The Status of Harmonia Axyridis (Pallas) (Coleoptera: Coccinellidae) in Greece: a Case of an Exotic Predator That Failed to Establish?

ENTOMOLOGIA HELLENICA 17 (2007-2008): 42-51

The status of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Greece: A case of an exotic predator that failed to establish?

D. C. KONTODIMAS1,*, G. J. STATHAS2 AND A. F. MARTINOU1

1Benaki Phytopathological Institute, Department of Entomology, Agricultural and Agricultural Zoology, 8 St. Delta, 14561 Kifissia, Greece 2Technological Educational Institute of Kalamata, School of Agricultural Technology, Department of Crop Production, 24100 Antikalamos, Greece

ABSTRACT

During 1994 -1999 several hundred thousands of Harmonia axyridis adults were released at various cultivations infested by aphids (citrus, vegetable and bean crops, maize, etc.) or in urban places on ornamental plants in central and southern Greece (mainly Attica and Peloponnessos region) as well as on several islands. During 1995-2007, samplings were conducted in some areas, in spring just before any new releases, in order to determine if H. axyridis overwintered in the field. In spring 1995 (the year that followed the first releases) as well in spring 1996-97 and 2000-07, no presence of H. axyridis was recorded in any of the orchards where the predator had been released. Only in spring 1998 and 1999 small colonies (<50 individuals) of overwintered H. axyridis adults were observed in Attica region. The above results indicate an inability of the H. axyridis released populations to establish in Greece, although in some areas this species became an important biocontrol agent during the season. In addition, some data collected regarding the composition of native coccinelid species pre- and post- release of H. axyridis could be an indication of no adverse effects imposed by H. axyridis on the native coccinellid fauna in Greece. Despite that, any re-initiation of releases of H. axyridis would not be wise because of its multiple negative effects observed in other countries of Europe and the USA. Contrary to this, the application of a survey and monitoring programme that will allow us to be prepared in case of a possible invasion of H. axyridis from northern Europe is suggested.

Introduction Belgium and the Netherlands, and was also intentionally released in at least nine other Native to Asia, Harmonia axyridis (Pallas) countries. It is now regarded as established (Coleoptera: Coccinellidae) is considered in thirteen European countries (Brown et an invasive alien ladybird in Europe and al. 2008a). In several European countries North America, where it was widely (Belgium, Netherlands, the United introduced as a biological control agent of Kingdom, France, the Czech Republic and aphids and coccids (Katsoyannos 1996, Switzerland) several working groups are Pervez & Omkar 2006). In Europe, H. mapping Coccinellidae species and axyridis was sold by various biological intensive monitoring of H. axyridis is control companies since 1995 in France, taking place, while, despite releases of H.

*Corresponding author, email: [email protected] KONTODIMAS ET AL.: The status of H. axyridis in Greece 43 axyridis in Portugal, Spain and Greece, coccinellid populations sampled at thirteen there is little evidence of its establishment locations for the years 1995 to 2007, are in southern Europe (Brown et al. 2008a). also presented. Its effectiveness as a biological control agent has been accompanied by the Materials and Methods adverse impact on other aphidophagous coccinellids (Adriaens et al. 2003, Koch & Harmonia axyridis rearing and releases Galvan 2008). An expectation has recently After the first releases (1994) of H. been expressed that, because of some life- axyridis in Attica, Chios, Arcadia and history parameters, this species may Crete (Katsoyannos et al. 1997), the become a serious competitor of Coccinella laboratory of Biological Control of the septempunctata (Hodek & Michaud 2008). Benaki Phytopathological Institute (BPI) In addition, H. axyridis caused problems to continued the rearing of the predator and fruit production (Koch 2003) and as a its releases until spring 1999. H. axyridis household nuisance it induces allergic originally obtained from France rhino-conjunctivitis to humans (Koch et al. (Katsoyannos et al. 1997) was reared 2006, Majerus et al. 2006, and Pervez & mainly on Aphis fabae (Hemiptera: Omkar 2006). Aphididae) on Vicia faba (Stathas et al. During spring 1994 approximately 620 2001) as well as occasionally on Dysaphis adults of H. axyridis were released in four crataegi (Hemiptera: Aphididae) on citrus growing areas of Greece (Marathon- squash (Cucurbita pepo, C. maxima and C. Attica, Campos-Chios, Leonidion-Arcadia, moschata) in controlled conditions at Chania-Crete) on orange, mandarin and 25±1νC, 65±2% R.H. and under a sour orange infested by aphids [Toxoptera photoperiod of 16:8 (L:D). During 1995- aurantii, Aphis spiraecola and A. gossypii 1999 more than 100.000 insectary-reared (Hemiptera: Aphididae)] (Katsoyannos et adults of H. axyridis were released in al. 1997). Over the next two months in various cultivations (citrus, vegetables, 1994, H. axyridis proved to be an effective beans and maize) infested by aphids or in biocontrol agent against the previously urban areas on ornamental plants, in mentioned aphids in two locations central and southern Greece (mainly Attica (Campos-Chios and Leonidion-Arcadia). and Peloponessos) and the islands: Chios, In outdoor cages H. axyridis overwintered Euvoia and Crete (Table 1). Moreover, at the adult stage (~30% of the adults of th during 1997-2002 several hundreds of the 4 generation survived), and under thousands imported H. axyridis individuals conditions of continuous surplus of aphids were released by private companies mainly it completed four overlapping generations in urban areas of the mainland (Attica, annually and it did not diapause during Peloponessos) and in the islands of Corfu, summer. In the field, aphid populations are Rhodos and Crete, although no intentional scarce in summer in Greece (Katsoyannos releases were made by (BPI) after 1999. et al. 1997). The purpose of the current study was to Sampling method present the status of H. axyridis in Greece During 1995-1999, samplings were during the years 1995-1999, when the conducted every spring just before any releases of the predator were continued releases, in thirteen locations (Table 2) in with increased numbers in expanded areas. order to determine if H. axyridis Additionally, data on other beneficial overwintered in the field. A second 44 ENTOMOLOGIA HELLENICA 17 (2007-2008): 42-51 sampling was conducted a month later in Twelve samples were collected from each order to calculate the population size of the crop at every location. In arboric exotic predator shortly after the release. cultivations or in ornamental trees, branch 44

TABLE 1. Releases of H. axyridis by the laboratory of Biological Control of Benaki

Phytopathological Institute, during 1995-1999.

KONTODIMAS AL.:ET statusThe of Released H. axyridis adults District Area Plant Aphid pest 1995 1996 1997 1998 1999 I. Marathon orange 350 640 1200 800 Attica* (Citrus sinensis) Toxoptera aurantii Marathon lemon Aphis spiraecola 640 700 640 Attica (Citrus limon) A. gossypii Marathon clementine 250 600 2200 800 Attica (Citrus reticulata) II. Varympopi faba beans Aphis fabae 400 740 400 800 Attica (Vicia faba) Varympopi rose (Rosa sp.) Macrosiphum rosae 260 200 320 Attica Varympopi Almond trees

Hyalopterus pruni 840 1400 H.axyridis Attica (Pyrus amygdalus) Varympopi lettuce Nasonobia 600 400 Attica (Lactuca sativa) ribis-nigri Central III. Glyfada sour orange Aphis spiraecola 600 1200 1400 in Greece Attica (Citrus aurantium) A. gossypii

Greece Glyfada rose (Rosa sp.) Macrosiphum rosae 240 420 180 Attica

IV. Aliartos squash Dysaphis crataegi 1200 3000 Voiotia (Cucurbita pepo) Aliartos cucumber Myzus persicae 800 2400 Voiotia (Cucumis sativus) Aliartos 44lucerne Acyrthosiphon 1200 2400 Voiotia (Medicago sativa) pisum squash Agrinio (Cucurbita Dysaphis crataegi 840 2000 400 Aitoloakarnania moschata) Filothei orange 1000 450 1400 Arta (Citrus sinensis) Toxoptera aurantii Aphis spiraecola Filothei lemon A. gossypii 860 800 Arta (Citrus limon) V. Campos mandarin 320 400 640 720 800 Chios* (Citrus delicioca) Toxoptera aurantii Chania orange Aphis spiraecola 560 240 Insular Crete* (Citrus sinensis) A. gossypii Greece Fodele orange 600 260 Crete (Citrus sinensis) Karystos lemon Aphis spiraecola 2000 560 1800 Euvoia (Citrus limon) A. gossypii

* release-locations of H. axyridis adults in 1994 (Katsoyannos et al. 1997) KONTODIMAS ET AL.: The status of H. axyridis in Greece 45

TABLE 1 (continued). Releases of H. axyridis by the laboratory of Biological Control of Benaki Phytopathological Institute, during 1995-1999. Released H. axyridis adults District Area Plant Aphid pest 1995 1996 1997 1998 1999 VI. Galatas clementine 360 550 1640 Troizinia (Citrus reticulata) Toxoptera aurantii Kiato lemon Aphis spiraecola 400 820 1260 Korinthos (Citrus limon) A. gossypii Vrachati orange 800 1260 1200 Korinthos (Citrus sinensis) Xylokastro orange Aphis fabae 640 1420 Korinthos (Citrus sinensis) Zeygolatio orange Macrosiphum rosae 800 800 Korinthos (Citrus sinensis) VII. Zeygolatio apricot tree Myzus persicae 950 880 Korinthos (Prunus armeniaca) Toxoptera aurantii VIII. Leonidion sour orange Aphis spiraecola 700 800 650 1100 Arcadia* (Citrus aurantium) A. gossypii Pelopon- orange Aphis spiraecola nesos Leonidion Arcadia 600 1000 800 2000 (Citrus sinensis) A. gossypii IX. Kalamata orange Macrosiphum rosae 1600 2000 3000 2000 Messinia (Citrus sinensis) X. Kyparissia orange Dysaphis crataegi 720 400 560 Messinia (Citrus sinensis) XI. Skala orange Myzus persicae 480 520 Lakonia (Citrus sinensis) Elaionas lemon Acyrthosiphon 640 520 1200 800 Achaia (Citrus limon) pisum Elaionas orange Dysaphis crataegi 900 1600 1200 420 Achaia (Citrus sinensis) XII. Akrata orange Toxoptera aurantii 800 700 1000 Achaia (Citrus sinensis) Aphis spiraecola Nea Kios orange A. gossypii 800 700 850 850 Argolida (Citrus sinensis) Dalamanara orange 260 650 440 Argolida (Citrus sinensis) Nayplion sour orange 240 580 540 640 Argolida (Citrus aurantium)

XIII. Gastouni orange 340 880 720 Ilia (Citrus sinensis) Lexaina orange Aphis spiraecola 420 700 540 Ilia (Citrus sinensis) A. gossypii * release-locations of H. axyridis adults in 1994 (Katsoyannos et al. 1997)

46 ENTOMOLOGIA HELLENICA 17 (2007-2008): 42-51 beating over a 1m2 canvas area was observed only at the location of applied, while in other cultivations Varympompi Attica, the only area where

(vegetables, beans, maize, ornamental H. axyridis was released in V. faba fields 46 shrubs) the 20cm-length shoot was used as infested by A. fabae. A similar case was sampling unit. During 2000-2007, observed by Soares et al. (2008) at Santa

sampling for coccinellid species was Maria of the Azores islands where more continued in the above locations, every than one hundred thousand H. axyridis KONTODIMAS AL.:ET statusThe of spring when aphid infestations occurred. (third larval stage) were released into several citrus orchards. Although after the Results and Discussion releases there were records of individuals that dispersed and fed on citrus, apple trees and bean plants, the exotic predator failed One month after the 1994 releases, H. to establish (Soares et al. 2008). axyridis was an important biocontrol agent Although the ecoclimatic indices for at the Campos-Chios and the Leonidion- Greece as predicted by Poutsma et al. Arcadia locations (Katsoyannos et al. (2008) are appropriate for H. axyridis 1997). However, in the spring 1995 no establishment in Greece, the predators presence of H. axyridis was recorded in seem to have failed to establish in spite of any of the orchards (Table 2). continued releases. In contrast, in the In the following years, despite the regions of USA where the climatic H.axyridis continued massive releases of H. axyridis, conditions are similar to those in Greece, only in spring 1998 and spring 1999 small H. axyridis established successfully (Koch colonies (<50 individuals) of overwintered and Galvan 2008). Data collected in the H. axyridis adults were found in the Attica thirteen locations mentioned herein inGreece region, although in some of the locations indicate the failure of the establishment of the released predator became an important H. axyridis in Greece at least to date. biocontrol agent during the season (Table Despite the fact that the efficiency of H. 1). The above result shows that although axyridis in biocontrol in Greece appears at H. axyridis has the ability to overwinter in first to overwhelm its negative secondary Greek climatic conditions, this has effects, further releases should not be occurred only rarely and in very low organized. Especially since predictive numbers of adults. modeling based on ecoclimatic indices The observed failure in establishment shows that the climate all over Greece is of H. axyridis at the release locations in suitable for the establishment of H. Greece could possibly be attributed to the axyridis (Poutsma et al. 2008). maladaptation of H. axyridis to switching Empirically, it is also known that the of prey between the rearing conditions climatic conditions in northern Greece prior to the release and the prey resemble mostly the conditions of encountered in the field. H. axyridis was mainland Europe where the predator is reared on Aphis fabae on V. faba seedlings, widely established. However, to date no while almost all the field releases of H. surveys have been undertaken in the axyridis occurred in citrus cultivations northern part of Greece. where T. aurantii, A. spiraecola and A. According to Table 2 it seems that the gossypii were the aphid pests. This native coccinellid species are not affected hypothesis is further enhanced by the fact by H. axyridis however more elaborate that overwintering H. axyridis adults were

TABLE 2. Composition of the coccinellid populations sampled at the wider area of thirteen localities before and after H. axyridis releases (sums KONTODIMASAL.:ET statusThe of of counted adults and larvae). After 1999 no releases of H. axyridis were undertaken by BPI or private companies.

1995 1996 1997 1998 1999 Location before after before after before after before after before after 2000 2001 2002 2003 2004 2005 2006 2007 release release release release release release release release release release I. A: 64 A: 160 A: 60 A: 20 no no A: 32 A: 85 no infestation A: 25 A: 15 A: 37 A: 78 A: 18 A: 28 A: 2 Marathon B: 40 B: 25 B: 45 B: 25 infesta- A: 6 infesta- B: 16 B: 33 no release B: 43 B: 23 B: 112 B: 42 B: 12 B: 4 B: 22 Attica H.a.: 45 H.a.: 15 H.a.: 115 H.a.: 156 tion tion

II. A: 4 A: 24 A: 21 no no no no no A: 14 A: 16 A: 16 A: 14 A: 8 Varympopi A: 25 A: 35 A: 8 B: 12 B: 5 B: 11 infesta- infesta- A: 22 A: 2 infesta- infesta- infesta- H.a.: 25 H.a.: 15 H.a.: 210 H.a.: 55 B: 5 Attica H.a.: 36 H.a.: 135 H.a.: 41 tion tion tion tion tion

III. A: 14 A: 7 A: 17 A: 12 no no A: 11 A: 5 A: 26 no infestation no infestation A: 2 B: 2 A: 3 Glyfada B: 10 B: 27 B: 30 B: 21 A: 2 infesta- infesta- B: 4 B: 31 B: 33 B: 43 no release no release B: 11 C: 3 B: 11 Attica H.a.: 15 H.a.: 35 H.a.: 145 C: 3 tion tion H.axyridis

IV. no no no no no infestation no infestation A: 64 A: 47 A: 33 no infestation Aliartos A: 131 A: 13 A: 2 A: 23 A: 62 infesta- infesta- infest infesta- no release no release C: 5 H.a.: 143 H.a.: 55 no release Voiotia tion tion a-tion tion

in Greece in V. A: 14 A: 9 A: 2 no no A: 9 A: 7 A: 3 A: 3 A: 10 A: 3 A: 9 A: 4 A: 4 A: 5 Campos B: 2 B: 8 B: 5 B: 11 B: 3 infesta- infestati A: 2 B: 11 B: 7 B: 5 B: 13 B: 6 H.a.: 5 B: 11 B: 4 B: 12 B: 21 Chios H.a.: 7 H.a.: 5 H.a.: 25 tion on

VI. A: 14 A: 7 A: 17 A: 6 A: 1 no no no no no A: 11 A: 5 no infestation A: 26 no infestation B: 2 Galatas B: 10 B: 27 B: 31, C:2 B: 21 B: 9 infesta- infesta- infesta- infest infesta- B: 31 B: 33 no release B: 43 no release C: 1 Troizinia H.a.: 15 H.a.: 35 H.a.: 145 C: 5 C: 3 tion tion tion a-tion tion

VII. A: 6 no no no no no no no no infestation no infestation A: 3 A: 5 A: 5 no infestation A: 9 Zeygolatio B: 7 infesta- infesta- infesta- infesta- infesta- infest infesta- no release no release B: 11 H.a.: 14 B: 3 no release B: 5 Korinthos H.a.: 45 tion tion tion tion tion a-tion tion

VIII. A: 8 A: 5 A: 16 A: 1 A: 7 A: 13 A: 17 A: 2 A: 1 A: 7 no no A: 11 A: 3

no infestation A: 4 B: 1

Leonidion B: 5 B: 13 B: 2 B: 7 B: 1, C:7 B: 21 B: 10 B: 5 B: 2 B: 2 infesta- infesta- B: 5 B: 1 47 no release B: 17 C: 2

Arcadia H.a.: 9 C: 1 H.a.: 23 C: 3 H.a.: 33 C: 5 H.a.: 13 C: 1 C: 3 C: 4 tion tion C: 5 C: 2

TABLE 2 (continued). Composition of the coccinellid populations sampled at the wider area of thirteen localities before and after H. axyridis 48 releases (sums of counted adults and larvae). After 1999 no releases of H. axyridis were undertaken by BPI or private companies.

1995 1996 1997 1998 1999 Location before after before after before after before after before after 2000 2001 2002 2003 2004 2005 2006 2007 release release release release release release release release release release A: 7 A: 21 IX. A: 5 A: 15 A: 7 A: 10 A: 2 A: 11 A: 3 no no no no infestation B: 5, C: B: 8, C: A: 5 A: 12 A: 2 Kalamata B: 7 B: 13 B: 11, C:1 B: 5 B: 5 B: 3 B: 7 infesta- infesta- infesta- A: 4 no release 4 3 B: 11 B: 12 B: 15

Messinia C: 2 C: 3 H.a.: 139 H.a.: 45 C: 1 C: 1 C: 2 tion tion tion

H.a.: 11 H.a.: 12 ENTOMOLOGIAHELLENICA A: 3 X. A: 11 A: 6 A: 9 no no A: 6 no no no no infestation B: 4, C: A: 9 A: 3 no infestation B: 4 Kyparissia B: 2 B: 18 B: 3, C:1 infesta- infesta- B: 7 infesta- B: 9 infesta- infesta- no release 1 B: 19 B: 9 no release C: 3 Messinia C: 1 H.a.: 2 H.a.: 3 tion tion C: 5 tion tion tion H.a.: 12

XI. A: 7 A: 11 no no A:2 A: 4 no no no no no infestation no infestation A: 11 A: 13 no infestation Skala B: 2 B: 2, C:2 infesta- infesta- B: 5 B: 19 infesta- infesta- infesta- infesta- no release no release B: 10 B: 7 no release Lakonia H.a.: 4 H.a.: 10 tion tion C: 4 C: 1 tion tion tion tion

A: 9 A: 112 XII. A: 17 A: 12 A: 12 no no no no no no infestation A: 3 B: 3, C: A: 8 no infestation B: 15 A: 3 A: 3 Akrata B: 5 B: 21 B: 4, C: 1 infesta- infesta- infesta- infesta- infesta- no release B: 5 1 B: 16 no release C: 2 C: 1 B: 2 Achaia H.a.: 14 C:4 H.a.: 9 tion tion tion tion tion H.a.: 12

A: 31 17

A: 11 A: 17 A: 24 A: 123 no no A: 36 no no A: 73

XIII. (2007 A: 12 no infestation no infestation A: 5 B: 12 A: 20 Gastouni B: 7 B: 5, C: 2 B: 20 B: 27 infesta- infesta- B: 11 infesta- infesta- B: 22 B: 4 no release no release B: 12 C: 5 B: 7 Ilia H.a.: 7 H.a.: 29 C:3 C: 7 tion tion C: 1 tion tion C: 7 H.a.: 59

2008):42 A: Coccinellini Propylea quatuordecimpunctata B: Scymnini C: Chilocorini H.a.: Harmonia axyridis Coccinella septempunctata, Adalia bipunctata Scymnus (Pullus) subvillosus Exochomus Hippodamia undecimnotata Adalia decempunctata Scymnus apetzi quadripustulatus Hippodamia variegata Synharmonia conglobata Scymnus rubromaculatus Chilocorus

- bibustulatus 51

KONTODIMAS ET AL.: The status of H. axyridis in Greece 49

data collection on coccinellid species, References 49 composition and abundances that would be based on a more extensive sampling regime Adriaens, T., E. Branquart and D. Maes. would have enabled us to ascertain this case 2003. The multicoloured Asian ladybird more accurately. In addition, a more Harmonia axyridis Pallas (Coleoptera: intensive sampling scheme could have Coccinellidae), a threat for native aphid provided some evidence on the effects of H. predators in Belgium? Belgian J. Zool. axyridis on other natural enemies of soft- 133: 195-196. bodied insects such as predators and Babendreier, D. 2007. Pros and cons of parasitoids while to date investigating the

biological control. In: Biological ENTOMOLOGIAHELLENICA effect of H. axyridis on other native to Invasions (Ed. W. Nentwig) Springer, Greece natural enemies has been neglected. Berlin pp. 403-418. In any case, given the current adverse Brown, P.M.J., T. Adriaens, H. Bathon, J. impact of H. axyridis in other European Cuppen, A. Goldarazena , T. Hägg, M. countries and North America, (Koch 2003, Kenis, B.E.M. Klausnitzer, I. Kovar, Koch et al. 2006, Roy et al. 2006, A.J.M. Loomans, M.E.N. Majerus, O. Babendreier 2007, Eschen et al. 2007, Nedved, J. Pedersen, W. Rabitsch, H.E. Brown et al. 2008a, b, Koch & Galvan Roy, V. Ternois, I.A. Zakharov and D.B. 2008)it would not be wise to continue with Roy. 2008(a). Harmonia axyridis in field releases of this insect. This has recently Europe: spread and distribution of a non- been concluded also by scientists working on native coccinellid. BioControl 53: 5–21.

1 risk assessment of biological control agents Brown, P. and H. Roy. 2007. The spread of 7

(van Lenteren et al. 2008, Roy & Wajnberg the harlequin ladybird Harmonia axyridis (2007 2008). (Pallas) in late 2006. Atropos 31: 32-33.

- It is predicted that the spread and Brown, P.M.J., H.E. Roy, P. Rothery, D.B. 2008):13 increase of H. axyridis within Europe will Roy, R.L. Ware and M.E.N. Majerus. continue and that it will become one of the 2008(b). Harmonia axyridis in Great

most widely distributed coccinellids of the -

Britain: analysis of the spread and 22 continent (Brown et al. 2008). We believe distribution of a non-native coccinellid. that it is necessary to develop and apply a BioControl 53: 55–67. survey and monitoring ladybird scheme Cardinale, B.J., J.J. Weis, A.E. Forbes, K.J. similar to those currently applied in Tilmon and A.R. Ives. 2006. Biodiversity European countries and the USA in order to as both a cause and consequence of obtain a database on the distribution and resource availability: a study of abundance of all coccinellid predators and reciprocal causality in a predator-prey especially H. axyridis. This way it will be system. J. Anim. Ecol. 75: 497-505. possible to prevent the establishment of this Eschen, R., D. Babendreier, S. Nauer, F. exotic predator. There is a great necessity to Bigler and M. Kenis. 2007. Surveys for increase public awareness on issues such as ladybirds (Coleoptera: Coccinellidae) in H. axyridis and invasive species and for this Switzerland and confirmation of the reason the collaboration between presence of the invasive ladybird species, entomologists, government officials, Harmonia axyridis Pallas. Mit. Schweiz. farmers, conservation organisations and park Entomol. Ges. 80: 7–14. managers is essential. Hodek, I. and J.P. Michaud. 2008. Why is Coccinella septempunctata so successful? Eur. J. Entomol., 105: 1-12.

50 ENTOMOLOGIA HELLENICA 17 (2007-2008): 42-51

Katsoyannos, P. 1996. Integrated Insect Pest Pervez, A. and Omkar. 2006. Ecology and Management for Citrus in Northern biological control application of Mediterranean Countries. Benaki multicoloured asian ladybird, Harmonia Phytopathological Institute, Athens, axyridis: a review. Biocontrol Sci. Techn. Greece. 16: 111-128. Katsoyannos, P., D.C. Kontodimas, G.J. Poutsma, J., A.J.M. Loomans, Ζ.B. Aukema Stathas and C.T. Tsartsalis. 1997. The and Ζ.T. Heijerman. 2008. Predicting the establishment of Harmonia axyridis potential geographical distribution of the (Coleoptera: Coccinellidae) on citrus and harlequin ladybird, Harmonia axyridis, some data on its phenology in Greece. using the CLIMEX model. BioControl Phytoparasitica 25 (3): 183-191. 53: 103–125. Koch, R.L. 2003. The multicolored Asian Roy, H.E., P.M.J. Brown and M.E.N. lady beetle, Harmonia axyridis: A review Majerus. 2006. Harmonia axyridis: A of its biology, uses in biological control, successful biocontrol agent or an and non-target impacts. J. Ins. Sci. invasive threat? In: An Ecological and 3(32):16pp. Societal Approach to Biological Control Koch, R.L., R.C. Venette and W.D. (eds.: J. Eilenberg & H. Hokkanen). Hutchison. 2006. Invasions by Harmonia Kluwer, Dordrecht, Netherlands. axyridis (Pallas) (Coleoptera: Roy, H.E. and E. Wajnberg. 2008. From Coccinellidae) in the Western biological control to invasion: the Hemisphere: implications for South ladybird Harmonia axyridis as a model America. Neotrop. Entomol. 35: 421-434. species. BioControl 53: 1–4. Koch, R.L. and T.L. Galvan. 2008. Bad side Soares A.O., I. Borges, P.A.V. Borges, G. of a good beetle: the North American Labrie and E. Lucas. 2008. Harmonia experience with Harmonia axyridis. axyridis: What will stop the invader? BioControl 53: 23–35. BioControl 53: 127–145. van Lenteren, J.C., A.J.M. Loomans, D. Stathas, G.J., P.A. Eliopoulos, D.C. Babendreier and F. Bigler. 2008. Kontodimas and J. Giannopapas. 2001. Harmonia axyridis: an environmental Parameters of reproductive activity in risk assessment for Northwest Europe. females of Harmonia axyridis BioControl 53: 37–54. (Coleoptera: Coccinellidae). Eur. J. Majerus, M.E.N., V. Strawson and H. Roy. Entomol. 98: 547-549. 2006. The potential impacts of the arrival of the harlequin ladybird, Harmonia KEYWORDS: Harmonia axyridis, axyridis (Pallas) (Coleoptera: invasive ladybirds, native ladybirds, Coccinellidae), in Britain. Ecol. Entomol. biocontrol agents, Greece, overwintering, 31: 207-215. Aphis fabae, Toxoptera aurantii, Aphis gossypii, Aphis spiraecola.

ENTOMOLOGIA HELLENICA 17 (2007-2008): 42-51 51

Δεδομένα ζχεηικά με ηο Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) ζηην Ελλάδα. Μια πεπίπηωζη εξωηικού αππακηικού που απέηυχε να εγκαηαζηαθεί;

Δ .Υ. ΚΟΝΣΟΔΗΜΑ΢1, Γ.Ι. ΢ΣΑΘΑ΢2 ΚΑΙ Α.Φ. ΜΑΡΣΙΝΟΤ1

1Μπενάκειο Φσηοπαθολογικό Θνζηιηούηο, Εργαζηήριο Ενηομολογίας και Γεωργικής Ζωολογίας, Ση. Δέληα 8, 14561 Κηθιζιά 2Τετνολογικό Εκπαιδεσηικό Ίδρσμα Καλαμάηας, Στολή Τετνολογίας Γεωπονίας, Τμήμα Φσηικής Παραγωγής, Εργαζηήριο Γεωργικής Ενηομολογίας & Ζωολογίας, 24100 Ανηικάλαμος

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Καηά ηε δηάξθεηα 1994-1999 εθαηνληάδεο ρηιηάδεο αθκαία ηνπ Harmonia axyridis εμαπνιύζεθαλ ζε δηάθνξεο θαιιηέξγεηεο πξνζβεβιεκέλεο από αθίδεο (εζπεξηδνεηδή, θαζόιηα, θαιακπόθη θ.α.) θαζώο θαη ζε δηάθνξα θαιισπηζηηθά θπηά ζε αζηηθό πεξηβάιινλ, ζηελ θεληξηθή θαη λόηηα Ειιάδα (θπξίσο ζηελ Αηηηθή θαη ζηελ Πεινπόλλεζν) θαζώο θαη ζε δηάθνξα λεζηά. Από ην 1995-2007 πξαγκαηνπνηήζεθαλ δεηγκαηνιεςίεο ζε δηάθνξεο πεξηνρέο, θάζε άλνημε πξηλ από ηηο λέεο εμαπνιύζεηο, κε ζθνπό λα δηαπηζησζεί εάλ ην H. axyridis θαηόξζσζε λα δηαρεηκάζεη. Τελ άλνημε ηνπ 1995 (δειαδή ηελ άλνημε κεηά ηηο πξώηεο εμαπνιύζεηο) θαζώο θαη ηελ άλνημε ησλ εηώλ 1996-1997 θαη 2000-2007, δελ θαηαγξάθεθε ην H. αxyridis ζε θακία από ηηο πεξηνρέο όπνπ είρε εμαπνιπζεί. Μόλν ηελ άλνημε ησλ εηώλ 1998 θαη 1999 κηθξέο απνηθίεο (<50 άηνκα) βξέζεθαλ λα δηαρεηκάδνπλ ζε πεξηνρή ηεο Αηηηθήο. Τα παξαπάλσ απνηειέζκαηα δείρλνπλ όηη νη πιεζπζκνί ηνπ H. axyridis πνπ εμαπνιύζεθαλ δελ θαηόξζσζαλ λα εγθαηαζηαζνύλ ζηελ Ειιάδα, παξόιν πνπ ην εμσηηθό απηό αξπαθηηθό απνηέιεζε ζεκαληηθό παξάγνληα θαηαπνιέκεζεο ζηηο πεξηνρέο πνπ εμαπνιύζεθε. Επίζεο δεδνκέλα πνπ θαηαγξάθεθαλ ζρεηηθά κε ηνπο πιεζπζκνύο ησλ ηζαγελώλ εηδώλ Coccinellidae πνπ ππήξραλ πξηλ θαη κεηά ηηο εμαπνιύζεηο ηνπ H. axyridis, απνηεινύλ έλδεημε γηα κε αξλεηηθέο επηπηώζεηο ηνπ H. axyridis ζηελ ηζαγελή θνηλόηεηα ησλ αθηδνθάγσλ Coccinellidae ηεο Ειιάδαο. Παξόια απηά, δεδνκέλσλ ησλ αξλεηηθώλ επηπηώζεσλ πνπ έρεη πξνθαιέζεη ζε ρώξεο ηεο Επξώπεο θαη ηεο Ακεξηθήο δελ ζπλίζηαηαη κε θαλέλαλ ηξόπν ε επαλέλαξμε ησλ εμαπνιύζεσλ ηνπ Η. axyridis ζηνλ ειιεληθό ρώξν. Αληηζέησο, πξέπεη λα νξγαλσζεί έλα πξόγξακκα παξαθνινύζεζεο θαη θαηαγξαθήο Coccinellidae θαη H. axyridis, νύησο ώζηε λα θαηαγξαθεί εγθαίξσο ηπρόλ εηζβνιή ηνπ εμσηηθνύ αξπαθηηθνύ από ηελ βόξεηα Επξώπε.