ISSN 0973-1555(Print) ISSN 2348-7372(Online) HALTERES, Volume 8, 25-29, 2017  ACE KEVIN S. AMARGA AND SHERYL A. YAP doi: 10.5281/zenodo.580473

Search for the blind vampire: First record of Eoctenes Kirkaldy in Southern Luzon, (: ), with key to the , ectoparasitic on bats in the Philippines

*Ace Kevin S. Amarga¹ and Sheryl A. Yap¹,²

¹Institute of Weed Science, Entomology, and Plant Pathology, College of Agriculture and Food Science, University of the Philippines Los Baños, Laguna, Philippines. ² Museum of Natural History, University of the Philippines Los Baños, Laguna, Philippines.

(Email: [email protected])

Abstract

Polyctenidae Westwood, also known as bat bugs, is a haematophagous group of hemipterans exclusively ectoparasitic on bats and is closely related to Latreille. These bugs are dorsoventrally flattened with conspicuous ctenidia, apterous, anophthalmus, possess well-developed legs, and reproduce via pseudoplacental viviparity. They are rare compared to other taxa ectoparasitic on bats as evinced by a relatively small number of museum collections and described taxa. Worldwide, it is represented by 2 subfamilies, 5 genera, and 32 species. In the Philippines, it is only represented by two species from the Eoctenes Kirkaldy: E. spasmae (Waterhouse) and E. intermedius (Speiser). The first Philippine record for the genus was reported in 1961 from Northern Luzon. This paper presents the first record of Eoctenes in Southern Luzon, with key to the Cimicoidea ectoparasitic on bats in the Philippines.

Keywords: Cimicoidea, Eoctenes, new record, Polyctenidae, Southern Luzon.

Received: 14 February 2017; Revised: 1 May 2017; Online: 10 May 2017.

Introduction A fraction of species from Cimicoidea bugs comprising of subfamilies Polycteninae (Hemiptera: ) are known to be Maa which is endemic to the Old World, and sanguinivorous in nature (Ryckman et al., 1981; Hesperocteninae Maa which is confined in the Maa, 1961, 1964). These parasitic species New World (Maa, 1964). The former is further belong to the families Cimicidae Latreille and subdivided to 4 genera: Adroctenes Jordan, Polyctenidae Westwood which are known to Eoctenes Kirkaldy, Hypoctenes Jordan, and occur in both the Old and New World. All Polyctenes Giglioli whereas the latter is only species belonging to Cimicidae are known to as represented by the Hesperoctenes Kirkaldy obligatory ectoparasites on various avian (Boyd, (Ryckman and Casdin, 1977). Polyctenid bugs 1951; Loye and Regan, 1991) and mammalian tend to prefer microchiropterans as host than taxa (Balvin, 2008) ranging from bats (Wilson megachiropterans (Pteropodidae) (Marshall, and Galloway, 2002; Reeves et al., 2005; Balvín 1982). Currently, there are 32 species that are et al. 2014) to humans (Booth et al., 2012). known worldwide (Ryckman and Sjogren, However, members of the family Polyctenidae 1980). tend to display a narrow host specificity. They As compared to other ectoparasitic are known to be only associated with bats on bats, polyctenid bugs can be (Mammalia: Chiroptera) (Ferris and Usinger, considered rare. This claim of rarity can be 1939). supported by relatively small number of Polyctenidae is a small group of bat museum collections and described taxa. The last

25

Ace Kevin S. Amarga and Sheryl A. Yap described species of Polyctenidae was from the row of curved bristles …. Eoctenes spasmae Aldabra group of islands in Seychelles (Maa, (Waterhouse) 1970). In the Philippines, the first recorded polyctenid bug is a single female specimen of Genus Eoctenes Kirkaldy, 1906 Eoctenes spasmae (Waterhouse) from Eoctenes Kirkaldy, 1906: 375. Megaderma spasma (Linnaeus) in Bucay, Abra Type species: Polyctenes spasmae Waterhouse, Province, Northern Luzon (Maa, 1961). Herein, 1879: 312. we present the first record of the genus Eoctenes Kirkaldy in Bicol Peninsula, Southern Luzon Eoctenes spasmae (Waterhouse, 1879) along with the key to the Cimicoidea Figure 1-2 ectoparasitic on bats in the Philippines. Polyctenes spasmae Waterhouse, 1879: 312. Eoctenes spasmae Kirkaldy, 1906: 375. Materials and Methods Bats were collected using a mobile mist Diagnosis: Eoctenes spasmae is closely similar netting (3 x 2.5 m) inside the cave. Fine- tipped to E. sinae Maa by virtue of the following sets of forceps were used to carefully obtain the taxonomic characters: denticles on anterior polyctenid bugs on the pelage of the bat host. ctenidium on antennal segment I rather regularly Collected polyctenid specimens were arranged; genal comb reaching the posterolateral temporarily placed in the Eppendorf vial angle of head; rostrum 4 segmented; posterior containing 90% ethanol prior to identification. margin of hypostoma bearing long and strong Specimens were cleared using 10% potassium setae; mesonotum shorter than wide but hydroxide (KOH) for 24 hours and mounted on subequal in length with reference to pronotum; slide using Canada balsam. Specimens were intercoxal process of prosternum triangular, examined using Leica DM 4000M versatile subacute; posterior margins of abdominal tergite upright microscope and was photographed using VII- VIII bearing complete row of long setae. Canon D5500. Specimens were identified using However, E. spasmae differs from the latter by available keys from published literature. having a longer labrum, antennal segment III Voucher material will be deposited in Crop and IV subequal in length, submedian line of Protection Cluster Insect Laboratory. hypostomal region bearing fine setae, antero- interior margin of coxa I bearing 4 stout abd 2-3 Key to the Cimicoidea ectoparasitic on bats in fine setae, legs II and III long and narrow, and the Philippines abdominal sternites bearing numerous setae 1. Eyes present; antennae longer than (Maa, 1961, 1964). pronotum; thoracic ctenidia absent………..2 - Eyes absent; antennae shorter than Description: Head capsule anteriorly rounded; pronotum; thoracic ctenidia present…….... 3 posterolateral angle of the head capsule acute 2. Tibiae I-III with apical tufts; hemelytral pad slightly reaching the anterolateral angle of rounded at all aspect; parameres bent at apex pronotum; antennae short; anterior ctenidium of ……………….……Cacodmus sumatrensis antennal segment I evenly arranged in an arcuate Ferris & Usinger line; dorsal comb on antennal segment II absent; - Tibia III without apical tufts; hemelytral pad genal comb extending to the posterior angle of rounded except for straight inner margin; the head capsule; lateroventral margin of labrum parameres evenly bent and tapering…... bearing 4 setigerous tubercles; rostrum 4 ……………...Loxaspis seminitens Horvath segmented; submedian line of hypostoma 3. Apical membranous lobe of tibia I bearing few fine setae; posterior of hypostomal subcylindrical; abdominal tergite VII-VIII region bearing 15 setae arranged in 2-3 rows; bearing no complete bristle rows …...…...… pronotum subquadrate, as long as wide; …………....Eoctenes intermedius (Speiser) denticles on pronotum shorter than denticles on - Apical membranous lobe of tibia I conical; mesonotum; mesonotum shorter than wide; abdominal tergite VII-VIII bearing complete comb on mesonotal lobe pronounced; mesonotal denticles shorter than occipital denticles;

26

First record of Eoctenes Kirkaldy in Southern Luzon, with key to the Cimicoidea, ectoparasitic on bats

Figure 1. Habitus in dorsal profile of female (A) and male (B) Eoctenes spasmae (Waterhouse). Scale= 200x.

Figure 2. Head of E. spasmae (Waterhouse). Scale= 200x.

27

Ace Kevin S. Amarga and Sheryl A. Yap metanotum pronounced; legs subequal, leg I Rothschild (the other two are L. malayensis shorter than legs II and III; intercoxal process of Usinger from Malaysia, and L. spinosa Usinger sternum subacute; apical membranous lobe of from Borneo) occurring in the Indo-Malayan tibia I conical; peg-like setae on tarsi II and III ecoregion (Ford, 1979; Ryckman et al., 1981), absent; abdominal tergite VII and VIII bearing only L. seminitens was documented in the complete row of long, curved bristles; lateral Philippines. The first specimen of L. seminitens bristles on abdomen conspicuous; abdominal in the Philippines was collected in Chaerephon sternite bearing numerous setae. plicatus (Buchanan) from Rizal, Luzon Island (Zipagan, 1990). Material examined: PHILIPPINES: LUZON: The expanse of the distribution of genus 5♂, 7♀, Albay, Batan Island, Brgy. Lagundi, 21- Eoctenes encompasses five ecozone: Palearctic, vi-2014, ex. Megaderma spasma (Linnaeus), A. Indo-Malaya, Afrotropics, Australasia, and K. S. Amarga leg. Oceania. Among its seven species, only two are found in the Philippines: E. spasmae and E. Distribution: India, Indonesia (Borneo, Java, intermedius. The former is widespread in Karimata Islands, Sumatra), Malaysia, Southeast Asia and can be considered as Indo- Philippines (Luzon: Abra; Bicol Peninsula, new Malayan endemic whereas the latter has a wider record), Sri Lanka, Thailand. distribution range (found in Indo-Malaya, Afrotropics, and Australasia). Furthermore, the Remarks: Maa (1961) noted a variability on the first record of E. intermedius in Philippines was length of occipital, pronotal, and mesonotal from a single specimen collected from denticles. Moreover, E. spasmae is known to be Montalban, Rizal in 1961 (Maa, 1964). distributed in the Indo-Malayan ecoregion The true breeding host of E. spasmae is particularly in Southeast Asia. Such geographic M. spasma (Chiroptera: Megadermatidae), distribution coincides with the distribution of its however, certain cases of accidental occurrences true host Megaderma spasma. can be observed as in the case of its presence on Megaderma lyra Geoffroy, Nycteris javanica Discussion Geoffroy, and Cynopterus sphinx (Vahl) Currently, there are four species under (Speiser, 1909; Maa, 1961, 1964). On the other Cimicoidea known to be associated with hand, the true host of E. intermedius are Chiroptera in the Philippines: Cacodmus Taphozous species (Maa, 1964). Its sumatrensis Ferris & Usinger, Eoctenes documentation on Rhinolophus and Rousettus intermedius (Speiser), Eoctenes spasmae needs further confirmation if it is accidental (Waterhouse), and Loxaspis seminitens Horvath. occurrence or cross contamination (Maa, 1961). The bat bugs, C. sumatrensis and L. seminitens, belongs to the subfamily Acknowledgement Cacodminae, a group known to occur in the Old The authors are grateful to DOST- World particularly in Indo- Malayan and ASTHRDP- NSC for the financial support; to Afrotropical ecozone (Coetzee and Segerman, the officials of Brgy. Lagundi and MacIan 1992; Kock et al., 1998). C. sumatrensis was Bechayda, for the accommodation and aid in the first described in 1957 from a Galeopithecus fieldwork; and to Dr. Jessamyn Adorada, for the (now Galeopterus Thomas), a genus of flying use of Leica DM 4000M versatile upright lemur in the island of Sumatra. Kock and Aellen microscope. (1987) stated that bats are the true host for this species and its occurrence on flying lemur is References erroneous. In the Philippines, this species was Balvín, O. 2008. Revision of the West recorded on Miniopterus sp. (Zipagan, 1990). Palaearctic species. Preliminary Furthermore, C. sumatrensis is recorded from report. Bulletin of Insectology 61(1): 129- Indonesia (Java, Sumatra), Malaysia, and 130. Philippines (Laguna) (Ford, 1979; Ryckman et Balvín, O., Bartonička, T., Simov, N., Paunović, al., 1981; Zipagan, 1990). Of the three Loxaspis M. and Vilímová, J. 2014. Distribution and

28

First record of Eoctenes Kirkaldy in Southern Luzon, with key to the Cimicoidea, ectoparasitic on bats

host relations of species of the genus Cimex Maa, T.C. 1961. Records and descriptions of on bats in Europe. Folia Zoologica 63(4): Polyctenidae (Hemiptera). Pacific Insects 281-289. 3(1): 1-10. Booth, W., Saenz, V.L., Santangelo, R.G., Maa, T.C. 1964. A review of the Old World Wang, C., Schal, C. and Vargo, E.L. 2012. Polyctenidae. Pacific Insects 6(3): 494-516. Molecular markers reveal infestation Maa, T.C. 1970. A new Hypoctenes from the dynamics of the bed bug (Hemiptera: Aldabra Atoll with notes on other species Cimicidae) within apartment buildings. and a key to adults and nymphs of the genus Journal of Medical Entomology 49(3): 535- (Hemiptera: Polyctenidae). Journal of 546. Medical Entomology 7(6): 736-744. Boyd, E.M. 1951. The external parasites of Marshall, A.G. 1982. The ecology of the bat birds: a review. The Wilson Bulletin 63(4): ectoparasite Eoctenes spasmae (Hemiptera: 363-369. Polyctenidae) in Malaya. Biotropica 1491): Coetzee, M. and Segerman, J. 1992. The 50-55. description of a new genus and species of Reeves, W.K., Loftis, A.D., Gore, J.A. and cimicid bug from South Africa (: Dasch, G.A. 2005. Molecular evidence for Cimicidae: Cacodminae). Tropical Zoology novel Bartonella species in Trichobius 5: 229-235. major (Diptera: Streblidae) and Cimex Ferris, G.F. and Usinger, R.L. 1939. The family adjunctus (Hemiptera: Cimicidae) from two Polyctenidae (Hemiptera: Heteroptera). southeastern bat caves, U.S.A. Journal of Microentomology 4: 1-50. vector Ecology 30(2): 339- 341. Ferris, G.F. and Usinger, R.L. 1957. Notes on Ryckman, R.E. and Casdin, M.A. 1977. The and descriptions of Cimicidae (Hemiptera). Polyctenidae of the World, a checklist with Microentomology 22(1): 1-37. Bibliography. California Vector Views Ford, L. 1979. The phylogeny and biogeography 24(7-8): 25-31. of the Cimicoidea (Insecta: Hemiptera). Ryckman, R.E. and Sjogren, R.D. 1980. A University of Connecticut, M.S. thesis 96 catalogue of the Polyctenidae. Bulletin of pp. the Society of Vector Ecologists 5: 1-22. Kirkaldy, G.W. 1906. Notes on the classification Ryckman, R.E., Bentley, D.G. and Archbold, and nomenclature of the hemipterous E.F. 1981. The Cimicidae of the Americas Superfamily Miroidea. Canadian and oceanic islands, a checklist and Entomologist 38(11): 369-376. bibliography. Bulletin of the Society of Kock, D. and Aellen, V. 1987. Cimicidae Vector Ecologists 6: 93-142. parasites de Chiroptera du Muséum de Speiser, P. 1909. The hemipterous family Genève (Insecta: Hemiptera). Revue Suisse Polyctenidae. Indian Museum Records de Zoologi 94(4): 873- 879. (Calcutta) 3: 271- 274. Kock, D., Happold, D.C.D. and Happold, M. Wilson, N.A. and Galloway, T.D. 2002. The 1998. Cimicidae and Polyctenidae from occurrence of the bat bug, Cimex pilosellus Malawian Chiroptera. Seckenbergiana (Horvárth) (Hemiptera: Cimicidae), in biologica 77(2): 235-239. Manitoba, Canada. Proceedings of the Loye, J. and Regan, T.W. 1991. The cliff Entomological Society of Manitoba 58: 5-7. swallow bug Oeciacus vicarious Zipagan, M. 1990. Insect ectoparasites of (Hemiptera: Cimicidae) in Florida: vertebrates in the Philippines. University of ectoparasite implications for hole- nesting the Philippines Los Baños, M.S.Thesis 240 birds. Medical and Veterinary Entomology pp. 5(4): 511-513.

29