ENTOMOLOGIA HELLENICA 20 (2011): 75-81

First record of the Nearctic (Heteroptera, , Harpactocorinae) in Europe

P.V. PETRAKIS1* AND P. MOULET2

1 N.AG.RE.F., Institute for Mediterranean Forest Ecosystem Research, Laboratory of Entomology, Terma Alkmanos, 11528 Athens, Greece 2 Museum Requien, rue Joseph Vernet, F-84000 Avignin, France

ABSTRACT

The Nearctic assasin bug Zelus reinardii was found for the first time in Attica, Greece, Europe. This species is a generalist predator which can contribute to the control of pests. This is also a known predator of several biological control agents of pests. Therefore, its naturalization in Greece is potentially problematic in economic settings since the insect may act as both an intraguild and a beneficial predator. The risky nature of importation in other areas (e.g. Hawaii) showed the possibility of these ecological roles.

KEYWORDS: Zelus renardii, distribution, invasive species.

Introduction Invasion of assassin bugs in non-native The leafhopper assassin bug Zelus renardii regions usually triggers interception measures Kolenati, 1857 (, Reduviidae, because of their commonly broad diet. Such Harpactocorinae) was found in three predatory heteropterans are known to also localities in Attica, Greece for the first time switch to plant feeding increasing their in Europe. It is native of the Nearctic region survivorship (Stoner et al. 1975, Cohen 1990, (continental USA, Mexico, Guatemala) and Torres and Boyd 2009). has been putatively introduced into Hawaii, Amongst the c. 6900 species of assassin the Philippines and Jamaica (Maldonado bugs known worldwide, including about 110 1990) and recently reported from Chile species in Europe and 40 species in Greece, (Curkovic et al. 2004). This species has been only 3 species (two cryptogenic and one considered as a generalist predator with alien) are adventitious to Europe (Putshkov restricted ability to suppress pests (Frank and and Putshkov 1996, Rabitsch 2008, 2010, Slosser 1996, Rosenheim et al. 2004). Aukema 2011). This work reports on the It was recently discovered that Z. introduction of the Nearctic species, Z. renardii disrupts classical biological control renardii, to Greece. programs by exhibiting strong intraguild predation (IGP) on other intermediate The records predators that cause population reduction of crop pests (Ables 1978, Cohen and Tang Zelus renardii was found in three locations in 1997, Cisneros and Rosenheim 1998, the Attica prefecture in Greece. The first Rosenheim et al. 1999, Howarth and Preston finding was a recently captured dead male 2002, Ponsard et al. 2002, contra Law and insect within the glass housing of a road light Rosenheim 2011). in the area Thracomacedones – Olympiako

*Corresponding author, e-mail: [email protected] 76 ENTOMOLOGIA HELLENICA 20 (2011): 75-81

Chorio (38o 7' 46''N, 23o 46' 25''E) on 15th rostrum thin and elongate; pronotum, August 2010. We also found this species elongate trapezoidal, lateral angles obtuse. eating a Synophropsis lauri (Horváth, 1897) The coloration varies greatly but is generally (Hemiptera: Auchenorrhyncha: Cicadellidae) cryptic. captured in an insect net in the district Zelus renardii is closely related to Z. Alsoupolis – Olympiako Stadio (38o 2' 10''N, luridus and Z. cervicalis but can be 23o 46' 25''E), between August 2nd, 2011 and distinguished from them by the reddish September 2nd, 2011 (Moulet collection); the pronotum, hemielytra and legs (cf. green in Z. prey was immobilized by the sticky raptorial luridus), apex of femora without a large and forelegs of the assassin bug. This assassin dark ring (cf. present in Z. luridus); and bug was also found in the pinewood outside humeral angles of pronotum obtuse (cf, the Forest Entomology laboratory in the elongate and acute tooth in Z. luridus, at most Institute of Mediterranean Forest Ecosystem with minute subtuberculate process in Z. (37o 58' 30'', 23o 46' 40''; August 29th, 2011). cervicalis) and (length) ≥ 5.8 × (width) in It is assumed that a single generation of males [for an identification key see Hart Z. renardii occurs in Greece because of the 1986; a taxonomic description of the extensive sampling effort in Attica (i.e. is urgently needed and is undertaken by G. approximately100 fortnightly inspected traps Zhang under the supervision of C. Weirauch]. all over the year). Biology and Distribution Identification Zelus renardii is a commonly encountered Zelus Fabricius, 1803 (Fig. 1) belongs to the species of Reduviidae throughout its most diverse genus of the family Reduviidae. geographic range (Hart 1986) and is usually It is represented by 60 species widely found in alfalfa, sweetpotato, potato and distributed in the American continent but cotton crops where it preys on all types of with the majority of species having restricted , even on intermediate predators distribution (Maldonado 1990). Seven (Rosenheim et al. (1999) for the effect of species are widespread and found both in intraguild predation (IGP) on the introduced North and South America [i.e. cervicalis predator Chrysoperla carnea (Stephens) for Stål, 1872; longipes (Linnaeus, 1767); classical biological control; Müller and minutus Hart, 1987; nugax Stal, 1872; Brodeur (2002) for the effect on biological renardii Kolenati, 1857; tetracanthus Stal, control in conservation; Law and Rosenheim 1862; vespiformis Hart, 1987] (Maldonado (2011) when the intermediate predator is 1990). Geocoris pallens Stål and the herbivore is Some species are known to invade Lygus hesperus Knight; Hemptinne et al. southern biotopes where they can become (2011) when the intermediate predator is a harmful to local insects (Funasaki et al. ladybird beetle) and it frequents the catches 1988, Rosenheim et al. 2004). of sweep nettings. In the source region the This species is recognized by the insect is a sit-and-wait predator and has a following characters: body length 12 – 16 population peak in late summer but smaller mm; cryptozoic coloration; body gracile populations exist in mid-summer (Ali and (thin and slender) with thin and long legs; Watson 1978). The same authors conducted the head is elongate and eyes not prominent; PETRAKIS AND MOULET: Zelus renardii a new American immigrant in Europe 77

FIG. 1. The insect Zelus reinardii, dorsal view.

Discussion laboratory experiments for the determination Mediterranean species of true bugs are of optimal temperature conditions for the repeatedly introduced in northern and mid- development and survival of Z. renardii. The latitude European countries but are usually o o greatest longevity occurs at 25 C but at 20 C go unnoticed, rarely reported in the the survival was substantially high except for literature, and do not often become the first instar for which the survival is 46%. established (Rabitsch 2008). In contrast, the Zelus renardii is able to vary many life cycle Nearctic species Z. renardii originated in parameters and morphometric values such as climatic conditions very similar to the the survival in various temperature regimes northern Mediterranean. As a result it is an and the duration of each instar. invasion risk for European countries. With regard to the classical biological In the invaded region the voltinism of Z. control Reduviidae being polyphagous may renardii has not yet been studied. However, not be useful as controlling agents of specific since the insect was trapped in late August – pest species. However, they are useful in early September it can be speculated that the situations where a variety of pest insect insect has an additional spring generation species exist. In all these situations reduviids (Ali and Watson 1978). The low population in general and Z. renardii in particular are levels are shown by the very low captures of suitable because they can kill significantly the insect in the set of more than one more prey than they can consume (Ambrose hundred fortnightly inspected traps. 2001). A problem that may arise when invading Z. renardii become abundant is phytophagy.

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When the prey is not enough or it cannot be Chagas disease. However, the research in easily captured the insect switches from these groups is scarce and a review is zoophagy to phytophagy to obtain the urgently needed. In addition haematophagy necessary nutrients (Stoner et al. 1975, evolved independently in different groups of Cohen 1990, Rosenheim et al. 1999, Torres Triatominae together with the fact that a and Boyd 2009). Field observations in switch to this feeding mode is not French Guiana and lab experiments have uncommon in reduviid bugs (Schaefer 2000, shown that Zelus araneiformis Haviland, Baena 2011). Diet shift to haematophagy 1931 is able to complete its whole larval cannot be excluded for Z. renardii since development only feeding on Cecropia trees research on digestive enzymes of Z. renardii (Bérenger and Pluot Sigwalt 1997). showed that there are many orderly Blatchley (1926) wrote that “our species … modifications of proteolytic enzymes that usually have the front legs thickly covered make this predatory insect more efficient with pollen grains, bits of petals, small seeds consumer of proteins than haematophagous and other minute parts of plants …” insects (Cohen 1993). As a result many However, this phytophagy does not decrease insects constitute a risk factor as they are longevity when the insect is a predator of hosts of an unknown number of pathogens pests of transgenic Bt-cotton (Ponsard et al. and the bites in birds, domestic and 2002). humans from newly imported assassin bugs The ability of the insect for an extra-oral should be carefully examined. digestion make it an efficient predator of The measures taken for the interception many prey sizes (Cohen 1993, Cohen and of the insect are the ones already applied for Tang 1997) from the very early the quarantine insects in Europe. However, developmental stages after hatching from the the ecological role of the insect is not exactly egg because of the sticky substance in the known and for this it is premature to include front legs which immobilizes prey (Law and this in the list of quarantine insects of the Sediqi 2010). However, when exists an European Plant Protection Organization intermediate predator, which is more prey (EPPO Reporting Service 2010). In the specific then Z. renardii exhibits IGP which meanwhile the examination of planted disrupts prey suppression. A supporting material and commercial plants has to be paradigm is the intermediate not practiced at the points of introductions cannibalistic predator Chrysoperla carnea (harbors, airports, and railway stations) in (Stephens, 1836) (Chrysopidae) (Cohen and lack of more specific tests. It is amazing that Tang 1997) for the disruption of the in many countries there are no common tests suppression; contra for the annibalistic that must be done on introduced bio-control predator Geocoris pallens (Stål, 1854) (Law parasitic agents despite the fact that many and Rosenheim 2011) for the enhancement cases of local extinctions have been reported of pest suppression. Nevertheless the (Petrakis 2007). situation is not easily decided and the dust from the quarrel of pest suppression has not Acknowledgements yet settled in IGP. Zelus renardii belongs in the subfamily We are deeply indebted to Nicoletta Harpactocorinae that is the most rich in Souliotis, Theodoros Kritikos and species. This subfamily differs from the Panaghiotis Tsopelas for providing Triatominae one that contains the biological material and Leonidas haematophagous insects which are capable Davranoglou for providing important in hosting protozoa species of genus literature. Emily Lahlou is thanked for Trypanosoma and are associated with helping in servicing and the sorting of the

PETRAKIS AND MOULET: Zelus renardii a new American immigrant in Europe 79

content of light traps. George Karetsos and Sylvia Papika are especially thanked for the Cohen, A.C. and R. Tang.1997. Relative information they gave on the planted species prey weight influences handling time and in Attica for the occasion of the 2004 biomass extraction in Sinea confusa and Olympic games. Zelus renardii (Heteroptera: Reduviidae). Environ. Entomol. 26: 559-565. References Cohen, A.C. 1990. Feeding adaptations of some predaceous Hemiptera. Ann. Ables, J.R. 1978. Feeding Behavior of an Entomol. Soc. Am. 83: 1215-1222. Assassin Bug, Zelus renardii. Ann. Cohen, A.C. 1993. Organization of digestion Entomol. Soc. Am. 71: 476-478. and preliminary characterization of Ali, A.-S. A. and T.F. Watson. 1978. Effect salivary trypsin-like enzymes in a of Temperature on Development and predaceous heteropteran, Zelus renardii. Survival of Zelus renardii. Environ. J. Insect Physiol. 39: 823-829. Entomol. 7: 889-890. Curkovic, T., J.E. Araya, M. Baena and Ambrose, D.P. 2001. Assassin Bugs M.A. Guerero. 2004. Presencia de Zelus (Reduviidae excluding Triatominae). In: renardii Kolenati (Heteroptera, Heteroptera of Economic Importance. Reduviidae) en Chile. Bol. S.E.A. 34: Ed. by C. W . Schaefer and A. R. 163-165. Panizzi. CRC Press, Boca Raton, FL. pp. EPPO Reporting Service. 2010. 695-712. Leptoglossus occidentalis: an invasive Aukema, B. 2011. Fauna Europaea: alien species spreading in Europe – Heteroptera. Fauna Europaea version 2.4, 2010/009. http://www.faunaeur.org 2010/Rse-1001.pdf four Iberian Heteroptera (Hemiptera). Frank, W.A. and J.E. Slosser. 1996. An Bol. Soc. Entomol. Aragonesa (S.E.A.) Illustrated Guide to the Predaceous 48: 399-401. Insects of the Northern Texas Rolling Bérenger, J.M. and D. Pluot-Sigwalt. 1997. Plains. MP1718, Texas Agricultural Relations privilégiées de certains Experiment Station, Texas A&M Hétéroptères Reduviidae prédateurs avec University, Vernon, TX. 28 pp. les végétaux. Premiers cas connus d’un Funasaki, G.Y., P.-Y. Lai, L.M. Nakahara, phytophage. C.R. Acad. J.W. Beardsley and A.K. Ota. 1988. A Sci. Paris, Sciences de la Vie, 320: 1007- review of biological control introductions 1012. I Hawaii: 1890 to 1985. Proceedings, Blatchley, W.S. 1926. Heteroptera, or true Hawaian Entomological Society 28: 105- bugs of eastern North America, with 159. especial reference to the faunas of HHart, E.R. 1986. Genus Zelus Fabricius in Indiana and Florida. The Nature the United States, Canada, and Northern Publishing Co., Indianapolis. 1116 pp. Mexico (Hemiptera: Reduviidae). Ann. Cisneros, J.J. and J.A. Rosenheim. 1998. Entomol. Soc. Am. 79: 535-548. Changes in the foraging behavior, within- Hemptinne, J.-L., A. Magro, C. Saladin and plant vertical distribution, and A.F.G. Dixon. 2011. Role of intraguild microhabitat selection of a generalist predation in aphidophagous guilds. J. insect predator. Environ. Entomol. 27: Appl. Entomol.

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Howarth, F.G. and D.J. Preston. 2002. Heteroptera of the Palaearctic region. Ed. Baseline Survey of (Insects by B. Aukema and C. Rieger. and Relatives) of Kahului Airport Netherlands Entomological Society, Environs Maui, Hawaii: Final report, Amsterdam, The Netherlands. pp. 148- Hawaii Biological Survey, Bishop 361. Museum, Honolulu. Edward K. Noda & Rabitsch, W. 2008. Alien true bugs of Associates Inc, 94 pp. Europe (Insecta: Hemiptera: Law Y,-H and A. Sediqi. 2010. Sticky Heteroptera). Zootaxa 1827: 1-44. substance on eggs improves predation Rabitsch, W. 2010. True Bugs (Hemiptera, success and substrate adhesion in newly Heteroptera). Chapter 9.1. In: Alien hatched Zelus renardii (Hemiptera: terrestrial arthropods of Europe. Ed. by Reduviidae) instars. Ann. Entomol. Soc. A. Roques, D. Lees, C. Lopez-Vamonde, Am. 103: 771-774. W. Rabitsch and J. Y. Rasplus. Pensoft, Law, Y.-H. and J.A. Rosenheim. 2011. Sofia, Bulgaria. BioRisk 4: 407-403. Effects of combining an intraguild Rosenheim, J.A., D.D. Limburg and R.G. predator with a cannibalistic intermediate Colfer. 1999. Impact of generalist predator on a species-level trophic predators on a biological control agent, cascade. Ecology 92: 333-341. Chrysoperla carnea: Direct observations. Maldonado, C. J. 1990. Systematic Ecol. Appl. 9: 409-417. Catalogue of the Reduviidae of the Rosenheim, J.A., T.E. Glik, R.E. Goeriz and World (Insecta, Heteroptera). Caribbean B. Raemert. 2004. Linking a predator‘s Journal of Sciences, University of Puerto foraging behavior with its effects on Rico, Mayaguez, 694 pp. herbivore population supression. Ecology Műller, C.B. and J. Brodeur. 2002. Intraguild 85: 3362-3372. predation in biological control and Schaefer, C.W. 2000. Adventitious biters— conservation biology. Biol. Control 25: "nuisance" bugs. In: Heteroptera of 216-223. Economic Importance. Ed by C.W. Petrakis, P.V. 2007. Current Insect Schaefer and A.R. Panizzi. CRC Press, Extinctions. In: Mass Extinctιons. Ed. by Boca Raton, FL. pp. 553-559. A.M.T. Elewa. Springer Verlag, Berlin. Stoner, A., A.M. Metcalfe and R.E. Weeks. pp. 195-251. 1975. Plant feeding by Reduviidae, a Ponsard, S., A.P. Gutierrez and N.J. Mills. predaceous family (Hemiptera). J. 2002. Effect of Bt-toxin (Cry1Ac) in Kansas Entomol. Soc. 48: 185-188. transgenic cotton on the adult longevity Torres, J.B. and D.W. Boyd. 2009. of four heteropteran predators. Environ. Zoophytophagy in predatory Hemiptera. Entomol. 31: 1197-120. Braz. Archiv. Biol. Technol. 52: 1199- Putshkov, P.V. and V.G. Putshkov. 1996. 120. Family Reduviidae Latreille, 1807 – assassin bugs. In: Catalogue of the

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Πρώτη αναφορά του Zelus renardii (Heteroptera, Reduviidae, Harpactocorinae) στην Ευρώπη

Π.B. ΠΕΤΡΑΚΗΣ1* KAI P. MOULET2

1 ΕΘΙΑΓΕ, Ινστιτούτο Μεσογειακών Δασικών Οικοσυστημάτων, Εργαστήριο Εντομολογίας, Τέρμα Αλκμάνος, 11528 Αθήνα 2 Museum Requien, rue Joseph Vernet, F-84000 Avignin, France

ΠΕΡΙΛΗΨΗ

Το νεαρκτικό είδος εντόμου Zelus reinardii βρέθηκε για πρώτη φορά στην Αττική, Ελλάδα, Ευρώπη. Ο εγκλιματισμός και η φυσική ενσωμάτωση αυτού του εντόμου στην Ελλάδα μπορεί να έχουν ωφέλιμη επίδραση στον έλεγχο επιζήμιων εντόμων σε καλλιέργειες καθώς το έντομο αυτό συμπεριφέρεται ως ωφέλιμο αρπακτικό. Ωστόσο, η εγκατάσταση και εξάπλωσή του μπορεί δυνητικά να έχουν και αρνητικά αποτελέσματα καθώς πρόκειται για πολυφάγο αρπακτικό που μπορεί να τρέφεται με άλλα αρπακτικά έντομα που υπάρχουν στα οικοσυστήματα ή χρησιμοποιούνται σε προγράμματα βιολογικής αντιμετώπισης εχθρών των καλλιεργειών στη χώρα μας. Η εισαγωγή του εντόμου σε άλλες περιοχές (π.χ. Χαβάη) έδειξε τη δυνατότητά του να έχει όλους αυτούς τους οικολογικούς ρόλους.