliance, 460 West 34th Street, 17th Floor, New York, NY 10001, USA 3Guangdong Entomological Institute, 105 Xingang Xi Road, Haizhu Distriction, Guangzhou, 510260, China 4 Corresponding author: E-mail: zhanglb@gdei.gd.cn

Scotophilus kuhlii is distributed in many urban environments, yet the ecology of this species is poorly known. The morphology, echolocation call structure, diet, and foraging areas of S. kuhlii were studied on Hainan Island, south China from March to November 2006. Data from 85 individuals indicate that S. kuhlii is a medium-sized bat with 50.41 1.36 (0 SE) mm forearm length and 19.81 3.47 g body mass. The wing morphology with high wing-loading (11.38 1.95 N/m2) and moderate aspect ratio (6.96 0.75) indicates that S. kuhlii flies fast and forages in open habitat and at the edges of cluttered environments. Echolocation calls of S. kuhlii consist of a fundamental and up to four harmonics, with a dominant frequency of 45.72 2.09 kHz, and call shape suggests that this species is adapted to forage in open environments. Data from mist-netting and acoustic detection indicated that S. kuhlii foraged mainly around the crown of trees and street lights. Nine insect orders were recorded in its diet, with Lepidoptera (97.46%, by frequency) and Coleoptera (64.72 2.37%, by volume) constituting the main prey, together with Hemiptera (19.99 1.25%) and Hymenoptera (9.43 1.14%). There was significant seasonal variation in the diet of S. kuhlii: Coleoptera increased from March to May, and then decreased to August, while Hemiptera and Hymenoptera showed the inverse trend. Key words: Hainan Island, bats, echolocation, morphology, ecology, diet, Scotophilus kuhlii

INTRODUCTION Wing morphology and echolocation calls, and their relationship to foraging ecology, are often studied as indicators of potential resource partitioning by insectivorous bats (Aldridge and Rautenbach, 1987; Jones et al., 1993; Fenton and Bogdanowicz, 2002; Jennings et al., 2004; Salsamendi et al., 2005). Wing morphology strongly affects the flight ability of bats (Norberg and Rayner, 1987) and is often quantified using the metrics of wing loading, wing aspect ratio and wing-tip shape index. Wing loading is considered to be positively correlated with minimum speed and negatively with maneuverability. High wing aspect ratios correspond to long narrow wings and energy-efficient flight, while wing-tip shape index describes the pointedness of wing tips and correlates with the hovering ability in bats (Aldridge and Rautenbach, 1987; Norberg and Rayner, 1987; Jennings et al., 2004).

Insectivorous bats use echolocation calls for object localization (e.g., prey) and for orientation in three-dimensional space (Griffin et al., 1960). The structure of echolocation calls reflects the degree of acoustic clutter encountered by the bat and is indicative of the size and type of prey taken (Schnitzler et al., 2003). Bats emitting loud, low frequency echolocation calls are able to detect prey over great distances but for the large prey only (Jennings et al., 2004). Bats alter the structure of their calls during foraging in different habitats to efficiently hunt prey (Schnitzler et al., 2003). In cluttered environments, the interval between pulses is reduced since bats need to obtain more information about the position of obstacles to rapidly adjust their flight (Findley and Black, 1983). Similarly, calls also tend to be reduced in duration as bats enter clutter to minimize pulse-echo overlap (Kalko and Schnitzler, 1993). The house bat, genus Scotophilus, consists of 13 species worldwide, ranging from Southeast Asia to Africa. In China, only two species (S. kuhlii and

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G. Zhu, A. Chmura, and L. Zhang a street about two km from roosts, 2) around the crowns of the trees (Ficus spp. and C. nucifera) covering an area of nearly 2 km2, 3) open areas two sites with an estimated total area of 3 km2 , a grassland surrounding with C. nucifera and 4) over water Hongchen Lake approximately 0.25 km2 located in the centre of Haikou city. Based on previous observations, four groups (one charged with recording at fixed sites while another checked mist-net in each group) were set in each habitat to check mist-nets and monitored bat feeding buzzes with a Pettersson D-980 bat detector during netting nights. Recordings were analysed in BatSound Pro v3.31 (Pettersson Elektronik AB, Sweden) software packages. Three U-shape mist-nets (20 meters long and 10 meters high, consisted of nine single mist-nets) were set every 500 meters at the 12 meter height in each habitat. Every mist-net were checked every two hours during a netting night (6:00 PM till 6:00 AM). Each habitat was sampled for 14 consecutive nights to determine the foraging areas. The identity of flying bats was confirmed for netted individuals, and all the netted bats were marked with a 3.5 mm aluminium alloy bat ring (Porzana, UK) on right forearm to avoid pseudoreplication. While mist-netting, feeding buzzes were monitored using bat detectors to determine feeding activity.

S. heathi) have been recorded. Scotophilus kuhlii is found primarily in south-east Asia (Simmons, 2005) and very little is known about its behaviour or ecology. This species uses leaf tents as day roosting site in the Philippines (Rickart et al., 1989; Bates and Harrison, 1997). In this paper, we describe the morphology, echolocation calls, foraging behaviour, and seasonal variation of the diet of S. kuhlii from Hainan Island, to better understand the natural history of this species. MATERIALS AND METHODS Study Area and Sampling
Eight colonies of S. kuhlii on the campus of Hainan Normal University, Haikou, Hainan Island, south China (1959.910N, 11020.399E) were studied. The roosts were located in a busy urban area, with the vegetation around the roost sites consisting of Cocos nucifera, Ficus microcarpa, Terminalia catappa and shrubbery.

Diet Analysis
Faecal pellets were collected between March and November 2006 from roosted under folded-down leaves, commonly known as tents, of C. nucifera (coco palms). No samples were collected between December and February as bats were absent from the site during this period (a minimum of 60 pellets each month). Faeces were collected from a plastic sheet placed under each of the eight roosts for three consecutive days in the middle of each month. Intact faeces were placed into two ml tubes containing 75% ethanol and analyzed using the method described by Kunz and Whitaker (1983). Insect remains in the droppings were identified to order under a dissecting microscope using the key of Zheng and Gui (1999). The percentage volume of insect orders in each faecal sample was estimated by eye. For Lepidoptera, only appearance frequency was recorded as it is very difficult to estimate the percentage volume (Kunz and Whitaker, 1983).

Morphological Measurements
Individuals of S. kuhlii were caught using a hand net attached to a telescopic pole. For each individual, we recorded the sex, measured body mass using a digital pocket scale (ShenZhen Viabetter Electronic Scale Limited, HF-07; accurate to 0.01 g), and took the following measurements using vernier callipers (Shanghai Everwin Tool Co., Ltd; accuracy 0.01 mm): length of the right forearm, right wing, ear, tragus, body (from the tip of the snout to the anus ventrally) and hind foot. The outline of the right wing (including the right tail membrane and the right half of the body) was traced onto paper and scanned into a computer with same format, calculated in Photoshop 7.0 software. Wing loading, aspect ratio and wing-tip shape index were calculated later according to Norberg and Rayner (1987).

Echolocation Call Recording

Echolocation calls were recorded from individual bats released at dusk from the centre of a soccer field located near the roost sites. Time expansion (10X) recordings were made with a Pettersson D-980 bat detector and digitized onto a laptop computer with a sampling rate of 44.1 kHz with 16-bit precision. BatSound Pro v3.31 (Pettersson Elektronik AB, Sweden), was used to generate spectrograms and power spectra using a 1024point FFT (with Hanning window), giving 342 Hz resolution. The dominant frequency was measured from the power spectrum. Start and end frequencies of the fundamental were obtained from the oscillogram in combined Hanning windows. Call duration and interpulse interval were measured from the oscillogram. Interpulse interval was measured from the beginning of one call to the beginning of the subsequent call.

Statistical Analysis
All data were analyzed using SPSS 13.0 (SPSS Inc, USA). Firstly, data normality and homoscedasticity were tested (P > 0.05). Then, the Students t-test for independent samples was used to determine if there were any differences in morphology and echolocation call parameters between male and female. Seasonal variation in the diet was compared using a KruskalWallis H-test, and Chi-squared test to determine the distribution of foraging area selectivity.

RESULTS Morphology Eighty five adult S. kuhlii (35 XX and 50 YY) from roosts in coco palms were captured. Morphologically, females had significantly longer forearm (XX: 51.3 1.57 mm, YY: 49.66 1.07 mm;

Foraging Area Investigation

Foraging areas were determined by mist-netting, acoustic detection (with bat detectors) and visual observations. Foraging habitats were classified as 1) around street lights, mainly in

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t = 5.30, d.f. = 83, P < 0.001) and larger hand-wing area (t = 1.15, d.f. = 83, P < 0.001) than those of males, but no other sexual dimorphism in body size or wing morphology was observed. S. kuhlii is a medium-sized bat with forearm length (50.41 1.36 mm) and body mass (19.81 3.47 g), with a high wing-loading (11.38 1.95 N/m2), moderate aspect ratio (6.96 0.75) and high tip shape index (1.30 0.52) (Table 1). Echolocation Calls Echolocation calls for S. kuhlii had a fundamental and up to four harmonics (Fig. 1). Each call begins with a steep frequency-modulated section and ends with a Quasi Constant Frequency part. The frequency with most energy (dominant frequency) was always in the fundamental. Independent-sample t-tests showed no significant difference between calls from males and females or any other parameters measured; therefore data of echolocation calls were combined from both sexes for subsequent analyses. The fundamental harmonic has a starting frequency of 89.07 7.25 kHz, a dominant frequency of 45.72 2.09 kHz, and an end frequency of 37.95 4.05 kHz. The pulse duration and pulse interval were 5.27 1.21 ms and 44.72 7.50 ms, respectively (Table 1).

Foraging Area and Diet One hundred and two individuals were netted during the 14 netting nights. Most (47.1%) were caught near the crowns of trees, 31.4% around street lights, 16.7% above the soccer field, and 4.9% over the lake. Frequencies of captured bats indicated a significant difference in the use of foraging habitats (2 = 40.82, d.f. = 3, P < 0.001), indicating that S. kuhlii mainly foraged near the crowns of trees and around the street lights. While, 12, 3, 1 and 0 feeding buzzes were recorded during 14 nights bat detecting in the four habitat types, crown of trees, around street lights, soccer field and above the lake respectively. This supports the results from mistnetting data (Table 2). Nine insect orders were identified from the faeces of S. kuhlii. By volume, in decreasing order were Coleoptera (64.72 2.37%), Hemiptera (19.99 1.25%), Hymenoptera (9.43 1.14%), and Diptera (5.49 0.14%), while Lepidoptera (97.46%) were recorded the highest by frequency. Odonata, Homoptera, Trichoptera, Orthoptera were occasionally recorded in the faeces (Table 3). The main prey items taken by S. kuhlii showed significant seasonal variation (Lepidoptera: 2 = 39.4, d.f. = 9, P < 0.001; Coleoptera: 2 = 402.7, d.f. = 9, P < 0.001; Hemiptera: 2 = 268.0, d.f. = 9, P < 0.001;

TABLE 1. The measurements of body size, wing morphology and echolocation calls from S. kuhlii on Hainan Island, south China. Data were obtained from 85 individuals (35 YY and 50 XX) captured in October 2006. A Students t-test was conducted on all the measured characters between female and male S. kuhlii Parameter Forearm length (mm) Body mass (g) Ear length (mm) Tragus length (mm) Hind foot length (mm) Body length (mm) Tail length (mm) Wing morphology Wing span (mm) Wing area (10-3 m2) Aspect ratio Wing loading (N/m2) Hand-wing area (10-3 m2) Arm-wing area (10-3 m2) Tip length ratio Tip area ratio Tip shape index Echolocation calls Dominant frequency (kHz) Start frequency (kHz) End frequency (kHz) Pulse duration (ms) Pulse interval (ms) Body size 0 SE XX 51.3 1.6 20.5 3.6 10.5 1.1 6.3 0.6 10.4 0.8 69.5 5.6 42.3 4.4 34.9 1.9 17.7 2.1 7.0 0.7 11.5 2.1 3.1 0.3 4.1 0.6 1.4 0.1 0.8 0.9 1.4 0.7 45.7 2.1 88.7 6.9 37.9 2.8 5.1 1.0 46.8 24.7 YY 49.7 1.1 19.1 3.8 10.5 1.2 6.3 0.7 10.2 1.2 67.2 5.4 40.2 4.3 33.9 1.5 16.6 1.9 7.0 0.8 11.3 1.9 2.8 0.3 4.0 0.6 1.4 0.1 0.8 1.0 1.3 0.5 45.8 2.2 89.4 7.9 38.1 5.2 5.4 2.1 43.0 25.2 XX 48.154.6 12.729.3 7.512.4 5.17.4 8.112.1 54.881.3 31.349.3 28.838.2 10.721.9 5.68.7 7.017.5 2.33.8 3.15.6 1.11.7 0.61.0 0.83.6 41.951.4 64.2103.2 31.044.1 2.98.1 13.5127.4 Range YY 48.051.9 12.530.3 8.313.4 5.17.2 8.313.8 54.882.1 31.550.1 30.436.6 12.820.1 5.310.0 8.016.7 2.23.4 2.75.0 1.11.5 0.51.0 0.62.8 39.950.2 71.0104.5 12.842.7 3.014.1 13.1127.4 P 0.000 0.091 0.846 0.707 0.448 0.056 0.069 0.060 0.021 0.954 0.704 0.000 0.232 0.454 0.110 0.441 0.870 0.780 0.840 0.490 0.530

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A
Amplitude (%)

B
Frequency (kHz)

Power (dB)

Power (dB)

Frequency (kHz) FIG. 1. Two sequential echolocation calls recorded from S. kuhlii in free flight after release from the hand. The three panels show the waveform (A), spectrogram (B) and power spectra (left call = C, right call = D)

Morphology, echolocation calls and diet of Scotophilus kuhlii TABLE 2. Data from mist-netting and feeding buzzes in the examined foraging area. Mist-netting was performed with Ushape mist net groups, each mist-net was checked about every two hours Habitats Around street light Crown of the trees Open areas Above lake Mist-netting Feeding buzzes (individuals caught) (quantity recorded) 32 48 17 5 3 12 1 0

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Hymenoptera: 2 = 244.9, d.f. = 9, P < 0.001) (Table 3). The percent volume for Coleoptera increased from March to May, and then decreased towards August, while Hemiptera and Hymenoptera showed an inverse trend. DISCUSSION Morphology This study showed that there were no significant morphological differences between male and female S. kuhlii except forearm length and hand-wing area. The morphological data is consistent with prior studies conducted outside of China (Goodman et al., 2005), except ear and hind foot lengths recorded were shorter. The average wing span of male S. kuhlii in this study is consistent with that recorded by Goodwin (1979). However, owing to the absence of measurements for females (Goodwin, 1979), no comparisons can be made for the wing span of female S. kuhlii. Due to lack of recorded data for body mass and wing area from Goodwin (1979) and limited sample size, little can be said about differences in wing loading and aspect ratio. Studies of other

insectivorous bats have suggested that species with low wing loading and aspect ratio have greater manoeuvrability (Jennings et al., 2004). This study indicates that S. kuhlii on Hainan Island has a high wing-loading (11.6 N/m2) and a moderate aspect ratio (6.96). This implies an ability to fly fast with low energy expenditure, but low manoeuvrability, indicating that S. kuhlii may fly and forage in open habitat or at the edge of cluttered environment. The present study found that S. kuhlii preferred foraging in relatively open area or around the street lights, supporting the predictions of the wing morphology. Echolocation Call Studies on echolocation have established that variations in the echolocation calls of bats exist at three different levels: species, individuals within a species, and calls of a given individual (Karry et al., 2001). Intraspecific echolocation variation between the sexes has been described for many species (Neuweiler et al., 1987; Suga et al., 1987; Jones et al., 1992, 1993). The present study found no difference between the sexes for S. kuhlii. Several studies have established a relationship between echolocation call structure, morphology, and foraging behaviour (Norberg and Rayner, 1987; Jones et al., 1993; Jennings et al., 2004; Salsamendi et al., 2005). Echolocation call structure has a relationship with body size (Jones et al., 1993; Zhang et al., 2007), with larger species usually emitting calls with a lower frequency and higher intensity compared to smaller species. The production of lower frequency and higher intensity pulses increases potential detection over long distances. The frequency with most

TABLE 3. Analysis of monthly dietary components from S. kuhlii. 789 faecal pellets (over 60 samples each month) were collected from March to November 2006. All the orders varied seasonally, all P < 0.001 Months March April May June July August September October November December Total 2 Frequency percentage Lepidoptera 95.8 100.0 100.0 100.0 89.1 92.4 97.3 100.0 100.0 100.0 97.5 39.4 Volume percentage (0 SE) Hemiptera Hymenoptera 22.1 0.6 17.3 0.8 13.1 0.4 18.1 0.5 23.4 0.5 23.2 0.6 18.4 0.8 24.7 0.7 26.6 0.9 19.6 0.1 20.0 0.3 268.0 7.5 0.5 6.7 0.5 6.4 0.3 8.5 0.3 9.1 0.3 18.6 0.9 7.1 0.3 7.3 0.4 8.6 0.7 11.4 0.7 9.4 0.2 244.9

Coleoptera 67.5 0.8 74.0 1.0 76.2 0.5 66.6 0.6 61.6 0.5 51.2 0.8 65.0 1.0 62.2 1.0 60.4 1.3 65.5 1.8 64.7 0.4 402.7

Diptera 2.0 0.4 2.0 0.4 4.3 0.3 6.4 0.2 5.8 0.2 7.0 0.3 7.5 0.7 5.0 0.4 3.9 0.4 3.2 0.8 5.5 0.1 195.0

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energy was in the fundamental, with a low frequency of 45.72 kHz, indicating that S. kuhlii can detect prey over long distances in open habitats, and may catch relatively large prey. It also emitted relatively broadband frequency-modulated echolocation calls with the fourth harmonic up to 200 kHz during flight, which may be well suited for obtaining detailed information about the target (Neuweiler, 1984). Diet and Foraging Area Although radio telemetry was regarded as an important and effective tool for investigating the activities and foraging areas of mammals and birds, ultrasound detectors (McAney and Fairley, 1988), lighttagging animals (Schofield and Morris, 1999) and the mark-recapture method (Handley et al., 1991) have been used to determine foraging areas of bats. In view of the fact that very weak and highly directional electronic signals of radio telemetry makes them difficult to detect in the field, data from ultrasound detectors obtained in such circumstances might be difficult to interpret. So, we used mist-netting, acoustic detection (via bat detectors) and visual observations together to determine the foraging areas of S. kuhlii bat in this study. Aldridge and Rautenbach (1987) showed that wing morphology and echolocation call structure could influence foraging site selection and foraging behaviour in insectivorous bats. Data from the present study revealed that S. kuhlii foraged predominately in open environments or at the edge of the cluttered environments, including the crowns of trees within the urban environment, around street lights, a soccer field, and over a lake, which supported our predtion based on the wing morphology and echolocation calls. The morphology of S. leucogaster is similar to S. kuhlii (Goodman et al., 2005) and it preys primarily on Hemiptera and Coleoptera (Barclay, 1985). Our data also indicated that S. kuhlii feed mainly on Coleoptera, Hemiptera, Lepidoptera and Hymenoptera. The volume of Coleoptera and Hemiptera in the diet approaches 80% every month. The frequency of occurrence of Lepidoptera was used instead of volume in diet analysis to prevent biased results (usually an overestimate because of array of scale in Lepidoptera). It is known that Lepidoptera insects have ability to detect ultrasound, but they were a frequently recorded item in S. kuhliis diet in our study. Although the best hearing range of moth is considered to be 2060 kHz, this varies among species. Fenton and Fullard

(1979) found that the ears of moths in Canada are most sensitive to sounds between 20 and 40 kHz. Scotophilus kuhlii emits calls with dominate frequency at 45 kHz, suggesting that it has the potential ability to feed on some moth species. Aldridge and Rautenbach (1987) showed that echolocation calls should be related to wing morphology, and reflect the character of the prey and the foraging habitat. The relatively low dominant frequency of S. kuhlii echolocation calls and high wind loading suggest a species foraging in open habitat and feeding on relatively large prey. Lepidoptera and Coleoptera, preyed on by S. kuhlii, are relatively large insects. ACKNOWLEDGEMENTS
We thank Prof. S. Y. Zhang, Prof. S. Parsons, J. S. Zhang, X. D. Zhao, and B. Liang for their comments on earlier drafts of this manuscript. We also thank F. Li, M. Li, J. Guilbert, and Z. H. Tang for their help in the field. We are very grateful for G. P. Wangs help with the faecal analysis. This project was supported by The Ministry of Science and Technology of the Peoples Republic of China (MOST grant no. 2006FY110500), National Natural Science Foundation of China (NSFC, No. 30800102), and Special Foundation for Young Scientists ([2008]02) of Guangdong Province Academy of Science.

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