Diptera Pupipara from bats of two large eastern Mediterranean islands, Crete and Cyprus
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1 Turkish Journal of Zoology Research Article Turk J Zool (2013) 37: TÜBİTAK doi: /zoo Diptera Pupipara from bats of two large eastern Mediterranean islands, Crete and Cyprus Martin ŠEVČÍK 1, *, Petr BENDA 2,3, Radek Kris LUČAN 3 1 Department of Zoology and Anthropology, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra, SK Nitra, Slovakia 2 Department of Zoology, National Museum, CZ Prague 1, Czech Republic 3 Department of Zoology, Faculty of Science, Charles University, CZ Prague 2, Czech Republic Received: Accepted: Published Online: Printed: Abstract: This paper presents a review of records of bat flies (families Nycteribiidae and Streblidae) from Crete and Cyprus, based on new findings and published data. Seven species representing 4 genera belonging to the family Nycteribiidae and 1 species from the family Streblidae from 5 bat species in Crete are reported, and 7 Nycteribiidae species (4 genera) and 1 Streblidae species from 9 bat species in Cyprus are reported. The bat flies Nycteribia latreillii (Leach, 1817), Basilia mongolensis nudior Hůrka 1972, Penicillidia conspicua Speiser, 1900, P. dufourii Westwood, 1835, and Brachytarsina flavipennis Macquart, 1851 are reported from Crete for the first time, and Phthiridium integrum (Theodor and Moscona, 1954), P. dufourii, and B. flavipennis are reported from Cyprus for the first time. Key words: Nycteribiidae, Streblidae, first records, distribution, hosts 1. Introduction The family Nycteribiidae Samouelle, 1819 comprises the dipterans parasitising on bats of all zoogeographical regions. According to the checklist by Graciolli and Dick (2008), more than 270 species occur in the world. Seventeen species (5 genera) are known from the western Palaearctic (Theodor, 1967; Hůrka and Soós, 1986a), and 14 species (5 genera) of them occur in the Mediterranean area (Hůrka, 1964; Theodor, 1967). No detailed information on Nycteribiidae has been available from Crete, except for several records of 3 species reported by Theodor (1967) and Kock (1974, 1989): Nycteribia pedicularia Latreille, 1805 (collected from Myotis capaccinii (Bonaparte, 1837)), Nycteribia schmidlii Schiner, 1853 (from M. capaccinii and Miniopterus schreibersii (Kuhl, 1817)), and Phthiridium biarticulatum Hermann, 1804 (from Rhinolophus ferrumequinum (Schreber, 1774)). A similar situation holds for the nycteribiid fauna of Cyprus: only scarce data have been available from this island, including records of 5 species, Nycteribia pedicularia (from M. capaccinii), N. schmidlii (from Rhinolophus euryale Blasius, 1853), Phthiridium biarticulatum (from R. euryale), Basilia daganiae Theodor and Moscona, 1954 (from Pipistrellus kuhlii (Kuhl, 1817)), and Penicilidia conspicua Speiser, 1900 (from M. schreibersii) (Bequaert, 1953; Theodor, 1956, 1967; Kock, 1974, 1984, 1989). * Correspondence: [email protected] The family Streblidae Kolenati, 1863 is represented by 4 species of 3 genera in the Mediterranean (Jobling, 1939; Hůrka and Soós, 1986b). Just one species, Brachytarsina flavipennis Macquart, 1851, occurs in Europe (Hůrka, 1972). So far, no record of this species has been available either from Crete or from Cyprus. 2. Materials and methods In October 2005, July and October 2006, and May and June 2008, bats were collected from Crete and Cyprus in the course of research trips (Benda et al., 2007, 2009). Mist nets were installed according to standard procedures (Kunz and Kurta, 1988) in front of water, and bats were also captured in their roosts (caves, mines). Each captured host was placed into a separate cloth bag and labelled. Hosts were inspected for bat flies, ectoparasites living in the fur of the body, which were collected with entomological tweezers and preserved in 75% ethanol. Samples for a species of host were stored in an Eppendorf tube. The age and sexual status (adult male ( ad), adult female ( ad), subadult female ( sad)) of the host is given for most samples, with the exception of the period of October 2010, when only the number and species of host were registered. All bat flies were observed freely under a magnifying glass, and keys were used for the determination and comparison of parasitic species: Theodor and Moscona (1954), Theodor (1967, 1975), and Hůrka (1972). Voucher specimens of 31
2 the parasites are deposited in the collection of the first author (cmš). The taxa are arranged alphabetically. The information for each species appears in the following format: synonyms available from the respective islands; published data; new material examined (number and developmental stage of specimens, locality, date, number of collection, age/number of host). 3. Results and discussion In total, 6 species representing 4 genera belonging to the family Nycteribiidae and 1 species of the family Streblidae were collected from Crete, and 4 species of 2 genera of the family Nycteribiidae and 1 species of Streblidae were collected from Cyprus Family Nycteribiidae (Samouelle 1819) Subfamily Nycteribiinae Samouelle, 1819, sensu Maa Nycteribia (Nycteribia) latreillii (Leach, 1817) Crete. New material examined: 1, 1, Lefkogeia, at Venetian bridge ca. 3 km E of Kato Preveli Monastery, 30 May 2008 (cmš , leg. P. Benda and V. Hanák) from 2 ad Myotis blythii. Remarks: Until Theodor (1954a), the species was reported in Europe under various names, as the proper name was erroneously used for N. kolenati Theodor and Moscona, The distribution of N. latreillii corresponds to the ranges of its primary host species, Myotis myotis (Borkhausen, 1797), M. blythii (Tomes, 1857), and M. punicus Felten, 1977, i.e. almost all of continental Europe (northern limit of 51 N 52 N), the Maghreb, the Middle East, and Central Asia (Hůrka, 1964; Theodor, 1967). In addition, it can also occur on other species of the genus Myotis Kaup, 1829, Miniopterus Bonaparte, 1837, and Rhinolophus Lacépède, 1799, as well as on other cavedwelling bats (see Theodor, 1967). Our findings represent the first evidence of this species from Crete. Although we did not find this bat fly in Cyprus, its occurrence is to be expected due the presence of one of the principal host species, M. blythii (Benda et al., 2007) Nycteribia (Nycteribia) pedicularia Latreille, 1805 Crete. Published records: Kock (1974): Piskokefalo at Sitia (host Myotis capaccinii). Cyprus. Published records: Kock (1974): Kyrenia (host Myotis capaccinii). Remarks: Nycteribia pedicularia has frequently been confused with N. latreillii and/or N. kolenati Theodor and Moscona, N. pedicularia is distributed in south-eastern Europe, and the northern limit of its range probably reaches the Alps and southern Carpathians (Hůrka, 1962). In the broader scale of the western Palaearctic, its distribution range encompasses Turkey, Palestine, Iran, Tunisia, and Algeria (Theodor and Moscona, 1954; Theodor, 1967). However, the record from Cyprus is doubtful, as the occurrence of the host species as well as the record itself is in doubt (see Benda et al., 2007). Host species of this bat fly are cave-dwelling bats of the genera Myotis, Miniopterus, and Rhinolophus (Theodor and Moscona, 1954) Nycteribia (Listropoda) s. schmidlii Schiner, 1853 Crete. Published records: Theodor (1967): Limnea (host Miniopterus schreibersii). - Kock (1974): Canea = Chaniá (host Miniopterus schreibersii), Piskokefalo bei Sitia (host Myotis capaccinii). New material examined: 2, 1, Dramia, Petres river bridge, 6 October 2006 (cmš 3400, leg. P. Benda and V. Hanák) from 1 ad Myotis capaccinii; 5, 9, Argyroupoli, Mouselas river, 3 June 2008 (cmš , leg. P. Benda and V. Hanák) from 2 ad Myotis capaccinii; 3, 3, Omalos Plateau, Tzani cave, 1 October 2006 (cmš , leg. P. Benda and V. Hanák) from collection 13 ad and 2 sad Miniopterus schreibersii. Cyprus. Published records: Theodor (1967): site unspecified (host Rhinolophus euryale). Remarks: The distribution of the western subspecies N. s. schmidlii corresponds to the distributional range of its principal host bat, Miniopterus schreibersii, viz. central and southern Europe, the Middle East, Afghanistan, and North Africa Phthiridium biarticulatum Hermann, 1804 Synonym: Stylidia biarticulata Hermann, 1804: Theodor (1967: 127). Crete. Published records: Theodor (1967): Gonia = Mount Gonias (host Rhinolophus ferrumequinum). - Kock (1989): Rethimnon (host Rhinolophus ferrumequinum). New material examined: 1, Kolymvari, mine above village, 9 October 2006 (cmš 3426, leg. P. Benda and V. Hanák) from 1 ad Rhinolophus ferrumequinum; 2, Omalos Plateau, Tzani cave, 1 October 2006 (cmš , leg. P. Benda and V. Hanák) from 2 ad Rhinolophus ferrumequinum. Cyprus. Published records: Theodor (1967): site undefined (host Rhinolophus euryale). New material examined: 1, Kakopetria, Troodos Forest, abandoned mine 5 km to SW, upper gallery, 13 October 2005 (cmš c07, leg. R.K. Lučan) from Rhinolophus ferrumequinum individual of unknown sex and age; 1, Afendrika, ruins of Panagia Chrysiotissa church and Asomatos church, 17 October 2005 (cmš c02, leg. R.K. Lučan) from 1 ad Rhinolophus ferrumequinum (Schreber, 1774); 3, 6, Kakopetria, Troodos Forest, abandoned mine 5 km to SW, upper gallery, 27 July 2006 (cmš 3335, 3336, leg. P. Benda) from 1 ad and 1 sad Rhinolophus blasii (Peters, 1866). Remarks: This cave-dwelling bat fly lives on representatives of the genus Rhinolophus. Its distribution 32
3 range is circum-mediterranean and reaches Tajikistan and Kyrgyzstan (Hůrka, 1964). While Rhinolophus ferrumequinum is the most frequent host of this bat fly (Hůrka, 1964), other (mostly cave-dwelling) bats, e.g., Miniopterus schreibersii, Myotis myotis and M. blythii, are less-parasitised hosts (Hůrka, 1964) Phthiridium integrum (Theodor and Moscona, 1954) Cyprus. New material examined: 3, Kantara, Kantara castle ruins 3 km to NE, 25 July 2006 (cmš 3328, leg. P. Benda) from 1 ad Eptesicus anatolicus. Remarks: This species was described by Speiser (1901) and redescribed by Karaman (1939) based on a record from Egypt. Findings are known from host species of the genera Taphozous Geoffroy, 1818, Rhinolophus and Hipposideros Gray, 1831 from the Middle East: Egypt, Palestine, Jordan, Saudi Arabia, and Yemen (Sanborn and Hoogstraal, 1953; Theodor and Moscona, 1954; Theodor, 1976; Kock and Nader, 1979; Amr and Qumsiyeh, 1993). This species is reported here for the first time from Cyprus and from a new host, Eptesicus anatolicus Felten, Basilia (Basilia) daganiae Theodor and Moscona, 1954 Cyprus. Published records: Bequaert (1953): Limassol (host Pipistrellus kuhlii). - Theodor (1956): Limassol, (host Pipistrellus kuhlii), site undefined, leg. Lilford (without host). - Theodor (1967): site undefined, leg. Lilford (host Pipistrellus kuhlii). - Kock (1974): Larnaka (host Pipistrellus kuhlii). Remarks: The distribution range of this species from the bathybothyra group covers the whole eastern Mediterranean: Cyprus, Turkey, Syria, Jordan, Egypt, Lebanon, and Palestine (Theodor and Moscona, 1954; Lewis and Harrison, 1962; Hůrka and Soós, 1986a; Benda et al., 2010). Its occurrence outside the eastern Mediterranean region is not excluded, considering the much broader distribution of its main host Pipistrellus kuhlii. B. daganiae has also been recorded from other species of the genus Pipistrellus: P. pipistrellus (Schreber, 1774) from Jordan (Benda et al., 2010) Basilia (Basilia) mongolensis nudior Hůrka, 1972 Crete. New material examined: 2, Meskla, above creek, 5 October 2006 (cmš 3393, leg. P. Benda and V. Hanák) from 1 ad Myotis aurascens; 1, 1, Katholiko monastery, Agiou Ioanni cave, 27 May 2008 (cmš 3958, leg. P. Benda) from 1 ad Myotis aurascens. Remarks: This subspecies from the bathybothyra group was described by Hůrka (1972) from the host Plecotus austriacus Fischer, The full expansion of this subspecies is unknown, and we expect it to be in the same area distribution as the host Myotis nattereri (Kuhl, 1817). Its occurrence on other arboreal host species is not excluded, but it occurs mostly in the mystacinus group, viz. M. alcathoe von Helversen and Heller, 2001 (Heddergott, 2009), and in our records from M. aurascens Kusjakin, Previous records are from Croatia, Greece (Hůrka, 1972), Bulgaria (Hůrka, 1984), Austria (Kock, 1984), Turkey (Aktaş and Hasbenli, 1994; Hasbenli, 1997), and Germany (Heddergott, 2009) Penicillidia (Neopenicillidia) conspicua Speiser, 1901 Crete. New material examined: 3, 3, Omalos Plateau, Tzani cave, 1 October 2006 (cmš , leg. P. Benda and V. Hanák) from collection 13 ad and 2 sad Miniopterus schreibersii; 2, Milatos, Milatou cave, 7 October 2006 (cmš , leg. P. Benda and V. Hanák) from collection 1 ad and 3 sad Miniopterus schreibersii. Cyprus. Published records: Kock (1989): Emba, Paphos Distr. (host Miniopterus schreibersii). New material examined: 1, 1, Neo Horio, Smigies Trail, ca. 3 km to NW, abandoned chromite mine system Magnesia Mine, 12 October 2005 (cmš c03, c04, leg. R.K. Lučan) from 2 Miniopterus schreibersii individuals of unknown sex and age. Remarks: Penicillidia conspicua is a species bound to its principal host, Miniopterus schreibersii, and its distribution range corresponds to the occurrence of this bat (Hůrka, 1964). Within this range, it has frequently been found also on Myotis myotis and other cave-dwelling bat species (Hůrka, 1964). This parasite species is reported from Crete for the first time here Penicillidia (Penicillidia) dufourii Westwood, 1835 Crete. New material examined: 2, 3, Lefkogeia, at Venetian bridge ca. 3 km E of Kato Preveli Monastery, 30 May 2008 (cmš , leg. P. Benda and V. Hanák) from 2 ad Myotis blythii; 1, 1, Dramia, Petres river bridge, 6 October 2006 (cmš 3400, leg. P. Benda and V. Hanák) from 1 ad Myotis capaccinii; 2, 2, Argyroupoli, Mouselas river, 3 June 2008 (cmš , leg. P. Benda and V. Hanák) from 2 ad Myotis capaccinii. Cyprus. New material examined: 2, Kakopetria, Troodos Forest, abandoned mine 4 km to SW, lower gallery, 15 October 2005 (cmš c05, leg. R.K. Lučan) from 1 ad Myotis blythii; 1, Kakopetria, Troodos Forest, abandoned mine 5 km to SW, upper gallery, 13 October 2005 (cmš c06, leg. R.K. Lučan) from Myotis nattereri individual of unknown sex and age. Remarks: The subspecies P. d. dufourii is distributed over continental Europe, North Africa, and south-western Asia to the western Himalayas and eastern Kazakhstan. Myotis myotis and M. blythii are the main hosts of this species, but it can also be found on Miniopterus schreibersii, though much more rarely. This parasite species is recorded here for the first time from Crete and Cyprus. 33
4 3.2. Family Streblidae Kolenati, Subfamily Brachytarsininae (Speiser, 1900) Brachytarsina (Brachytarsina) flavipennis Macquart, 1851 Crete. New material examined: 1, Patsos, Agiou Antoniou cave, 3 October 2006 (cmš 3388, leg. P. Benda and V. Hanák) from 1 sad Rhinolophus ferrumequinum; 2, Katholiko monastery, Agiou Ioanni cave, 27 May 2008 (cmš 3958, leg. P. Benda) from 1 ad Myotis aurascens. Cyprus. New material examined: 1, Kakopetria, Troodos Forest, abandoned mine 5 km to SW, upper gallery, 13 October 2005 (cmš 08, leg. R.K. Lučan) from Rhinolophus ferrumequinum individual of unknown sex and age; 1, 2, Kakopetria, Troodos Forest, abandoned mine 5 km to SW, upper gallery, 27 July 2006 (cmš 3336, leg. P. Benda) from 1 sad Rhinolophus blasii. Remarks: B. flavipennis is the only streblid species occurring in the Mediterranean portion of the Palaearctic. This species has a circum-mediterranean distribution range, and in Europe it reaches the latitude of 40 N 43 N, roughly corresponding to the areas of mean January temperatures of 8 to 10 C (Jobling, 1951; Hůrka, 1972). Jobling (1934, 1939) indicated the occurrence of this species in Cyprus and Theodor s record (1954b) is uncertain, since a direct finding has not been reported. This bat fly is recorded here from both large islands for the first time. In conclusion, the combination of our new data with previously published information has resulted in an increase in the total number of species of the Nycteribiidae family on Crete from 3 to 7 species, and from 5 to 7 species on Cyprus. In addition to the above discussion, we may expect other species from this family (genera Nycteribia Latreille, 1796, Basilia Miranda-Ribeiro, 1903, and Eucampsipoda Kolenati, 1857) on the individual islands. Nycteribia (Acrocholidia) vexata Westwood, 1835 is a species with a relation to the extension of the principal hosts Myotis myotis and M. blythii (as N. latreilii), whereas the second host was confirmed on the island of Crete (Benda et al., 2008). The principal host of Basilia nana Theodor, 1954, in Middle Eastern countries is M. nattereri (Turkey - Aktaş and Hasbenli, 1994; Hasbenli, 1997; Jordan - Amr and Qumsiyeh, 1993; Benda et al., 2010), and on this basis we can expect this parasitic species to confirm this host from Cyprus (Benda et al., 2007). In addition, on the same island there probably occurs the parasitic species of the host Rousettus aegyptiacus (Geoffroy, 1810), viz. Eucampsipoda aegyptia (Macquart, 1851). The occurrence of this species on island has already been considered by Theodor (1952, 1954a, 1955; see also Kock and Nader, 1979). This host species has been confirmed on Cyprus by several authors (summary in Benda et al., 2011). The fauna of Streblidae is represented by a single species, which was confirmed for the first time on both islands. Acknowledgements This research was supported by grants from the Czech Science Foundation (#206/09/0888), the Ministry of Culture of the Czech Republic (#DKRVO ), and the University Grant Agency of the Constantine of Philosopher University in Nitra, Slovakia (VII/36/2011). Appendix Appendix I. Gazetteer. Only the originally recorded sites are mentioned. Crete. Prefecture of Chania: Argyroupoli [Αργυρούπολη], Mouselas river, old building, N, E, 105 m a. s. l.; - Katholiko Monastery [Μονή Καθολικού], Agiou Ioanni cave, N, E, 80 m a. s. l.; - Kolymvari [Κολυμβάρι], mine, N, E, 44 m a. s. l.; - Meskla [Μεσκλά], creek, N, E, 206 m a. s. l.; - Omalos Plateau [Οροπέδιο Ομαλού], Tzani cave, N, E, 1025 m a. s. l.; Prefecture of Rethymno: Dramia [Δράμια], Petre river bridge, N, E, 2 m a. s. l. - Lefkogeia [Λευκόγεια], Venetian bridge ca. 3 km E of Kato Preveli Monastery, N, E, 45 m a. s. l.; - Patsos [Πατσός], Agiou Antoniou cave, N, E, 200 m a. s. l.; Prefecture of Lasithi: Milatos [Μίλατος], Milatou cave, N, E, 129 m a. s. l. Cyprus. Northern Cyprus: Afendrika (= Panagia Afentrika [Παναγια Αφεντρικα]), ruins, İskele District, N, E, ca. 25 m a. s. l.; - Kantara (= Kantara [Κανταρα]), Kantara castle ruins 3 km to NE, İskele District, N, E, ca. 625 m a. s. l.; - Southern Cyprus: Kakopetria [Κακοπετρια], Troodos Forest, mine 5 km to SW (upper gallery), Lefkosia District, N, E, ca m a. s. l.; - Kakopetria [Κακοπετρια], Troodos Forest, mine 4 km to SW (lower gallery), Lefkosia District, N, E, ca m a. s. l.; - Neo Horio [Νεο Χωριο], Smigies Trail ca. 3 km to NW, abandoned chromite mine system Magnesia Mine, Akamas Peninsula, Pafos District, N, E, ca. 305 m a. s. l. 34
5 Appendix II. Checklist of Nycteribiidae and Streblidae with their hosts from the islands of Crete and Cyprus. Checklist of 7 species, with 4 genera of bat flies Nycteribiidae and 1 species of Streblidae known from Crete and the same number of species and genera from both parasitic families documented from Cyprus, based on both literature data and new records obtained during recent field studies. The first record of the parasite (*) and the first record from the host (**) of the respective island are indicated. Country / Family / Subfamily / Genus / Species Species of host Country: CRETE Family: NYCTERIBIIDAE Samouelle, 1819 Subfamily: Nycteribiinae Samouelle, 1819 Genus: Nycteribia Latreille, 1796 Nycteribia latreilii (Leach, 1817)* Myotis blythii (Tomes, 1857)** Nycteribia pedicularia Latreille, 1805 Myotis capaccinii (Bonaparte, 1837) Nycteribia schmidlii schmidlii Schiner, 1853 Myotis capaccinii (Bonaparte, 1837) Miniopterus schreibersii (Kuhl, 1817) Genus: Phthiridium Hermann, 1804 Phthiridium biarticulatum Hermann, 1804 Rhinolophus ferrumequinum (Schreber, 1774) Genus: Basilia Miranda-Ribeiro, 1903 Basilia mongolensis nudior Hůrka, 1972* Myotis aurascens Kusjakin, 1935** Genus: Penicillidia Kolenati, 1863 Penicillidia conspicua Speiser, 1901* Miniopterus schreibersii (Kuhl, 1817)** Penicillidia dufourii Westwood, 1835* Myotis blythii (Tomes, 1857)** Myotis capaccinii (Bonaparte, 1837)** Family: STREBLIDAE Kolenati, 1683 Subfamily: Brachytarsininae (Speiser, 1900) Genus: Brachytarsina Macquart, 1851 Brachytarsina flavipennis Macquart, 1851* Rhinolophus ferrumequinum (Schreber, 1774)** Myotis aurascens Kusjakin, 1935** Country: CYPRUS Family: NYCTERIBIIDAE Samouelle, 1819 Subfamily: Nycteribiinae Samouelle, 1819 Genus: Nycteribia Latreille, 1796 Nycteribia pedicularia Latreille, 1805 Myotis capaccinii (Bonaparte, 1837) Nycteribia schmidlii schmidlii Schiner, 1853 Rhinolophus euryale Blasius, 1853 Genus: Phthiridium Hermann, 1804 Phthiridium biarticulatum Hermann, 1804 Rhinolophus blasii Peters, 1867** Rhinolophus euryale Blasius, 1853 Rhinolophus ferrumequinum (Schreber, 1774)** Phthiridium integrum (Theodor and Moscona, 1954)* Eptesicus anatolicus Felten, 1971** Genus: Basilia Miranda-Ribeiro, 1903 Basilia daganiae Theodor and Moscona, 1954 Pipistrellus kuhlii (Kuhl, 1817) Genus: Penicillidia Kolenati, 1863 Penicillidia conspicua Speiser, 1901 Miniopterus schreibersii (Kuhl, 1817) Penicillidia dufourii Westwood, 1835* Myotis blythii (Tomes, 1857)** Myotis nattereri (Kuhl, 1817)** Family: STREBLIDAE Kolenati, 1683 Subfamily: Brachytarsininae (Speiser, 1900) Genus: Brachytarsina Macquart, 1851 Brachytarsina flavipennis Macquart, 1851* Rhinolophus blasii Peters, 1867** Rhinolophus ferrumequinum (Schreber, 1774)** 35
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