©Staatl. Mus. f. Naturkde Karlsruhe & Naturwiss. Ver. Karlsruhe e.V.; download unter www.zobodat.at

Andrias 20 (2014): 51-55; Karlsruhe, 1.12.2014 51

Alien in Belgium: a threat for our biodiversity or agroforestry?*

Mi c h e l De t h i e r & Fr é d é r i c Ch é r o t

Abstract documented and analyzed in European e.g. During the two past decades, various nonindigenous species of Heteroptera (Insecta, ) were col- Austria (Ra b i t s c h 2008), Great Britain (Ki r b y et lected for the first time in Belgium. We provide an an- al. 2001), The (Au k e m a 2003) and notated checklist of these exotic species and we briefly foreign countries e.g. Canada (Wh e e l e r et al. discuss the potential consequences of their presence 2006). The estimation of the magnitude of the- in our country. se changes, their causes, and their ecological consequences are not always easy to establish. Keywords: Hemiptera, Heteroptera, Belgium, alien Some authors proposed a methodological ap- species. proach, dividing the set of all species of an area or country into different categories (Ki r b y et al. Kurzfassung 2001, De t h i e r & Ba u g n é e 2002): Exotische Wanzen (Insecta: Heteroptera) in Bel- gien: Eine Bedrohung für unsere Artenvielfalt oder – Species known for a long time, without signifi- Land- und Forstwirtschaft? cant alterations of occurrences and distribution. Während der letzten beiden Jahrzehnte sind mehrere – Species known for a long time (for example: nichteinheimische Arten von Wanzen (Insecta: Hetero- XIXth century) but that appear to have recently ptera) neu in Belgien aufgetreten. Wir stellen diese expanded or reduced their range. Arten mit kurzen Kommentaren vor und besprechen – Species recently discovered but known for kurz die möglichen Auswirkungen ihres Auftretens in many years in the surrounding areas and pro- Belgien. bably overlooked in the past (for taxonomical or biological reasons). Authors – Finally “exotic” species recently arrived. The Dr. Mi c h e l De t h i e r , Agro Bio Tech Gembloux, Universi- ty of Liège, B-4030 Liège; exotic species could have been introduced by E-Mail: [email protected]. man, voluntary or accidentally, or could have Dr. Fr é d é r i c Ch é r o t , Direction de la Nature et de l’Eau, altered their range themselves. They can be DEMNA, DG03, SPW, B-5030 Gembloux; classified according to their origins or accor- E-Mail: [email protected] ding to the stage of their colonization (first arrival, establishment of a viable population, expansion of the species etc.). Introduction In the present work, we focus on this last catego- Ten years ago, Ba u g n é e et al. (2003) published ry. We provide an annotated checklist of the exo- a list including 624 species of Heteroptera (In- tic species collected in Belgium during the two secta, Hemiptera) for Belgium. Today, the spe- past decades presented by chronological order cific richness of our fauna is higher. The family of the first occurrence and we briefly discuss the alone accounts at least 15 additional potential consequences of their presence in our species. Among these new species for the country. country, we observe numerous “exotic” spe- cies, most of them originating from the Medi- Results terranean region, the remainder coming from Nezara viridula (Li n n a e u s , 1758) (Pentatomidae). other continents, including North America and This big green bug was reported in Belgium for Southeast Asia. the first time by Sc h m i t z (1986), who found a Several recent changes in the local Heteroptero- male collected in Auderghem in 1950! Later Ga l - fauna – including arrival of alien species – were l a n t (1996) and De t h i e r & Ga l l a n t (1998) pub- lished six additional occurrences. Nowadays, specimens are frequently found in student col- lections preserved at AgroBioTech (Gembloux) * Dr. Ch r i s t i a n Ri e g e r , honouring his 70th birthday. or mentioned on several Internet Web sites. ©Staatl. Mus. f. Naturkde Karlsruhe & Naturwiss. Ver. Karlsruhe e.V.; download unter www.zobodat.at

52 Andrias 20 (2014)

This bug is now present in all the tropical and Xylocoris afer (Re u t e r , 1884) (Anthocoridae). In subtropical regions (Indo-australian, Ethiopian, the harbour of Antwerp, on tropical woods im- Nearctic and Palearctic). In Europe, the species ported from Gabon, in 2006 and 2009 (Ch é r o t is reported from the whole Mediterranean basin et al. 2011). and the Balkan region. It is a pest on cultivated Corytucha ciliata (Sa y , 1832) (Tingidae). Since plants favored by tropical green-houses, probably 2006 and 2007 in Antwerp (several places); also introduced in numerous areas by importation of in Brussels (2007) and East Flanders (2008) fruits and vegetables, but is also able to colonize (Au k e m a et al. 2007, 2009). Since, found in nu- remote places due to its flying abilities. merous other places. This Nearctic species (the flavilinea (Co s t a , 1860) (Miridae). genus is restricted to the New World) was cited Collected for the first time in Belgium in 1994, for the first time in Europe (Italy) in 1964 (Se r v a - this bug was regarded as endemic in Italy until d e i 1966). Today, C. ciliata is present everywhere its recent extension in Western Europe (Ch é r o t in South, Central and East Europe. The species 1998). is a pest on different species of planetrees, espe- Tuponia hippophaes (Fi e b e r , 1861) (Miridae). cially in the U.S.A. The sucking on the underside Collected for the first time in Belgium onTamarix of the leaves induce the appearance of mould. sp. in great numbers at De Panne, West Flanders Amphiareus obscuriceps (Po pp i u s , 1909) (An- in August 2003 (Ch é r o t & Ba u g n é e 2004); also re- thocoridae). In the provinces of East Flanders, cently found in the province of Namur (Cl a e r b o u t Antwerp and Liège since 2007 (Au k e m a et al. leg. and in litt.). Originating from the Mediterra- 2007). From Japan, Korea, South Siberia, Ne- nean basin, Eastern and Central Europe and liv- pal… First record in Europe in 1987 (Pé r i c a r t & ing on Tamarix spp. – a genus not indigenous in St e h l i k 1998) and today all over the continent. Belgium, sometimes planted in gardens. The bug preys upon tiny (such as Pso- Stephanitis takeyai Dr a k e & Ma a , 1955 (Tingi- coptera) in dead organic matter. dae). Observed first in Belgium in 2003 and 2004 Arocatus longiceps St å l , 1872 (Lygaeidae). In in the provinces of East Flanders, Antwerp and Belgium since at least 2007, found also in 2008 Limburg (Au k e m a et al. 2005a); the species has and 2009 in the provinces of West and East Flan- been known in Europe since 1994 (Au k e m a 1996). ders, Antwerp and Liège (Au k e m a et al. 2009). This Japanese bug lives on Pieris japonica, an From Southeastern Europe (remarkable expan- ornamental plant frequently imported for garden- sion since 1995), Caucasus, Near and Middle ing. Presently S. takeyai is present in India, North East. On planetrees, where nymphs and adults America and, in Europe, in The Netherlands, feed mainly on seeds. Very close to A. roeselii Belgium, Italy, Germany and Great Britain. The (Sc h i l l i n g , 1829), much rarer in Belgium (Au k e m a sucking induces yellowing and leaf drop. et al. 2007). Nysius huttoni F. B. Wh i t e 1878 (Lygaeidae). First rhododendri (Do l l i n g , 1972) (Miri- records in Belgium in West and East Flanders dae). In East-Flanders, Antwerp and Brabant, in and in Brabant in 2003-2004. In The Netherlands 2007 (Au k e m a et al. 2007). Prey upon other small since 2002 (Au k e m a et al. 2005b, 2007). Imported insects in the terminal buds of . from New Zealand, where N. huttoni is an eco- Originated from the eastern U.S.A. but described nomically important species. In New Zealand, from London (Do l l i n g 1972). several cultivated plants including Brassica sp., Leptoglossus occidentalis He i d e m a n n , 1910 (Co- lucerne, clover and wheat are attacked. Control is reidae). In Belgium since 2007 (Ostend, West difficult because usually the bug feeds on weedy and East Flanders). Since 2008 in the provin­ plants of waste lots and roadsides in the vicinity ces of Antwerp and Namur and now all over the of fields and only migrates to crops in dry years. country (Au k e m a & Li e b e e r 2007, Au k e m a , Br u e r s Dyroderes umbraculatus (Fa b r i c i u s , 1775) (Pen- & Vi s k e n s 2009, Ch é r o t et al. 2013, Cl a e r e b o u t tatomidae). Observed for the first time in Belgium 2011). Ch é r o t et al. mention 392 observations in in 2004 and subsequently in 2005, in a nature our country and note that during 2010-2011 the reserve near Brussels (the “Moeraske”, i.e. the expansion of the species was exponential. L. oc­ little marsh) (Br a c k e et al. 2006). D. umbraculatus cidentalis originated from the western U.S.A. but is a Mediterranean and an East European spe- since the fifties, the species expanded eastward. cies living on different Galium species. Its north- It was discovered for the first time in Europe in bound expansion is perhaps natural (Br a c k e et 1999 near the harbour of Venice (Italy). Today al. 2006). the species is present everywhere in South and ©Staatl. Mus. f. Naturkde Karlsruhe & Naturwiss. Ver. Karlsruhe e.V.; download unter www.zobodat.at

De t h i e r & Ch é r o t : Alien Heteroptera in Belgium 53

Central Europe. L. occidentalis is considered by climatic changes (D. umbraculatus, N. viri­ as a pest in North America because it feeds on dula, R. nebulosa), most of the exotic species sprouts and seeds of different conifers (mainly observed in our country during the two past de- Pinus) but also in California on Pistacia vera. cades were introduced accidentally by man as a Up to now, no damages have been observed consequence of ornamental plants (for example in Europe. The bug flies well and overwinters in D. flavilinea, T. hippophaes, S. takeyai etc.), exo- houses, sometimes in very high numbers, an ad- tic fruits and vegetables (for example N. hutto­ ditional nuisance (Mi t c h e l l 2000). ni, maybe some N. viridula) or tropical woods Fulvius anthocoroides (Re u t e r , 1875) (Miridae). (F. anthocoroides, N. lestoni,…) importations. In the harbour of Antwerp, on tropical woods, in Consequently, the main doorways seem to be 2008, 2009 and 2011 (Ch é r o t et al. 2011 and harbours like Antwerp but airports could be also 2013). This bug, described from the harbour of involved, as they are for other groups of insects, Rouen (France), comes from Africa but now is like mosquitos. cited from Seychelles, India, Sri Lanka, Taiwan, Ra b i t s c h (2008) considers that 42 exotic species Central and South America, Antilles, U.S.A. and of Heteroptera are now introduced in Europe, 12 some Pacific Islands. The bug feeds on larvae of of them coming from other continents, a figure xylophagous beetles and moths. already not up to date. It is difficult to predict the Neuroctenus lestoni Ko r m i l e v , 1966 (Aradi- development of such introductions: Establish- dae). In the harbour of Antwerp, under the bark ment (i.e. installation of permanent populations) of trunks of tropical woods, in 2009 (Ch é r o t et or extinction? The factors influencing the fate al. 2011). This species comes from Ghana and of the colonizers are very numerous (Ra b i t s c h Cameroun and, like the other Aradidae, is prob- 2008) and the “rule of ten” – one of 10 import­ ably mycetophagous. ed species would settle in the wild, one of 10 of Tropidosteptes pacificus( Va n Du z e e , 1921) (Miri- such introduced species would become esta- dae). In Deurne (near Antwerp harbour) in 2009 blished and one of 10 such established species (Au k e m a 2010); also in The Netherlands (Au- would become “invasive” (Wi l l i a m s o n & Fi t t e r k e m a , Sc h w a r t z & De n Bi e m a n 2009). Imported 1996) – knows numerous exceptions. Belonging (as eggs?) from British Columbia (Canada) and to the exotic Heteroptera recently found in Bel- north-east U.S.A. with plant material of North gium, some species such F. anthocoroides, F. American ash tree (Fraxinus pennsylvanica). carayoni, F. subnitens, N. lestoni and X. afer will Also on poplar and maple. The bug is a pest on probably be not able to start permanent popula- ornamental ashes and induces foliar chlorosis tions. Some other, such as A. longiceps, C. cilia­ and wilting of branches. ta, D. flavilinea, N. huttoni, L. occidentalis and N. Fulvius subnitens (Po pp i u s , 1909) (Miridae). In viridula are obviously established, the status of harbour of Antwerp, on tropical woods, in 2009 remaining species being unclear. and 2011 (Ch é r o t et al. 2011). This species, de- Are these invading bugs threats for our agricu- scribed from Papua, is now largely distributed lture, horticulture or forestry? Most of them are around the world. It is cited from some places relatively minor pests in their country of origin in U.S.A, Africa, Indonesia and Pacific Islands. and don’t seem to be really injurious in Belgi- Feed on beetle larvae. um. However, the cases of L. occidentalis and N. Fulvius carayoni Pl u o t -Si g w a l t & Ch é r o t , 2013 huttoni could become problematic and should be (Miridae). A species found in 2011, also in the monitored. harbour of Antwerp, on tropical woods. Distribut- Are these invading bugs threats for our environ- ed in West and Central Africa. ment? A protocol of impact estimation of alien invading species on Belgian natural ecosystems Discussion has been established (http://ias.biodiversity.be), Au k e m a (2003) emphasizes that if turnover of based on various criteria sometimes difficult to species of local fauna may be considered a appreciate, particularly for relatively poorly known natural process, habitat changes, international Heteroptera (for example: dispersion potential). trade and global warming have largely contri- It seems nevertheless, the impact on the eco­ buted to the recent changes observed in Dutch systems of a majority of alien Heteroptera recent- Heteropterofauna. The same is probably true ly introduced in Belgium should be restricted. This in Belgium. Although the arrival in Belgium of would be the case even for a large and invasive some Mediterranean species may be explained species such L. occidentalis (Ch é r o t et al. 2013). ©Staatl. Mus. f. Naturkde Karlsruhe & Naturwiss. Ver. Karlsruhe e.V.; download unter www.zobodat.at

54 Andrias 20 (2014)

Do these exotic species represent a threat for Au k e m a , B., Br u e r s , J. & Vi s k e n s , G. (2007): Nieuwe the Belgian biodiversity? The ecological biodiver- en zeldzame Belgische wantsen II (Hemiptera: sity is function of the specific richness and the Heteroptera). – Bulletin de la Société royale belge evenness, the relative abundance of species in d‘Entomologie 143: 83-91. Au k e m a , B., Br u e r s , J. & Vi s k e n s , G. (2009): Nieuwe the community. Initially, the installation of exotic en zeldzame Belgische wantsen III (Hemiptera: species in a community will increase the local Heteroptera). – Bulletin de la Société royale belge specific richness and then the biodiversity. La- d‘Entomologie 145: 25-31. ter, the effect of the exotic one will depend on Au k e m a , B. & Li e b e e r , R. (2007): Eerste waarneming its impact on the native species and on their re- van Leptoglossus occidentalis in België (Hetero­ lationships in the community: If different native ptera: Coreidae). – Bulletin de la Société royale bel- species disappear or if the evenness is strongly ge d’Entomologie 143: 92-93. reduced, the biodiversity will be also modified. Au k e m a , B., Sc h w a r t z , M. & De n Bi e m a n , K. (2009): However, this will not necessarily be the case. A Tropidosteptes pacificus (Va n Du z e e , 1921), another replacement of a native species by an exotic one Nearctic mirid in Europe (Hemiptera: Heteroptera: Miridae: ). – Zootaxa 2135: 65-68. does not modify ecological biodiversity as de- Ba u g n é e , J.-Y., De t h i e r , M., Br u e r s , J., Ch é r o t , F. & Vis- fined by Shannon index even if it is a loss in the k e n s , G. (2003): Liste des punaises de Belgique (He- biological heritage. Because the effects of exotic miptera Heteroptera). – Bulletin de la Société royale Heteroptera establishment in Belgium – a step belge d’Entomologie 139: 41-60. not passed yet for some species – remain largely Br a c k e , A., Co pp é e , J.-P., Do o r n a e r t , A. & Ha n s s e n s , B. hypothetical, it is difficult to predict an eventual (2006): Note sur la découverte en Belgique de Dyrode­ impact on biodiversity. res umbraculatus (Fa b r i c i u s , 1775) (Heteroptera: Pen- tatomidae) dans un espace vert de la Région bruxel- Acknowledgments loise. – Notes fauniques de Gembloux 59: 56-58. We are very grateful to Mrs. J. Bo r t e l s (Gembloux Ch é r o t , F. (1998): Au sujet de Deraeocoris (s. str.) fla­ AgroBioTech), M. J. Br u e r s (Antwerp), M. S. Cl a e r b o u t vilinea (Co s t a , 1862) et de Deraeocoris (s. str.) ruber (Centre Marie Victorin, Treigne), M. J. Co n s t a n t (Institut (Li n n é , 1758) (Insecta, Heteroptera : Miridae). – Lam- des Sciences naturelles, Brussels) and Mrs. G. Vi s k e n s billonea 98(4): 523-529. (Antwerp) for the numerous data and specimens provi- Ch é r o t , F. & Ba u g n é e , J.-Y. (2004): L’hétéroptère Miridae ded to the second author, to M. A. Ma t o c q (Muséum na- Tuponia hippophaes (Fi e b e r , 1861) nouveau pour la tional d’Histoire naturelle, Paris) for the identification of faune de Belgique: une espèce en expansion ? – Xylocoris from Antwerp and to Dr. P. L. Mi t c h e l l (Win- Bulletin de la Société royale belge d’Entomologie throp University, Rock Hill) and Dr. B. Au k e m a (Renkum) 140: 27-30. for a private review of the manuscript. Ch é r o t , F., Au k e m a , B., Br u e r s , J. & Vi s k e n s , G. (2011): Exotic species of Aradidae and Miridae (Insecta: Hemiptera, Heteroptera) recently found in Antwerp References Harbour, Belgium. – Bulletin de la Société royale Au k e m a , B. (1996): Stephanitis takeyai on Pieris japo­ belge d’Entomologie 147: 15-19. nica. – Mededelingen Plantenziektenkundige Dienst Ch é r o t , F., Ba u g n é e , J.-Y., Cl a e r e b o u t , S., De r u m e , M. 179: 46-47. & He n i n , J.-M. (2013): Leptoglossus occidentalis Au k e m a , B. (2003): Recent changes in the Dutch He­ He i d e m a n n , 1910 (Hemiptera Heteroptera Coreidae) teroptera fauna (Insecta: Hemiptera). – Proceedings en Belgique: état des lieux de l’invasion quatre ans 13th International Colloque EIS, September 2001: après la première mention pour le pays. – Bulletin 39-52. de la Société royale belge d’Entomologie 149. Au k e m a , B. (2008): De invasieve noord-amerikaanse Cl a e r e b o u t , S. (2011): Conquête de l’Europe par une wants Leptoglossus occidentalis bereikt ook Neder- punaise nord-américaine invasive: la punaise amé- land (Heteroptera: Coreidae). – Nederlands Faunis- ricaine des pins (Leptoglossus occidentalis He i d e - tische Mededelingen 29: 78-80. m a n n , 1910). – L’Erable 35(1): 14-21. Au k e m a B., (2010): Nieuwe en zeldzame Belgische De t h i e r , M. & Ba u g n é e , J.-Y. (2002): Estimation des mo- wantsen IV (Hemiptera: Heteroptera). – Bulletin de difications récentes de la faune des hétéroptères de la Société royale belge d‘Entomologie 146: 181-183. Belgique: approche méthodologique. – Bulletin Insti- Au k e m a , B., Br u e r s , J. & Vi s k e n s , G. (2005a): Nieu- tut royale de Science naturelle Belgique, Biologie 72 we en zeldzame Belgische wantsen (Hemiptera: (suppl.): 119-123. Heter­optera). – Bulletin de la Société royale belge De t h i e r , M. & Ga l l a n t , J.-B. (1998): Hétéroptères re- d‘Entomologie 141: 33-37. marquables pour la faune belge. – Natura Mosana Au k e m a , B., Br u e r s , J. & Vi s k e n s , G. (2005b): A New 51(4): 75-86. Zealand endemic Nysius established in The Nether- Do l l i n g , W.R. (1972): A new species of Dicyphus Fi e b e r lands and Belgium (Heteroptera: Lygaeidae). – Bel- (Hem., Miridae) from southern England. – Entomolo- gian Journal of Entomology 7: 37-43. gist’s Monthly Magazine 107: 244-245. ©Staatl. Mus. f. Naturkde Karlsruhe & Naturwiss. Ver. Karlsruhe e.V.; download unter www.zobodat.at

De t h i e r & Ch é r o t : Alien Heteroptera in Belgium 55

Ga l l a n t , J.-B. (1996): Note hémiptérologique. Ne­ Heteroptera, Miridae, Cylapinae, Fulviini). – Zoosys- zara viridula (L.) (Heteroptera, Pentatomidae), tema 35(1): 45-68. espèce en progression sur notre territoire? – Bul- Ra b i t s c h , W. (2008): Alien true bugs of Europe (Insec- letin de la Société royale belge d’Entomologie ta : Hemiptera : Heteroptera). – Zootaxa 1827: 1-44. 132: 405-406. Sc h m i t z , G. (1986): Captures “insolites” d’Hétéroptères. Ki r b y , P., St e w a r t , A. & Wi l s o n , M. (2001): True bugs, – Bulletin de la Société royale belge d’Entomologie leaf- and planthoppers and their allies. – In: Ha wk s - 122: 33-37. w o r t h , D. L. (ed.): The Changing Wildlife of Great Se r v a d e i , A. (1966): Un Tingide nearctico comparso in Britain and Ireland. – Systematics Association Spe- Italia (Corythucha ciliata Sa y ). – Bollettino della Soci- cial Volume Series 62: 262-299. eta Entomologica Italiana 96: 94-96. Mi t c h e l l , P. L. (2000): Chapter 11. Leaf-Footed Bugs Wh e e l e r , A. G. Jr., He n r y , T. J. & Ho e b e k e , E. R. (2006): (Coreidae). – In: Sc h a e f e r , C. W. & Pa n i z i , A. R. (eds): Palearctic plant bugs (Hemiptera, Miridae) in New- Hetero­ptera of Economic Importance: 828 pp.; CRC foundland, Canada: First North American records Press. for Phytocoris longipennis Fl o r and Pilophorus cin­ Pé r i c a r t , J. & St e h l í k , J. L. (1998): Amphiareus obscuri­ namopterus (Ki r s c h b a u m ), new records of eight other ceps (Po pp .) in the Czech Republic and in the Balkan species, and review of previously reported species. Peninsula (Heteroptera: Anthocoridae). – Acta Musei – In: Ra b i t s c h , W. (ed.): Hug the Bug. For the love of Moraviae, Scientiae biologicae 83: 217-218. true bugs. Festschrift zum 70. Geburtstag von Er n s t Pl u o t -Si g w a l t , D. & Ch é r o t , F. (2013): Données bio­ He i s s . – Denisia 19: 997-1014. logiques et anatomiques, régime alimentaire et taxi­ Wi l l i a m s o n , M. & Fi t t e r , A. (1996): The varying success nomie d’un nouveau Fulvius afrotropical (Insecta, of invaders. – Ecology 77: 1661-1666. ©Staatl. Mus. f. Naturkde Karlsruhe & Naturwiss. Ver. Karlsruhe e.V.; download unter www.zobodat.at

56 Andrias 20 (2014)