BioRisk 4(2): 669-776 (2010) Apeer-rev ‘iewed open-access journa 1] Ha tnaee et tars BioRis www.pensoftonline.net/biorisk Hymenoptera Chapter 12 Jean-Yves Rasplus', Claire Villemant’, Maria Rosa Paiva’, Gérard Delvare', Alain Roques* | UMR Centre de Biologie et de Gestion des Populations, CBGP (INRA/IRD/CIRAD/Montpellier SupAgro), Campus international de Baillarguet, CS 30016, 34988 Montferrier-sur Lez, France 2 UMR Origine, Struc- ture et Evolution de la Biodiversité, OSEB, (MNHN/CNRS) CP50, Muséum National d'Histoire Naturelle 45 rue Buffon, 75005 Paris, France 3 DCEA, Faculdade de Ciéncias e Tecnologia, Universidade Nova de Lisboa, 2829-516 Campus de Caparica, Lisbon, Portugal 4 INRA UR633, Zoologie Forestiére. Centre de recherche d Orléans, 2163 Avenue de la Pomme de Pin, CS 40001 Ardon, 45075 Orléans Cedex 2, France Corresponding author: Jean-Yves Rasplus (rasplus@supagro.inra.fr), Claire Villemant (villeman@mnhn. fr), Maria Rosa Paiva (mrp@fct.unl.pt), Gérard Delvare (delvare@supagro.inra.fr), Alain Roques (alain. roques@orleans.inra.fr) Academic editor: David Roy | Received 31 March 2010 | Accepted 26 May 2010 | Published 6 July 2010 Citation: Rasplus J-Y et al. (2010) Hymenoptera. Chapter 12. In: Roques A et al. (Eds) Arthropod invasions in Europe. BioRisk 4(2): 669-776. doi: 10.3897/biorisk.4.55 Abstract We present the first review of Hymenoptera alien to Europe. Our study revealed that nearly 300 species of Hymenoptera belonging to 30 families have been introduced to Europe. In terms of alien species diversity within invertebrate orders, this result ranks Hymenoptera third following Coleoptera and Hemiptera. Two third of alien Hymenoptera are parasitoids or hyperparasitoids that were mostly introduced for biological control purposes. Only 35 phytophagous species, 47 predator species and 3 species of pollinators have been introduced. Six families of wasps (Aphelinidae, Encyrtidae, Eulophidae, Braconidae, Torymidae, Pteromalidae) represent together with ants (Formicidae) about 80% of the alien Hymenoptera introduced to Europe. The three most diverse families are Aphelinidae (60 species representing 32% of the Aphelinid European fauna), Encyrtidae (55) and Formicidae (42) while the Chalcidoidea together represents 2/3 of the total Hymenoptera species introduced to Europe. The first two families are associated with mealy- bugs, a group that also included numerous aliens to Europe. In addition, they are numerous cases of Hy- menoptera introduced from one part of Europe to another, especially from continental Europe to British Islands. ‘These introductions mostly concerned phytophagous or gall-maker species (76 %), less frequently parasitoids. The number of new records of alien Hymenoptera per year has shown an exponential increase during the last 200 years. The number of alien species introduced by year reached a maximum of 5 species per year between 1975 and 2000. North America provided the greatest part of the hymenopteran species Copyright J-Y. Rasplus et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which ermits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 670 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) alien to Europe (96 species, 35.3%), followed by Asia (84 species, 30.9%) and Africa (49 species, 18%). Three Mediterranean countries (only continental parts) hosted the largest number of alien Hymenoptera: Italy (144 spp.), France (111 spp.) and Spain (90 spp.) but no correlation was found with the area of countries. Intentional introduction, mostly for biological control, has been the main pathway of introduc- tion for Hymenoptera. Consequently, the most invaded habitats are agricultural and horticultural as well as greenhouses. To the contrary, Hymenoptera alien in Europe are mostly associated with woodland and forest habitats. Ecological and economic impacts of alien Hymenoptera have been poorly studied. Ants have probably displaced native species and this is also true for introduced parasitoids that are suspected to displace native parasitoids by competition, but reliable examples are still scarce. The cost of these impacts has never been estimated. Keywords Hymenoptera, alien, Europe, biological invasions 12.1. Introduction Hymenoptera is one of the four large insect orders exceeding 100 000 species in the world, the other major orders being Coleoptera, Lepidoptera and Diptera (Gauld and Bolton 1988, Goulet and Huber 1993). The Hymenoptera order contains about 115 000 described species and authors estimated that there are between 300,000 and 3,000,000 species of Hymenoptera (Gaston 1991), possibly around 1,000,000 (Shar- key 2007). These estimates mean that only 1/10 has been described so far and 9/10 awaits description. However, the number of Hymenoptera species is difficult to esti- mate with accuracy, as most of the mega diverse regions of the world have not been extensively studied and inventoried regarding this group (LaSalle and Gauld 1993). In Europe, about 15,000 species have been reported belonging to 73 families, but undoubtedly thousands of species remains to be discovered and described. From our recent review of the literature, the alien species of Hymenoptera comprise 286 species belonging to 30 families. The order ranks third just following the Coleoptera and the Hemiptera in terms of alien species diversity (Roques et al. 2008). Additionally, 71 European species have been translocated from one part of Europe to another (add- ing 5 more families) and 11 species are considered cryptogenetic. All together within Europe, at least 368 Hymenoptera species have been introduced in different parts of the continent. Hymenoptera have been traditionally subdivided into three assemblages (the para- phyletic sub-order Symphyta and the monophyletic Aculeata and Parasitica belong- ing to the sub-order Apocrita). Each group exhibits different biology. “Symphyta’ are mostly phytophagous and are the most primitive members of the order. Parasitica are mainly parasitic species but some of them have returned secondarily to phytophagy, while Aculeata encompass a larger spectrum (predators, pollinators, parasitoids); all eusocial hymenoptera belong to this last group. Members of the Hymenoptera are familiar to a general audience and common names exist for a large variety of groups: “wasps’, “bees”, “ants”, “bumblebees”, “saw- Hymenoptera. Chapter 12 671 flies”, “parasitic wasps”. Hymenoptera adult sizes range from the very small Mymaridae (0.5 mm) to the large aculeate wasps (up to 5 cm long in Europe). ‘This group of man- dibulate insects is well defined by the combination of several characters: they have two pairs of functional wings (with the exception of apterous species) bearing fewer veins than most other insect groups and rarely more than seven cross veins. The abdominal tergum | is fused to the metanotum and in most Hymenoptera the metasoma (appar- ent gaster) is joined to the mesosoma (apparent thorax) by a petiole. Hymenoptera have two main larval types. ‘Symphyta’ have larvae that are cat- erpillar-like, but true caterpillars (Lepidoptera) have at most four pairs of prolegs (abdominal segments 3-6) while sawflies larvae have at least five pairs of prolegs (ab- dominal segments 2-6). Furthermore the prolegs of Symphyta do not bear crochets, whereas those of Lepidoptera larvae do. ‘Apocrita’ have legless grub-like larvae that are nearly featureless unless they have a differentiated head (Goulet and Huber 1993). All Hymenoptera have haplodiploid sex determination (haploid males and diploid females). Arrhenotoky is the most common mode of reproduction in Hymenoptera (Heimpel and de Boer 2008). The males develop parthenogenetically from unferti- lised eggs while the females develop from fertilised eggs. Females can control fertilisa- tion by releasing sperm to an egg upon oviposition, and can thus adjust the sex-ratio of their progeny. Ecologically and economically few groups of insects are as important to mankind as the Hymenoptera. Bees provide the vital ecosystem service of pollination in both natural and managed systems (Gallai et al. 2009) while parasitic Hymenoptera control popula- tions of phytophagous insects (Ischarntke et al. 2007) and can be effective agents for control of pest insects (Bale et al. 2008, Brodeur and Boivin 2004, Jonsson et al. 2008). Some of the phytophagous hymenoptera have an intimate association with their host- plants (Nyman et al. 2006) and can also be considered as major pests to forests (e.g. Diprionidae) (De Somviele et al. 2004, Lyytikainen-Saarenmaa and Tomppo 2002). Ant invasions cause huge economic and ecological costs (Holway 2002, Lach and Tho- mas2008) and Hymenoptera stings, specifically those of wasps, hornets and bees cause serious allergic reactions and anaphylaxis (Flabbee et al. 2008, Klotz et al. 2009). 12.2. Taxonomy of alien species The 286 species of Hymenoptera alien zo Europe belong to 30 different families (Table 12.1), which also have native representatives. Among these alien species, 35 species are phytophagous, 1 detritivorous, 3 pollinators, 47 predators whilst 200 are parasitoids or hyperparasitoids. These results show that only 13.3% of the alien wasp and bee spe- cies are phytophagous (including pollinators), the great majority of which (86.4 %) are predators and parasitoids (respectively 16.4% and 70.0%). Most parasitoids were intentionally introduced to control pests. Interestingly, among the 71 Hymenoptera that have been introduced from one part of Europe to another (aliens i7 Europe - Table 12.2), an opposite proportion is observed. Fifty-four species (76.0 %) are phytopha- 672 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) gous and only 17 (23.9%) are parasitic or predatory. These species have mostly fol- lowed their host plants throughout Europe. Consequently, most alien Hymenoptera in Europe belong to the sub-order Para- sitica (228 spp. and 20 families, 79.4% of the species), while Aculeata (51 spp. and 7 families, 17.8%) and Symphyta (8 spp. and 3 families, 2.8%) are less represented. Six families of wasps (Aphelinidae, Encyrtidae, Eulophidae, Braconidae, Torymidae, Pteromalidae) represent together with ants (Formicidae) about 80% of the alien Hy- menoptera in Europe. Each of these families has more than 10 introduced species in Europe. The three most diverse families in terms of alien species are Aphelinidae (60 species), Encyrtidae (55) and Formicidae (42). By far the richest superfamily is the Chalcidoidea that includes 198 alien species (69.2% of the total alien Hymenoptera). Below we give a short synopsis for all Hymenoptera families containing introduced species to Europe (including cryptogenic and translocated species). Suborder Symphyta Argidae. The second largest family of ‘Symphyta with about 1000 species described, but only 60 in Europe. Alien species to Europe have not yet been found. One species only, Arge berberidis, is considered as introduced from one part of Europe to another,. Females deposit eggs in leafs of various angiosperms and the larvae are phytophagous, feeding mostly on woody plants (Salicaceae, Rosaceae, Betulaceae). Blasticotomidae. This is a very small family represented by one species only, Blas- ticotoma filiceti, in northern and central Europe. Larvae are stem borers, developing within the rachis of ferns (e.g., Athyrium filix-femina (L.) Roth) (Schedl 1974). B. filiceti has been infrequently introduced into Great Britain from continental Europe, mostly with horticultural plants. Diprionidae. A small family of “Symphyta that mostly occurs in northern Europe. It comprises about 100 species in the northern hemisphere, of which 20 occur in Eu- rope. The larvae attack softwood trees (e.g. conifers) and are considered as major pests in forestry. Diprioninae develop on Pinaceae and Monocteninae on Cupressaceae, but only the first subfamily contains invaders. Alien species have not yet been recorded. However, five species are considered as alien in Europe. Neodiprion sertifer and Gilpinia hercyniae cause severe damage to pine and spruce plantations. Females of some spe- cies produce pheromones that attract males. The larvae consume needles, sometimes eregariously, and when mature drop to the ground, pupate and overwinter within a cocoon (rarely upon trees). Diapause can last for more than one winter (Pschorn Wal- cher 1991), the wasps emerging and dispersing in the early spring. Pamphiliidae. A small holarctic family containing about 60 species in Europe (van Achterberg and van Aartsen 1986, Viitasaari 2002). Only Cephalcia alashanica is an al- ien species introduced from temperate Asia. Six other species are alien in Europe, most of them having been introduced from the Alps to northern countries with their host trees. Some species attack conifers and are considered as forest pests. Females lay eggs Hymenoptera. Chapter 12 673 in a slit cut in a needle, the normally gregarious larvae either spin silk webs in which they develop (Cephalciinae) or roll the host plant leaves (Pamphiliinae). They over- winter as pupae within pupal chambers in the soil and adults emerge in early spring. Siricidae. A small Holarctic family (16 European species) of large and conspicuous wasps (woodwasps). Nine species are considered as alien in Europe, with only 5 alien species introduced from North America with imported timbers. The family is subdi- vided into two subfamilies, the Siricinae attacking conifers and the Tremecinae that attack angiosperm trees. The females, which do not feed, oviposit in recently fallen or dying trees and introduce spores of symbiotic fungus along with the eggs. ‘The larvae develop in 2 or 4 years as woodborers and pupate in the bark. Tenthredinidae. This cosmopolitan family is the most diverse group of ‘Symphyta’ including 1050 species in Europe of which only two are alien zo Europe , Nematus (Pteronidea) tibialis (a pest of black locust) and Pachynematus (Larinematus) itoi (a larch pest) and 23 alien im Europe. Some native European species are also considered serious pests in North America where they have been introduced. All species are phytopha- gous and the larvae are mostly external feeders on diverse species of angiosperms and conifers. The females embed their eggs in the tissue of the plant, using their ovipositor as a saw. The larvae feed singly on leaves, or are stem borers, gall makers or leaf miners. Tenthredinidae mostly overwinter as prepupae in the ground, sometimes as mature larvae or eggs, the adults emerge relatively early in the spring. Suborder Apocrita Parasitica Chalcidoidea Agaonidae. A small-sized family with only 6 species of wasps reported in Europe, four of which are introduced from tropical Asia, along with two ornamental trees Ficus microcarpa L.f. and EF religiosa L. Agaonidae are the pollinators of fig trees and are mutualistically associated with their host plant. Several groups of non-pollinating fig wasps are associated with figs, either as gall-makers, inquilines or parasitoids. ‘Their taxonomic position has been discussed and they are here grouped within Agaonidae for convenience (Boucek 1988, Rasplus et al. 1998). Aphelinidae. ‘This is a moderately sized family of wasps represented in Europe by less than 200 species of which sixty are aliens. Aphelinidae species have been intro- duced from diverse geographic areas as biological control agents. Along with encyrtid, the Aphelinidae is the most important family for biological control. Species are pri- marily endoparasitoids or ectoparasitoids, sometimes hyperparasitoids, of sternorrhyn- chous Hemiptera (mostly Aphidoidea, Coccoidea or Aleyrodoidea). Some species may have complicated ontogeny (Hunter and Woolley 2001) and males and females may attack different hosts either as parasitoids or hyperparasitoids. Chalcididae. A small family of chalcid wasps comprising about 80 species in Eu- rope, including one alien species, introduced from North Africa to control fruit flies. 674 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) The hosts of these obligate parasitoids or hyperparasitoids are mostly Lepidoptera and Diptera, less frequently Coleoptera, Neuroptera or Hymenoptera (Delvare 1995, Del- vare 2006). The females lay eggs within the host larva and the pupation take place in the host pupa. Encyrtidae. A \arge family of wasps represented by more than 700 species in Eu- rope (Trjapitzin 1989), of which 55 are considered to be alien, introduced from differ- ent parts of the world for biological control of economically important pests (Noyes and Hayat 1994). Most of the Encyrtidae are endoparasitoids of scale insects. Some species also develop as endoparasitoids of other insect orders, mostly Lepidoptera, Co- leoptera and Hymenoptera). The egg is laid inside the host and the larva develop as a parasitoid sometimes as an hyperparasitoid, and pupates within the host. Eulophidae. A \arge family of wasps that contains 1100 species in Europe (Gauld and Bolton 1988), including 29 alien species. Most alien species have been introduced for biological control but a few (3) are gall makers that develop at the expense of plant tissue of Eucalyptus (Branco et al. 2009). Eulophid are primarily solitary parasitoids of eggs, pupae or larvae of various endophagous insects (Diptera, Coleoptera, Thysanop- tera, Lepidoptera or Hymenoptera). Some species attack economically important leaf miners or gall makers (e.g. Agromyzidae, Cecidomyiidae). Eupelmidae. A small family represented by about 100 native (Gibson 1995) and 5 alien species in Europe (Eupelmus and Anastatus spp.). Eupelmidae are primarily ectoparasitoids (idiobionts) of egg or larval stages of various insects and spiders (Askew et al. 2000). Some species within this family are generalist parasitoids. Eurytomidae. A medium-sized family with about 300 species in Europe (Zerova 1978), of which seven are alien. Interestingly, these alien species are not parasitoids but phytophagous and pests of crops or horticultural plants whilst most eurytomids are primarily ectoparasitoids or hyperparasitoids of extremely diverse groups of endopha- gous insects (Lotfalizadeh et al. 2007). Phytophagous species are either stem-borers or seed-feeders or gall-makers on different host-plant groups (e.g. Graminaceae, Legumi- nosae). Some species are both entomophagous then phytophagous during their larval development. Mymaridae. A medium-sized family including about 450 species in Europe, of which only two are alien, Anaphes nitens and Polynema striaticorne. All mymarids are internal, solitary (rarely gregarious) parasitoids of the eggs of various insects (Huber 1986). The most common hosts are eggs of Hemiptera Auchenorrhyncha (Cicallidae, Cixiidae) but mymarids also parasitize eggs of other insects (Coleoptera, Hemiptera). Female oviposit within concealed eggs, and there are 2 to 4 larval stages. Perilampidae. A small family of chalcid wasps that includes 40 European spe- cies. The only alien species in this family (Steffanolampus) originates from North America and is a parasitoid of wood-boring Coleoptera. Most perilampids are hy- perparasitoids of Lepidoptera through Tachinidae (Diptera) or Ichneumonoidea (Steffan 1952). Females deposit their eggs away from the host, however the young larvae (planidium) are mobile, and may either attach themselves to the primary host, at any stage of larval development, or enter the host to attach to its endopara- Hymenoptera. Chapter 12 675 sitoids. In some species, an adult host carries the larva to a suitable location where host larvae occur (Darling 1999). Pteromalidae. A \arge, paraphyletic family including more than 1100 species in Europe (Graham 1969). Only ten are considered alien species, most of which were un- intentionally introduced with their hosts, some (3) for biological control purposes. The diversity of the group is reflected by the diversity of the biology exhibited. Pteromalids are mostly ectoparasitoid idiobionts, but some species are koinobionts. Miscogasterinae are larvo-pupal endoparasitoids of dipteran leaf miners. Eunotinae (e.g. Moranila) are predators on Coccoidea eggs within the female body (Boucek and Rasplus 1991). Signiphoridae. A small family of tiny chalcids (0.5—2 mm) comprising only 8 Eu- ropean species, one of which is an introduced hyperparasitoid (Chartocerus) (Woolley 1988). Signiphoridae are known as parasitoids (sometimes hyperparasitoids) of cyclor- rhaphous dipterans, scale-insects (Coccoidea) or white-flies (Aleyrodidae). Torymidae. A medium-sized family that includes about 350 European species (Grissell 1995, Grissell 1999), of which 13 are considered as alien to Europe. Most of the alien species (12) belong to the genus Megastigmus and are considered pest of coni- fer seeds (Roques and Skrzypczynska 2003). Most torymines are idiobiont ectoparasi- toids of gall-makers (Cynipidae and Cecidomyiidae) and other endophytic insects but most Megastigminae are specialist phytophages. Megastigmus females lay their eggs in the ovules of conifers before fertilization has taken place (Roques and Skrzypczynska 2003) (Figure 12.9). Megastigmus biological habits have been shown to be particularly prone to invasion. Since most of their development takes place within seed, their pres- ence is usually overlooked in traded seed lots, the infested seeds showing up only when X-rayed (Figure 12.10). In addition, insect are able to become dormant during the larval stage, for up to 5 years (prolonged diapause) following the annual size variations of the seed crop, thus broadening the chances that adult emergence will occur under favourable circumstances near a suitable new host. Moreover, some species such as the Douglas-fir seed chalcid, M. spermotrophus, appear capable of preventing the abortion of unfertilized seeds. The invasive insect larva may thus achieve its development in un- pollinated, unfertilized seeds by altering the physiology of the ovule so that it allocates de novo resources to the larva (von Aderkas et al. 2005). Trichogrammatidae. A moderately-sized family containing about 150 European species. The nine alien species belong mostly to three genera: Trichogramma, Oligosota, Uscana and have been introduced to Europe for the control of agricultural pests (Lepi- doptera and Coleoptera) (Pintureau 2008). Trichogrammatids are primarily solitary or gregarious endoparasitoids of insect eggs (mostly Lepidoptera, Hemiptera, Coleoptera) and can sometimes develop as hyperparasitoids. Ichneumonoidea Ichneumonidae. This is the first megadiverse Apocrita family in Europe with about 5500 species, six of them are considered as alien to Europe. ‘These species have been in- 676 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) tentionally introduced for biological control. ‘The family is divided into more than 30 subfamilies. Consequently, the biology of ichneumonids is extremely diverse. Ichneu- monids mostly parasitize the immature stages of the Holometabola, and are frequently associated with Lepidoptera and sawflies (Hymenoptera). Ectoparasitism is considered the primitive condition and endoparasitism has evolved several times independently within the family. Braconidae. Braconids represent the second megadiverse family with nearly 3500 European species, 16 of which are considered as alien. Altogether, Ichneumonoidea may account for nearly 10000 species in Europe. Like ichneumonids, braconids ex- hibit a large range of biological characteristics. They are mostly parasitoids of other insects. Some of the braconid groups are larvo-nymphal koinobiont parasitoids; others are idiobiont ectoparasitoids. Introduced species are mostly koinobiont endoparasitoids and are associated with aphids (Aphidiinae), moths (Miscogasterinae), and fruit flies (Opiinae). Ceraphronoidea Ceraphronidae. A small family represented by 100 European species, only one of which is considered as alien, Aphanogmus bicolor. Their biology is poorly known but some species are endoparasitoids of nematocerous dipterans whilst others attack Thy- sanoptera or Neuroptera. Some species are considered as antagonists of biological control agents since they are parasitoids of predaceous midges or hymenopteran pri- mary parasitoids. Cynipoidea Cynipidae. A medium-sized family confined to the Holarctic and containing 350 Eu- ropean species. Only the chesnut gall wasp, Dryocosmus kuriphilus, is alien to Europe (Figure 10.8). Six more species, mostly from the genus Andricus, are considered as aliens in Europe. Most Cynipinae are gall inducers on Quercus, Rosa and some Com- positae but others (Synergini) are inquilines. Figitidae. This medium-sized family contains ca. 400 species in Europe, the fam- ily as presently understood includes the previous Eucoilidae, Charipidae and Anach- aritidae (Ronquist 1995). Only one species (Aganaspis daci) is considered as alien and has been introduced to Europe for the control of fruitflies. Figitid larvae develop as internal parasitoids of other endophytic insect larvae. The hosts are mostly dipteran larvae but Charipinae Alloxystini are hyperparasitoids of aphids through Braconidae Aphidiinae and Aphelinidae. The egg is deposited inside a young host larva, which continues to develop normally (koinobionts), the parasitoid larvae emerges before the host death and can achieve its development as an ectoparasitoid. Hymenoptera. Chapter 12 677 Platygastroidea Platygastridae. A medium-sized family with about 500 species in Europe but only two (Amitus spp.) are considered as alien, having been introduced into Europe for the control of whiteflies. Many Platygastridae are endoparasitoids of gall-making dipterans whilst others attack immature hemipterans or ant larvae. The biology of most species re- mains largely unknown. Some species are thelytokous and very few polyembryonnic. The larvae have an uncommon appearance and superficially resemble cyclopoid copepods. Scelionidae. A medium-sized family that includes about 600 species in Europe, three of them considered as alien. Scelionids are primarily endoparasitoids in a wide variety of insect eggs (few on other arthropods), more rarely hyperparasitoids. Intro- duced species attack Hemiptera or Lepidoptera eggs and have been used for pest con- trol. The family has been synonymized with Platygastridae but we still keep it apart for consistency (Murphy et al. 2007). Suborder Apocrita Aculeata Chrysidoidea Bethylidae. A medium-sized family represented by about 230 species in Europe. Four species are considered alien. Cephalonomia waterstoni, Holepyris syluanidis and Plastan- oxus laevis are cosmopolitan. They were introduced into Europe with stored products. Laelius utilis is a parasitoid of Anthrenus. Bethylidae mainly attack larvae of Lepidop- tera and Coleoptera. The female stings and paralyses the host, and then lays several eggs on its skin. Larvae develop as ectoparasitoids. For a few species, females tend the eggs and developing larvae. Pupation occurs next to the host remains. Chrysididae. A medium- sized family that comprises 420 European species. Cu- koo- wasps are parasitoids or kleptoparasitoids of Aculeate wasps. The nests of the host are sought out by the female chrysid that oviposits into the host cells. A true parasitoid larva develops as an ectoparasitoid on the host larva whilst a kleptoparasite larva kills the egg or the young larva of the host before consuming the stored food. One East Eu- ropean species introduced in western parts of Europe, Chrysis marginata, is considered as alien iz Europe (Pagliano et al. 2000). Dryinidae. A medium-sized family that comprises about 100 species in Europe. All dryinids are parasitoids of immature and adult Hemiptera Auchenorrhyncha. The larva is rather endoparasitoid than ectoparasitoid during the last instars, forming a bag (thyl- acium) constituted by the exuviae of the parasitoid and bulging from the host abdomen. Only one species alien to Europe, Neodryinus typhlocybae, was introduced in northern Italy and subsequently in France for biological control of the Nearctic planthopper Met- calfa pruinosa (Hemiptera, Flatidae) (Malausa et al. 2003, Malausa et al. 2008). 678 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) Apoidea Apoidea represents a superfamily including more than 2000 species in Europe. De- pending on the classification used, the group comprises seven families (ancient sub- families of the single family Apidae) to eleven families if sphecid wasps, the sister group of bees, are included (Sharkey 2007). Here we followed the more recent classification system and adopted a subdivision into several families. Bees are flower visitors and efh- cient pollinators of angiosperms. Their larvae are phytophagous and develop on a mix- ture of pollen and nectars. Bees are now recognized as an important group of ecosystem engineers that modulate resources availability (i.e. plants) to other organisms (Jones et al. 1994). Two families of bees contain alien species in Europe. Sphecid wasps comprise 4 families of wasps that feed their progeny with a wide range of preys (mainly insects or spiders), depending on genera. All alien species belong to the family Sphecidae. Apidae. This small family of eusocial bees includes social species, with colonies attaining large sizes. It comprises less than 70 species in Europe, all except one (Apis meliffera) belonging to the genus Bombus. Some of these pollinator species have been introduced from some parts of Europe into other European regions for crop pollina- tion purposes and honey production. Megachilidae. This family comprises about 480 species in Europe, two are consid- ered as alien. The alfalfa leafcutter bee, Megachile rotundata, is a west European species that has been used commercially for pollination of alfalfa, and introduced in Russia. Osmia cornifrons is an alien species that has been introduced from Japan into Denmark for pollination of fruit trees. Megachilidae nest in burrows in soil or in pithy stems. A few species build stony mud nests. Cells of Megachilidae are made of foreign materials (leaf pieces for Megachile species) brought into the nest. Sphecidae. This family in its narrow sense comprises about 70 species, four of which are alien species accidentally introduced into Western Europe from North America (Sceliphron caementarium and Isodontia mexicana) or from Asia (S. curvatum and S. deforme). Adults of most species (e.g., /sodontia) prey on orthopteroids but some of them, such as Sceliphron spp., catch Araneae. While S. deforme has possibly not established in the Balkans, both other species became established and threaten autochtonous species of Sceliphron (Cetkovic et al. 2004). While sodontia puts its preys in pre-existing cavities, Sceliphron are mud-daubers that often built their nests in or around buildings (Bitsch and Barbier 2006, Bitsch et al. 1997). Vespoidea Formicidae. This family includes about 650 species in Europe, 42 of which are alien to Europe, one is cryptogenetic and seven are European species introduced into other areas of Europe. Ants exhibit a remarkable range of life histories. They have colonized most habitats and form colonies of variable sizes in the soil, plant debris, trees and infrastructures of human origin. The nest contains one to several reproductive females as well as workers and broods. Males are produced seasonally. Mating usually takes Hymenoptera. Chapter 12 679 place outside the nest but may occur inside the nest. In Europe, the argentine ant Line- pithema humile (Mayr) is extremely abundant throughout the Mediterranean basin, causing economic damage by fostering some hemipteran pests and upsetting the action of natural enemies; However, it may occasionally act as a beneficial natural enemy in forest ecosystems (Way et al. 1997). Vespidae. This medium-sized family comprises 300 species in Europe classified into four subfamilies: Masarinae, Eumeninae, Polistinae and Vespinae (22 species). Vespinae are social wasps that built aerial or subterranean nests made of carton and composed of several combs protected by an envelope. Recently, a hornet species alien to Europe, Vespa velutina nigrithorax, was accidentally introduced from Asia into southern France (Haxaire et al. 2006, Villemant et al. 2006) (Figure 10.11). The European yellowjack- ets, Vespula germanica (Fabricius, 1793) and V. vulgaris (Linné, 1758) were introduced to Iceland from continental Europe, the last into Feroe Islands (Olafsson 1979). For nine families the number of alien species exceeds 5% of the species known in Europe (Figure 12.1). Four of these families are small (Agaonidae, Signiphoridae, Siricidae and Sphecidae) and consequently the number of alien species is marginal. However Aphelinidae, Encyrtidae, Trichogrammatidae and Formicidae are medium- sized families comprising between 150 and 700 species and consequently the number of alien taxa is relatively important. Interestingly, the number of alien Aphelinids in- troduced into Europe for biological control represents about one third of the specific diversity of the family in Europe. Aphelinidae, Encyrtidae and Trichogrammatidae, three families largely used for biological control, rank among the top five in terms of proportion of alien species in the European fauna. Aphelinidae and Encyrtidae are mostly biological control agents of the three mealybug families that include most of the pest species alien to Europe (Diaspididae, Pseudococcidae and Coccidae; see Chap- ter 9.3). Finally, Formicidae also include a large proportion of alien species to Europe and represent a major group of alien species to Europe. 12.3. Temporal trends First records in Europe are known for 262 of the 286 hymenopteran species alien to Europe (92%). Dates given here are relatively imprecise, as most species may have been introduced two to five years before they were reported. Furthermore, we did not try to check all literature and collections in order to report the dates of first interception within Europe. The number of new records per time period shows an exponential increase in the number of alien Hymenoptera to Europe during the last 200 years (Figure 12.2). The mean number of new records of alien hymenoptera varies from less than one species per year during the period (1800-1924) to about 5 species per year between 1975 and 2000. Interestingly, we observed a decrease in the number of Hymenoptera reported during the last 10 years. This overall increase in the number of introduced species also corresponded to an increase in the number of hymenopteran families newly found in Europe. 680 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) % species % species 10 20 30 80 60 40 20 0 0 Aphelinidae Encyrtidae Formicidae Eulophidae Braconidae Torymidae Pteromalidae Alien vs. native species Trichogrammatidae I Eurytomidae Ichneumonidae Eupelmidae Siricidae Agaonidae Bethylidae Sphecidae Scelionidae Mymaridae Platygastridae Tenthredinidae Ceraphronidae Chalcididae Cynipidae Dryinidae Figitidae Megachilidae Pamphiliidae Perilampidae Signiphoridae Vespidae Alien species WEP is. a ak eit ~~ Figure 12.1. Taxonomic overview of the alien Hymenoptera. Right- Relative importance of the hy- menopteran families in the alien entomofauna. Families are presented in a decreasing order based on the number of alien species. Species alien to Europe include cryptogenic species. The number over each bar indicates the number of alien species observed per family. Left- Percentage of aliens vs. total species in each Hymenoptera family in Europe. The number over each bar indicates the total number of species observed per family in Europe. From 1800 to 1924 (125 years) only 35 species, representing 8 families, of alien hymenoptera were reported in Europe. Most of them are biological control agents or ants. Only one species of chalcid wasp (furthermore a hyperparasitoid) is reported from that period while Chalcidoidea is the most diverse group of alien Hymenoptera. How- ever, during that period of time the European fauna was still poorly known and little studied (which is still the case for the majority of families) and the number of alien spe- cies is likely to have been underestimated. Nevertheless, over 1/3 of the alien ant species presently known in Europe were introduced between 1847 and 1929. About 79% of the alien Hymenoptera were introduced in Europe in the last 60 years. During that period of time, 61.5% of the phytophagous alien and only 38.3% of the predator alien were introduced into Europe. Among the three most diverse families of alien Hymenoptera (namely Formicidae, Aphelinidae and Encyrtidae), Formicidae exhibited a relatively stable pattern, regarding the number of introductions per year over time, varying between 0.08 and 0.36, with a maximum of introductions during the periods 1925-1949 and 1975-1999 (Figure 12. 3). Aphelinids and encyrtids both show a relatively similar pattern, but somewhat different to the pattern exhibited by ants. [hese two families, largely used in biological control, showed a peak of introduc- Hymenoptera. Chapter 12 681 Mean number of new alien species recorded per year during the period 0 | vs 3 4 5 1492-1799 1800- 1849 1850-1899 1900-1924 1925-1949 1950-1974 1975-1999 2000-2006 Time period Figure 12.2. Temporal trend in number of alien Hymenoptera to Europe per period of 25 years from 1492 to 2006. Cryptogenic species excluded. The number above the bar indicates the number of species introduced. tions during the period 1950-1999 (between 0.52 and 1.32 species per year), which roughly corresponds to the ‘golden years’ of biological control. More specifically, our analysis showed that 77.5% of the total number of parasitoids alien to Europe were introduced between 1950 and 1999. In the last 10 years, the rate of introduction drops to less than 0.1 species per year. This trend is probably due to both the decreas- ing interest in research on biological control and to the growing concern over possible nontarget effects of biological control. 12.4. Biogeographic patterns Origin of alien species We could ascertain a region of origin for 272 (95.1%) alien wasp species intro- duced to Europe. Overall there are no major difficulties in identifying the areas of origin of these wasps. The distribution of the genera of the hosts or the plant-hosts and also the origin of the taxonomists describing these species provide evidence of likely origins. However, for subsequent spread within Europe it is difficult, without genetic analyses, to separate spreading from adjacent countries from independent colonization events. 682 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) Mean number of new alien species recorded per year during the period 0 0.4 0.8 LZ 1850-1899 WO Aphelinidae I Formicidae 1900-1924 i Encyrtidae 1925-1949 1950-1974 1975-1999 2000-2006 Time period Figure 12.3. Rates of introduction of the three most diverse families of invasive Hymenoptera during the two last centuries. North America provided the greatest part of alien Hymenoptera occurring in Eu- rope (96 species, 35.3%), followed by Asia (84, 30.9%) and Africa (49, 18%) (Fig- ure 12.4). This pattern is similar to the one found for Diptera (see Chapter 10) but dif- fers from that observed in most other insect groups. Whatever the main areas of origin, trends of introduction are similar over time, and there is no evidence of a change in the origin of alien species through time (Figure 12.5). The only difference seemed to be a decrease of the afro-tropical species in the last 30 years, whereas rates of introduction still increased for both North America and Asia. However it must be noted that origins of alien species can differ from one country to another and general trends are not sup- ported in all countries. Israel for example received more species from Asia and Africa than from North America (Roll et al. 2007). Interestingly, the composition of the introduced guilds originating from different continents differed taxonomically. The alien guilds introduced from North America contains several phytophagous species (Siricidae, Torymidae, Eurytomidae) and sev- eral species of Ichneumonoidea that are absent from oriental invader guilds. Overall, phytophagous aliens mostly originate from North America and temperate Asia. This is the case for xylophagous Siricidae, most Megastigmus seed-feeders (Torymidae), several Eurytomid species. Introduced plants (e.g. Ficus and Eucalyptus) came into Europe with species of their phytophagous guilds (Agaonid and Eulophidae gall-makers). Al- ien Formicidae originates from Africa (10 species), Asia (14) and South America (7) while only two were introduced from North America. South American ants mostly originated from areas with Mediterranean-like climate. Parasitoid wasps originated from all continents with no particular trends. Hymenoptera. Chapter 12 683 Cryptogenic C&S America 8.4% \ Africa 74% | 16.5% ' Asia North America 28.3% 32.3% Australasia 7.1% Figure 12.4. Origin of the 286 alien species of Hymenoptera established in Europe. Distribution of alien species in Europe Alien Hymenoptera species and families are not evenly distributed throughout Europe and large differences exist between countries (Figure 12.6, Table 12.3). However, results might have been influenced by large variations in the number of taxonomists involved, as well as by the intensity of the studies and of the samplings conducted in different regions. Little information is available for some countries of central and north-eastern Europe and consequently these areas appear to host comparatively few alien species of Hymenoptera. Continental Italy hosts the largest number of alien Hymenoptera (144 spp.), followed by continental France (111 spp.) and continental Spain (90 spp.). Bosnia, Andorra and Latvia are the countries from which the lowest number of invasive Hy- menoptera has been reported so far, with only one alien species. No correlation with the country surface area has been found but there is a latitudinal trend of decreasing number of alien species to Europe from southern to northern Europe As most of the alien hymenopterans are biological control agents, they were mostly introduced in one or few countries by national research projects that attempted to control target pest. Large-scale European projects for biological control are rare and consequently wasps have been introduced on a local scale. About 150 alien species (i-e., more than 50% of the total species) have been report- ed from only one or two countries. In contrast, 31 species are reported from at least 10 countries, among them 13 of the 36 species were introduced before 1924. These aliens mostly belong to the three diverse families of alien Hymenoptera (namely Aphelinidae, Encyrtidae and Formicidae). Most of these widespread alien wasps were parasitoids introduced for biological control. For example, Aphelinus mali against the woolly apple aphid, Eriosoma lanigerum (Hausmann); Aphidius colemani and A. smithi as generalist 684 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) Mean number of new alien species recorded per year during the period 0 04 08 1.2 1.6 2 1850-1899 BE Africa PE Asia 1900-1924 GEE North America 1925-1949 1950-1974 1975-1999 2000-2006 Time period Figure 12.5. Evolution of the rate of alien Hymenoptera from different origin through time. parasitoids used against several species of pest aphids, i.e., Acyrthosiphon pisum (Har- ris), Aphis gossypii Glover and Myzus persicae (Sulzer); Cales noacki against the aleyrodid Aleurothrixus floccosus (Maskell), a pest on Citrus; Encarsia formosa mostly as a bio- logical control agent of greenhouse whitefly, Trialeurodes vaporariorum (Westwood); Leptomastix dactylopii Howard against Planococcus citri (Risso); Aphytis mytilaspidis as a parasitoid of the oystershell scale, Lepidosaphes ulmi (L.), and some other diaspidid scales; Eretmocerus eremicus as a parasitoid of the Bemisia complex (Hemiptera, Aleyro- didae) in the native range; and, Mesopolobus spermotrophus against the seed chalcid pest Megastigmus spermotrophus. Only three of the widespread alien Hymenoptera are phytophagous and were introduced during the 19th century (Megastigmus spermotrophus, Nematus tibialis, Sirex cyaneus). Seven species of Formicidae appear widely distributed in Europe: Hy- poponera punctatissima (31 countries), Lasius neglectus (10), L. turcicus (15), Linepithe- ma humile (17), Monomorium pharaonis (23), Paratrechina longicornis (13), Pheidole megacephala (14) 12.5. Main pathways to Europe Intentional introductions represent a large proportion of the introduced species in Europe (180 of 286, 63%) and this is mostly due to the high number of introduced Hymenoptera. Chapter 12 685 Number of alien species no data 6-30( | so-so NY 101-145 ss. s s - <0 51-100 Figure 12.6. Colonization of continental European countries and main European islands by hymenop- teran species alien to Europe. Archipelagos: | Azores 2 Madeira 3 Canary Islands. biological control agents. Among the 106 species clearly accidentally introduced in Europe, 32 (30.1%) are phytophagous species, only 24 (22.6%) parasitoids or hyper- parasitoids that were sometimes unintentionally introduced with their parasitic hosts although the real status of some of these parasitoids is difficult to ascertain, while the majority (47 species; i.e., 44.3%), are social Hymenoptera and Sphecidae. Several species are cryptogenic and represent ancient introductions in Europe, mostly with stored products. Identifying the origin of accidental introductions is not easy but clearly introductions of plants for planting (e.g. cultivated conifers, orna- mental trees) and plant seeds appeared to be the main pathways of introduction for phytophagous Hymenoptera. Thus, the lack of regulatory measures for seed imports in Europe probably resulted in the repeated establishment of alien species of Megastigmus seed chalcids since the beginning of the 20th century. Aliens presently represent 43% of the total fauna of tree seed chalcids in Europe (Roques and Skrzypcezynska 2003). The development of trade in plant material through the Internet is likely to increase 686 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) this process because there is less control, especially for tree seeds which can be moved quite freely all over the world. 12.6. Most invaded ecosystems and habitats Most of the habitats colonized by Hymenoptera alien to Europe correspond to habi- tats strongly modified by humans (Figure 12.7). About half of the species occur in agricultural and horticultural habitats and this proportion reaches 2/3 of the species if greenhouses are considered. Only 20% of the aliens to Europe occur in woodland and forest habitats. However, the proportion is reversed if we consider Hymenoptera alien in Europe; in this case, half of the translocated species are phytophagous pests of trees. 12.7. Ecological and economic impact The ecological impacts of alien invertebrate species have been recently reviewed by Kenis et al. (2009) and Hymenoptera represent well all impact categories described in this review. Biological control programmes against pests, using introduced parasitoids, were initiated in Europe about 100 years ago. These programs using relatively host- specific parasitoids are long supposed to decrease the risk to nontarget species, however there is increasing concern about the ecological costs of biological control (Louda et al. 2003, Simberloff and Stiling 1996). All introduced natural enemies present a certain Percentage of alien hymenopterans living in the habitat 0 10 20 30 40 50 B - Coastal habitats C - Inland surface water habitats D - Mire, bog and fen habitats E - Grassland and tall forb habitats F - Heathland, scrub and tundra habitats G - Woodlands and forests 48 H - Inland without vegetation - | - Agricultural and horticultural lands ] - Buildings, houses J100 - Greenhouses X - Large parks and domestic gardens II) Alien to Europe Alien in Europe 193 Habitats Figure 12.7. Main European habitats colonized by the species of Hymenoptera alien zo Europe and ali- en in Europe. The number over each bar indicates the absolute number of alien hymenopterans recorded per habitat. Note that a species may have colonized several habitats. Hymenoptera. Chapter 12 687 degree of risk to non-target species and there is clear evidence of non-target effects (Lynch and Thomas 2000). Indeed, some butterfly populations have suffered a range reduction likely due to parasitism from an introduced wasp (Benson et al. 2003a, Ben- son et al. 2003b). Recently, Babendreier et al. (2003) found in laboratory experiments that Trichogramma brassicae (a parasitoid largely used against Ostrinia nubilalis (Hiib- ner) on maize) parasitizes eggs of 22 out of 23 lepidopteran species tested, including several which are listed on the Swiss red list of endangered species. Because researchers have not looked systematically for non-target effects, they are probably underestimated in Europe. Biological control is potentially a valuable control strategy against invasions of alien insect pest species in agricultural and forest ecosystems. Nevertheless, post- release monitoring of biological control agents on target and nontarget species has yet to be developed. This is an ethical responsibility of scientists (Delfosse 2005) and it could help to resolve uncertainties in the impact of releases. One of the most pernicious effects of introduced ants is the elimination or dis- placement of native ants and potential cascading effects on other trophic levels. In- deed, invasive ant species have huge colonies that exploit local resources and therefore represent a considerable threat to native ants. This ecological advantage of invasive ant species is partly attributed to their unicoloniality that promotes high worker densities and to the presence of several queens that accelerate colony growth and propagation Figure 12.8. Chestnut gall induced by the chestnut gall wasp, Dryocosmus kuriphilus (Credit: Milka Glavendeki¢). 688 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) Figure 12.9. Female of cedar seed chalcid, Megastigmus schimitscheki, ovipositing on a cedar cone. (Cre- dit: Gaélle Rouault). (Giraud et al. 2002), sometimes coupled with diet plasticity allowing them to exploit human residues. Introduced alien parasitoids have also been suspected to displace native parasitoids by competition; however, reliable examples are still rare. One reported case in Europe is the probable displacement of Encarsia margaritiventris (Mercet), a parasitoid of the whiteflies Aleurotuba jelineki (Frauenfeld) following the introduction of Cales noacki (Viggiani 1994b). There is still debate about the extent to which an introduced bee could alter native pollinator communities. Some studies clearly show that introduction of non-native bees may have strong impacts on local communities of bees (Goulson 2003), but their effects have been poorly documented in Europe. However, it is important to keep in mind that generalist polylectic bees (i.e. Apis, Bombus) may compete with native flower visitors (bees, wasps, butterflies, moths, beetles and flies) (Ings et al. 2006), as well as competing for nest sites. There is also evidence that introduced bees could bear pathogenic, commensal and mutualistic organisms, that could be co-introduced and transmitted to native Apidae (Goka et al. 2001). Exotic bees could also disrupt native pollinator services and could be the only pollinators of weeds, improving their seed set and spread. Genetic impacts of Hymenoptera are clearly underestimated and there is strong risk that introduced species may hybridize with localy adapted populations. ‘This case has been reported for Bombus and Apis, and there is a strong risk that commercial and native subspecies will hybridize with alien ones (Goulson 2003, Ings et al. 2005, Hymenoptera. Chapter 12 689 Figure 12.10. X-ray picture of Douglas fir seeds showing seeds infested by larvae and pupae of the Douglas-fir seed chalcid, Megastigmus spermotrophus (Credit: Jean-Paul Raimbault). Figure 12.11. Nest of Asian Hornet, Vespa velutina nigrothorax (Credit: Claire Villemant) 690 Jean-Yves Rasplus et al. / BioRisk 4(2): 669-776 (2010) Kanbe et al. 2008). Introduction of Mediterranean subspecies of Apis mellifera, A. m. carnica and A.m. ligustica, in northern Europe has led to extended gene flow and in- trogression between these subspecies and the native black honeybee, A. m. mellifera in different parts of Europe (De La Rua et al. 2002, Jensen et al. 2005). Introduced phytophagous Hymenoptera may also have strong economic and eco- logical impact. During mass-outbreaks they defoliate trees, reduce their growth and lead, sometimes, to their death. This is the case for diprionid outbreaks (De Somviele et al. 2004, Lyytikainen-Saarenmaa and Tomppo 2002) as well as for xylophagous siricids that threaten pine plantations (Yemshanov et al. 2009). Economic impacts of alien Hymenoptera have received little attention In Europe and consequently are clearly underestimated. However introduced alien ant species account for over $120 billion of annual costs in the United States alone (Gutrich et al. 2007, Pimentel et al. 2000, Pimentel et al. 2005, Vis and Lenteren 2008). Intro- duced siricids in the United States are considered as an economically serious threat with a total projected loss of more than $ 0.76 billion over 30 years (Yemshanov et al. 2009). The recent introduction in France of Vespa velutina would also have a sig- nificant impact on beekeeping because this hornet mainly preys on honeybees (see factsheet 14.62). 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