Apeer-reviewed open-access journa BioRisk 4(2): 553-602 (2010) i d op ji I doi: 10.3897/biorisk.4.53 RESEARCH ARTICLE B | O R IS k www.pensoftonline.net/biorisk Diptera Chapter 10 Marcela Skuhrava', Michel Martinez”, Alain Roques? | Bitovskd 1227/9, 140 00 Praha 4, Czech Republic 2 INRA Centre de Biologie pour la Gestion des Popu- lations (CBGP), Campus International de Baillarguet, 34988 Montferrier-sur-Lez, France 3 INRA UR633 Zoologie Forestiére, 2163 Av. Pomme de pin, 45075 Orléans, France Corresponding authors: Marcela Skuhravd (skuhrava@quick.cz), Michel Martinez (martinez@supagro.inra. fr), Alain Roques (alain.roques@orleans.inra.fr) Academic editor: David Roy | Received 4 February 2010 | Accepted 24 May 2010 | Published 6 July 2010 Citation: Skuhrava M et al. (2010) Diptera. Chapter 10. In: Roques A et al. (Eds) Alien terrestrial arthropods of Europe. BioRisk 4(2): 553-602. doi: 10.3897/biorisk.4.53 Abstract Of the 19,400 native species and 125 families forming the European diptera fauna, 98 species (less than 0.5%) in 22 families are alien to Europe. ‘These aliens constitute 66 species (18 families) of the suborder Brachycera and 32 species (4 families) of the suborder Nematocera. By family in this category, there are 23 Cecidomyiidae species, 18 Drosophilidae, nine Phoridae, eight Tachinidae and seven Culicidae. Another 32 fly species belonging to five families are considered to be alien iz Europe. These invasives native to other European countries are composed of 14 species of Cecidomyiidae, seven Syrphidae, five Culicidae and three species each of Anthomyiidae and Tephritidae. The date of the first record in Europe is known for 84 alien species. Arrivals of alien species of Diptera have accelerated rapidly since the second half of the 20 century. North America appears to be the dominant contributor of the alien flies. The majority of alien Diptera were introduced into or within Europe unintentionally, with only three predators released intentionally for biological control. Alien Diptera are predominantly phytophagous (35.6%), while a lesser portion are zoophagous (28.6%) or detrivorous /mycetophagous (29.6%). Ecological impacts on native fauna and flora have not been documented for any of the alien species established in Europe. How- ever, 14 alien species have economic impacts on crops. Keywords alien, Europe, Diptera Copyright Skuhrava M et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 554 Marcela Skuhravd, Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) 10.1 Introduction Diptera is one of the largest insect orders, with a worldwide distribution. The order includes 172 to 179 families (depending on authors) with about 132,000 species de- scribed which probably underestimates the actual fauna by at least a half. About 19,400 native species and 125 families have been recorded in Europe (Fauna Europaea). ‘The alien entomofauna is comparatively very limited with only 98 species observed to date, i.e. less than 0.5% of the total dipteran fauna in Europe. Commonly called true flies, mosquitoes, midges, deer- and horseflies and house- flies feature among the most familiar Diptera. Flies are not only abundant in popu- lar perception but also have particular veterinary and medical importance for vecto- ring diseases and as pests of agriculture, forestry and husbandry. However, some spe- cies are useful to man as parasitoids and predators of insect pests and as plant pollina- tors. Generally, adults are minute to small, soft-bodied insects with a highly mobile head, large compound eyes, antennae of variable size and structure, and sucking mou- thparts. They have only one pair of functional wings, the second pair being changed into small head-like bodies called halteres. Legs are usually long, with five-segmented tarsi. Adults are usually very active and are found in all major habitats. They are often associated with flowers and with decaying organic matter, but females of some groups are blood-sucking. Larvae are eruciform and legless in most species. They develop ma- inly in moist or wet habitats such as soil, mud, decaying organic matter, and in plant or animal tissues. Only a small proportion of larvae is truly aquatic. The majority are liquid-feeders or microphagous. 10.2. Taxonomy of the Diptera species alien to Europe The 98 species of Diptera alien to Europe belong to 22 different families (Table 10.1), which all have native representatives. A larger number of aliens belong to the sub- order Brachycera (66 species and 18 families) than to the suborder Nematocera (32 species and 4 families). However, this apparently large diversity is confusing. More than 40% of the alien species are either midges (Cecidomyiidae- 23 species) or fruit flies and their relatives (Drosophilidae- 18 species). The other 20 families show less than 10 species each (Figure 10.1). The arrival of these alien species has largely modi- fied the composition of some families such as Braulidae and Drosophilidae where at present aliens respectively account for 33.3% and 14.8% of the total fauna ob- served in Europe. However, the native entomofauna includes 103 additional fami- lies for which no alien species has yet been recorded in Europe, especially for some ecologically and economically- important groups such as Chironomidae, Syrphidae, Asilidae, Tipulidae and Anthomyiidae. The alien dipterans belong to the following families: Diptera. Chapter 10 555 Suborder Brachycera Agromyzidae. All species in the family are phytophagous, including a number of seri- ous pests of cultivated plants. Larvae live in plant tissues, usually forming characteristic galleries as mines. Most larvae live in the parenchyma of leaves, or mine stems, few attack fruits and seeds. The majority of the species are monophagous, some of them are widely polyphagous, attacking different plants of several families. To date, only five alien species have been observed in Europe relatively to 903 recorded native species (Fauna Europaea). However, the alien fauna includes three species of Liriomyza (L. chinensis, L. huidobrensis - see factsheet 14.23, and L. trifolii) which are highly damag- ing to vegetable crops (Arzone 1979, Martinez 1982, Trouvé et al. 1991). Braulidae. Larvae live as commensals within cells of honey-bee nests (Apis species). They feed on pollen, honey and organic debris. Adults are “food-parasites” of adult bees, attaching themselves to the body of the queen or rarely to a worker. They feed on liquids from the mouth of the bees. There is only one genus present in Europe, Braula, which includes one alien species, B. schmitzi (Dobson 1999), and two native species. Calliphoridae. This is a key family for human health. Adults are potential vectors of bacteria, viruses, protozoaires and helminthes because they actively search for and sit on feces, fresh and cooked meat, fish, dairy products, and wounds. Larvae are para- sitoids or predators of living snails, or feed on blood of nestling birds. A few species are obligate producers of myiasis in various animals. Only one alien species, Chrysomya albiceps (Mercier 1927), has been observed in Europe compared to 112 native species. Canacidae (=Tethinidae). Most species are strictly associated with salty habitats (halobionts), e.g. coastal salt marshes, seashore wrack, sandy beaches, shores of inland salt lakes, alkaline springs etc, and only a few species are also known from habitats that are apparently without increased salinity (forests, meadows, deserts). Some species have been reared from deposits of seaweed. ‘There is only one alien species, Pelomyia oc- cidentalis (Irwin et al. 2001), compared to a total of 39 native species. Ceratopogonidae. Biting adults of this family are potential vectors of major ani- mal diseases. In particular, Culicoides species transmit bluetongue orbivirus between ruminant hosts. A species of Afro-Asian origin, C. imicola Kieffer, has been conside- red as the main agent of the recent outbreaks of bluetongue disease in Europe althou- gh some native species could also be involved (e.g., C. pulicarius L. and C. newsteadi Austen complexes (Purse et al. 2007)). However, it seems that the most likely mode of incursion of C. imicola in Europe was via passive transport on the wind as aerial plank- ton (Mellor et al. 2008, Purse et al. 2007). Thus, this species was not considered in this chapter. Dolichopodidae. Adults and larvae of most species are predaceous and feed on soft- bodied invertebrates. They occupy all terrestrial habitats from coastal beaches to high elevations, but they generally prefer humid areas. Larvae are mostly found in moist so- ils or in the litter layer while a few others depend on sap runs and tree rot holes for the- ir development. There is only one alien species, Micropygus vagans (Chandler 2004), in comparison to 790 native species in Europe. 556 Marcela Skuhravd, Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) % species 12 8 4 1800 585 620 790 1185 Cecidomyiidae Drosophilidae Phoridae Tachinidae Culicidae Agromyzidae Sphaeroceridae Tephritidae Ephydridae Milichiidae Muscidae Stratiomyidae Ulidiidae Mycetophilidae Sciaridae Braulidae Calliphoridae Canacidae Dolichopodidae Fanniidae Heleomyzidae Hippoboscidae Chironomidae Syrphidae Ceratopogonidae Asilidae Anthomyiidae Tipulidae Bombyliidae Sarcophagidae Simuliidae Tabanidae ooocoocceo°o°co % species 20 Alien species 30 Figure 10.1. Relative importance of the families of Diptera in the alien and native entomofauna in Eu- rope. Families are presented in a decreasing order based on the number of alien species. Species alien to Europe include cryptogenic species. Only the most important families of native species (> 50 spp.) have been considered. The number over each bar indicates the number of species observed per family. Drosophilidae. Species in this family show very diverse biological habits. The lar- vae of most species develop in fermenting substrates, but some mine living plants. Some species are used as important laboratory animals. Drosophilids occur in all ter- restrial habitats, from lowlands up to alpine meadows. They may be found near the habitats of their insect hosts or preys (mealybugs, bees, wood-boring beetles), around toadstools (Polyporales) and in the flower heads of thistles. Aliens include 18 speci- es in the genera Drosophila (8 species) (Bachli et al. 2002, Grassi et al. 2009), Chy- momyza (4 species) (Band 1994, Carles-Tolra and Andersen 2002, Perju 1959, Trent Band et al. 2005), Zaprionus (3 species) (Chassagnard and Kraaijeveld 1991, Monclus 1976, Tsacas et al. 1977), Scaptomyza (2 species) (Nicoli Aldini 2005, Nicoli Aldini and Baviera 2002) and Dettopsomyia (1 species) (Prevosti 1976) compared to 104 na- tive species. Ephydridae. Adults are usually associated with moist substrates, especially shores, marshes and wet meadows. Some develop in decomposing matter or excrement, other are leaf miners or parasitoids. Aquatic and semiaquatic habitats are typical of the fami- ly. A total of 335 native species occur in Europe with only three alien species - in the genera Elephantinosoma, Placopsidella and Psilopa (Gatt and Ebejer 2003). Diptera. Chapter 10 DDT Fanniidae. Species inhabit forests, rarely open landscape and wetlands. Larvae are generally saprophagous and mostly feed on decaying organic matter as human or ani- mal faeces, decaying material in gardens, and rotting leaf litter. Some species have been reared from fungi, others occur in bird nests, burrows of vertebrates, and nests of social Hymenoptera. There is only one alien species, Fannia pusio (Carles-Tolra and Andersen 2002), compared to 82 native species. Heleomyzidae. Larvae develop in sporocarps of fungi or live in association with my- celia in forest soil, some are necrophagous or saprophagous. ‘There is only one alien spe- cies, Prosopantrum flavifrons (Ismay and Smith 1994) compared to 145 native species Hippoboscidae. Adults are bloodsucking ectoparasites of birds and mammals. Fe- males of all species are macrolarviparous, i.e. retaining the larva in the uterus to the end of the third instar. There is only one alien species, Crataerina melbae (Popov 1995), compared to 29 native species. Milichiidae. Larvae are saprophagous and develop in decaying vegetation, wood detritus, in nests of birds, ants (myrmecophilous species) and of other social insects, but also in excrements, carrion, dead insects and snails. Adults of some species are com- mensals or kleptoparasites of predatory insects and spiders. ‘There are two alien species, in the genus Desmometopa (Rohacek (2006b)), compared to 41 native species. Muscidae. Larvae develop in various kinds of decaying organic matter, often showing facultative or even obligatory carnivorous behaviour. Larvae of some species appear to be predaceous during their entire larval life. Adults feed on nectar or plant sap, sometimes also on decaying liquids and some species are predaceous. Some spe- cies are adapted to anthropogenically-altered ecosystems. Blood-sucking species are of medical and veterinary importance, being vectors of some diseases. There are two alien species, the sorghum pest Athrerigona soccata (Vercambre et al. 2000), and a pre- dator of house flies, Hydrotaea aenescens (Rozkosny 2006, Sacca 1964), compared to 585 native species. Phoridae. Adults are found in all types of terrestrial habitats, particularly in forests and meadows but also in steppe-like and xerothermic sites. Food preferences of lar- vae appear to be remarkably different. Most species are polysaprophagous with diffe- rent degrees of specialisation. Parasitic species are often found in the nests of ants and termites. Some fungus breeders feed on the fungi but others are obligate predators or parasitoids of other fungus feeders such as larval Sciaridae. There are nine alien species in the genera Megaselia (three species) (Campobasso et al. 2004, Disney 2008, Disney and Durska 1999), Chonocephalus (two species) (Disney 1980, Disney 2002), Dohr- niphora (two species) (Disney 2002, Disney 2004), Hypocerides (one species) (Disney 2004), and Puliciphora (one species) (Disney 1983) in comparison to a total of 596 native species. Sphaeroceridae. Larvae and adults are saprophagous. Larvae develop in diverse or- ganic matter and feed as saprophages on microorganisms destroying rotting plants, dung, carrion or fungi and also on the decomposed liquid substances. Adults occur in all habitats that contain the breeding media of the larvae, preferably in damp places. A few polyphagous species are synanthropic, living near human habitats. Many copro- 558 Marcela Skuhravd, Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) phagous species develop in dung heaps near stables or in pastures. There are four alien species, belonging to the genera Thoracochaeta (two species feeding on seaweeds) (Ro- hacek and Marshall 2000), Coproica (one species) (Carles-Tolra and Andersen 2002), and Trachyopella (one species) (Rohacek (2006a)), in comparison to a total of 253 native species. Stratiomyidae. Terrestrial and aquatic larvae of this family live as scavengers. Adults feed on nectar of flowers, exploiting a wide range of flowering plants, especially umbels alongside water margins but also in open sunny places. ‘There are two alien species, the scavenger Hermetia illucens (Venturi 1956), which has been used to control house fly, and a soldier fly, Exaireta spinigera (Lapeyre and Dauphin 2008), compared to a total of 138 native species. Tachinidae. Larvae live as endoparasitoids of arthropod larvae. Many species are parasitoids of important pests of agricultural crops and forest trees and are regarded as economically beneficial. Aliens include 8 species of different genera (Blepharipa, Ca- tharosia, Clytiomya, Phasia, Leucostoma, Sturmia, Trichopoda and Zeuxia) (Carles-Tolra and Andersen 2002, Cerretti 2001, Clemons 2001, Colazza et al. 1996, Vanhara et al. Tschorsnig 2006) in comparison to a total of ca. 870 native species. Tephritidae. So called “fruit flies” because larvae of most species inhabit the fruits or other seed-bearing organs of flowering plants. Larvae are phytophagous, some being leaf miners and stem-borers and others developing in roots. Many species are associated with Asteraceae. Adults feed on pollen and nectar. Some species are pests but others are used as biological control agents of weeds. Aliens include 4 species in the genus Rhago- letis (3 species) (Duso 1991, Lampe et al. 2005, Merz 1991) and the major fruit pest Ceratitis capitata (see factsheet 14.28) in comparison to a total of 264 native species. Ulidiidae. The biology and immature stages are largely unknown. Adults occur in dry, sunny habitats, such as steppe meadows, and thin steppe forests. Larvae are mostly saprophagous and develop in rotting matter, under bark or in dung but a few seem to be phytophagous. Adults live in marshland habitats, woodland areas, sandy, salty or steppe meadows. They are often observed on flowers, shrub leaves, tree trunks, and on excrement and manure heaps. There are only two aliens, compared to a total of 106 native species, Euxesta pechumani, living on carrion and dung (Delage 1969) and Euxesta notata living on bulbs (such as onions) and sometimes considered as a pest (Martinez, unpublished). Suborder Nematocera Cecidomyiidae. Larvae of gall midges are either phytophagous, zoophagous or myco- phagous. Phytophagous species cause galls on various parts of their host plants (hen- ce the common name “gall midges“) but some larvae live free in flower heads or in the stems without making galls, or in conifer cones, or are associated with cambi- um layers of various trees. Some gall-causing species are serious pests of cultivated plants and forest trees. The zoophagous larvae are predators of the larvae of other gall Diptera. Chapter 10 559 midges, aphids, mites, coccids, and other arthropods and some of them are used for biological control of pests. Larvae of several species are endoparasites of aphids, psyl- lids and tingids. This is the dominant group of aliens in Diptera with 23 species (see Table 10.1 for references) but altogether 1800 native midge species are known to occur in Europe. Culicidae. Larvae develop in water. Females of most species are haematophagous and feed by sucking the blood of vertebrates, whereas males may feed on flower nec- tar. Adults may transmit various disease pathogens, viz. viruses, malaria and filarioses. Most Culicidae are distributed in tropical and subtropical areas of the world. Whereas the European native fauna only includes 93 species within this family, seven alien spe- cies have established in Europe: two species belonging to the genus Aedes (the Asian tiger mosquito, A. albopictus- see factsheet 14.27, and the Asian rock pool mosquito, A, japonicus (Schaffner et al. 2009)); three Asian species of the genus Culex (Adhami 1987, Ramos et al. 1998, Samanidou and Harbach 2003) and two species of Ochlero- tatus (Romi et al. 1999, Schaffner et al. 2001). Aedes aegypti, the vector of yellow fever which has been present in Europe for a long time, now seems to be extinct; no exotic species of Anopheles has yet established (Schaffner et al. 2001). Mycetophilidae. Larvae are mycophagous, feeding on the mycelia or fruit bodies of various fungi or myxomycetes. Adults fly in the undergrowth of forests, on meadows and steppe habitats. There is only one alien species, Leia arsona (Halstead 2004) com- pared to a total of ca. 950 native species. Sciaridae. Larvae are mostly free living in the upper soil layer of nearly all terrestrial habitats. Some species develop inside plant stems, leaves or decaying wood. They feed on fungal mycelia or decomposing plant tissue. There is only one alien species, Brady- sia difformis (White et al. 2000), compared to a total of 629 native species. 10.3. Temporal trends of introduction in Europe of alien Diptera The date of the first record in Europe is more or less precisely known for 84 (ie., 86%) of the alien species of Diptera, whilst it remains unknown for the other 14 species (Table 10.1). Considering, cautiously, this first record in Europe as a proxy, the arrival of alien dipterans showed a significant, exponential acceleration since the second half of the 20" century (Figure 10.2). The mean number of new records per year increased from 0.25 during 1900-1950 to 2.2 during 2000-2008. In parallel, an increasing di- versification of the dipteran families involved in the arrivals was observed. Only a few aliens, mostly Cecidomyiidae, were newly recorded during the 19" century. Probably originating from the subtropics, the midge Fe/tiella acarisuga was first found and described in France in 1827 (Vallot 1827) . It was subsequently disco- vered in several other European countries to be finally introduced intentionnally in a large part of the world as a biological control agent for red spider mites in greenhouses. Four more alien dipterans, of which three midges and one fruit fly, were subsequently recorded during the second half of the 19" century, each showing different patterns of 560 Marcela Skuhravd, Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) Mean number of new alien species recorded per year during the period 0 | 2 3 1492-1799 [800-1849 1850-1899 1900-1924 1925-1949 1950-1974 1975-1999 — 2000-2009 Time period Figure 10.2. Temporal changes in the mean number of records per year of dipteran species alien to Europe from 1800 to 2009. The number over each bar indicates the absolute number of species newly recorded per time period. expansion in Europe. Contarinia quinquenota (Cecidomyiidae), developing in flower buds of Hemerocallis fulva (Liliaceae), was first found in Austria in 1885 (Low 1888 and subsequently in 11 other countries. Clinodiplosis cattleyae (Cecidomyiidae), which forms conspicuous swellings on the aerial roots of Cattleya species (Orchidaceae), was first observed in England in 1885 but later only in France (Molliard 1902). Orseolia cynodontis (Cecidomyiidae) was first observed in 1892 in Italy (Massalongo 1892) and then in three other countries. The fruit fly Ceratitis capitata (Tephritidae) was discove- red in Italy in 1873 and subsequently in 15 other European countries. The first half of the 20" century saw the arrival of 13 more alien dipterans of which six are Cecidomyiidae, five Drosophilidae, one Calliphoridae and one Stratiomyidae. Two of these species have not shown any expansion in Europe. A cecidomyiid from tropical Asia, Procontarinia matteiana, was only first observed in 1906 within the Bo- tanical Garden of Palermo (Sicily), galling leafs of a plant imported from India, Man- gifera indica (Anacardiaceae) (Kieffer and Cecconi 1906). According to recent infor- mation, the host plant has subsequently died out; this alien midge may be considered as extinct in Europe. Discovered in England in 1913, a North American midge, Rho- palomyia grossulariae, causing galls on Ribes grossularia (Grossulariaceae), has not been found anywhere else since that time (Theobald 1913). On the contrary, an other North American midge, Janetiella siskiyou (=Craneiobia lawsonianae), which develops in co- nes of Chamaecyperis lawsoniana (Cupressaceae), was first observed in the Netherlands Diptera. Chapter 10 561 in 1931 (Meijere 1935) and subsequently in 10 further countries. A gall midge of Asi- an origin, Rhopalomyia chrysanthemi, damaging leaves of cultivated Chrysanthemum (Asteraceae), was observed in France and Denmark in 1935 (Bovien 1935) and subse- quently found in greenhouses of eight more countries. An other Asian midge, Stenodi- plosis panici, developing in inflorencesces of Panicum miliaceum (Poaceae), was disco- vered in southern Russia in 1926 (Dombrovskaja 1936) and then in four other coun- tries. The African predatory midge, Dicrodiplosis pseudococci, attacking the scale Plano- coccus citri (Pseudococcidae) was found in Italy in 1914 (Felt 1914) and then in Spain. Five Drosophila species of unknown origin were first found in Great Britain in 1900 and then in several countries of northern and central Europe. The cryptogenic Chryso- myia albiceps (Calliphoridae) was recorded in 1927 in France (Mercier 1927) and later expanded to most of southwestern and central Europe. Finally, a Stratiomyidae, Her- metia illucens, was first discovered in Malta in 1936 but subsequently spread to 6 more countries (Venturi 1956). The second half of the 20th century consisted of two distinct periods of invasion of alien dipteran species. From 1950 to 1974, only seven new alien species (i.e. 0.2 speci- es per year on the average) were recorded. ‘They belong to families Cecidomyiidae (Con- tarinia citri (Genduso 1963) and Stenodiplosis sorghicola (Starostin et al. 1987), both of African origin), Dolichopodidae (Micropygus vagans found in Great Britain in 1970 (Chandler 2004)), Muscidae (a north American predator of house fly, Hydrotaea aenese- cens (Sacca 1964)), and Sciaridae (Bradysia difformis recorded from Great Britain in 1965 (White et al. 2000) and subsequently found in Northern Europe). In contrast, a total of 39 alien species were subsequently observed in Europe from 1975 to 1999 (i.e. 1.6 species per year on the average). These later invasions involved a much larger number of dipteran families than previously. By order of importance, families include Drosophilidae (eight species), Cecidomyiidae (six species), Culicidae (six species among which the tiger mos- quito, Aedes albopictus, arrived in 1979 in Albania (Adhami 1987)), Phoridae (five speci- es, including the mushroom pest Megaselia tamilnaduensis in 1999 (Disney and Durska 1999), Tachinidae (three species), Tephritidae (three species of Rhagoletis fruit pests), Ag- romyzidae (three species among which the crop pests Liriomyza trifolii in 1979 (Agui- lar & Martinez 1979) and L. huidobrensis in 1989 (Trouvé et al. 1991)), and one speci- es in the families Braulidae, Heleomyzidae, Hippoboscidae, Muscidae, and Mycetophili- dae. Since 2000, alien dipterans were observed in Europe at a proportionally higher rate, with 20 species newly recorded from 2000 to 2009, i.e. an average of 2.2 species per year. In addition to families already represented by alien species such as Phoridae (four speci- es) (Disney 2002, Disney 2004), Cecidomyiidae (four species among which the quick- ly spreading Obolodiplosis robiniae galling Robinia pseudoacacia (Duso C and Skuhrava 2003) - see factsheet 14.26) (Calvo et al. 2006, Gagné 2004, Harris and Goftau 2003), Drosophilidae (three species), Agromyzidae (two species) (Bella et al 2007, Siiss 2001), Culicidae (Schaffner et al. 2003), Stratiomyidae (Lapeyre and Dauphin 2008) and Ulidii- dae (one species each) (Martinez, unpublished), representatives of two new families were observed: Ephydridae shore flies (three species mostly linked to poultry dung) (Gatt and Ebejer 2003) and Canacidae (one species) (Irwin et al. 2001). 562 Marcela Skuhravd, Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) 10. 4. Biogeographic patterns of the dipteran species alien to Europe 10.4.1. Origin of alien species A region, or more simply a continent, of origin could be traced for only 78 of the 98 dipteran species alien to Europe, i.e. in ca. 80% of the species. However, in a number of cases, the origin of the dipteran species could only be assumed from that of its host. Several species of Cecidomyiidae illustrate the difficulties and uncertainties in assigning origins. Some species were found and described for the first time in Europe but it is likely that they are non-native and introduced together with their host. For example, the Asian origin of a gall midge Procontarinia matteiana, first described in Sicily (Kieffer and Cecconi 1906), and the African origin of Orseolia cynodontis, another gall maker on Cynodon dactylon (Poaceae), first discovered at Verona (Italy) (Massalongo 1892), were assumed from the source of their host plants, imported from India and North Africa, respectively. Similarly, that of Dicrodiplosis pseudococci, a predator midge of a scale, Planococcus citri (Pseudococcidae), also discovered in Sicily (Felt 1914), was assumed from the subtropical and tropical origin of its insect prey. Ihe cases of Rhopalomyia grossulariae and Dasineura gibsoni are even more com- plex. The larvae of Rhopalomyia grossulariae which develop in enlarged, deformed leaf buds of Ribes uva-crispa (Grossulariaceae) were first discovered in Ohio (USA) and were later found in Great Britain (Theobald 1913); specimens of Dasineura gibsoni were described developing in flower heads of Cirsium arvense (Asteraceae) in Ot- tawa, Canada (Gagné 1989), before being also found in Great Britain (Harris 1976). Both species were thus considered to be native of the Nearctic, and then introduced to Europe. However, both host plants are not Nearctic species but archaeophytes of Eurasian origin. Therefore, R. grossulariae as well as D. gibsoni might also be of such origin. However, neither larvae nor adults of these two species have been discovered in continental Europe until now. Further genetic studies may contribute to tracking the exact origin of such species. In contrast to the general trend observed for arthropods and insects, North Amer- ica appears to be the dominant contributor of the alien dipteran fauna, with almost one-third of the species originating from this continent, far beyond Asia whilst a sig- nificant percentage of species came from Africa (Figure 10.3). The 30 alien species originating from North America consists of Cecidomyiidae (10 species), Drosophilidae (6 species), Sphaeroceridae (3 species), Tephritidae (3 spe- cies; the fruit fly pests Rhagoletis completa, R. cingulata and R. indifferens), Ulidiidae (2 species), and Agromyzidae, Canacidae, Culicidae, Muscidae, Stratiomyidae, and Ta- chinidae (one species each). ‘The insects originate from various part of this large con- tinent; for example Janetiella siskiyou (Gagné 1972) and Resseliella conicola (Gagné 1989, Skuhrava et al. 2006) developing in cones of Abies and other conifers (Pinace- ae) from the northwestern region whereas Obolodiplosis robiniae and Dasineura gledit- chiae (Gagné 1989) developing in leaflet galls on Gleditsia triacanthos (Fabaceae) arri- ved from the northeast. Diptera. Chapter 10 563 Africa Cryptogenic ; 20.4% 6.3% Tropical 3.1% C&S America =~ —_ Asia 5.1% 19.4% Australasia / 5.1% North America 30.6% Figure 10.3. Origin of the 98 species of Diptera alien zo Europe. The 19 dipteran species coming from Asia consists of six species of Cecidomyiidae, five species of Culicidae, two species of Agromyzidae, Phoridae and Tachinidae, and one species of Drosophilidae and Ephydridae. Most species originate from the tem- perate, eastern Asia such as Contarinia quinquenotata damaging flower buds of He- merocallis fulva (Liliaceae), Epidiplosis filifera, a predator of the coccid scale Ceratopla- tes floridensis on citrus fruits (Nijveldt 1965), and probably Rhopalomyia chrysanthemi (Cecidomyiidae) (Barnes 1948) whilst Cerodontha unisetiorbita (Agromyzidae) (Siiss 2001), Aedes japonicus (Culicidae) (Schaffner et al. 2009) and Drosophila curvispina (Drosophilidae) (Bachli et al. 2002) originate from Japan. However, tropical Asia, ma- inly India, has also contributed to the alien entomofauna, having supplied Aedes al- bopictus (Eritja et al. 2005), Culex tritaebiorhynchus (Samanidou and Harbach 2003), C. vishnui (Culicidae) (Adhami 1987), Placopsidella phaenota (Ephydridae) (Gatt and Ebejer 2003), Procontarinia matteiana (Kieffer and Cecconi 1906), Horidiplosis fici- folii (Cecidomyiidae), causing leaf galls on Ficus benjamina (Moraceae) (Harris and Goffau 2003), and Megaselia tamilnaduensis (Phoridae) (Disney and Durska 1999). A few species came from Middle East (Leucostoma edentata; Tachinidae) (Chassagnard and Kraaijeveld 1991) and Western Asia (Ochlerotatus subdiversus, Culicidae) (Schaff- ner et al. 2001). The 16 species coming from Africa consist of Cecidomyiidae (five species), Droso- philidae (three Zaprionus species), Phoridae (three species), Ephydriidae (two species), and one species of Tephritidae (Ceratitis capitata), Culicidae and Mycetophilidae. In addition to the species mentionned above (D. pseudococci and O. cynodontis), midges include Stenodiplosis sorghicola associated with Sorghum (Poaceae), and Contarinia cit- ri developing in flower buds of Citrus sp. (Rutaceae), which probably originates from Mauritius. The Phoridae species came from tropical Africa. 564 Marcela Skuhravd, Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) Five alien dipteran species of different families are known to originate from Cent- ral and South America. They include Clinodiplosis cattleyae (Cecidomyiidae) from Bra- zil (Gagné 1994), Liriomyza huidobrensis (Agromyzidae) from South America (Trouvé et al. 1991) before having been introduced in Central America, Asia and Africa, Fan- nia pusio (Fanniidae) (Hill et al. 2005), Prosopantrum flavifrons (Heleomyzidae) (Ismay and Smith 1994), and the recently- arrived, Phytoliriomyza jacarandae (Agromyzidae) (Bella et al 2007). Another 5 dipteran species originate from Australasia, viz. Micropygus vagans (Do- lichopodidae) from New Zealand (Chandler 2004), Megaselia gregaria (Phoridae) from Tasmania (Disney 2002), Coproica rufifrons (Sphaeroceridae) from Papua-New Gui- nea (Carles-Tolra and Andersen 2002), Exaireta spinigera (Stratiomyidae) from Austra- lia (Lapeyre and Dauphin 2008), and Dohrniphora cornuta (Phoridae) from Australa- sia (Disney 2002). Three other dipteran species are only known to originate from the tropical and subtropical parts of the world. They include Dettopsomyia nigrovittata (Drosophilidae), which has been found only once in Canary islands (Prevosti 1976), Puliciphora borin- quenensis (Phoridae), found only once in Great Britain (Disney 1983) and Megaselia scalaris (Phoridae), a saprophagous species which may be dangerous to human health and has largely spread in western and central Europe (Disney 2008). 10.4.2. Distribution of alien species in Europe Alien dipteran species and families are not evenly distributed throughout Europe. Large differences exist between countries in the number of alien species present within each territory (Figure 10.4). As for the other arthropod groups, it may reflect differences in sampling intensity and in the number of local taxonomists specialized in these families. The number of alien dipterans is significantly and positively correlated with the country surface area (after log-transformation; P= 0.0282). Indeed, Great Britain hosts the largest number of aliens (36 species of 11 families), followed by continental Spain (33 species; 17 families), continental France (29 species; 13 families) and continental Italy (28 species; 11 families). However, the family diversity is similar in three coun- tries of Central Europe of much smaller size, the Czech Republic, Switzerland, and Slo- vakia which host each 11 families of alien dipterans for ca. 20 species. Although the western and southern countries seem to host more aliens (Figure 10. 4), the number of species per country relatively to their size is not correlated with longitude (P= 0.4106) nor with latitude (P= 0.3896). The European islands host proportionally more alien dipterans than continental countries relatively to their size (Kruskall- Wallis test on the number of aliens per km’; P=0.0098). Thus, 14 alien species of 10 families were found in the small island of Malta occupying 316 km? in the Mediterranean Sea. Most alien dipterans still have a very restricted distribution. More than 30% of the species (30 species) have been observed in only one country such as Culex deserti- cola (Culicidae) and Dohrniphora papuana (Phoridae) as yet only recorded from Spain Diptera. Chapter 10 565 Number of alien species [nodata || 10-19 I 30-39 a > Figure 10.4. Comparative colonization of continental European countries and islands by dipteran spe- cies alien zo Europe. Archipelago: | Azores 2 Madeira 3 Canary islands. (Disney 2004, Eritja et al. 2000, Ramos et al. 1998), Chymomyza wirthi (Drosophi- lidae) in Great Britain (Gibbs 1994), Placopsidella phaenota (Ephydridae) in Malta (Gatt and Ebejer 2003), and Exaireta spinigera (Stratiomyidae) in France (Lapeyre and Dauphin 2008). Another 17 species are present in only two, often nearby, coun- tries such as Cerodontha unisetiorbita (Agromyzidae) found in Italy and Albania (Siiss 2001), Drosophila suzukii (Drosophilidae) in Spain and Italy (EPPO 2010) and Culex tritaeniorhynchus (Culicidae) in Albania (Adhami 1987) and Greece (Samanidou and Harbach 2003). No alien Diptera is present in more than 24 of the 65 countries and large islands of Europe. Only 9 species have been introduced or have expanded in 15 countries or more. Most are plant pests such as the agromyzid leaf miners Liriomyza huidobrensis (24 countries) (EPPO 2006, Fauna Europaea) and L. trifolii (22 coun- tries) (Fauna Europaea), a midge Obolodiplosis robiniae (20 countries) (Glavendeki¢ et al. 2009), and a fruit fly Ceratitis capitata (20 countries) (Fauna Europaea). The Tiger mosquito, Aedes albopictus, and the predator midge, Feltiella acarisuga are also 566 Marcela Skuhravd, Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) present in 13 and 21 countries, respectively. In most cases, it is not known whether the species has expanded naturally once established in a country or if the extended distribution corresponds to repeated introductions from abroad. However, very pa- tchy distributions probably result from independent introductions. Thus, Hypoceri- des nearcticus (Phoridae) was found in Spain and Sweden (Disney 2004), and Copro- ica rufifrons (Sphaeroceridae) in Malta and in the Canary islands (Carles-Tolra and Andersen 2002). In contrast, the occurence of an alien species within a whole geo- graphic region is likely to proceed, at least partly, from natural dispersion such as for Pelomyia occidentalis (Canacidae) which is currently present throughout Central Eu- rope (Czech Republic, Germany, Hungary, Poland and Slovakia) (Roha¢ek (2006a), Rohacek (2006c)). Some other species are known to combine both methods of dis- persal. Aedes albopictus was introduced independently by human activity in Albania, France, Italy, Netherlands but probably spread naturally along the Adriatic coast (see map on factsheet 14.27). The honeylocust gall midge, Obolodiplosis robiniae, also spread very rapidly throughout Europe (Glavendeki¢ et al. 2009). Four years after its discovery in Italy in 2003, it occupied a large area from southern England in the west to eastern Ukraine in the east and from northern Germany to southern Italy (see map on factsheet 14.26). Dipterans alien in Europe, i.e. originating from one part of Europe and introdu- ced through human activity in an other part, are a matter of debate because it is of- ten difficult to discriminate between a natural expansion, an introduction, or simply a lack of previous information regarding the actual species* native range. Table 10.2 present some of these species. They include species of Mediterranean origin, likely to have been introduced with their Mediterranean hosts in more northern countries, for example Monarthropalpus flavus, a gall-maker of common box (Buxus sempervirens) in Central-European countries. In addition, the date of first record is likely to differ lar- gely from the date of arrival for a few species specifically associated with archaeophyte plants. For instance, two gall midges, Contarinia pisi and C. lentis, specifically galling plants in the family Fabaceae, Pisum sativum and Lens culinaris respectively, have been recorded in Europe only rather recently, although their host plants have been introdu- ced for cultivation since the prehistoric times, probably from the Mediterranean region or the Middle East. Other species followed their host plant introduced from continen- tal Europe to islands on which the plant was absent. Dipterans specifically related to larch such as several species of Strobilomyia larch cone flies (Anthomyiidae) (Ackland 1965; Roques, unpubl.) and a larch gall midge, Dasineura kellneri (Hill et al. 2005) or to spruce (a spruce cone gall midge, Kaltenbachiola strobi) (Hill et al. 2005) are thus considered to be alien zz Great Britain. 10.5. Main pathways of introduction to Europe of alien dipteran species Intentional introductions represent a much smaller proportion of alien arrivals in Dip- tera than the average in arthropods in general (3.1% vs. 10%). Only three dipteran Diptera. Chapter 10 567 predators of different families were introduced intentionally for biological control and have subsequently become established. Two of them, Hydrotaea aenescens (Muscidae) and Hermetia illucens (Stratiomyidae), were released from North America to control houses flies in poultry farms and stables (Sacca 1964). The third species, Feltiella aca- risuga (Cecidomyiidae), is a cryptogenic species of cosmopolitan distribution preying exclusively on tetranychid red spider mites. Larvae and adults were found in several countries of Europe, in northern Africa, Asia, North America, Australia and New Ze- aland. It has been intentionally released, mostly in glasshouses, in Italy, Denmark and Poland, to protect crops. Similarly, as for the other taxa, trying to identify pathways for the remaining 97% of accidental introductions is not a straightforward task. In a number of cases, it how- ever could be inferred from the species biology, for that of the plant/animal host or from repeated interceptions with merchandise at borders. Thus, eggs and larvae of the Asian tiger mosquito, Aedes albopictus, and those of the Asian rock pool mosquito, A. japonicus, have been shown to be imported as stowaway through the trade of second- hand tyres (Reiter 1998, Schaffner et al. 2009). Larvae of A. albopictus were also found inside bags watering “lucky bamboos” (Dracaena senderiana) for horticultural markets. Larvae, such as these of Liriomyza spp., that are leaf-miners of vegetable crops, are regularly intercepted at borders along with agriculture imports, as well as fruits infested by larvae of Ceratitis capitata and Rhagoletis spp. More generally, pathways can be hypothesized for about a half of the 95 alien Diptera which were accidentally introduced. Horticultural and ornamental trade is probably the most significant pathway, with a total of 30 species more or less closely associated. Horidiplosis ficifolii, a midge causing leaf galls on Ficus benjamina (Mora- ceae) was probably imported with infected fig plants in containers from South-eastern Asia (Taiwan) as well as the midge Asphondylia buddleia, developing in swollen aborted flowers of Buddleia racemosa (Scrophulariaceae), from El Salvador to southern France (Beguinot 1999). A similar process is likely to have occurred for the agromyzids Cero- dontha unisetiorbita with Phyllostachys bamboos imported from south Asia (Stiss 2001), and Phytoliriomyza jacarandae developing on ornamental blue Jacaranda trees (Jacaran- da mimosifolia) introduced to Sicily and mainland Italy (Bella et al. 2007). Some other gall midges are assumed to have been transported to Europe with seedlings of plants for planting as very small larvae hidden in undeveloped plant organs, as for example Odo- lodiplosis robiniae, Dasineura gleditchiae, Dasineura oxycoccana and Prodiplosis vaccinii, the two last species developing in bud galls of cultivated species of Vaccinium (Erica- ceae) in North America (Gagné 1989). Orchid trade was probably responsible for the transport of the midge Clinodiplosis cattleyae whereas cone and seed trade can be assu- med as the vector of a seed midge, Janetiella siskiyou, infesting Chamaecyprais lawson- niana (A. Murr.) Parl. and a cone midge, Resseliella conicola on Picea sitchensis (Bong.) Carriére. Comparatively few species (10) have larvae that appear to be associated with the trade of vegetable crops (the agromyzids L. huidobrensis and L. trifolii with a large number of different crops; L. chinensis with Allium; the cecidomyiids Stenodiplosis pa- 568 Marcela Skuhravd, Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) nici with Panicum and S. sorghicola with Sorghum) and fruit crops (the midge Conta- rinia citri with Citrus, and the tephritids Ceratitis capitata, Rhagoletis completa, R. cin- gulata and R. indifferens). The movement of stored products seems responsible for the introduction of another 10 species, mostly drosophilds but also several species associ- ated with the mushroom trade such as the phorids Megaselia tamilnaduensis (Disney and Durska 1999) and M. scalaris (Disney 2008) and the mycetophilid Leia arsona (Halstead 2004). Movement of compost is the problable pathway for two species of Stratiomyidae, Exaireta spinigera (Lapeyre and Dauphin 2008) and Hermetia illuscens (Venturi 1956). Finally, three species are associated with animal husbandry such as Crataerina melbae (Hippoboscidae) (Popov 1995) and Chonocephatus depressus (Phori- dae) (Disney 2002). 10.6. Ecosystems and habitats invaded in Europe by alien dipteran species Alien dipterans predominantly exhibit phytophagous habits (35 species- 35.6%). However, zoophagous and detrivorous/mycetophagous species each represent nearly one-third of aliens (28.6% and 29.6%, respectively) whilst the feeding habits remains unknown for ca. 2% of the species. Leaves constitute the most important feeding niche for the alien phytophagous species (24 species), far beyond fruits (10 species including cones and seeds). Leaves are exploited by “true” leaf miners (agromyzids and cecidomy- ids) and by gall-makers (cecidomyids) but not by external feeders. About 85 % of the alien Diptera seem to have firmly established in their new Eu- ropean environment and its habitats. However, there is little evidence of the establis- hment status of the 15 % remaining species which have been recorded only once or twice. Nearly 65% (64.1%) of the alien Dipteran species established in Europe are only present in man-made habitats, essentially around and in buildings, in agricul- tural lands, parks and gardens and glasshouses (Figure 10.5). This proportion is not significantly different from the average value observed for all arthropods. In addition, 16 of the 35 phytophagous aliens (45.7%) remain strictly related to their original, ex- otic plants used as ornamentals at the vicinity of human habitations such as Cerodon- tha unisetiorbita on bamboo, Dasineura gleditchiae on Gleditsia, Asphondylia buddleia on Buddleia, Obolodiplosis robiniae on honey locust Robinia pseudoacacia. Woodlands and forests have been colonized by a few alien species (11.7 %). The remaining species occur quite equally in diverse natural and semi-natural habitats, viz. in coastal areas, inland surface waters, mires and bogs, grasslands, and heathlands. 10.7. Ecological and economic impact of alien dipteran species Like most insects, alien dipteran species are better known for their economic and sani- tary impact than for their ecological impact. Indeed, ecological impacts on native fauna and flora are not documented at all for any of the species established in Europe. Nega- Diptera. Chapter 10 569 Percentage of alien dipterans living in the habitat l0 20 30 oO Coastal areas- B (0 6 Inland surface waters- C 4 Mires and bogs- D -( 4 Grasslands- E Heathlands- F (0) 4 Woodlands and Forests- G (12 Inland without vegetation- H | i Agricultural lands- | (00 18 Parks and gardens- |2 (008 17 Buildings, houses- | (i 25 Greenhouses- ]|00 (0 c Habitats Figure 10.5. Main European habitats colonized by the established alien species of Diptera. The number over each bar indicates the absolute number of alien dipterans recorded per habitat. Note that a species may have colonized several habitats. tive economic impacts on crops have been recorded for a total of 14 species. They in- clude the agromyzid leaf miners Liriomyza trifolii and, more especially, L huidobrensis, whose larvae mine a wide range of vegetables and ornamental plants in glasshouses in a large part of Europe but also outdoors in the Mediterranean basin (see factsheet 14.23, 14.24). Of economic importance are also the tephritid fruit flies. Ceratitis capitata damage fruits of many host plants and has a large impact on fruit crops, especially cit- rus fruits and peach, all over the Mediterranean basin but also in some countries of cen- tral Europe (see factsheet 14.28). Other fruit fllies in the genus R/agoletis, affect cherry (R. cingulata and R. indifferens) (Lampe et al. 2005, Merz 1991) and walnut crops (R. completa) (Duso 1991, Merz 1991) in Western Europe. The recently introduced Dro- sophila suzukii is also a fruit pest (EPPO 2010). Some mycetophagous species have a local impact on cultivated mushrooms (Megaselia tamilnaduensis, Megaselia gregaria, and Bradysia difformis) (Disney 2008, Disney and Durska 1999, White et al. 2000). Two other species of midges, Stenodiplosis panici and Stenodiplosis sorghicola developing in inflorescences of Panicum and Sorghum, respectively, may become economic pests in the future if the development conditions become more suitable for outbreaks. Positive impacts are considered for the 3 dipteran species deliberately introduced to Europe for biological control of house flies and tetranychid mites (see 10.5). However, their possible ecological impact on the native, non-target fauna is not documented. 570 Marcela Skuhravd, Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) Figure 10.6. Some alien midges and their damage. a Unopened and swollen flower bud (right) of Heme- rocallis fulva caused by larvae of Contarinia quinquenotata b leaflets of Gleditsia triacanthos changed into galls by larvae of Dasineura gleditchiae ¢ Leaf bud gall on Pisum sativum caused by larvae of Contarinia pisi d Fruits of Pyrus communis heavily deformed by larvae of Contarinia pyrivora e female of Dasineura kell- neri sitting on the bud of Larix decidua and laying eggs f Swollen buds of Larix decidua capped with resin caused by larvae of Dasineura kellneri g Galls in form of indistinct shallow blisters apparent on both sides of the leaf of Buxus sempervirens, caused by larvae of Monarthropalpus flavus h Rolled leaf margins of Py- rus communis caused by galls of Dasineura pyri. Diptera. Chapter 10 571 Some other alien predators which have been accidentally introduced such as Dicro- diplosis pseudococci and Epidiplosis filifera, may be used for biological control of coccids in the future. A total of 7 alien dipterans may have a sanitary impact on human and animal health. Six of the 7 introduced species of mosquitoes in the family Culicidae are capa- ble of transmitting diseases through female bites (Taylor et al. 2006). The most impor- tant one, Aedes albopictus, is now established along the Mediterranean coast from south eastern France to northern Greece and is the vector of Chykungunya disease as well as many arboviruses, avian plasmodia and dog heartworm filariasis (see factsheet 14.27). Other alien culicids may be vectors of the West Nile virus (Aedes japonicus (Schaffner et al. 2009), Culex tritaeniorhynchus, C. vishnui, O. atropalpus), Japanese encephali- tis (A. japonicus, C. tritaeniorhynchus) and Sindbis virus (C. tritaeniorhynchus). In ad- dition, a detrivorous phorid, the scuttle fly Megaselia scalaris, may be a cause of aller- gies whilst it is reported in tropical areas to cause wound and intestinal myiasis in hu- mans (Disney 2008). Besides their measurable economic impact, some other alien dipterans may have an aesthetic impact because their oubreaks drastically changes the foliage of ornamen- tal species in town parks and private gardens, even if the damage occurs on exotic, introduced trees. Such aesthetic impact has been observed for three midges at least, Dasineura gleditchiae causing galls on leaflets of Gleditsia triacanthos (Dini-Papanastasi and Skarmoutsos 2001), Obolodiplosis robiniae causing galls on leaf margins of Robinia pseudoacacia (Glavendekié et al. 2009, Skuhrava et al. 2007), and Contarinia quinqueno- tata preventing flowering of Hemerocallis fulva in gardens (Halstead and Harris 1990). References Aartsen van B (2001) Rhagoletis indifferens, een nieuwe boorvlieg voor de Nederlande fauna (Diptera: Tephritidae). Nederlandse Faunistische Mededelingen 14: 19-22. Ackland DM (1965) Two new british species of Anthomyiidae (Diptera) with taxonomic notes on related species. 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Vv SLADIVIS DYASVBIYT MS ‘IS “AS ‘Ld (9007) 3P2°°W “(Z007) asnoy “Td ‘ON ‘AD SNOIOA (OIGI ‘Poon) Adusiq] ‘(ZO0Z) UesIopuy pur eITOT -sapreD | woosysnpy Vid “ad ‘ZD vIsepersny nq] WV VIAVBIAS DYASUBIY SNOJOA (996| “Joleurs10q) (F007) Aeusiq SA ‘F007 BOY -n0q| VW snaysavau sapisav0dE] SNOJOA GO6I ‘sonig (F007) AeusIG, Sa ‘F007 POL nog] V vuundnd voy diusgoq spuryst pure serunos | pue sdomg asurs satgad§ S2TUIIIFOY eugqey popeauy] UI prosar3s— | aaney swIssy | snieI¢ Ayrure.y DID Diptera. Chapter 10 Jolepol gy 8/61 Tesnpy (1007) 13943929 LI ‘S661 eIsy | /olisereg V VI~IUMPI VULOISOINIT Jorepai (Z881 ‘ouyosii+y) (L007) suoweyD uMouyuy) AD ‘L007 | 2uesoidAry | ponisereg}] 5 SUOMIGLDG VISBY Joep (68Z] “Jezueg) (ZOOZ) USsIOpuY pur eI[OT -sopreT uMouyuy) qd ‘Sq otuasoiddry | jomisereg) 9 ynuruos ploy’) Ld Joyepary (SI8T ‘U9TTed) (ZOOT) UasIopUY pur eI[O] -sopTe7) uMmouyur) ‘dD ‘Sa ‘dV otuasoiddry | jomisereg) 5 VAVULBAG VISOLVYID’) (9007) srusioMpsy, fe 39 Sra Oe pete (GE6I ‘TEUSET) ereyurA “(ZQO0T) Uasiopuy pur eI[OT -sapre7 uMOUxu() ‘Sq “ZOD SAV oruasoid Ary /onisereg ey TAIUIYIS vdiavy dag seprurygoey, So asnoy jo JosIUOD IOy pesn ‘soary Ld 2aq ‘Arinod ‘LW ‘LI Ud (9S6T) ‘sdeoy ‘NVO-Sa “IVE eoLouy | snosoa (9CZ] ‘snavuurq) LINIUIA ‘(ZYOZ) Uasopuy Pur eI[OT -SapIeD) isoduroo aS Ota SETS) yMoN nog] Vv SUaINGL VIPGULLIET sasnoy SNOJOA (OE8T ‘UUPUTApsI\\ ) (8007) urydneq pur asdadey] soduro7) I Wi UWA ‘8007 | elsepensny -n9q} WV paadtuids vIastUxy seprAWonens MS ‘LW ‘NH “AYONUD 9861 (P9007) 7>2F4°U snoseyd ‘NVO-Sa ‘Sa eolouy | snosoa TTeysIePy 29 yoovyoy ‘(TOOT) Ussiopuy pur vITOT -sopIe7) -o1des ip whe Baka YON -9q V DIULULVAIS wyjad oly Ive]. aS POLIOWy SnOIOA (SZ6I Jeynds) (000Z) TTe4sIeEWY pure yooeyoy poomeag ‘ON ‘9D SIG TD ‘6661 YON nq] WV VISOIIJAS DIQVYIOIVLOY I. eoriaury | SMOJOA (SZ6T seynds) (000Z) TTe4SIeEW pure yooeyoy poomeas LI ‘aD TD ‘6661 YON -noq| VW 1uosugol vIaVYIOIVAOY] spuryst yunos pure sermunos | pue sdomyg aSuri satgad§ SdTUIIIFOY eugqey poprauy] UI p10daI IST JATIVNT swIssy | snieI¢ Ayrure.y Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) Z > Marcela Skuhrav 596 *‘(poreangyno) voloury | snosey ZTEG] “uUeIIND (L661) 249 | SUNY sauna ral HD} HO ‘E861 qYON| -o4yg] Vv suasaffipus st4ajoovyy (6661) BUNZeZ Pur xellas IS ‘LI YH Wa voloury | snoseyd 6Z6I ‘uossaiy (1661) ZW “(P007) Odd ‘(166T) Osnq | sumuy sumpsnf CI] “Ad “HO “IV LI ‘T661 qYON| -o4yg] Vv pyapqusoa si4ajo5vyy (vUu1q01aS aq npod g UNIAD Ef (9007) 249925 “(SO0Z) ‘Te 2°| pyr) sara is voloury | snoseyd ZOQI ‘MOOT odurey “(Z00Z) Odd ‘(1007Z) Uesuey ueA EAE cI“D| “IN ‘OH “ad Ad “€66l yon | -ovyg) V VIVINSULI S14aJ05vYY Us ‘IS “‘GVW:Ld ‘OZV-Ld ‘Ld “AW ‘OIS-LI VSL TT ‘D “Ud “NVO “Sd “TVa-Sa (0961) ¥9+40d “(900Z) PACTOYUDY (snoSeyd LOE TON TAC) snoseyd (PZQ] “uURWIApar\ ) ‘(ZQOZ) UasIOpuY pur eI[O] safe | -Ajod) samms7 I ‘gq “LV “IV LI ‘EZ81 POLY -o1Ayg V vavidvd siqiqvsa’y seppnydey, Jolepoi gy IZG6[ ‘Sieruofoyy (1007) 13943979 uMOUyU/) LI ‘S661 eIsy | /onisereg| VW puvlaz vIXnIz snqyuns uaaI3 (9661) Te 39 usJayNos JIS-LI volo | Jowporg (I8ZI ‘snouge,) PZZE[OD “(TOOT) USsIopuY puR eI[OT-sare_D | ‘snq ysenbs TT Ma “Si “TV YON | oniseieg| VW sadiuuad vpodoys14] (vo1qUuBLY ‘stsdoapy) soTpso1ng Joepori J (PT8I (ZOOT) UasIopuUY pure eI[O] -sopIe7) preueq g}oruasoiddAry | jonisereg| 3 uaa) Y7/2g VIMANIS spuryst yuNOD pure sermunos | pue sdomyg asuel satgad§ SIDUIIIFAY eugqey poprauy] UI proser3s— | aaneyy swIssy | snieI¢ Ayrure,y 597 Diptera. Chapter 10 (P900Z) YooRyoy ‘voedoiny euney “(696[) asejaq ‘(Z00Z) Uesiopuy pur esjOT -sapre| (peystjqnduy)) zounseyy SIDUDIIFIY sunp SUOLIIED) aenqeH MS ‘Ud ‘Sd “HO ‘Od Spuryst pur soiun0s peprauy Ud “6961 pure odoimyq UI pro0daI IST POLIOWYy YON POLIOUIY YON oSuvri DATION SNOJOA -19q é snoseyd -olAyg ‘snOIOA -10q WISI snjejsg See “uRIIND tupungoad vysaxnq (O€ST ‘UURWAprT\) VIVIOU VISAXNT oepmPAN satgad§ Ajrurey Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) , os Marcela Skuhrav 598 (ZT6T) US8](NL “(L LT) PreqoPuL, “(226 1) Seung (9007) ‘ye Jo PAPIYNYS “(1G6G6T) ‘Je 39 PAPIYNYAS ‘(GQOZ) ‘Te I9 PARIYNYS (6007) AaeryNyYS pure PaeryNys “(Q9G61) AaesyNyS pur earrynyS ‘(Q00G) TR PRAL eAOUNS “OG6T) Te 1 gor -eAOUNIS “(OC61) WO ‘IS “AS urkoyps ‘(Z/6]) aeysnelyposua, pur sryppojig (6C6T) nlsag ‘AY ‘SU “OU “Td ‘ON “IN ‘AT ‘IT ‘ ‘Te 19 srystuyeyeg ‘ aTaflayy ‘ eAd | (9002) ‘Te 39 srysTupeyed “(1 161) he ‘(696T) PAceUEY] ‘AH ‘49 Wa ‘la (OS81) M20T “(EEGT) JoIeYIOIUTY\ pure Jouny “(ZP6T) [easly] winatqws Waa ZO BD visy| snoseyd (OS8I ‘(8681) PHD “(7Z6T) SMISIOT “(GE6T) TYN ‘(8C61) sMIqUIy UST ‘Dd “AGSLV TV] « wreasayy| — -o1dyq | ‘Mo07) 57d vrutumquop uvoUe IIo} (1661) ‘Te 9 PAPIyNyS SADUIINI IS -Ipayy | snoseyd PEGI ‘POV ‘(6861) PARIYMAS “(S9GT) UBNOD “(ZPG6) sSApneg “(FH6T) POV Hise Deb ada Zo: a usoisey | — -014y SHAT UME) SNUAAVIV uvouedial | snoseyd (8681 ‘Tuejois) (SOOZ) ‘Te 2° [FH ‘(9Z61) SHIEH SNUULDOY -Ipey 1z40q vypuogdsy (2ePlspoPy) sdomy (9007) ‘Te stqa1qgV yanos (9681 SHEN) 19 srysTUpeyeT “(COGT) PUlSYysoarny pur aseureyy (9/61) sIeH saoapy (2) AY ‘AT ‘AD Tenuey suaign saajopiydy sepriAwopse’) (S961 “pueppy) (peystjqnduy) sonboy *(¢96T) pueppy| dds xzuv7 qD “IN ‘Na “Ad DIUVIAUL DIAULO]IG OLS snoseyd (8761 ‘e™) (peystjqnduy) sonboy *(¢96T) pueppy| dds x7 D5! IN ‘NC ‘9D “Ag sdjy| -oidyg| ost vidmopigoms snoseyd (S961 ‘PUePPY) (peystfqnduy) sonboy *(¢96T) pueppy| dds xzu7 5] IN ‘9D ‘Nd “ag sdjy| -oidyg | suanbaufur vidwmojigo.s sepndwoyjuy spuryjst pue saad SIIUIIIFIY SSOP] ,eugqey | sersunos popeauy Aprure,y ‘O10Z/Z0/S0 epdn seq *({] x1pueddy 99s) SINAN” 0 JajoI suoMerAciqge jeigqey *([ x1ipuaddy 922s) 99 ¢€ OS] 01 Jafar suONeTAdIqqe sapoo A1IUNO’) ‘soMsTIAIOeVIeYD pur sr] ‘odomny wz uate soiods vsadiq *7°Q] FIGeL 229 uvoueiia | snoseyd (LOGI ‘soseary) (9261) SHIPH (8661) I (PA) IPUCYD | 472 smI4anQ) I dD “IPI | -01dyd | 2eafi9009 sssop dipopde UPOUPIIO (FGT) uox3]ye pA ‘(OOZ) “Te 39 BARING (ZL6T) “Te Mite 19 PARIUNYS *(600TZ) AAvIyNYS pure vavesyNys ‘(09G61) AAvIyNyS WA “aS ‘OU! wr2YIOs pure vavrynys “(Th6T) 819q4y “(G66T) Foyyose[ pure AW | swavtasaduas “Td “IN ‘NH ‘AD ‘eIsy | snoseyd (QZZI “yueryos) ‘(OZG61) SIIeH ‘(ZG6[) UeMnoayT uva s19190C] ‘(8CG6T) shiquiy suxng I} “Ad ‘ZO ‘HD ‘IV uIOISa/\ -oikyg | snavyf sndvdosqiavuopy adoinq | snoseyd (€C8T ‘ZIOUUTA\ ) (poystjqnduy)) sanboy ‘(¢Q0Z) ‘Te 39 [TFH ‘(9Z6T) SuIeH | Sazqv vag ¢r) 1s¥d-YION 1G044S DIOLYIVQUIYV YT (9261) SHIH ‘(8661) I (PA) 9TPueYO (HY6L) U>IBTTEM (9007) ye Jo PARIyNYAS “(GOQOT) ‘Te 39 TIH “(OZG1) SHIeH “(TZG[) snissio0j Diptera. Chapter 10 (S007) ‘Te 2° TH “(9Z61) sureH UinaUtonssal uospuap HOP a eh STUNUMOD SNM ynpisap XUDT cD as ‘ON “AD ‘Td “AC sureyunoUr ‘oadoimyq qanos ‘yerUa_) eIsy ISSMYINOS ‘odoinq usoqsea ‘yerUa_) surly} -edie) ‘sdy ‘odomy jesqua) snoseyd -ovdy J snoseyd -ovdy snoseyd -ovdy (6061 FH) LAPUuapopoya DANIUISVDCT (LPT ‘pypnog) hd vanauisvgq (¢ Z81 ‘Peyosus}{) IIUI] Ie VANIUISYC] (S007) ‘Te 2° TTFH “(9Z61) suseH SA1QD VIN ES adom7y qsed-Y1ION snoseyd “oud (O88T ‘Jeyosua}) ypsaduaiqv vinaulsvcy (FYI) UaIsyeEN “(ZZ61) sI8uNdg ‘(990Z) “Te 19 BALIYNYS ‘(dard uy) Aavrymys pur paerynys “(9007) PFW ‘(9L61) SEH SIDUDIIFIY STUNUMOI sn s}sop]] JenqeH as ‘ON ‘AT “AD “AG spurysr pue $31JJUNOD poperauy eIsy JSSMYINOS ‘odomy UIOISPD ‘TeruaZ) snoseyd “oud (988i ‘Aeqre) eloatsdd VIULAYIUO) sa19ad¢ Ajrurey Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) , > Marcela Skuhrav 600 (sisaroj €r) sdoiny ould) Jequou royepoid -1U07) OFG6I [ere] Jowpe2] UI]JOD) SHItUopatva (6661) sdrryg pur [feats sprydy qy) /omiseseg sng dudsavutvg’) seprydaks syeurrue p2pooyg-30y ‘(Surq) TOPE pet 8SLT “WT (900Z) ‘Je 39 JOpART, ueunyy jomisereg | sagsyou suardid xan’) sop ‘(suliq) odoimg | rorwpaig 9¢81 (900Z) ‘Je 39 JOpART, ueunyy usoyseq | /onisereg | Tayyeny suvgtssay xayny adomy Sop ‘(suriq) jequou | so1eperg (SI8I (9007) ‘Je 19 JOjAeT, ueunyy {‘d q5 110’) | /oMIseseg | Uastay[) smasauts sapay adomy (sur1q) Jequsu | soIwperg (O€8I (9007) ‘Je 19 JOjAeL, uewmnyy Cie q5 -1u07) | /oniseseg | “uasioyy) suyxaa sapay seproiyn’y suery} -edie) ‘sdiy CL6I “eysudzoddAzry¢ (9007) ‘Te 3° pnp1sap ‘sdomy | snoseyd unsohav.gnas BAPIYNYS ‘(CG6T) ‘Te 29 eysudzodAzry¢ ‘(poystjqnduy)) sonboy XLLVT IN ‘AD ‘Nd “Ag jenuay) DUAUYASSIM DY Of1IsnsUD ueoUeI IO} (€C6| ‘souseq) (6661) Joyypse{ pue radaypy | = ynpuvavT IVINPUVAV] VIJAassagy spurys! pue satgads S9IUIIIFOY s}SOP] eugqepy | seiunos popeauy Ayrure,y 601 QINPpe) (wnylp -uogds unas IVAIFL ) poomsoZy jo JOVUTTOg ‘(BAIP] -s}sazoy ourd pur sonids) odoin [equou -11U07) Diptera. Chapter 10 ioyepaid iorepaig (LIST ‘UATed) (000Z) SHIOPY pure jeg | yearey prydy /olisereg saprog dads puozoLgy (sisoIOF) odoin ioyepaid jequou | so1eperg (QSZI ‘snoeuury) (000Z) SHIOPY pure [eg | pearey pryudy -1U07) | /OTIseIEg VIUDAAI VUOZOIT (sisd10J adomy suid ‘zaurd jequou snugovy -1U07) ~02149) ioyepaid Jowpe1] PCR] ‘MOOT (TOOT) Wey pue sqqnas | yeasey prydy /omiseseg VIPAULdaqUL VAVICT Qynpy) e193 adomy -TTPequiy) jequou pue -1U07) srnIUnNUDy JOYUTTOg ‘(SISIIOJ sonids) royepaid rorepeig | (Q96] {005 Jap ueA) (ZOOT) Afeq pue sqqnas | yearey prydy jomisereg | sesuarnisf sng dadshsoq spuryjst pue satgads S9DUIIOFOY sIsOP] SoLUNOD popeauy Ayrore,y Michel Martinez & Alain Roques / BioRisk 4(2): 553-602 (2010) , > Marcela Skuhrav 602 (pq JOMOP) uvoueiiol| snoseyd (PPS ‘M20T) (ZOOT) UOIsunIYA | sexoyOHIy -Ipsyy | -ovdyg stusomasnf vIada], (speoy adomy JOMOP) yequou SISUaQAD -u07) | snoseyd (FP8T ‘M20T) (FRG) Uasey uUeA pur sogey ‘(F00Z) seuol vinpuayv’) -ouy xovavad siqtsg day, uvoueisol | snoseyd (OGL ‘Issoy) 27270 (F861) JopueMYosuoNdNy EH) -Ipsy | -o1dyg (SNINIV) VABIONIVE sepnisyday, Jolepoid odoin jeasey prydy yequsu | Jorepsig (TSG6I “UNJOD) (000Z) SHIOYY pur [eq Cr) U0) | /onisesreg | sapjauyvu sng dudsvny sqnq} = 1D ‘ZI odomy Jjeqenyq pure jequou | soIwpe1g (BELT ‘snio1iqe.q) (SO00Z) ‘Je 2° [TH SNSSIOIeN /omuisereg stugsanba uoposayy spurys! pue satgads S9IUIIIFOY s}sOP] euqepy | selunos popeauy Ayrore,y