<<

Hellenic Plant Protection Journal 5: 49-56, 2012

SHORT COMMUNICATION

Records of Aedes albopictus and Aedes cretinus (Diptera: Culicidae) in from 2009 to 2011

Α.K. Giatropoulos1,2, A.Ν. Michaelakis3, G.Th. Koliopoulos1 and C.M. Pontikakos4,5

Summary Aedes (Stegomyia) albopictus, an invasive mosquito species of great medical importance, was fi rst recorded in , Greece, in 2008. Its presence raised awareness among people and as a consequence numerous “tiger-like” mosquito specimens were sent to Benaki Phytopathological Insti- tute for identifi cation and relevant information. The results of the adult mosquito specimens, collected for three years (2009-2011), revealed that Aedes albopictus occurs in many around Ath- ens, in , and in many parts of the country. The mosquito samples confi rmed also the presence of the native species Aedes (Stegomyia) cretinus. Our data, based on people awareness and an- noyance, suggest the need to implement appropriate surveillance programs for monitoring the pres- ence and population densities of Stegomyia mosquitoes in the frame of an integrated mosquito con- trol program.

Additional key words: Aedes albopictus, Aedes cretinus, Attica, Greece, Stegomyia

The Asian tiger mosquito Aedes (Stegomyia) including Italy (1990), France (2000), Switzer- albopictus (Skuse 1894) is a species native to land (2003), Spain (2004), Croatia (2004) and tropical and subtropical of South- the Netherlands (2005) (24), with Italy to be East Asia, which has undergone an aston- considered the most heavily infested Euro- ishing expansion of its range within the last pean country nowadays (8). few decades (3, 9). The international trade The geographic position and climat- of used tires has primarily facilitated Ae. al- ic conditions of Greece have been consid- bopictus spread around the world via trans- ered highly suitable for a potential invasion portation of its eggs (14). and establishment of Asian tiger mosquito In Europe, it was recorded for the fi rst (15, 18). Hence, Ae. albopictus was fi rst de- time in in 1979 (1). Ever since the spe- tected in Greece in the North-western part cies has been reported in 11 other countries, of the country near Albania and Italy in the of and in 2003 (22). Subsequently, it was found in northern 1 Laboratory of Biological Control of Pesticides, Benaki Greece in the Prefecture of in 2007 Phytopathological Institute, 8 St. Delta Str., GR-145 61 Kifi ssia (Athens), Greece (25) and the following year in central-west 2 Laboratory of Agricultural Zoology and Entomolo- Greece in Aitoloakarnania Prefecture (16). gy, Agricultural University of Athens, 75 Iera Odos Str., GR-118 55, Athens, Greece Aedes albopictus is an anthropophilic 3 Laboratory of Agricultural Entomology, Department species that causes serious nuisance prob- of Entomology and Agricultural Zoology, Benaki Phy- topathological Institute, 8 St. Delta Str., GR-145 61 Ki- lems and can play an important role in the fi ssia (Athens), Greece transmission of a wide range of human 4 Laboratory of Informatics, Division of Informatics, pathogens. This mosquito is a laboratory- Mathematics and Statistics, Agricultural University of Athens, 75 Iera Odos Str., GR-118 55 Athens, Greece competent vector of at least 22 arboviruses, 5 Prefecture of Attica, Parks and Landscaping Directo- notably Dengue virus, the most important rate, 4 Evelpidon Str., GR-113 62 Athens, Greece Corresponding author: [email protected] arboviral disease in humans (13). The recent [email protected] cases of autochthonous transmission of

© Benaki Phytopathological Institute 50 Giatropoulos et al.

Dengue in France (2010) and Croatia (2010) Herein, we review the results of records and Chikungunya virus in Italy (2007) and of Ae. albopictus and Ae. cretinus in Greece France (2010) justify the awareness of Ae. al- based on samples sent to BPI during a 3-year bopictus related potential risk for introduc- period (2009-2011). The results were record- tion and spread of serious diseases in conti- ed on maps referring to the specimen in- nental Europe (11, 12, 17, 19). cidence and the origin sites for both Ste- The presence of Ae. albopictus in the cap- gomyia species in chronological order for ital of Greece, Athens, was confi rmed for the and in the rest Prefectures fi rst time in 2008 from mosquito specimens of Greece, indicating the fi rst records. The originated from the Rizoupoli area in Mu- administrative units, either municipalities of nicipality of Athens (16). After the media an- Attica or , where sam- nouncement on fi nding this invasive mos- ples came from, were color marked in the quito in Athens, and the description of its aforementioned maps, even in case of single medical importance, the public awareness mosquito specimens. We consider that infor- in Greece was raised resulting in more than mation about the presence of Stegomyia, es- 100 specimens of “tiger-like” adult mosqui- pecially for Ae. albopictus, although limited, toes, which have been sent to Benaki Phyto- is very important for the committees of Mu- pathological Institute (BPI) for identifi cation nicipalities and Prefectures, which are mainly within the following three years (2009- responsible for the regional mosquito man- 2011). Most of these specimens were sent to agement programs in Greece. In Figure 1 the BPI by civilians, pest control companies or fi rst specimen of Ae. albopictus in 2008 is also offi cial authorities with the note for “aggres- presented and mentioned as “fi rst point”. sive day-time biting mosquitoes”. In a total of 76 Stegomyia specimens, 71 The majority of the specimens were mos- were in good condition for identifi cation quitoes of subgenus Stegomyia (Diptera: Cu- and had been sent from 35 Municipalities licidae) although other mosquito species or of the Attica Prefecture (including Munici- mosquito resembling dipterous insects (e.g. pality of Athens). During the 3-years period, Tipulidae, Chironomidae) were also record- Ae. albopictus was found in 24 Municipali- ed. Mosquito species identifi cation was per- ties, which are located mainly in central and formed using appropriate dichotomous keys south-east part of Attica. Aedes cretinus adults (6, 20). Most mosquito samples were identi- were collected from 15 Municipalities locat- fi ed as Ae. albopictus, whereas some of them ed primarily in central and northern areas of belonged to the indigenous Aedes (Stegomy- Attica, while in 4 cases (localities) both Ste- ia) cretinus. This species is closely related to gomyia species were present. Overall, Ae. al- Ae. albopictus and has a limited distribution bopictus was recorded from 7 Municipalities across the world (Greece, Cyprus, Georgia and in 2009, 11 in 2010 and 13 in 2011. According ) (2, 7). In Greece, it has been reported to Figure 1, its presence was recorded for the to exist in , Macedonia and some parts fi rst time in 6, 8 and 9 diff erent Municipalities of Attica (21). Aedes cretinus is described as an in the years 2009, 2010 and 2011, respective- aggressive day-time biting mosquito causing ly. Accordingly, Ae. cretinus specimens were considerable irritation to humans (7, 21). It is sent in a total of 12 Municipalities in 2009, 8 a container-breeding mosquito but little ap- in 2010 and only 2 in 2011, while fi rst reports pears to be known about its biology (2). of this species were declining (11 in 2009, 3 in For all the specimens an offi cial answer 2010 and only 1 in 2011) (Figure 2). was produced by the BPI experts or advisory With regards to the rest of Greece, a to- services via telephone communication were tal of 35 Stegomyia specimens were collect- provided, including a synopsis of the biolo- ed from 15 out of 52 Prefectures, during the gy of the identifi ed species, medical impor- 3-years period, mostly from southern Greece tance and appropriate protection measures ( and Crete) and the northern especially for Ae. albopictus. parts of the country (Macedonia). Overall,

© Benaki Phytopathological Institute Stegomyia mosquito species in Greece 51

Figure 1. Municipalities* of Attica where Ae. albopictus was fi rst reported over a 3-year period (2009-2011). The fi rst spec- imen of Ae. albopictus in 2008 is also presented and mentioned as “fi rst point”. *Municipalities are displayed according to the Greek administrative unit system until 2010.

© Benaki Phytopathological Institute 52 Giatropoulos et al.

Figure 2. Municipalities* of Attica where Ae. cretinus was fi rst reported over a 3-year period (2009-2011). *Municipalities are displayed according to the Greek administrative unit system until 2010.

© Benaki Phytopathological Institute Stegomyia mosquito species in Greece 53

Ae. albopictus and Ae. cretinus adults were show that Ae. albopictus was fi rst found in 4 recorded from 8 Prefectures each. Aedes al- and 3 Prefectures, while Ae. cretinus was fi rst bopictus specimens were sent from 5 Pre- found in 5 and 1 Prefectures for the years fectures in 2009 and 2010 and 2 in 2011. Ae- 2009 and 2010, respectively. In 2011, there des cretinus was detected in 6 Prefectures in was no fi rst record of Ae. albopictus, whereas 2009, 2 in 2010 and 2 in 2011. Figures 3 and 4 Ae. cretinus was recorded for the fi rst time in

Figure 3. Prefectures* of Greece where Ae. albopictus was fi rst reported over a 3-year period (2009-2011). Previous litera- ture reports, concerning Ae. albopictus presence, are also presented for 2003, 2007 and 2008. *Prefectures are displayed according to the Greek administrative unit system until 2010.

© Benaki Phytopathological Institute 54 Giatropoulos et al.

1 Prefecture. In Figure 3, except the records many parts of the country and in many sub- for the 3-year period, previous literature re- urbs in and around Athens, where almost ports concerning Ae. albopictus presence half of the population of Greece live. The cur- are also presented (2003, 2007 and 2008). rent review of Ae. albopictus and Ae. cretinus Our results revealed that 8 years after samples in Greece, based on people aware- the fi rst detection of Ae. albopictus in north- ness and annoyance, indicates the presence , this species is present in of these two Stegomyia species and com-

Figure 4. Prefectures* of Greece where Ae. cretinus was fi rst reported over a 3-year period (2009-2011). *Prefectures are displayed according to the Greek administrative unit system until 2010.

© Benaki Phytopathological Institute Stegomyia mosquito species in Greece 55 prises useful information while organizing 4. Capelli, G., Drago, A., Martini, S., Montarsi, F., mosquito surveys. Although it is general- Soppelsa, M., Delai, N., Ravagnan, S., Mazzon, L., Schaff ner, F., Mathis, A., Di Luca, M. and Romi, R., ly believed that the public awareness may Russo, F. 2011. First report in Italy of the exotic result in exaggeration, fear and unreason- mosquito species Aedes (Finlaya) koreicus, a po- able reactions and behavior, we also have to tential vector of arboviruses and fi lariae. Para- take into account that members of the pub- sites and Vectors, 4: 188-192. lic can also be a great source of information 5. Crowl, T.A., Crist, T.O., Parmenter, R.R., Belovsky, G. and Lugo, A.E. 2008. The spread of invasive by reporting new invasions, recording phe- species and infectious disease as drivers of eco- nological changes associated with invasions system change. Frontiers in Ecology and the Envi- or disease outbreaks, and fi nally can partici- ronment, 6: 238–246. pate in management eff orts (5). 6. Darsie, R.F.Jr. and Samanidou-Voyadjoglou, A. A recent mosquito surveillance in Ath- 1997. Keys for the identifi cation of the mosqui- toes of Greece. Journal of the American Mosquito ens, using ovitraps, verifi ed the presence of Control Association, 13: 247-254. both Stegomyia species and revealed that Ae. 7. Darsie, R.F.Jr. 1999. Description of the pupa of albopictus has currently developed consid- Aedes cretinus Edwards, a key to the pupae of erably high populations, displaying a trend the Albopictus subgroup, subgenus Stegomyia of increase over time, in the urban environ- Theobald, genus Aedes Meigen, and characters to separate the European Stegomyia species ment of the Greek capital (10). Moreover, (Diptera: Culicidae). Proceedings of the Entomo- the co-occurrence of Ae. albopictus and Ae. logical Society of Washington, 101: 614-618. cretinus, mainly in some Municipalities of At- 8. ECDC 2009. European Centre for Disease Pre- tica, arises the need for a better study on the vention and Control. Development of Aedes al- biology of Ae. cretinus and suggests the im- bopictus risk maps. Retrieved online from: http:// www.ecdc.europa.eu/en/publications/Publica- plementation of surveillance programmes tions/0905_TER_Development_of_Aedes_Al- using ovitraps and other surveillance meth- bopictus_Risk_Maps.pdf (last visit 1/5/2012). ods in order to investigate the population 9. Enserink, M. 2008. A mosquito goes global. Sci- dynamics of each species and the possible ence, 320: 864-866. interspecifi c competitive interactions. 10. Giatropoulos, Α., Emmanouel, N., Koliopoulos, Surveillance programs will be also use- G. and Michaelakis A. 2012. A study on distribu- tion and seasonal abundance of Aedes albopictus ful to prevent the introduction and establish- (Diptera: Culicidae) population in Athens, Greece. ment of other invasive container-breeding Journal of Medical Entomology, 49: 262-269. Aedes species with medical importance such 11. Gjenero-Margan, I., Aleraj, B., Krajcar, D., Le- as Ae. aegypti, Ae. japonicus, Ae. atropalpus, Ae. snikar, V., Klobučar, A., Pem-Novosel, I., Kurečić- koreicus and Ae. triseriatus. These species have Filipović, S., Komparak, S., Martić, R., Đuričić, S., Betica-Radić, L., Okmadžić, J., Vilibić-Čavlek, been reported the recent years as introduced T., Babić-Erceg, A., Turković, B., Avšić-Županc, into various European countries (4, 23). T., Radić, I., Ljubić, M., Šarac, K., Benić, N. and Mlinarić-Galinović, G. 2011. Autochthonous den- gue fever in Croatia, August–September 2010. Eurosurveillance, 16: 19805. Retrieved online Literature cited from: http://www.eurosurveillance.org/ViewAr- ticle.aspx?ArticleId=19805 (last visit 1/5/2012). 1. Adhami, J. and Reiter, P. 1998. Introduction and establishment of Aedes (Stegomyia) albopictus 12. Grandadam, M., Caro V., Plumet S., Thiberge M., Skuse (Diptera: Culicidae) in Albania. Journal of Souarès Y., Failloux A., Hugues J., Budelot M., the American Mosquito Control Association, 14: Cosserat D., Leparc-Goff art I. and Desprès, P. 340-343. 2011. Chikungunya Virus, Southeastern France. Emerging Infectious Diseases, 17: 910-913. 2. Becker, N., Petric´, D., Zgomba, M., Boase, C., Ma- don, M., Dahl, C. and Kaiser, A. 2010. Mosqui- 13. Gratz, N.G. 2004. Critical review of the vector toes and Their Control, 2nd ed. Springer, Berlin- status of Aedes albopictus. Medical and Veteri- Heidelberg, Germany. nary Entomology, 18: 215-227. 3. Benedict, M.Q., Levine, R.S., Hawley, W.A. and 14. Knudsen, A.B. 1995. Global distribution and Lounibos, L.P. 2007. Spread of the tiger: Global continuing spread of Aedes albopictus. Parassi- risk of invasion by the mosquito Aedes albopic- tologia, 37: 91–97. tus. Vector-Borne and Zoonotic Diseases, 7: 76-85. 15. Knudsen, A.B., Romi, R. and Majori, G. 1996. Oc-

© Benaki Phytopathological Institute 56 Giatropoulos et al.

currence and spread in Italy of Aedes albopictus licidae) of Greece. European Mosquito Bulletin, with implications for its introduction into other 10: 13-20. parts of Europe. Journal of the American Mosqui- 21. Samanidou-Voyadjoglou, A. and Koliopoulos, G. to Control Association, 12: 177-183. 1998. Some notes on Aedes (Stegomyia) cretinus 16. Koliopoulos, G., Lytra, I., Michaelakis, A., Kioulos, Edwards (Culicidae) in northern Athens, Attiki, E., Giatropoulos A. and Emmanuel, N. 2008. Asian Greece, pp. 194-195. In Fourth International Con- tiger mosquito. First record in Athens. Agriculture gress of Dipterology, 6-13 September, Oxford, crop and animal husbandry, 9: 68-73 [in Greek]. United Kingdom. 17. La Ruche, G., Souarès, Y., Armengaud, A., 22. Samanidou-Voyadjoglou, A., Patsoula, E., Span- Peloux-Petiot, F., Delaunay, P., Desprès, P., Len- akos, G. and Vakalis, N.C. 2005. Confi rmation of glet, A., Jourdain, F., Leparc-Goff art, I., Charlet, Aedes albopictus (Skuse) (Diptera: Culicidae) in F., Ollier, L., Mantey, K., Mollet, T., Fournier, J.P., Greece. European Mosquito Bulletin, 19: 10-12. Torrents, R., Leitmeyer, K., Hilairet, P., Zeller, H., 23. Schaff ner, F. and Van Bortel, W. 2010. Current Van Bortel, W., Dejour-Salamanca, D., Grandad- status of invasive mosquitoes in Europe. Euro- am, M. and Gastellu-Etchegorry, M. 2010. First pean Centre for Disease Prevention and Con- two autochthonous dengue virus infections in trol. Retrieved online from: http://www.ecdc. metropolitan France, September 2010. Euro- europa.eu/en/activities/sciadvice/Lists/ECDC%20 surveillance, 15: 19676. Retrieved online from: Reviews/ECDC_DispForm.aspx?List=512ff74f-77d4- http://www.eurosurveillance.org/ViewArticle. 4ad8-b6d6-bf0f23083f30&ID=758&RootFolder=/en/ aspx?ArticleId=19676 (last visit 1/5/2012). activities/sciadvice/Lists/ECDC%20Reviews &Master- 18. Mitchell, C.J. 1995. Geographical spread of Ae- Page=1 (last visit 1/5/2012). des albopictus and potential for involvement 24. Scholte, E.-J. and Schaff ner, E. 2007. Waiting for in arbovirus cycles in the Mediterranean basin. the tiger: establishment and spread of the Asian Journal of Vector Ecology, 20: 44-58. tiger mosquito in Europe. Emerging Pests and 19. Rezza, G., Nicoletti, L., Angelini, R., Romi, R., Fin- Vector-Borne Diseases in Europe (ed. by W. Tak- arelli, A.C., Panning, M., Cordioli, P., Fortuna, C., ken & B. Knols), pp. 241-260. Wageningen Aca- Boros, S., Magurano, F., Silvi, G., Angelini, P., Dot- demic Publishers, Wageningen. tori, M., Ciufolini, M.G., Majori, G.C. and Cassone, 25. Voutsina, G. and Karagiannidis, G. 2007. Aedes A. 2007. Infection with chikungunya virus in It- albopictus: monitoring program in Serres Pre- aly: an outbreak in a temperate . Lancet, fecture. 12th Pan-Hellenic Congress of Entomolo- 370: 1840–1846. gy, 13–16 November, Larnaca Cyprus. 20. Samanidou-Voyadjoglou, A. and Harbach, R.E. 2001. Keys to the adult female mosquitoes (Cu- Received: 7 January 2012; Accepted: 22 May 2012

ΣΥΝΤΟΜΗ ΑΝΑΚΟΙΝΩΣΗ

Στοιχεία της παρουσίας των Aedes albopictus και Aedes cretinus (Diptera: Culicidae) στην Ελλάδα για την τριετία 2009-2011

Α.K. Γιατρόπουλος, Α.N. Μιχαηλάκης, Γ.Θ. Κολιόπουλος και Κ.Μ. Ποντικάκος Περίληψη Το Aedes (Stegomyia) albopictus είναι ένα επεκτατικό είδος κουνουπιού με μεγάλη υγειονομι- κή σημασία, του οποίου η παρουσία καταγράφηκε για πρώτη φορά στην Αθήνα το 2008. Τα επόμενα 3 έτη (2009-2011) πολυάριθμα δείγματα κουνουπιών από την Αττική και την Ελλάδα γενικότερα εστάλη- σαν στο Μπενάκειο Φυτοπαθολογικό Ινστιτούτο προς αναγνώριση και παροχή σχετικών πληροφοριών, ως αποτέλεσμα της όχλησης των κατοίκων ορισμένων περιοχών καθώς και της ανησυχίας που προκλή- θηκε από την παρουσία και υγειονομική σημασία του συγκεκριμένου είδους κουνουπιού. Από την ερ- γαστηριακή εξέταση των δειγμάτων προέκυψε ότι το Ae. albopictus δραστηριοποιείται σε αρκετούς Νο- μούς της χώρας και Δήμους της Αττικής. Επιπλέον, επιβεβαιώθηκε η παρουσία και του συγγενούς είδους κουνουπιού Aedes (Stegomyia) cretinus. Αν και τα δεδομένα βασίζονται κυρίως σε δείγματα πολιτών, κα- ταδεικνύουν την ανάγκη εφαρμογής κατάλληλων μεθόδων μελέτης της παρουσίας των συγκεκριμένων ειδών στα πλαίσια της ολοκληρωμένης αντιμετώπισης του γενικότερου προβλήματος των κουνουπιών.

Hellenic Plant Protection Journal 5: 49-56, 2012

© Benaki Phytopathological Institute