Diptera: Culicidae: Aedini) Into New Geographic Areas

European Mosquito Bulletin, 27 (2009), 10-17. Journal of the European Mosquito Control Association ISSN 1460-6127; w.w.w.e-m-b.org First published online 1 October 2009

Recent introductions of aedine species (Diptera: Culicidae: Aedini) into new geographic areas

John F. Reinert

Center for Medical, Agricultural and Veterinary Entomology (CMAVE), United States Department of Agriculture, Agricultural Research Service, 1600/1700 S.W. 23rd Drive, Gainesville, FL 32608-1067, USA, Email: [email protected].

Abstract

Information on introductions to new geographic areas of species in the aedine generic-level taxa Aedimorphus, Finlaya, Georgecraigius, Halaedes, Howardina, Hulecoeteomyia, Rampamyia, Stegomyia, Tanakaius and Verrallina is provided.

Key words: Aedimorphus, Finlaya, Georgecraigius atropalpus, Halaedes australis, Howardina bahamensis, Hulecoeteomyia japonica japonica, Rampamyia notoscripta, Stegomyia aegypti, Stegomyia albopicta, Tanakaius togoi, Verrallina

Introduction World. Dyar (1928), however, notes that there are no nearly related species in As indicated in the series of papers on the American continent, but many such the phylogeny and classification of in the Old World, especially in Africa, mosquitoes in tribe Aedini (Reinert et and he considered that it was probably al., 2004, 2006, 2008), some aedine the African continent from which the species have been introduced into new species originated”. Christophers also geographical areas in recent times. noted that “The species is almost the Species of Aedini found outside of their only, if not the only, mosquito that, with natural ranges are listed below with their human agency, is spread around the literature citations. whole globe. But in spite of this wide zonal diffusion its distribution is very Introductions of Aedine Species to strictly limited by latitude and as far as New Areas present records go it very rarely occurs beyond latitudes of 45o N. and 35o S.” Stegomyia aegypti (Linnaeus) represents Dyar (1928) stated “In the early days of the oldest species of Aedini with navigation, with long voyages and water recorded information on introductions to conserved in open wooden receptacles, new geographic areas. Christophers the species readily bred on board ship, (1960) in his book on this species and was carried wherever the vessel reported “It has been suggested that the went”. Dyar also suggested that the original home of A. aegypti was the New species was brought to America in the

early days, perhaps by Columbus number of areas such that the species is himself. Mattingly (1957) tended to now apparently absent around much of favor the southern Palaearctic Region the Mediterranean basin and has become over Africa south of the Sahara as the scarce or localized in the southern possible sites of origin of St. aegypti. United States of America (USA) (see Belkin (1962), however, reported that O’Meara et al., 1993) partly due to this species is undoubtedly a native of competitive displacement by the more the Ethiopian Region (currently known recently invasive St. albopicta. as the Afrotropical Region) where the majority of the other members of the Stegomyia albopicta (Skuse), a species group are found. He also indicated that of probable Asian origin, has been “The dispersal of aegypti may very well introduced into many areas of the world have been started by the Portuguese in by the used tire trade, as summarized by their circuitous route to the Indies, which Mitchell (1995) and Reiter (1998). included stops in West Africa and Ventrillon (1904) first reported this eastern Brazil before rounding the Cape species in Madagascar but the wider of Good Hope. Belkin et al. (1970) current distribution in this country is stated “The ubiquitous and universally provided by Fontenille & Rodhain known aegypti is an African species now (1989). Examples of introductions of widely distributed throughout the world this species during the recent past have within the 20o C isotherms, usually in been reported from the USA (e.g., close association with human Sprenger & Wuithiranyagool, 1986; settlements”. Powell et al. (1980) O’Meara et al., 1993; Reiter, 1998; reported on a multivariate discriminant Madon et al., 2002, 2003), Brazil analysis that was based on sequences of (Forattini, 1986), Albania (Adhami & St. aegypti from 34 populations collected Murati, 1987; Adhami & Reiter, 1998), in Africa, Asia, the Caribbean, North Italy (Sabatini et al., 1990; Dalla Pozza America and South America. Their & Majori, 1992), Fiji Islands (Laille et results indicated that these populations al., 1990; Mitchell, 1995), Australia were sufficiently genetically (Kay et al., 1990; Ritchie et al., 2006), differentiated to allow a strong inference South Africa (Hunt et al., 1990; Cornell of the geographical origin of a & Hunt, 1991), Nigeria (Savage et al., population. Tabachnick (1991) provided 1992), Dominican Republic (Pena, insights on introductions, reintroductions 1993), New Zealand (Laird et al., 1994), and multiple introductions of St. aegypti Mexico (Ibáñez-Bernal & Martínez- into various areas of the world based Campos, 1994; Casas-Martínez & primarily on the genetic composition of Estrata, 2003), Papua New Guinea the various populations. It is noted that (Mitchell, 1995), Guatemala (Ogata & evaluation of the sources and times of Samayoa, 1996), Argentina (Rossi et al., population introductions to the New 1999), Cuba (Broche & Borja, 1999), World has been complicated by the France (Schaffner & Karch, 2000; attempts during the 1960s to eradicate Schaffner et al., 2001), Cameroon (Toto previous St. aegypti populations from & Fontenille, 2001), Equatorial Guinea much of this geographical area. During (Toto et al., 2003), Serbia and recent decades, the range and prevalence Montenegro (Schaffner, 2003), Trinidad, of St. aegypti have been reduced in a West Indies (Chadee et al., 2003),

Belgium (Schaffner et al., 2004), Florida, USA (Pafume et al., 1988; Nicaragua (Lugo et al., 2005), Croatia O’Meara et al., 1995). (Klobucar et al., 2006; Merdic et al., 2009), Spain (Aranda et al., 2006), the Two aedine species that have been Netherlands (Scholte et al., 2007, 2008), introduced into the Hawaiian Islands, St. Gabon (Coffinet et al., 2007), Lebanon aegypti (widespread by 1892) and St. and Syria (Haddad et al., 2007), albopicta (numerous in 1902), were Germany (Pluskota et al. 2008), and noted by Usinger (1944). Ward (1984) other countries as listed by Reiter provided a case history of mosquitoes, (1998), i.e. Barbados, Bolivia, Cayman including species of Aedini, introduced Islands, Columbia and El Salvador. onto the western Pacific island of Guam These countries are only a partial listing (Mariana Islands). Laird et al. (1994) of those recently inhabited by this discuss the importation of the following species, which poses a risk to human exotic species into New Zealand: health as a potential vector of pathogens. Halaedes australis (Erichson), The article by Enserink (2008) “A Hulecoeteomyia japonica, Rampamyia mosquito goes global” records how notoscripta (Skuse) and Stegomyia rapidly this species has spread albopicta. Belkin (1962) provided throughout new areas. interesting observations on the “Bionomics and Dispersal” of Introductions continue as exemplified by mosquitoes (p. 46) and “Mosquitoes and the discovery of Hulecoeteomyia Human Migrations” (p. 65). In the latter japonica japonica (Theobald) in the section (pp. 65−66) he discussed the eastern USA (Peyton et al., 1999), 21 spread of aedine species in the southern states in the USA and Canada (Widdel et Pacific islands of the following generic- al., 2005), Washington, USA (Roppo et level taxa: Aedimorphus Theobald, al., 2004, Sames & Pehling, 2005), Finlaya Theobald, Rampamyia Reinert, Hawaii, USA (Larish & Savage, 2005), Harbach & Kitching, Stegomyia Oregon, USA (Irish & Pierce, 2008), Theobald and Verrallina Theobald. France and Belgium (Schaffner et al., 2003) and Switzerland (Schaffner & Acknowledgements Mathis, 2009). Fonseca et al. (2001) attempted to identify the putative source Appreciation is expressed to Ralph E. of populations in the eastern USA of Hl. Harbach (The Natural History Museum, japonica. Also, Tanakaius togoi London, UK) and Graham B. White (Theobald) was introduced into the (Department of Entomology and Pacific southwest of Canada and Nematology, University of Florida, northwest of the USA (Meredith & Gainesville, FL) for critically reviewing Phillips, 1973; Trimble & Wellington, the manuscript and providing valuable 1979; Wood et al., 1979; Belton, 1980; comments, and to Kenneth J. Linthicum Belton & Belton, 1990; Sames et al., and Gary G. Clark (CMAVE) for 2004); Georgecraigius atropalpus providing research facilities. (Coquillett) was introduced into Italy (Romi et al., 1997) and Howardina bahamensis (Berlin) was introduced into

References structure. The University Press, Adhami, J. & Murati, N. (1987) Prani e Camridge, UK. mushkonjës Aedes albopictus në Carnevale, P. & Pages, F. (2007) First Shqipëri. Revista Mjekësore 1, record of Aedes albopictus in Gabon. 13−16. Journal of the American Mosquito Adhami, J. & Reiter, P. (1998) Control Association 23, 471−472. Introduction and establishment of Casas-Martínez, M. & Torres-Estrada, Aedes (Stegomyia) albopictus J.L. (2003) First evidence of Aedes Skuse (Diptera: Culicidae) in albopictus (Skuse) in sountern Albania. Journal of the American Chiapas, Mexico. Emerging Mosquito Control Association 14, Infectious Diseases Journal 9(5), 2 340−343. pp. Aranda, C., Eritja, R. & Roiz, D. (2006) Chadee, D.D., Fat, F.H. & Persad, R.C. First record and establishment of the (2003) First record of Aedes mosquito Aedes albopictus in albopictus from Trinidad, West Spain. Medical and Veterinary Indies. Journal of the American Entomology 20, 150−152. Mosquito Control Association 19, Belkin, J.N. (1962) The mosquitoes of 438−439. the South Pacific (Diptera, Cornel, A.J. & Hunt, R.H. (1991) Aedes Culicidae) [sic]. Volumes I and II. albopictus in Africa? First records of University of California Press, live specimens in imported tires in Berkeley and Los Angeles, CA. Cape Town. Journal of the American Belkin, J.N., Heinemann, S.J. & Page, Mosquito Control Association 7, W.A. (1970) Mosquito studies 107−108. (Diptera, Culicidae) XXI. The Dolla Pozza, G. & Majori, G. (1992) Culicidae of Jamaica. Contributions First record of Aedes albopictus of the American Entomological establishment in Italy. Journal of the Institute (Ann Arbor) 6(1), 1−458. American Mosquito Control Belton, P. (1980) The first record of Association 8, 318−320. Aedes togoi (Theo.) in the United Dyar, H.G. (1928) The mosquitoes of States−aboriginal or ferry passenger the Americas. Carnegie Institution of ? Mosquito News 40, 624−626. Washington, USA. Belton, P. & Belton, O.C. (1990) Aedes Enserink, M. (2008) A mosquito goes togoi comes abroad. Journal of the global. Science 320(5878), 864−866. American Mosquito Control Fonseca, D.M., Campbell, S., Crans, Association 6, 328−329. W.J., Mogi, M., Miyagi, I., Toma, Broche, R.G. & Borja, E.M. (1999) T., Bullians, M., Andreadis, T.G., Aedes albopictus in Cuba. Journal of Berry, R.L., Pagac, B., Sardelis, the American Mosquito Control M.R. & Wilkerson, R.C. (2001) Association 15, 569−570. Aedes (Finlaya) japonicus (Diptera: Christophers, S.R. (1960) Aëdes aegypti Culicidae), a newly recognized [sic] (L.) the yellow fever mosquito, mosquito in the United States: its life history, bionomics and Analyses of genetic variation in the United States and putative

source populations. Journal of (1994) Japanese Aedes albopictus Medical Entomology 38, 135−146. among four mosquito species Fontenille, D. & Rodhain, F. (1989) reaching New Zealand in used tires. Biology and distribution of Aedes Journal of the American Mosquito albopictus and Aedes aegypti in Control Association 10, 14−23. Madagascar. Journal of the Larish, L.B. & Savage, H.M. (2005) American Mosquito Control Introduction and establishment of Association 5, 219−225. Aedes (Finlaya) japonicus Forattini, O.P. (1986) Identificacão de japonicus (Theobald) on the island Aedes (Stegomyia) albopictus no of Hawaii: Implications for arbovirus Brasil. Revista Saude Publica transmission. Journal of the São Paulo 20, 244−245. American Mosquito Control Haddad, N., Harbach, R.E., Chamat, S. Association 21, 318−321. & Bouharoun-Tayoun, H. (2007) Laille, P.M., Fauran, P. & Rodhain, F. Presence of Aedes albopictus in (1990) Note sur la presence d’Aedes Lebanon and Syria. Journal of the (Stegomyia) albopictus dans American Mosquito Control les Iles Fidji. Bulletin de la Societe Association 23, 226−228. de Pathologie Exotique 83, 394−398. Hunt, R.H., Cornel, A.J. & Coetzee, M. Lugo, E.C., Moreno, G., Zachariah, (1990) Aedes albopictus: An M.A., López, M.M., López, J.D., unwelcome introduction to Delgado, M.A., Valle, S.I., Cape Town. South African Journal Espinoza, P.M., Salgado, M.J., of Epidemiology and Infect. 5, 9−10. Pérez, R., Hammond, S.N. & Harris, Ibáñex-Bernal & Martínez-Campos, C. E. (2005) Identification of Aedes (1994) Aedes albopictus in Mexico. albopictus in urban Nicaragua. Journal of the American Mosquito Journal of the American Control Association 10, 231−232. Mosquito Control Association 21, Irish, S.R. & Pierce, C.S. (2008) Update 325−327. on the distribution of Ochlerotatus Madon, M.B., Mulla, M.S., Shaw, japonicus in Oregon and M.W., Kluh, S. & Hazelrigg, J.E. Washington. Journal of the (2002) Introduction of Aedes American Mosquito Control albopictus (Skuse) in southern Association 24, 110−111. California and potential for its Kay, B.H., Ives, W.A., Whelan, P.I., establishment. Journal of Vector Barker-Hudson, P., Fanning, I.D. & Ecology 27, 149−154. Marks, E.N. (1990) Is Aedes Madon, M.B., Hazelrigg, J.E., Shaw, albopictus in Australia? Medical M.W., Kluh, S. & Mulla, M.S. Journal of Australia 153, 31−34. (2003) Has Aedes albopictus Klobucar, A., Merdic, E., Benic, N., established in California? Journal of Baklaic, Z. & Krcmar, S. (2006) the American Mosquito Control First record of Aedes albopictus in Association 19, 297−300. Croatia. Journal of the American Mattingly, P.F. (1957) Genetical aspects Mosquito Control Association 22, of the Aëdes aegypti problem I.– 147−148. Taxonomy and bionomics. Annals of Laird, M., Calder, L., Thornton, R.C., Tropical Medicine and Parasitology Syme, R., Holder, P.W. & Magi, M. 51(4), 392–408.

Merdic, E., Zitko, T., Jelicic, Z. & Peyton, E.L., Campbell, S.R., Candeletti, Klobucar, A. (2009) Spreading of T.M., Romanowski, M. & Crans, Aedes albopictus on Croation islands W.J. (1999) Aedes (Finlaya) by boats and yachts. Paper 5.1, japonicus japonicus (Theobald), a Conference Programme and Abstract new introduction into the United Book, 5th European Mosquito States. Journal of the American Control Association Workshop, Mosquito Control Association 15, Turin, Italy. 238−241. Meredith, J. & Phillips, J.E. (1973) Pluskota, B., Storch, V., Braunbeck, T., Ultrastructure of anal papillae from a Beck, M. & Becker, N. (2008) First seawater mosquito larva (Aedes record of Stegomyia albopicta togoi Theobald). Canadian Journal (Skuse) (Diptera: Culicidae) in of Zoology 51, 349–353. Germany. Journal of the European Mitchell, C.J. (1995) Geographic spread Mosquito Control Association 26, of Aedes albopictus and potential for 1−5. involvement in arbovirus cycles in Powell, J.R., Tabachnick, W.J. & the Mediterranean basin. Journal of Arnold, J. (1980) Genetics and the Vector Ecology 20, 44−58. origin of a vector population: Aedes Ogata, K. & Samayoa, A.L. (1996) aegypti, a case study. Science 208, Discovery of Aedes albopictus in 1385−1387. Guatemala. Journal of the Reinert, J.F., Harbach, R.E. & Kitching, American Mosquito Control I.J. (2004) Phylogeny and Association 12, 503−506. classification of Aedini (Diptera: O’Meara, G.F., Evans, L.F. Jr., Gettman, Culicidae) based on morphological A.D. & Patterson, A.W. (1995) characters of all life stages. Exotic tank bromeliads harboring Zoological Journal of the Linnean immature Aedes albopictus and Society 142, 289−368. Aedes bahamensis (Diptera: Reinert, J.F., Harbach, R.E. & Kitching, Culicidae) in Florida. Journal of I.J. (2006) Phylogeny and Vector Ecology 20, 216−224. classification of Finlaya and allied O’Meara, G.F., Gettman, A.D., Evans taxa (Diptera: Culicidae: Aedini) Jr., L.F. & Curtis, G.A. (1993) The based on morphological data from all spread of Aedes albopictus in life stages. Zoological Journal of the Florida. American Entomologist 39, Linnean Society 148, 1−101. 163−172. Reinert, J.F., Harbach, R.E. & Kitching, Pafume, B.A., Campos, E.G., Francy, I.J. (2008) Phylogeny and D.B., Peyton, E.L., Davis, A.N. & classification of Ochlerotatus and Nelms M. (1988) Discovery of Aedes allied taxa (Diptera: Culicidae: (Howardina) bahamensis in the Aedini) based on morphological data United States. Journal of the from all life stages. Zoological American Mosquito Control Journal of the Linnean Society 153, Association 4, 380. 29−114. Pena, C. (1993) First report of Aedes Reiter, P. (1998) Aedes albopictus and (Stegomyia) albopictus (Skuse) from the world trade in used tires, the Dominican Republic. Society 1988−1995: The shape of things to of Vector Ecology 24, 4−5. come? Journal of the American

Mosquito Control Association 14, American Mosquito Control 83−94. Association 20, 105−109. Ritchie, S.A., Moore, P., Carruthers, M., Savage, H.M., Ezike, V.I., Nwankwo, Williams, C., Montgomery, B., C.A.N., Spiegel, R. & Miller, B.R. Foley, P., Ahboo, S., van den Hurk, (1992) First record of breeding A.F., Lindsay, M.D., Cooper, B., populations of Aedes albopictus in Beebe, N. & Russell, R.C. continental Africa: Implications for (2006) Discovery of a widespread arboviral transmission. Journal of infestation of Aedes albopictus in the the American Mosquito Association Torres Strait, Australia. Journal of 8, 101−103. the American Mosquito Control Schaffner, F. (2003) Mosquitoes in used Association 22, 358−365. tyres in Europe: Species list and Romi, R., Sabatinelli, G., Savelli, L.G., larval key. European Mosquito Raris, M., Zago, M. & Malatesta, R. Bulletin 16, 7−12. (1997) Identification of a North Schaffner, F. & Karch, S. (2000) American mosquito species, Aedes Première observation d’Aedes atropalpus (Diptera: Culicidae), in albopictus (Skuse, 1894) en France Italy. Journal of the American métropolitaine. Comptes Rendus de Mosquito Control Association 13, l’Academie des Sciences Paris, 245−246. Sciences de la vie/Life Sciences 323, Roppo, M.R., Lilia, J.L., Maloney, F.A. 373−375. & Sames, W.J. (2004) First Schaffner, F. & Mathis, A. (2009) occurrence of Ochlerotatus Emergence of Aedes japonicus in japonicus in the state of Washington. central Europe. Paper 5.2, Journal of the American Mosquito Conference Programme and Abstract Control Association 20, 83−84. Book, 5th European Mosquito Rossi, G.C., Pascual, N.T. & Krsticevic, Control Association Workshop, F.J. (1999) First record of Aedes Turin, Italy. albopictus (Skuse) from Argentina. Schaffner, F., Boulétreau, B., Guillet, B., Journal of the American Mosquito Guilloteau, J. & Karch, S. (2001) Control Association 15, 422. Aedes albopictus (Skuse, 1894) Sabatini, A., Raineri, V., Travato, G. & established in metropolitan France. Coluzzi, M. (1990) Aedes albopictus Journal of the European Mosquito in Italia e possiblile diffusione della Control Association 9, 1−2. specie nell’area mediterranea. Schaffner, F., Chouin, S. & Guilloteau, Parassitologia 32, 301−304. J. (2003) First record of Ochlerotatus Sames, W.J. & Pehling, D. (2005) (Finlaya) japonicus japonicus Update on Ochlerotatus japonicus in (Theobald, 1901) in metropolitan the state of Washington. Journal of France. Journal of the American the American Mosquito Control Mosquito Control Association 19, Association 21, 98−99. 1−5. Sames, W.J., Herman, W.E., Frorin, Schaffner, F., van Bortel, W. & D.A. & Maloney, F.A. (2004) Coosemans, M. (2004) First record Distribution of Ochlerotatus of Aedes (Stegomyia) albopictus togoi along the Pacific coast of in Belgium. Journal of the American Washington. Journal of the

Mosquito Control Association 20, Usinger, R.L. (1944) Entomological 201−203. phases of the recent dengue epidemic Scholte, E-J., Jacobs, F., Linton, Y-M., in Honolulu. Public Health Reports, Dijkstra, E., Fransen, J. & Takken, United States Public Health Service W. (2007) First record of Aedes 59(13), 423−430. (Stegomyia) albopictus in the Ventrillon, E. (1904) Description de Netherlands. Journal of the culicids de Madagascar. Bulletin European Mosquito Control Museum Naturelle Histoire Paris 12, Association 22, 5−9. 143−145. Scholte, E-J., Dijkstra, E., Blok, H., de Widdel, A.K., McCuistaon, L.J., Crans, Vries, A., Takken, W., Hofhuis, A., W.J., Kramer, L.D. & Fonseca, D.M. Koopmans, M., de Boer, A. & (2005) Finding needles in the Reusken, C.B.E.M. (2008) haystack: Single copy microsatellite Accidental importation of the loci for Aedes japonicus (Diptera: mosquito Aedes albopictus into the Culicidae). American Journal of Netherlands: A survey of mosquito Tropical Medicine and Hygiene 73, distribution and the presence of 744−748. dengue virus. Medical and Ward, R.A. (1984) Mosquito fauna of Veterinary Entomology 22, Guam: Case history of an introduced 352−358. fauna. Chapter 8, pp. 143−162. In: Sprenger, D. & Wuithiranyagool, T. Laird, M. (ed.). Commerce and the (1986) The discovery and spread of pests and disease distribution of Aedes albopictus in vectors. Praeger Scientific, New Harris County, Texas. Journal of the York. American Mosquito Control Wood, D.M., Dang, P.T. & Ellis, R.A. Association 2, 217−219. (1979) The insects and arachnids of Tabachnick, W.J. (1991) Evolutionary Canada Part 6. The mosquitoes genetics and arthropod-borne of Canada Diptera: Culicidae. disease: The yellow fever Canadian Government Publishing mosquito. American Entomologist Centre, Supply and Services Canada, 37(1), 14-24. Hull, Quebec, Canada. Toto, J-C., Abaga, S., Carnevale, P. & Simard, F. (2003) First report of the Oriental mosquito Aedes albopictus on the west African island of Bilko, Equatorial Guinea. Medical and Veterinary Entomology 17, 343−346. Toto, J-C. & Fontenille, D. (2001) Aedes (Stegomyia) albopictus (Skuse), as potential new dengue vector in southern Cameroon. Emerging Infectious Diseases 7, 1066−1067. Trimble, R.M. & Wellington, W.G. (1979) Colonization of North American Aedes togoi. Mosquito News 39, 18−20.