Introduction
Ectoparasites are externally borne organisms that are well-adapted as blood or lymph feeders (Patterson et al., Reference Patterson, Ballard and Wenzel1998; Patterson et al., Reference Patterson, Dick and Dittmar2007). Early studies on bat ectoparasites in the Philippines were on various arthropod groups including bat flies (Ferris, Reference Ferris1924a,Reference Ferrisb, Reference Ferris1925a,Reference Ferrisb; Theodor Reference Theodor1955, Reference Theodor1963; Maa, Reference Maa1962, Reference Maa1966, Reference Maa1968, Reference Maa1971, Reference Maa1975; Cuy, Reference Cuy1980a,Reference Cuyb, Reference Cuy1981), fleas (Hopkins and Rothschild, Reference Hopkins and Rothschild1956), chiggers (Womersley, Reference Womersley1957), ticks (Kohls, Reference Kohls1950), laelaptoids (Delfinado, Reference Delfinado1960), spinturnicid mites (Delfinado and Baker, Reference Delfinado and Baker1963; Baker and Delfinado, Reference Baker and Delfinado1964; Prasad, Reference Prasad1970; Cuy, Reference Cuy1979) and sarcoptid mites (Klompen, Reference Klompen1992). The most recent literature on bat ectoparasites in the Philippines include those by Zabat and Eduardo (Reference Zabat and Eduardo2011) and Alvarez et al. (Reference Alvarez, Lit and Alviola2015).
Although there is an immense diversity of ectoparasites associated with bats, they are often disregarded or neglected in the study of bat ecology (Messenger et al., Reference Messenger, Rupprecht, Smith, Kunz and Fenton2003). For instance, only a few studies have reported on the ectoparasites of bats in Mindoro. In his synopsis of Philippine bat flies, Cuy (Reference Cuy1980a,Reference Cuyb) reported only four species from Mindoro. In addition, Theodor (Reference Theodor1963) described two new species (Penicillidia oligacantha and P. acuminata) which was erroneously reported by Ferris (Reference Ferris1924b) as Penicillidia jenynsii. In 1981, Cuy also noted the presence of Eucampsipoda philippinensis in the island. Thus, only seven bat fly species are known in Mindoro.
These ectoparasites are of veterinary importance as potential vectors that enable pathogens and potentially pathogenic microorganisms to bypass barriers such as fur and skin (Messenger et al., Reference Messenger, Rupprecht, Smith, Kunz and Fenton2003; Dick and Patterson, Reference Dick, Patterson, Morand, Krasnov and Poulin2006). In the Philippines, bats were recently shown to harbour parasitic protozoans (Murakoshi et al., Reference Murakoshi, Recuenco, Omatsu, Sano, Taniguchi, Masangkay, Alviola, Eres, Cosico, Alvarez, Une, Kyuwa, Sugiura and Kato2016) and viruses (Watanabe et al., Reference Watanabe, Masangkay, Nagata, Morikawa, Mizutani, Fukushi, Alviola, Omatsu, Ueda, Iha, Taniguchi, Fujii, Tsuda, Endoh, Kato, Tohya, Kyuwa, Yoshikawa and Akashi2010; Taniguchi et al., Reference Taniguchi, Watanabe, Masangkay, Omatsu, Ikegami, Alviola, Ueda, Iha, Fujii, Ishii, Mizutani, Fukushi, Saijo, Kurane, Kyuwa, Akashi, Yoshikawa and Morikawa2011; Tsuda et al., Reference Tsuda, Watanabe, Masangkay, Mizutani, Alviola, Ueda, Iha, Taniguchi, Fujii, Kato, Horimoto, Kyuwa, Yoshikawa and Akashi2012), although their zoonosis are still indefinite. Bat flies are also reported to harbour fungi belonging to Order Laloulbeniales (Blackwell, Reference Blackwell1980; Marshall, Reference Marshall and Kunz1982).
In this paper, we provide an update on the bat fly and flea fauna present in Mindoro Island, particularly in the vicinities of Naujan Lake National Park.
Materials and methods
Field sampling of bats and ectoparasites
Mist nets were used to capture bats. Upon removal from the nets, captured bats were placed separately in clean cloth bags for further identification and ectoparasite collection. We followed the treatment of Ingle and Heaney (Reference Ingle and Heaney1992) regarding bat nomenclature. Bats were identified to species level (Table 1). Voucher specimens were also collected for each species as stipulated in the Gratuitous Permit No. 2011-0002 issued by the Philippine Department of Environment and Natural Resources (DENR), and were deposited at the University of the Philippines Los Baños Museum of Natural History (UPLB MNH), Philippines. Bats that were not sacrificed and preserved as voucher specimens were released back to the wild. Prior to release, bats were fed with sugar–water solution for energy.
Species of bats inspected for ectoparasites at Naujan Lake National Park, Mindoro Island, Philippines in 2011
Bats that were sacrificed were euthanized with ethyl acetate. Afterwards, the surface of the bats was inspected closely with particular attention to body parts typically preferred by certain parasites, i.e. head, patagia and axilla. Ectoparasites were collected with a pair of forceps and placed in vials containing 70% ethanol.
Ectoparasite preparation and identification
Ectoparasites were identified using the identification key of Cuy (Reference Cuy1980a,Reference Cuyb) and Hopkins and Rothschild (Reference Hopkins and Rothschild1956). Streblidae, Ischnopsyllidae and representative individuals of Nycteribiidae were cleared in 10% potassium hydroxide (KOH) and mounted in modified Hoyer's medium. Unmounted specimens of nycteribiids were stored in 70% ethanol. Host and distribution records were based on available literature on ectoparasites of bats in the Philippines (Cuy, Reference Cuy1980a,Reference Cuyb, Reference Cuy1981; Alvarez et al., Reference Alvarez, Lit and Alviola2015). Voucher specimens were deposited at the Entomological Collections, UPLB MNH.
Results
From the 11 species of bats that were collected, 83 individuals of ectoparasites, including seven species of nycteribiid flies, five species of streblid flies and one species of ischnopsyllid flea were documented (Table 2). This number includes five new host and eight new island records. Raymondia pagodarum (Diptera: Streblidae) is a new record to Mindoro and the Philippines. These species are given below.
Summary of bat ectoparasite species recorded in the Philippines and Mindoro Island, from previous studies and current study
+Species recorded in Mindoro.
−Species not recorded in Mindoro.
*New species record for the Phillipines.
Ectoparasite accounts
This species was previously recorded on Harpyionycteris whiteheadi (Cuy, Reference Cuy1980b) and Ptenochirus jagori (Alvarez et al., Reference Alvarez, Lit and Alviola2015; present study). It is endemic to the Philippines and previously recorded only from Mindanao (Maa, Reference Maa1968) and Luzon (Alvarez et al., Reference Alvarez, Lit and Alviola2015). The current collection represents a new distribution record for C. garrula.
Specimens examined: On P. jagori, one female (UPLBMNH DIP-1588).
Previously recorded from the pteropodids Pteropus vampyrus, P. hypomelanus, P. speciosus, Acerodon jubatus and Rousettus amplexicaudatus (Cuy, Reference Cuy1980b, Reference Cuy1981), this bat fly species is newly recorded on Pteropus pumilus, a bat species endemic to the Philippines. Cyclopodia horsfieldi is widespread in Thailand, Cambodia and Indonesia. In the Philippines, it is recorded in Luzon, Mindoro, Palawan (Busuanga, Culion, Balabac), Leyte, Panay, Guimaras and Mindanao (Camiguin, Jolo) (Cuy, Reference Cuy1980b).
Specimens examined: On P. pumilus, four males and eight females (UPLBMNH DIP-1589 to 1600).
Eucampsipoda inermis is a parasite of the pteropodids Rousettus amplexicudatus and Eonycteris spelaea. In the Philippines, it is distributed in Luzon, Catanduanes, Mindoro, Palawan (Busuanga, Balabac), Samar, Leyte, Cebu, Negros and Mindanao (Samal, Jolo). It is also widely distributed in Myanmar, Thailand and Indonesia (Cuy, Reference Cuy1980b).
Specimens examined: On R. amplexicaudatus, 13 males and six females. (UPLBMNH DIP-1601 to 1613, 1615 to 1620); on E. spelaea, one male (UPLBMNH DIP-1614).
This endemic species was previously recorded from Luzon, Leyte, Mindoro, Negros, Polillo and Marinduque. Host records include Eonycteris robusta, Hipposideros diadema, R. amplexicaudatus, Miniopterus schreibersii (Cuy, Reference Cuy1980b, Reference Cuy1981) and P. jagori (Alvarez et al., Reference Alvarez, Lit and Alviola2015).
Specimens examined: On R. amplexicaudatus, one male, one female (UPLBMNH DIP-1633, 1634).
Eucampsipoda sundaica is parasitic on R. amplexicaudatus and E. spelaea (Cuy, Reference Cuy1980b). This species is widely distributed in India, Myanmar, Laos, Cambodia, Thailand, Malaysia, Indonesia and the Philippines (Luzon, Mindoro, Palawan, Leyte, Negros and Mindanao) (Cuy, Reference Cuy1980b, Reference Cuy1981).
Specimens examined: On E. spelaea, two females (UPLBMNH DIP-1621, 1622).
This subspecies is recorded on the fruit bats Cynopterus brachyotis, P. jagori, Haplonycteris fischeri, Macroglossus minimus, E. spelaea and the insectivorous bat H. diadema. This endemic subspecies is distributed in Luzon, Leyte, Panay, Guimaras, Negros, Camiguin, Mindanao and recently reported for the first time in Mindoro.
Specimens examined: On C. brachyotis, one male, two females (UPLBMNH DIP-1623, 1624, 2431).
This is another endemic species that is parasitic on the fruit bats P. jagori, C. brachyotis, R. amplexicaudatus, E. robusta and M. minimus. Cuy (Reference Cuy1980b) noted that this species is distributed in Luzon, Mindoro, Leyte, Bohol, Cebu, Negros, Camiguin and Mindanao.
Specimens examined: On P. jagori. two males and one female (UPLBMNH DIP-1625, 1627, 1628); on C. brachyotis, one female (UPLBMNH DIP-1626).
In the synopsis of Cuy (Reference Cuy1980a), Megastrebla parvior is parasitic on the vespertilionids Miniopterus australis and M. schreibersii, the hipposiderid H. diadema and the pteropodids R. amplexicaudatus, E. spelaea and E. robusta. In the current survey, it is newly recorded from the pteropodid M. minimus. This species is also newly reported in Mindoro, adding to its distribution in Luzon, Leyte, Negros, Cebu, Palawan, Balabac, Mindanao and Samal (Cuy, Reference Cuy1980a). It is also found in India, Myanmar, Thailand, Malaysia and Indonesia (Cuy, Reference Cuy1981).
Specimens examined: On M. minimus, one male (UPLBMNH DIP-1630); on R. amplexicaudatus, one male and two females (UPLBMNH DIP-1629, 1631, 1632).
This species is common in the Oriental and Australian regions. In the Philippines, it is distributed in Luzon, Polillo, Tablas, Mindanao and in this study, it is recorded for the first time in Mindoro. In his account on the bat flies of the Philippines, Cuy (Reference Cuy1980a) noted that B. amboinensis is parasitic on M. australis, M. schreibersii, M. tristis, R. amplexicaudatus, E. spelaea, Rhinolophus sp. and Hipposideros coronatus. This study reports its presence in H. diadema.
Specimens examined: On H. diadema, one female (UPLBMNH-DIP-1575); on Rhinolophus arcuatus, four females (UPLBMNH-DIP-1580, 1581, 2437, 2438).
This is an endemic species previously recorded only from the hipposiderid H. diadema and the pteropodid E. robusta. This study reports its presence in R. arcuatus. In addition to its record in Luzon and Mindanao (Cuy, Reference Cuy1980a), its distribution extends to Mindoro.
Specimens examined: On R. arcuatus, one male and two females (UPLBMNH-DIP-2444 to 2446).
The occurrence of this streblid bat fly in the Philippines is reported for the first time, extending its known geographical distribution. In the Oriental region, this species has overlapping distribution with R. pseudopagodarum but extends to tropical South Pacific islands such as the Solomon Islands, Papua (New Guinea) and New Britain (Maa, Reference Maa1962). In this study, it was recorded only from Hipposideros bicolor.
Specimens examined: On H. bicolor, three females (UPLBMNH-DIP-2403 to 2405).
This species is widely distributed in the Southeast Asia region, including Borneo, China, Malaya and the Philippines. In the country, it is recorded from Palawan, Negros, Mindanao, Luzon and currently in Mindoro (additional record). In the Philippines, it is known to parasitize R. arcuatus, R. rufus, R. virgo, Hipposideros galeritus (=H. diadema), Miniopterus schreibersii, M. australis, R. amplexicaudatus and E, spelaea (Cuy, Reference Cuy1980a).
Specimens examined: On R. arcuatus, one male, nine females (UPLBMNH-DIP-2432 to 2436, 2439 to 2443).
This species is similar to T. breviceps but can be distinguished by the form of the clasper and crochet in males, and the large sinus and small number of bristles (≤6) on sternite VII in females. The two species also overlap in their host species.
Thaumapsylla longiforceps is distributed in the Oriental and Australian regions. In its Oriental range, it is reported from Miniopterus tristis (Philippines), R. amplexicaudatus (Java) and C. brachyotis (Borneo) (Hopkins and Rothschild, Reference Hopkins and Rothschild1956). Its distribution extends to New Guinea where it is a parasite of H. diadema (Hopkins and Rothschild, Reference Hopkins and Rothschild1956). This is the first record of this species in Mindoro. Previously, it was collected from Montalban, Rizal Province in Luzon Island (Hopkins and Rothschild, Reference Hopkins and Rothschild1956).
Specimens examined: On R. amplexicaudatus, three males, one female (UPLBMNH-SIP-0001 to 0004).
Discussion
Prior to this survey, there were only seven species of ectoparasites recorded from bats in Mindoro. For the recent collection, we documented an additional seven species, including R. pagodarum, which is a new record to Mindoro and the Philippines. Thus, 14 species of bat ectoparasites are currently known from the island. This also includes four species and one subspecies endemic to the Philippines. This number, however, is probably an underestimate and subsequent collections of other bat species will likely add to the ectoparasite fauna of Mindoro.
The pteropodid fauna of Mindoro island has amongst the most endemic species compared to any other island in the Philippines, with two endemic species, Desmalopex microleucopterus (Esselstyn et al., Reference Esselstyn, Garcia, Saulog and Heaney2008) and Styloctenium mindorensis (Esselstyn, Reference Esselstyn2007). However, we were only able to capture four pteropodid species. Other pteropodids known from the island include A. jubatus, D. microleucopterus, E. robusta, H. fischeri, H. whiteheadi, P. vampyrus and S. mindorensis (Heaney et al., Reference Heaney, Dolar, Balete, Esselstyn, Rickart and Sedlock2010). From these bat species that were not collected in the current study, it is possible to document at least 16 species of bat flies which are not previously reported on the island. Information on the ectoparasites of the recently described species of bats (i.e. D. microleucopterus and S. mindorensis) from Mindoro is non-existent.
During our survey, we were able to capture only five species of insectivorous bats. However, a further 21 species of bats have been recorded in Mindoro. These insect bats are usually cave dwelling and we failed to document any cave within the vicinities of Naujan Lake. More extensive collections are necessary to document more ectoparasite species that could be new host and locality records or new to science. Large samples are also necessary to determine and establish patterns of host–parasite relationships. During our sampling, we used the typical mist nets, which are less efficient in capturing echolocating bats that easily evade these nets. Thus, use of multiple methods to capture host bats is recommended for future studies.
Acknowledgements
We dedicate this study to the memory of Luisito Salandanan Cuy who continues to inspire young wildlife biologists and arthropod systematists in the Philippines, but who unfortunately perished together with six others during a forestry practicum and wildlife fieldwork on Lake Naujan in May 1982. The study was part of the UPLB MNH project ‘Naujan Lake National Park Site Assessment and Profile Updating’ under the leadership of one of the authors, Dr Ireneo L. Lit, Jr. We acknowledge with sincerest thanks the funding provided by the Mindoro Biodiversity Conservation Foundation, Inc. (MBCFI) through the initiative of Executive Director Grace Diamante. MBCFI also arranged collection permits in the area. We thank colleagues from the UPLB Museum of Natural History. We also thank Mr Jeremy Carlo B. Naredo for assisting in specimen preparations. Special thanks to the anonymous reviewer for improving the manuscript.
