Introduction

The Delivering Alien Invasive Species Inventory for Europe (DAISIE) project provides an outstanding resource for synthesising trends in biological invasions in Europe (DAISIE 2009; Hulme and Roy 2010; Roques et al. 2010). The infrastructure of DAISIE was achieved through a consortium of researchers from 19 institutions and 15 countries across Europe resulting in 182 individual contributors of data. DAISIE comprises an inventory, distribution maps (on a country-scale) and accounts for a selection of alien species across Europe. The DAISIE inventory, The European Alien Species Database (http://www.europe-aliens.org/), was compiled from national and regional lists of alien fungi, bryophytes, vascular plants, invertebrates, fish, amphibians, reptiles, birds and mammals. The alien terrestrial invertebrates proved to be a major challenge because there were no checklists available for this group even though invertebrates comprise the largest proportion of alien animals (Nentwig and Josefsson 2010) and are one of the taxonomic groups with the most species causing impacts (mainly economical) in Europe (Hulme and Roy 2010). Here we review the DAISIE inventory, using its recent update of alien arthropods by Roques et al. (2010), to provide a review of the established (self-sustaining populations in the wild) alien arthropod predators and parasites (mostly parasitoids).

Alien arthropod predators and parasites

Alien arthropod predators and parasites are a particularly interesting group to consider because they generally have a positive impact on the economy or environment (through introduction as biological control agents for the control of pest insects) but, in a few cases, can also have negative impacts (through interference with other beneficial insects). There are many examples of predators and parasitoids providing cost-effective biological control particularly in glasshouse systems (van Lenteren 2007; De Clercq et al. 2011). However, there are a few examples of a biological control agent becoming a pest and threatening non-target organisms (Kenis and Branco 2010). The harlequin ladybird, Harmonia axyridis Pallas (Coleoptera: Coccinellidae) is one such example (Roy and Wajnberg 2008). The release of generalist predators, such as H. axyridis, is extremely risky and can impact on ecosystem services and processes through trophic cascades (Kenis and Branco 2010).

There are currently 1590 terrestrial arthropod species identified as alien to Europe (Roques 2010). Of these, 513 are predators or parasites, mainly parasitoids but also some mites (Table 1). The largest group is the insects (409 species constituting 79.7%), followed by spiders (47 species constituting 9.2%, data from Nentwig and Kobelt 2010), myriapods (34 species constituting 6.6%, data from Stoev et al. 2010) and mites (23 species constituting 4.5%, data from Navajas et al. 2010) as the next most speciose groups. The taxonomy of species within these alien groupings is extremely diverse, as highlighted by the large number of families represented (115 families). However, only 24 families have five or more species. The richest families with respect to alien insect species all belong to the Hymenoptera: Aphelinidae, Encyrtidae, Formicidae and Eulophidae (Fig. 1a). Furthermore, Hymenoptera constitute the largest proportion of the alien insects (Fig. 1b, 259 species constituting 63.3%, data from Rasplus et al. 2010) followed by Coleoptera (Fig. 1b, 62 species constituting 15.2%, data from Denux and Zagatti 2010; Roy and Migeon 2010). The six additional insect orders comprise less than 35 alien species each (Fig. 2, data from Kenis and Roques 2010; Rabitsch 2010a; Rasplus and Roques 2010; Reynaud 2010; Skuhravá et al. 2010).

Table 1 List of the alien species of parasitoids and predators established in Europe until 2008, modes of introduction (U = Unintentional; I = Intentional), status (A = Alien; C = Cryptogenic), date of first record on the continent, and number of invaded countries and major European islands (including oceanic islands)
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Fig. 1
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a Number of alien predator and parasite species within the 24 arthropod families which are represented by five or more alien parasites and predators in Europe (including major islands). b Proportion of the alien predator and parasite species within each family intentionally introduced to Europe (including major islands). Number above the bar = total number of species. Data from Denux and Zagatti (2010), Kenis and Roques (2010), Navajas et al. (2010), Nentwig and Kobelt (2010), Rabitsch (2010b), Reynaud (2010), Roy and Migeon (2010), Skuhravá et al. (2010), Stoev et al. (2010)

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Fig. 2
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Number of alien parasite and predator species intentionally and accidentally introduced to Europe (including major islands) per insect order. Number above bars = percentage of parasite and predator species within the order from the total number of alien parasites and predators (409 spp.). Data from Denux and Zagatti (2010), Kenis and Roques (2010), Rabitsch (2010b), Rasplus and Roques (2010), Reynaud (2010), Roy and Migeon (2010), Skuhravá et al. (2010)

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Invasion pathways

The majority (86%) of alien arthropods in Europe arrived unintentionally but 14% were deliberately introduced, mainly as biological control agents (Rabitsch 2010b). It is, therefore, not surprising that the proportion of alien predators and parasites introduced intentionally is higher than for other functional groups. At least 174 (33.9%) predatory and parasitic species have been introduced intentionally, mainly for biological control purposes, whilst 339 (66.1%) other species arrived accidentally (Fig. 2). Roques et al. (2009) reported the number of intentional introductions as only 131 alien terrestrial invertebrate species. However, the analysis presented here is based on a major update to the DAISIE inventory, undertaken to account for the underestimation of hymenopteran parasitoids released as biological control agents but which subsequently established within Europe (Roques 2010; Rasplus et al. 2010).

Species introduced intentionally as biological control agents

The majority of predator and parasitoid species have arrived into Europe unintentionally but intentional introduction through the release of exotic (=alien) biological control agents is undoubtedly an important invasion pathway for many arthropod species into Europe. The definitive pathways involved are diverse and in some cases difficult to monitor (Rabitsch 2010b).

There is considerable variation between families in the proportion of alien predator and parasite species that have been intentionally introduced within Europe. So, for example, a very high proportion (approximately 90%) of alien parasitoids in the family Aphelinidae found in Europe have been intentionally introduced (Fig. 1b; from Rasplus et al. 2010). This family comprises a diverse range of small parasitic wasps which have been widely used in biological control. Encarsia formosa Gahan (Hymenoptera: Aphelinidae) is a well known example. It was extensively introduced to control the glasshouse whitefly Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae) (Vet et al. 1980; van Lenteren et al. 1996; De Clercq et al. 2011) and now established in the wild (Roques et al. 2009). The Coccinellidae is another family for which the majority of alien species (predatory ladybirds) have been intentionally introduced as biological control agents (Roy and Migeon 2010). Similarly the Trichogrammatidae, small chalcid parasitic wasps, comprise a group widely used in biological control strategies (Smith 1996). In contrast, there are 42 species of alien Formicidae (ants) in Europe and none are considered to have been introduced intentionally but are likely to have arrived as contaminants and stowaways (Rabitsch 2011).

Species introduced unintentionally as contaminants and stowaways

Escape from captivity is a common pathway for many alien species, including arthropods. Arthropods are rarely domesticated but insects used for biological control in contained environments, such as glasshouses and open fields are an important source of alien introductions into Europe. The harlequin ladybird, H. axyridis, was introduced into glasshouses as a biological control agent of aphids but subsequently escaped into the wider countryside and spread dramatically across Europe (Majerus et al. 2006; Roy et al. 2006; Roy and Wajnberg 2008; Roy and Roy 2010; De Clercq and Bale 2011; Evans et al. 2011a).

Many alien arthropods have arrived in Europe as contaminants or stowaways with plants (including fruit and vegetables), stored products or timber (Rabitsch 2010b). However, the majority of these are herbivorous insects. Honeybee imports are responsible for the introduction of a number of infamous parasites including the tracheal mite, Acarapis woodi (Rennie) (Trombidiformes: Tarsonemidae), and Varroa destructor Anderson & Trueman (Parasitiformes: Varroidae) (Coffey 2007). Hymenoptera have a history of introduction as stowaways (Rabitsch 2010b). The oriental mud dauber, Sceliphron curvatum Smith (Hymenoptera: Sphecidae), arrived with air cargo from Asia into Austria. This predatory species feeds paralysed spiders to its larvae within distinctive mud nests (Schmid-Egger 2004; Rabitsch 2010b).

Alien ants are among the most invasive species globally (Holway et al. 2002; Rabitsch 2011). Colonies are transported in the soil with ornamental plants or, indeed, other plant material or anything that provides shelter (Rabitsch 2010b). The expression “tramp ants” is derived from this reliance on human-mediated transport (Hölldobler and Wilson 1990; Passera 1994). The Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae), arrived as a stowaway in Madeira and mainland Portugal in the nineteenth century (Rabitsch 2010b). Linepithema humile routinely move their nests and colonise potted plants and refuse. This can facilitate dispersal through subsequent human movement of the material (Rabitsch 2011). Furthermore, L. humile can be transported as small nest fragments on land vehicles and in sea freight. Only one queen and ten workers are required for colony establishment (Suarez et al. 2001).

Invasion corridors

Transport routes can provide pathways for the movement of alien species. Harmonia axyridis has been found on trains, cars and boats and these mechanisms have undoubtedly contributed to the dramatic spread of this species across Europe (Roy et al. 2006; Brown et al. 2008a). A number of other species are likely to have benefited from global transport networks but it is difficult to separate the role of the network from contaminant and stowaway pathways (Roques et al. 2009; Rabitsch 2010b). For example, the alien mosquito Aedes albopictus Skuse (Diptera: Culicidae) is reported to be transported by ship and aircraft traffic (Tatem et al. 2006) but is also commonly implicated as stowaways, for example in second-hand tyres and with plants (Roques et al. 2009).

Leading-edge dispersal following intentional and unintentional introduction

Alien species can arrive in a new region from a donor region, where it is also alien, unaided. This is termed “leading-edge dispersal” (Rabitsch 2010b; Lawson Handley et al. 2011). The majority of alien arthropod species in Europe are thought to have followed a classic invasion route: introduction, establishment and spread. However, acclimatization, whereby abiotic and biotic barriers to survival and reproduction are overcome, is a fundamental process that alien species have to achieve prior to establishment (Richardson et al. 2000). The spread into neighbouring countries is unsurprising once a species has acclimated and established in one new region. Again H. axyridis provides a well-studied example of a species that has undergone leading edge dispersal which has resulted in its spread across much of Europe within two decades (Brown et al. 2008a; Brown et al. 2011b; Lawson Handley et al. 2011). Another example of a species that has spread rapidly through leading edge dispersal is the fast spreading Platygaster robiniae Buhl & Duso (Hymenoptera: Platygastridae), a parasitoid of the black locust gall midge, Obolodiplosis robiniae (Haldeman) (Diptera: Cecidomyiidae). This parasitoid was accidentally introduced from North America to Europe along with its host. Obolodiplosis robiniae was first found in Italy in 2003. It rapidly colonized most of Europe within five years. However, the parasitoid was only detected in 2005, again in Italy, but it quickly followed the host expansion. In 2008, the host midge and the parasitoid appeared simultaneously in Switzerland and Montenegro (Glavendekić et al. 2010).

Temporal trends

Many of the alien arthropods in Europe are often not discovered until they are established and spreading primarily because of the difficulties in determining their introduction pathways (Roques 2010). Therefore, it is difficult to determine the precise date of arrival for many alien species. However, the DAISIE inventory has the date of first record for 89.4% of the 1590 alien arthropods (Roques 2010). The proportion of alien arthropod predators and parasites for which there is a date of first record is similarly high (88.1%). The number of new arrivals has been progressively increasing since 1500, with the rate accelerating during the last 100 years (Fig. 3). However, the 1980s appear to represent a peak: 66 alien arthropod predators and parasites were recorded from 1980 to 1989. Although the total number of alien arthropods recorded each year is still increasing (with approximately 20 new species recorded in the period 2000–2008) this is mainly attributed to phytophagous species rather than predators and parasites (Roques 2010). The observed decrease in number of alien predators and parasites, recorded in recent decades, is a measure of the reduced number of intentional introductions over this period (Fig. 3). There has been an increase in the number of species recorded as a consequence of unintentional introductions which mirrors the trend for phytophages (Figs. 3, 4). The release of biological control agents through the 1980s has undoubtedly contributed to the trends observed in records of new alien species.

Fig. 3
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Mean number of new alien predator and parasite species recorded, following intentional and unintentional introductions, in Europe (including major islands) per year during the time periods. Number above the bar = total number of introduced species per period. Data from Roques et al. (2010)

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Fig. 4
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Mean number (±SE) of new alien arthropod species recorded per year in Europe (including major islands) from 1500 to 2008. a total arthropods (Best fit: y = −0.411 − 0.407x + 0.304x 2; r 2 = 0.965) b total and mean number per functional group. (Updated from Roques 2010)

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Classical and augmentative biological control of insects has been applied for 120 and 90 years, respectively (van Lenteren et al. 2006). More than 2000 species of natural enemy have been released worldwide and populations of at least 165 pest species have been permanently reduced (Greathead 1995; Gurr and Wratten 2000). Until recently the potential risks of biological control agents for control of arthropod pests have not been considered in pre-release evaluations (van Lenteren et al. 2003; van Lenteren et al. 2006). This has largely been attributed to the very low number of reports of negative effects of such releases (van Lenteren et al. 2006). However, in recent years the situation has changed and in many countries more stringent regulatory requirements need to be met before an exotic biological control agent can be released (FAO 1996; van Lenteren et al. 2003; Kairo et al. 2003; Hunt et al. 2007). This has undoubtedly resulted in a decline of intentional introductions and is responsible for the trends observed in Fig. 3.

Biogeographic trends

The origin of 19.3% of the alien predators and parasites in Europe is unknown and they are regarded as cryptogenic (Fig. 5). Of those where origin is known, however, more than a quarter originated from Asia (27.9%). North America and Africa contributed 22.9% and 15.8%, respectively (Fig. 5). Interestingly, the recruitment of species into Europe from each continent has varied considerably over time. Arrival of species from North America has been declining since 1980 but from Asia a linear increase can be observed until 2000 after which there has been a slight decline (Fig. 6).

Fig. 5
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Region of origin of the arthropod parasite and predator species alien to Europe (including major islands). Numbers indicate the total. Data from Roques et al. (2010)

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Fig. 6
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Percentage of the arthropod predator and parasite species in relation to the total of all alien arthropods recorded over time for each region. Data from Roques et al. (2010)

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Spread in Europe

One-fifth (20.7%) of the alien arthropod predators and parasites were recorded first in Italy. France and Great Britain have also been the first recipients of a large number of species with 41 (9.7%) and 31 (7.4%) alien species being recorded first in these countries, respectively. The spread of most species is extremely limited: only 12 species (3.3%) are observed in 30 countries or more and 257 species (50.1%) are only present in one or two countries (Fig. 7). Not surprisingly, the spread of a species is strongly correlated with the date of arrival (Spearmann rank correlation between the number of colonized countries and the duration of the presence in Europe since first record (until 2008): r = 0.45; P < 0.001; n = 452). 46.6% of the species recorded before 1900 are now present in more than ten countries, whereas only 7.1% of the species recorded from 1975 to 1999 are similarly widespread (Fig. 8). None of the species recorded since 2000 have spread to more than ten countries.

Fig. 7
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Spread of arthropod predator and parasite species alien in Europe expressed as the number of countries (and major islands) in which the species has been recorded as established and their frequency. Number above the bar is the number of alien predators and parasites recorded. Data from Roques et al. (2010)

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Fig. 8
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Percentage of alien arthropod predators and parasites present in either three (or less), ten (or more) or 20 (or more) European countries against date first recorded. Data from Roques et al. (2010)

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Alien arthropod predators and parasites are distributed heterogeneously across Europe (Fig. 9). Italy has a high representation of these species which could relate to the widespread use of biological control agents in this region (supported also by the high proportion of first records of alien arthropod predators and parasites from Italy). A number of European islands are at the other end of the range with very few alien arthropod predators and parasites represented. The distribution of alien species within Europe appears to be positively correlated with the trading activity of the country: the more imports a country receives the more alien species are recorded (Kobelt and Nentwig 2008; Roques 2010; Pyšek et al. 2010; Essl et al. 2011). Undoubtedly the size of a country and number of available habitats will also influence the number of alien species recorded. Britain is a relatively small country but has the fifth highest number of alien predators and parasites. Perhaps an indication of trading activity but also the predominantly urban landscape, particularly in England, could be favouring alien species (Roques et al. 2009; Roy et al. 2011).

Fig. 9
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Distribution of alien parasites and predators in European countries and major islands (1 = Azores; 2 = Madeira and 3 = Canary Islands). Data from Roques et al. (2010)

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Ecological and economical impacts

Alien arthropod species can have both ecological and economical impacts. Many of the economic impacts are attributed to phytophagous alien species that directly reduce productivity (Roques et al. 2009). However, some species are considered a nuisance to humans because of their behaviour (Roy et al. 2009). The problems associated with nuisance insects are varied, ranging from human health (vectors of disease, allergens and irritants, pain through biting and stinging), annoyance when in high numbers (tendency to occur in large numbers results in intolerable annoyance) to being household pests (damaging or destroying the contents of houses including fabrics, structural timbers and stored products). Harmonia axyridis and a number of alien ant species are considered to be a nuisance because of their propensity to reach high numbers in houses and gardens. Harmonia axyridis aggregates in buildings in autumn and reports of more than one thousand individuals in a single household are not unusual (Majerus et al. 2006; Roy et al. 2006; Brown et al. 2008b).

Alien arthropod predator and parasite species can have profound ecological impacts within invaded ranges (Kenis et al. 2009). Perhaps the greatest threat is to native biodiversity through direct interactions such as hybridisation with native species (Lawson Handley et al. 2011), preying or parasitising native species (Kindlmann et al. 2011). Additionally, they can have indirect impacts on native species and ecosystems through competition, carrying diseases or sharing natural enemies with native species (Kenis et al. 2009; Roy et al. 2011). The concept of invasional meltdown, in which a number of alien species interact synergistically resulting in dramatic alterations to ecosystems (O’Dowd et al. 2003; Simberloff 2006), outlines the most extreme outcome of the subsequent arrival of invasive alien species. There are many examples of alien arthropods causing ecological impacts on oceanic islands (Causton et al. 2006), including invasional meltdown (O’Dowd et al. 2003), but there are very few examples of alien arthropods (mainly predators) adversely affecting native biodiversity or ecosytems in Europe (Kenis et al. 2009; Roques et al. 2009).

The ecological impacts of alien arthropod predators found in Europe have been well documented although in some cases from studies on other continents. Invasive ants, such as L. humile, displace native ants and other animals both through resource competition and direct predation as has been shown through studies in the US (Human and Gordon 1996). Harmonia axyridis outcompetes and displaces native aphidophagous insects (Brown et al. 2011b; Aebi et al. 2011). The Asian hornet, Vespa velutina nigrithorax de Buysson (Hymenoptera: Vespidae), is established and spreading in south-west France and preys on honeybees, Apis mellifera L. (Hymenoptera: Apidae), and may consequently have an economic impact through diminished pollination services (Beggs et al. 2011). Similarly a number of introduced parasitoid species have displaced native aphelinids (Viggiani 1994; Viggiani and Gerling 1994). There is considerable scope for further research on the ecological impacts of alien arthropod predators and parasites. This, coupled with an increased understanding of invasion pathways, could facilitate more effective risk assessment and surveillance.

Future trends

The dramatic increase in the establishment of alien invertebrates, including arthropod predators and parasites, is anticipated to continue over the next few decades as global trade continues to expand (Roques et al. 2009). Intentional introductions of species have decreased in recent years but this is offset by an increase in unintentional translocations. Additionally, environmental change, particularly climate change and habitat destruction, is predicted to promote the arrival, establishment and spread of alien species in Europe (Evans et al. 2011b). Many of the alien arthropod records are from urban or man-made habitats. Few alien species seem to have colonised natural ecosystems. Mature, natural communities are considered more resistant to potential invaders because they have lower levels of niche opportunity (Shea and Chesson 2002), i.e. low availability of resources. However, whether such predictions are upheld because they reflect reality or whether there is simply a lack of data from natural systems requires addressing.