RAFFLES BULLETIN OF ZOOLOGY 2015 Conservation & Ecology RAFFLES BULLETIN OF ZOOLOGY 63: 91–96 Date of publication: 14 April 2015 http://zoobank.org/urn:lsid:zoobank.org:pub:27F5BCC3-B549-49FB-94CB-9BE6D47384C0 Dietary analysis of five insectivorous bat species from Kamphaeng Phet, Thailand. Robbie Weterings1,2*, Joske Wardenaar3, Scott Dunn4, Chanin Umponstira2 Abstract. This study provides a baseline for several bat species in Thailand that have never been studied with regard to diets. The diets of five bat species from Northern Thailand were analysed based on faecal pellets. The percentage volume of insect orders in the diet of Hipposideros armiger (30 pellets) consisted for 28.2% of Hemiptera, 20.5% of Lepidoptera and 20.1% of Coleoptera. The diet of this species was not dominated by a single order. The diet of Hypsugo cadornae (30 pellets) consisted for 49.3% of Hemiptera and 43.7% of Coleoptera. Rhinolophus thailandensis (31 pellets) had remains in its pellets consisting of 43.2% Coleoptera, 32.0% Hemiptera and 12.3% Homoptera. Rhinolophus thailandensis and H. cadornae both feed on large numbers of insects that have thick exoskeletons. For Taphozous melanopogon (30 pellets) the diets was comprised of 45.1% Hemiptera, 19.0% Lepidoptera and 15.3% Coleoptera. The diet of T. longimanus (30 pellets) consisted of 30.7% Diptera, 23.7% Lepidoptera and 19.0% Hemiptera. The large amount of Diptera and relative large numbers of Culicidae in the diet of this urban population might have potential implications for the control of vector mosquitoes. Key words. Hipposideros armiger, Hypsugo cadornae, Rhinolophus thailandensis, Taphozous longimanus, Taphozous melanopogon, diet INTRODUCTION Despite the rich diversity of 104 insectivorous bat species in Thailand (Bumrungsri et al., 2006), little is known about the Insectivorous bats provide important ecological services such diets of most of these species. To date, the diet of only a few as pest control (Boyles et al., 2011). In the United States, for species have been studied in Thailand, including Tadarida example, the economic importance of bats in agriculture has plicata (Leelapaibul et al., 2005) and Taphozous longimanus been estimated to be as high as US$ 22.9 billion annually (Boonkird et al., 2004). It is therefore of particular interest (Boyles et al., 2011). The value of bats in agriculture to acquire information about the types of insects these bats is also likely to be high elsewhere, where agriculture is prey upon, because this can have major implications for the of importance. For example in Thailand, Leelapaibul et biological control of agricultural pest and disease vectors al. (2005) estimated that the total Thai Tadarida plicata such as mosquitoes. population feeds on approximately 54.8 tons of insects nightly. The diet of this species consisted of at least 41% In the investigation of bat diets, studies show that some of agricultural pest species therefore its impact on pest species can be considered specialist feeders while most control can be considered to be significant (Leelapaibul et species are generalists (Freeman, 1979; Bogdanowicz et al., 2005). Some studies have shown that some bat species al., 1999; Aguirre et al., 2003; Weterings & Umponstira, feed on mosquitoes, which makes them interesting for vector 2014). It is thought that certain species prefer soft-bodied control as well (Rydell et al., 2002; Reiskind & Wund, 2009). insects or moths while others do not show any preference Reiskind & Wund (2009) experimented with with caged bats for specific prey items (Freeman, 1979; Bogdanowicz et and ovipositing mosquitoes, they found a 32% reduction al., 1999; Aguirre et al., 2003; Ghazali & Dzeverin, 2013; of egg rafts in areas with bats compared to bat-free areas. Weterings & Umponstira, 2014). Insectivorous bats can be classified into four categories based on their diet: generalists, hard bodied insect feeders, soft bodied insect feeders and Lepidoptera specialists (Freeman, 1979; Bogdanowicz et al., 1999; Aguirre et al., 2003). However, these categories are 1Cat Drop Foundation, Boorn 45, 9204 AZ, Drachten, The Netherlands; Email: not very strict, and diet can be dependent on locality, season [email protected] (*corresponding author). and climate (Leelapaibul et al., 2005; Zhang et al., 2005). 2Faculty of Agriculture Natural Resources and Environment, Naresuan University, 99 Moo 9 Phitsanulok-Nakhonsawan Road Tambon Tapho, Muang Phitsanulok, 65000 Thailand; Email: [email protected] (CU) The aim of this study was to provide insights into the 3Fauna Futura Ecologica, Frankenstraat 28, 2582 SL Den Haag, The Netherlands feeding habits of five bat species occurring in north-western 4Southport College, Mornington Rd, Southport, PR9 0TT, United Kingdom; Email: Thailand. We investigated the diet of the great roundleaf [email protected] (SD) bat (Hipposideros armiger; Hodgson, 1835), the Cadorna’s © National University of Singapore pipistrelle (Hypsugo cadornae; Thomas, 1916), the Thailand ISSN 2345-7600 (electronic) | ISSN 0217-2445 (print) 91 Weterings et al.: Dietary analysis of five Thai bat species horseshoe bat (Rhinolophus thailandensis; Wu et al., combined methods produce reliable results without invasive 2009), the long-winged tomb bat (Taphozous longimanus; techniques such as mist netting (Hughes et al., 2010). Hardwicke, 1825) and the black-bearded tomb bat (Taphozous melanopogon; Temminck, 1841). While the diet of both tomb Insectivorous bats digest their food very rapidly and do not bat species has been investigated in China, India and Thailand thoroughly chew their prey. Therefore, faecal pellets often (Boonkird et al., 2004; Srinivasulu & Srinivasulu, 2005; contain many parts of prey items that can still be used to Wei et al., 2008), there are no known published studies on identify the prey to the taxonomic order and sometimes to the diet of the other three species investigated in this study. higher taxonomic levels (Whitaker et al., 2009; Whitaker & Castor, 2010). Identification of prey items from faecal pellets METHODS is therefore almost as reliable as stomach content analysis (Whitaker et al., 2009). The advantage of analysing faecal Bat faecal pellets were collected at four different sites in the pellets is that this technique is not invasive. We used the Kamphaeng Phet province in north-western Thailand. When guidelines and identification keys provided in by Whitaker collecting faeces we searched for the freshest pellets, which et al., (2009) and Whitaker & Castor (2010) for analysing were recognised by the darker colour and softer texture. the faecal pellets. We added other insect orders to these Faecal pellets from H. armiger and R. thailandensis were guidelines that were common in the area but were not present collected at two separate areas in a cave in Khong Lan in the guidelines. Pellets were dissected with a needle and national park on 6 February 2013. This cave consisted of insect parts were identified with help of a digital microscope several chambers that were connected via narrow tunnels. (CMOS USB Digital Microscope). We identified insect parts Each species occupied different chambers. Hipposideros to the highest possible taxonomic level, which was often armiger was found in a chamber of which the ceiling reached the order but sometimes the family level. We calculated the a height of approximately five to six meters. Rhinolophus percentage volume of every insect order or family found in thailandensis was only found in a chamber of which the the pellets for each bat species. The percentage frequency ceiling was approximately two meters high. We collected per insect order or family was also calculated for each bat only fresh faecal pellets directly under the roosting bats in species. The percentage frequency represents the percentage order to reduce any chances of cross-species contamination. of pellets in which a specific insect order or family was Faecal pellets from H. cadornae were collected from under found (Whitaker & Castor, 2010). We calculated the ratio a sugar palm (Borassus flabellifer) on 13 February 2013. of percentage volume versus the percentage frequency to This palm was used as roosting site and was located in a rice find any discrepancies between the two measures. These paddy near the village Lan Dok Mai. Kamphaeng Phet city ratios were then compared using ANOVA and Tukey’s hosts a large colony of T. longimanus, which roosts under the post-hoc test. All analysis were conducted in Rstudio version bridge that crosses the Ping River. Faecal pellets from this 0.98.1028 (RStudio, 2012) built on R 3.0.2 (R Development species were collected under the bridge on 25 January 2013. Core Team, 2013). The faecal pellets from T. melanopogon were collected in a very small cave in a predominantly agricultural landscape RESULTS near Phran Kratai town on 28 January 2013. During several surveys we only found this cave to be occupied by this A total of 151 faecal pellets were analysed; 30 pellets for T. species, therefore cross-species contamination is unlikely. longimanus, T. melanopogon, H. cadornae and H. armiger In addition, we only collected fresh faecal pellets to reduce and 31 pellets for R. thailandensis. Insect fragments were any chances of cross-species contamination. identified from 11 insect orders (Table 1). Hemiptera and Coleoptera were the most common food items, occurring in Faecal pellets were separately stored in glass containers filled 56.3% and 46.4% of the total number of pellets respectively. with alcohol. Bats were identified with combined techniques. Other important insect orders were Lepidoptera (41.7%), Echolocation calls were recorded and photographs of the Diptera (25.2%) and Homoptera (17.9%). bats were taken. A Petterrson 240X and a Baton (Batbox) Bat Detector with recording devices were used to record the In terms of percentage volume, the diet of H. cadornae echolocation calls. With help of existing species-presence- consisted mainly of Hemiptera (49.3%) and Coleoptera absence models (Hughes et al., 2010) we could narrow down (43.7%). This was the only species for which we did not the number of species that are likely to be present in the find any moth (Lepidoptera) fragments or scales in the study area. Some species have a strong overlap in their call faecal pellets. In one faecal sample of this species we found frequencies, therefore narrowing the number of species was nine individual mites (Acarina), mites were not detected essential in order to reliably identify the species. We used in the pellets of any other species. The percentage volume Audacity software (version 2.0.0, Oetzmann & Mazzoni, of Coleoptera in its diet was higher than that of all other 2013) for analysing the recorded echolocation calls. The species except for R. thailandensis. The diet of T. longimanus calls were compared with calls from previously identified consisted mainly of Diptera (30.7%), Lepidoptera (23.7%), bats in the region based on published and unpublished data Hemiptera (19.0%) and Coleoptera (14.5%). The amount (Furey et al., 2009; Zhang et al., 2009; Hughes et al., 2010; of Diptera (including Culicidae) in the diet of this species Hughes et al., 2011, Boonman unpublished data). Photographs was higher than that of the other species. Diptera occurred were then used to corroborate species identification. These in 36.7% of the samples. Taphozous longimanus fed on 92 RAFFLES BULLETIN OF ZOOLOGY 2015 n y elanopogo Frequenc(%) – 38.7 32.3 – – – 32.3 22.6 77.4 22.6 6.5 29.0 3.2 – 61.3 – – – 3.2 m s ou e phoz olum(%) – 15.3 7.4 – – – 7.4 1.9 45.1 7.1 3.2 10.3 0.8 – 19.0 – – – 0.2 a V T y s c u n ngiman Freque(%) – 30.0 46.7 3.3 3.3 3.3 56.7 6.7 33.3 10.0 – 10.0 – – 63.3 – – – 10.0 o l s u aphozo olume (%) – 14.5 25.7 2.7 1.3 1.0 30.7 2.2 19.0 3.0 – 3.0 – – 23.7 – – – 7.0 T V nsis ncy ailande Freque(%) – 58.1 16.1 – – – 16.1 6.5 45.2 3.2 9.7 12.9 3.2 – 25.8 – 6.5 3.2 3.2 h t s u h e p m nolo olu(%) – 43.2 5.5 – – – 5.5 1.9 32.0 2.6 9.7 12.3 0.3 – 3.5 – 0.6 0.5 0.2 hi V R es. y died speci dornae Frequenc(%) 3.3 70.0 6.7 3.3 – – 6.7 – 76.7 3.3 – 3.3 3.3 – 3.3 – – – – u a from the st Hypsugo c olume (%) 0.2 43.7 1.2 0.3 – – 1.2 – 49.3 2.5 – 2.5 2.7 – 0.2 – – – – s V e c e a f orders in bat s armiger Frequency (%) – 34.5 13.8 – – – 13.8 20.7 48.3 24.1 10.3 34.5 – 3.4 55.2 3.4 – – 6.9 nsect sidero e i o m of all Hipp Volu(%) – 20.1 4.0 – – – 4.0 4.5 28.2 7.0 8.6 15.6 – 1.6 20.4 2.1 – – 3.6 e m u ol a d v a pter frequency an Family Unidentified Culicidae Psychodidae Tipulidae Total Dipter Unidentified Cicadellidae Total Homo e g a able 1: Percent Order Acarina Coleoptera Diptera Ephemeroptera Hemiptera Homoptera Hymenoptera Isoptera Lepidoptera Neuroptera Orthoptera Trichoptera Unidentified T 93 Weterings et al.: Dietary analysis of five Thai bat species little Hemiptera compared to all other species except H. (Whitaker et al., 2009). This results in a low Lepidoptera armiger. For T. melanopogon the percentage frequency of percentage volume because only a few scale are found, but in Diptera (32.2%) was similar to that of T. longimanus but a higher frequency because they are present in many faecal the percentage volume (7.4%) was much lower. The diet pellets. These differences can cause a bias when interpreting of T. melanopogon mainly consisted of Hemiptera (45.1%) the diet of bats. It is therefore important to consider both followed by Lepidoptera (19.0%), Coleoptera (15.3%) and percentage volume and percentage frequency because both Homoptera (7.1%). For R. thailandensis the diet mainly measures capture different and additive information. consisted of Coleoptera (43.2%), Hemiptera (32.0%) and Homoptera (12.3%) in terms of percentage volume. The Taphozous longimanus and Taphozous melanopogon. We diet of this species was the most diverse in terms of insect found high numbers of Diptera in the diet of T. longimanus orders, containing insects from nine different orders compared (30.7% volume), which was contrary to previous studies that to eight for H. armiger, seven for H. cadornae, seven for found that bats that feed on large numbers of Diptera and T. melanopogon and five for T. longimanus. Rhinolophus Lepidoptera are often small and have high call frequencies thailandensis was the only species for which we found (Bogdanowicz et al., 1999; Weterings & Umponstira, 2014). insect fragments in the orders Trichoptera (1 pellet) and In constrast, T. longimanus is a relative large insectivorous Orthoptera (2 pellets). The percentage volume of insect bat, with a mean body weight of 27 g (Smith et al., 2003), and orders in the diet of H. armiger was highest for Hemiptera has a relatively low call frequency (frequency of maximum (28.2%), Lepidoptera (20.5%) and Coleoptera (20.1%). energy is 30.8 kHz; Hughes et al., 2011). Large bats with low Hipposideros armiger was the only species for which we call frequencies are more likely to have a diet that consists found Neuroptera (1 pellet) and Isoptera (1 pellet) fragments mainly of insects with thick exoskeletons such as Coleoptera in the faecal pellets. The percentage volume of Hemiptera or Hemiptera. The similarly sized T. melanopogon also had was highest for this species. relatively high Diptera content in the diet (7.4% volume), although it was not as high as for T. longimanus. In the five main food items there were significant differences in the ratio of percentage volume and percentage frequency Diet studies of the two species seem to indicate that (F = 4.84, d.f. = 4, P-value = 0.007): Coleoptera 0.57 ±0.13, Diptera content may vary owing to habitat or seasonal Diptera 0.31 ±0.15, Hemiptera 0.62 ±0.06, Homoptera 0.56 availability. Srinivasulu et al (2005) investigated the diet ±0.28 and Lepidoptera 0.25 ±0.15. The post-hoc test showed of T. melanopogon in two different habitat types and found that the ratio of Lepidoptera was significantly lower than higher Diptera content for diets from bats roosting in a that of Coleoptera and Hemiptera. In addition, the ratio for semi-urban habitat compared to those in a forest habitat. A Diptera was also significant lower than that of Hemiptera. Chinese study also investigated the diets of T. melanopogon and found that Diptera also made up a relative large part of DISCUSSION the diet of this species, with an overall percentage frequency of 11.1% during a five-month period that had a single month Our analyses give some important baseline information peak of 73.2% (Wei et al., 2008). On the other hand, in about five bat species from Thailand. We found large Bangkok the diet of T. longimanus was found to only consist differences in the diets of some species (e.g., H. cadornae of 2.54% Diptera and 53.04% of Lepidoptera (Boonkird et vs. T. melanopogon) but small difference in the diets of other al., 2004). Hence, it is likely that both T. longimanus and T. species (e.g., H. armiger vs. T. melanopogon). The diets melanopogon may be opportunistic feeders that can exploit are discussed per species in further detail in the following a wide diversity of available insects. paragraph. Note that these results should be interpreted carefully as diets of bats are very dependent on region and The high Diptera content in the diet of T. longimanus is season (Leelapaibul et al., 2005; Zhang et al., 2005). There is interesting especially because the sampled population is often much variation found in the diet of bats from the same located in an urban area. Culicidae made up at least 8.8% species coming from different regions (Kurta & Whitaker, of the total volume of Diptera found in this species therefore 1998; Srinivasulu & Srinivasulu, 2005). It is therefore it might be potentially important in the control of urban difficult to use such information to make generalisations disease vectors in this insect family. about one species. Hypsugo cadornae. The diet of H. cadornae mainly When comparing the percentage volume and frequency of consisted of Coleoptera and Hemiptera but did not contain occurrence of prey items for this study, the ratio appeared any Lepidoptera. This diet is in line with what would be to be lower for Lepidoptera and Diptera in comparison to expected based on the the relative low call frequency (37.5 Coleoptera, Hemiptera and Homoptera. This difference in kHz, Boonman unpublished data), which is an indication Diptera can be explained by the fact that Diptera are often towards low Lepidoptera content and a high content of smaller and softer than insects from the other orders (Lease insects with thick exoskeletons (Bogdanowicz et al., 1999; & Wolf, 2010). A single dipteran prey will take up less Weterings & Umponstira, 2014). The species is relative volume in a faecal pellet but will still be counted as present small with a mean body mass of 5.9 g and a forearm length resulting in a higher volume-frequency ratio. For Lepidoptera, of 12.9 mm (Francis, 2008). Small bats are more agile and this difference could be explained by the fact that the wing therefore more likely to feed on smaller insects, this might scales often remain in the digestive tract for a longer period for example explain some of the Culicidae content in its diet. 94 RAFFLES BULLETIN OF ZOOLOGY 2015 The presence of mites (Acarina) in one faecal pellet was ACKNOWLEDGEMENTS also very interesting. Mites are common parasites on bats and have reported for a range of bat species (Whitaker et al., The authors would like to thank the faculty of Agriculture, 1983). There are many species of mites that are associated Natural Resources and Environment of Naresuan University with bats (Baker & Craven, 2003). Not many studies have and the Cat Drop Foundation for financial support of this reported the presence of mites in faecal pellets, nevertheless, study, Dr John Whitaker Jr. for supplying information about they are commonly found on bats and could possibly end the methodology and Sara Bumrungsri and Michael Barbetti up in the faeces if ingested during grooming (Miková et al., for commenting on an early draft. We are thankful to the 2013). For some bat species it is know that mite infestations anonymous reviewers whose comments really improved increase grooming activities (Giorgi et al., 2001; Godinho et the manuscript. We would also like to show our gratitude al., 2013). Mites are relative small and will mostly remain to the monks at the Hom Chom Phra Yai temple in Phran intact while passing the digestive tract of a bat. Therefore, Kratai and the Department of National Parks, Wildlife and they would easily be recognised when they are present in Plant Conservation for allowing us to enter the caves at faecal pellets and it would be very likely that they would their premises. have been reported more often. Hence, the fact that mites were only found in a single faecal pellet together with the LITERATURE CITED high number of mites (nine) in one pellet suggests that these mites are likely not parasites from the bat but from one of Abbot P & Dill LM (2001) Sexually transmitted parasites and sexual selection in the milkweed leaf beetle, Labidomera clivicollis. the food items. The faecal pellet that contained these mites Oikos, 92: 91–100. consisted for 95% of Coleoptera fragments. Parasitic mites Aguirre LF, Herrel A, Van Damme R & Matthysen E (2003) are also found on Coleoptera (Abbot & Dill, 2001; Almane The implications of food hardness for diet in bats. Functional & Elnov, 2009). 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