Bat-parasitic Cimex species (Hemiptera: Cimicidae) on the Balkan Peninsula, with zoogeographical remarks on Cimex lectularius Linnaeus Author Simov, Nikolay Author Ivanova, Teodora Author Schunger, Isabel text Zootaxa 2006 2006-05-01 1190 59 68 journal article 27031 10.5281/zenodo.2646185 1393a7bd-6860-4916-96f0-593ecbe197f7 1175-5326 2646185 8A403022-6F11-4332-9F50-04A27E886056 Cimex dissimilis (Horváth) Bulgaria : village of Devetaki , Devetashkata cave ( 43° 13 N , 24° 53 E , 250 m a. s. l. ), 19.05.2004 ­ 1 ♀ on a male Nyctalus noctula , mist­netted near the entrance to a large summer roost with about 2000 N. noctula , leg. I. Schunger , C. Dietz ; village of Cherven ( 43° 37 N , 26° 0 1 E , 200 m a. s. l. ), bat­boxes transect near the village (the transect has existed since 2004 and bat­boxes are checked regularly once a month), 0 1.10.2005 4 ♂♂ , 3 ♀♀ and 10 larvae in a bat box with Nyctalus noctula , leg. I. Borisov ; village of Cherven ( 43° 37 N , 26° 0 1 E , 200 m a. s. l. ), bat­boxes transect near the village (the transect has existed since 2004 and bat­boxes are checked regularly once a month), 31.10.2005 1 ♂ , 1 ♀ and 13 larvae in a bat box with Nyctalus noctula , leg. I. Borisov ; village of Cherven ( 43° 37 N , 26° 0 1 E , 200 m a. s. l. ), bat­boxes transect near the village (the transect has existed since 2004 and bat­boxes are checked regularly once a month), 0 4.12.2005 1 ♂ , 2 ♀ and 10 larvae in a bat box with Nyctalus noctula , leg. I. Borisov ; town of Plovdiv ( 42° 0 8 N , 24° 45 E , 160 m a. s. l. ), Gerdzhika Bridge , 0 3.11.2005 1♂ and 1♀ , on 1 male and 1 female individuals of Nyctalus noctulà , captured by hand in the roost with about 900 hibernating bats, leg. E. Tilova. Greece : Thrace , Evros Province , village of Soufli , bridge south of the village ( 41°08 N , 26°17 E ) 23.09.2004 ­ 3 ♂♂ on 3 male individuals of Nyctalus noctulà , captured by hand in a roost with about 40 bats, leg. I. Schunger , C. Dietz.. Discussion The finding of Cimex dissimilis on the Balkan Peninsula is not unexpected. This parasitic species is distributed throughout the nursing territory of its host, Nyctalus noctula ( Péricart 1996 ; Strelkov 1997 ; Kaòuch & Cel’uch 2004 ). The noctule bat is a migrating species, and females give birth to their young in the area of deciduous forests from western Europe to Russia ( Strelkov 1969 ). The southern border of the continuous area of reproduction runs from the northern coast of the Black Sea through the Czech Republic , Germany , and France ( Strelkov 2000 ). Single nursery colonies can be found separated from this main territory in several countries of Central and Southern Europe, occasionally also on the Balkans ( Hanak & Josifov 1959 ; Hanak et al. 2001 ; Dietz, Schunger & von Helversen, own data), but usually the Balkans are inhabited during the summer months by male N. noctula only. These males form colonies of up to several hundred individuals. Females and their offspring migrate in autumn from the areas of reproduction to the south to mate and to hibernate. In winter the sex ratio is about 1: 1 in the Nyctalus colonies. The migratory part of the population can cover considerably long distances of up to 1600 km ( Gebhard & Bogdanowicz 2004 ). The eastern Balkan Peninsula is part of the migratory flyway from Central Europe and European Russia ( Buresch 1941 ; Buresch & Beron 1962 ; Strelkov 1969 ). At the moment we do not know if Cimex dissimilis lives permanently on male N. noctula in their colonies and can form a stable population there, or if they are transferred regularly by the migrating part of the population. The situation is similar in Italy , where C. dissimilis has also been recorded only on mist­netted individuals of N. noctula ( Lanza 1999 ) . At least C. dissimilis seems to be quite rare at one of our study sites. Only one out of 70 N. noctula captured during the summer at the roost entrance carried a single C. dissimilis .. The higher proportion of one observed Cimex per inspected bat at the second study site in Greece occurred already during migrating time, when females had been already present in the area (Schunger, own data) and might have introduced their parasites. Based on the data available at present, Cimex dissimilis could be seen as a vagrant species that does not form a stable population on the local resident bat populations, but arrives occasionally, transferred by migrating bats. The position of Cimex emarginatus nov. sp. in the genus Cimex is unclear (for the main characteristics of species groups in the genus Cimex see Usinger [1966]). The new species is similar in its chromosome formula to Cimex adjunctus Barber and Cimex brevis Usinger & Ueshima from the Cimex pilosellus ­ group ( Ueshima 1966 ). Regarding the shape and hairiness of the paragenital sinus, the new species is similar to the Cimex lectularius ­ group ( Cimex lectularius Linnaeus , Cimex columbarius Jenyns ) and to the Cimex hemipterus ­group ( Cimex hemipterus (Fabricius) . Cimex lectularius and Cimex columbarius differ from Cimex emarginatus nov. sp. by the fewer autosomes (13 autosomal bivalents) and by the longer hind femora (ratio of length/ width of hind femur 3.4­4.1). Cimex hemipterus differs from the new species by the chromosome formula (2n= 28+ X 1 X 2 Y), by the smaller Y chromosome, and by the lower ratio of width to length of the pronotum (1.9­2.3). Cimex adjunctus and Cimex brevis differ from the new species by the shape of paragenital sinus (rounded with bristles), by the smaller Y chromosome, by the longer bristles at edges of pronotum, and by the shorter hind femora (ratio of length/ width of hind femur 2.1­2.8). The species from the Cimex pipistrelli ­ group differ from the new species by the hairiness of the paragenital sinus (cleft and naked) and by the lower value of the ratio of width to length of the pronotum (2.0­2.5). A more detailed study on the bat parasitic true bugs in the regions adjacent to the Balkan peninsula could reveal a larger distribution of Cimex emarginatus nov. sp. On the other hand, this study confirmed the absence of Cimex lectularius parasitizing bats in the Balkan Peninsula. The species was not found despite the survey of several thousand bats and their roosts. C. lectularius is also absent from the Apennine ( Lanza 1999 ) and the Iberian Peninsula ( Zahn & Rupp 2004 ). In recent times the species has been found parasitic on bats only in Central and Northern Europe ( Povolný 1957 ; Usinger & Beaucournu 1967 ; Roer 1969 ; Gottschalk 1970 ; Kock & Aellen 1987 ; Morkel 1999 ; Kulzer 2002 ). In this area the main host, Myotis myotis , roosts in buildings during summer. The hypothesis that C. lectularius changed its host from bats to humans in the Pleistocene at the time when both hosts lived together in caves in the northern Mediterranean ( Horváth 1914 ; Kiritshenko 1951 ; Sailer 1952 ; Povolný 1962 ) cannot explain why bat­parasitizing C. lectularius is absent from the Mediterranean nowadays. We favor the following scenario of an historical host shift of C. lectularius : The species was a parasite primarily linked to bats ( Reuter 1913 ; Horváth 1914 ; Kiritshenko 1951 ; Sailer 1952 ; Povolný 1962 ; Usinger 1966; Usinger & Povolný 1966 ; Péricart 1972 ), especially to Myotis myotis ( Povolný 1957 ; Usinger & Beaucournu 1967 ; Roer 1969 ; Gottschalk 1970 ; Kock & Aellen 1987 ; Morkel 1999 ; Kulzer 2002 ). During the Pleistocene the present­day distribution area of C. lectularius was unsuitable for the parasite and its host because of several ice ages. But M. myotis has been known since the Middle Pleistocene in Western Europe and later spread its range to the East ( Popov 2000 ). Most probably the relation between C. lectularius and humans dates from the late Pleistocene, when humans, bats, and bed bugs inhabited caves together in the Northern Mediterranean and Central Asia. At this period the climate of caves was dry and arid, being favorable for C. lectularius , a species negatively susceptible to high humidity ( Drenski 1928 ; Kemper 1936 ; Omori 1941 ). Later, during the Holocene, the climate of caves in the northern Mediterranean became much more humid. At that time C. lectularius abandoned parasitization on bats still roosting in the now­unfavorable caves in the Balkans ( Horáček 1983 ), and host­shifted to humans living in buildings which offered suitable climatic conditions for the bugs. In Central and Northern Europe C. lectularius persisted as a parasite on Myotis myotis , because the roosts in buildings offer the climatic conditions favorable for the parasite ( Usinger & Povolný 1966 ; Usinger & Beaucournu 1967 ; Usinger & Povolný 1967 ; Morkel 1999 ; Kulzer 2002 ). This scenario might be an adequate explanation for the recent absence of bat­parasitic C. lectularius from the Mediterranean and the existence of bat­parasitic populations of the species in Central Europe. Acknowledgements We thank Dr. N. Spassov and Dr. M. Josifov for useful discussions on Pleistocenå environment and zoogeography of Heteroptera, and A. Gueorguieva, E. Papadatou, T. Pröhl, E. Tilova, I. Borisov, and C. Dietz for their valuable help in capturing the host bats of the parasitic Cimex species presented here. References Benda, P. & Horáček, I. ( 1998 ) . Acta Societatis Zoologicae Bohemicae , 62 , 255–313 . Benda, P. , Ivanova, T. , Horáček, I. , Hanák, V. , Červený, J. , Gaisler, J. , Gueorguieva, A. , Petrov, B. & Vohralík, V. ( 2003 ) . Acta Societatis Zoologicae Bohemicae , 67 , 245–357 . Buresch, I. ( 1941 ) . Revue de l’Academie bulgare des Sciences et des Arts , Sofia , 61 ( 2 ), 51–72 . [in Bulgarian, German summary] Buresch, I. & Beron, P. ( 1962 ) . Bulletin de’l Institut de Zoologie et Musée , 11 , 47–57 . [in Bulgarian, German summary] Decu, V. , Murariu, D. & Gheorghiu, V. ( 2003 ) . Institotul de Speologie "Emil Racoviṭă", Bucureşi , 521 pp. Drenski, P. ( 1928 ) . Arbeiten der Bulgarischen Naturforschenden Gesellschaft , 13 , 63– 96 . [in Bulgarian, German summary] Gebhard, J. & Bogdanowicz, W. ( 2004 ) . In: Krapp F. (Ed.), Handbuch der Säugetiere Europas. Band 4: Fledertiere. Teil II: Chiroptera II . AULA­Verlag, Bonn , pp. 607–694 . Gottschalk, C. ( 1970 ) . Zoologische Abhandlungen Staatliches Museum für Tierkunde in Dresden , 30 ( 11 ), 143–147 . Grozeva, S. & Nokkala, S. ( 2002 ) . Caryologia , 55 , 189–192 . Hanák, V. , Benda, P. , Ruedi, M. , Horáček, I. & Sofianidou, T. ( 2001 ) . Acta Societatis Zoologicae Bohemicae , 65 , 279–346 . Hanak, V. & Josifov, M. ( 1959 ) . Säugetierkundliche Mitteilungen , 7 , 145–151 . Horáček, I. ( 1983 ) . In: Dinev, L (Ed.), Proceedings of European Regional Conference on Speleology, Sofia, vol.1 . Bulgarian Federation of Speleology, Sofia , pp. 163–169 . Horváth, G. ( 1914 ) . IX e Congres International de Zoologie , Monaco , 294–299 . Josifov, M. ( 1963 ) . Bulletin de’l Institut de Zoologie et Musée , 13 , 93–132 . [in Bulgarian, German summary] Josifov, M. ( 1964 ) . Die Fauna Thrakiens , 1 , 207–245 . [in Bulgarian, German summary] Kaňuch, P. & Cel’uch, M. ( 2004 ) . Myotis , 41/ 42 , 125–127 . Kemper, H. ( 1936 ) . Zeitschrift für Kleintierkunde und Pelztierkunde “Kleintier und Pelztier ” , 12 ( 3 ), 1–107 . Kiritshenko, A. N. ( 1951 ) . In: Pavlovskii (Ed.), Keys to the Fauna of the USSR. 42 . Publishing House of Academy of Scienses of the USSR, Moscow, Leningrad , 423 pp. [In Russian]. Kock, D. & Aellen, V. ( 1987 ) . Revue Suisse de Zoologie , 94 , 873–879 . Kulzer, E. ( 2002 ) . Michael in Entringen, Krs. Tübingen. Nyctalus (N.F.) , Berlin , 8 ( 2 ), 141–158 . Lanza, B. ( 1999 ) . Monografie XXX, Museo Regionale di Scienze Naturali, Torino , 318 pp. Morkel, C. ( 1999 ) . Hessische Faunistische Briefe , 18 (2/ 3 ), 38–48 . Omori, N. ( 1941 ) . Journal of the Medical Association of Formosa , 60 , 555–729 . Péricart, J. ( 1972 ) . In: Balachowsky, A. S. (Ed.), Faune de l’Europe et du Bassin méditerranéen 7 . Masson & Cie éditeurs, Paris , 402 pp. Péricart, J. ( 1996 ) . In : Aukema, B. & Rieger, C. (Eds.), Catalogue of the Heteroptera of the Palaearctic Region , Vol. 2 . The Netherlands Entomological Society, Amsterdam , pp. 141–146 . Popov, V. ( 2000 ) . In : Kozłowski, J. K. , Ginter, B. & Laville, H. (Eds.), Temnata Cave, Excavation in Karlukovo Karst Area, Bulgaria. Volume 2 . Jagellonian University, Cracow , pp. 159–240 . Povolný, D. ( 1957 ) . Folia Zoologica , 6 ( 20 ), 57–80 . Povolný, D. ( 1962 ) . Zeitschrift für angewandte Zoologie , 49 , 53–59 . Reuter, O. M. ( 1913 ) . Zeitschrift für wissenschlaftiche Insektenbiologie , 9 , 325– 364 . Roer, H. ( 1969 ) . Bonner zoologische Beiträge , 4 ( 20 ), 355– 359 . Sailer, R. I. ( 1952 ) . Pest Control , 20 ( 10 ), 22–72 . Strelkov, P.P. ( 1969 ) . Acta Zoologica Cracoviensia 16 , 393–439 . Strelkov, P.P. ( 1997 ) . Russian Journal of Zoology , 76 ( 9 ), 1073–1082 . Strelkov P.P. ( 2000 ) . Myotis , 37 , 7–25 . Ueshima, N. ( 1966 ) . In : Usinger R.L. (Ed.), Monograph of Cimicidae (Hemiptera – Heteroptera) . Thomas Say Foundation , pp. 183–237 . Usinger, L. R. ( 1966 ) . Thomas Say Foundation, i–xi , 585 pp. Usinger, L. R. & Beaucournu, J.­C. ( 1967 ) . Annales de Parasitologie , Paris , 42 , 269–271 . Usinger, R.L. & Povolny, D. ( 1966 ) . Acta Musei moraviae , 51 , 237–242 . Vinokurov, N. N. & Kanyukova, E. V. ( 1995 ) . Yakutian Scientific Centre, Yakutsk , 62 pp. [in Russian, English summary]. Zahn, A. & Rupp, D. ( 2004 ) . Journal of Zoology, London , 262 , 383–391 .