Longhorn beetles ( Coleoptera , Cerambycidae ) Chapter 8 . 1

A total of 19 alien longhorn beetle species have established in Europe where they presently account for ca. 2.8 % of the total cerambycid fauna. Most species belong to the subfamilies Cerambycinae and Laminae which are prevalent in the native fauna as well. Th e alien species mainly established during the period 1975–1999, arriving predominantly from Asia. France, Spain and Italy are by far the most invaded countries. All species have been introduced accidentally. Wood-derived products such as woodpackaging material and palettes, plants for planting, and bonsais constitute invasive pathways of increasing importance. However, only few species have yet colonized natural habitats outside parks and gardens. Present ecological and economical impacts, and future trends are discussed.


Introduction
Th e coleopteran family Cerambycidae (longhorn beetles) is currently classifi ed in the superfamily Chrysomeloidea, along with the families Vesperidae and Distenidae (Hunt et al. 2007, Szeoke andHegyi 2002).Cerambycidae is a large family comprising about
Th e 19 alien species established in Europe belong to only 3 of these subfamilies, Cerambycinae, Laminae and Prioninae (Table 8.1.1).Th e alien species are mostly represented by the subfamily Cerambycinae, followed by Lamiinae but the relative proportion of aliens compared to the total cerambycid fauna is still limited (<6%) in these two subfamilies.By contrast, the proportion of aliens is much more important in Prioninae with 2 species adding to 10 native ones (Fig. 8.1.1.).In addition, Parandrinae, a subfamily which is not represented in the native European entomofauna, is represented by Parandra brunnea, a North American species introduced in Germany (Nüssler 1961).
Table 8.1.2gives a list of species of European origin introduced through human activity in another part of Europe (aliens in Europe).Th ese species are mostly of Mediterranean origin introduced in more northern areas and species from Continental Europe introduced to the Atlantic islands.

Major biological characteristics of the cerambycid species alien to Europe
Lepturinae but also Prioninae and Parandrinae share some biological characteristics that reduce their probability of introduction.Larvae in these subfamilies develop in decaying wood and are rarely imported with wood products or living plants.Interceptions have shown that they are mainly introduced through accidental importation in industrial packages or in stocks of perishable vegetables.Only a few species of Lepturinae (Tribe Rhagiini, and some Lepturinii) developing on recently felled trees are likely to be successfully introduced through the wood trade.Th e importation of living potted plants is also a potential new pathway for Prioninae.
Once a population is introduced, the capability for natural dispersal constitutes an important factor for establishment success.Although our knowledge about the dispersal behaviour of alien longhorn beetles is still rather limited and mostly concerns only a few species of recent invaders such as Anoplophora glabripennis (Smith et aol. 2001) and A. chinensis (Adachi 1990, Komazaki andSakagami 1989), this variable is important when designing an eradication attempt (MacLeod et al. 2002).).With the increased speed of international transport from 1850 to 1925, species with shorter life cycles were able to reach Europe alive and become established, e.g.Neoclytus acuminatus (Reineck 1919, Sama 2002, Tassi 1969).Later, only two species were introduced from North America to Europe via the US eff ort to supply extra furniture and increase military material after the 1 st World War (i.e., Parandra brunnea, Neoclytus acuminatus).Subsequently, 50 years passed until a second wave of introduction arrived alongside with the rapid development of international exchange of goods and transportation after the 2 nd World War.During the recent period, two further species have been detected in the wild -Anoplophora chinensis in 2000 in Italy (Colombo and Limonta 2001) and A. glabripennis in 2001 in Austria (Dauber and Mitter 2001).

Temporal trends of introduction in Europe of alien Cerambycids
Th e number of interceptions of Cerambycids is still increasing throughout Europe.However, more eff ective control at borders is like to have reduced establishments following interception or introductions.Th e importation of exotic plants also off ers opportunities for introduction but also constraints the establishment of some alien species.For example, Phoracantha spp.could not have been introduced without the importation and mass cultivation of its host plants, Eucalyptus spp. in the Mediterranean basin.In south-eastern France, an Australian cerambycid, Bardistus cibarius (Newman, 1841) could survive only on its original host plant, an introduced grass tree (Xanthorrhoea sp., Xanthorrhoeaceae); the beetle population disappeared immediately after the infested host plants were removed (Cocquempot 2007).Th e case of Batocera rufomaculata (DeGeer, 1775) found in Munster's Zoo (Germany) is similar (Cocquempot 2007) although this tropical species has established in Israel since at least 1948 (Bahillo de la Puebla and Iturrondobeitia-Bilbao 1995, Plavilstshtikov 1934, Sama et al. 2010).Th e combination of importation of longhorn beetle species with their specifi c host plant or groups of plants followed by establishment is rare.However the establishment of A. chinensis is an exception.Other species are frequent intercepted at border controls, e.g.Mimectatina meridiana (Matsushita, 1933) with Cycas fruits from Japan (Cocquempot 2007) or Trichoferus campestris (Faldermann 1835) with Salix timber from China (Cocquempot 2007).
Th e degree of polyphagy is also an important factor in the likelihood of establishment.Polyphagous species appear to have a higher potential to establish than oligophagous and monophagous species.Th e large number of hosts utilised by Anoplophora spp.(Cocquempot et al. 2003, Hérard and Roques 2009, Maspero et al. 2007a) is a main factor in the diffi culty in eradicating this species for example.Th ese diffi culties appear much less important for oligophagous species such as Callidiellum rufi penne (Bahillo and Iturrondobeitia-Bilbao 1995, Campadelli and Sama 1988, Plavilstshtikov 1934)  or Phoracanthine species.It is also the case for the North American wood borer Saperda candida (Fabricius, 1787), which was introduced in Germany in 2008 but apparently did not established yet (EPPO 2008, Nolte Krieger 2008).By contrast, Monochamus species have a regime close to polyphagy, including a large number of conifer species, and may spread throughout Europe.Th ere is no example of establishment in Europe of a strictly monophagous exotic long-horned beetle.Species with a limited host range do not seem to be capable of going beyond the interception or introduction stage, e.g.Bardistus cibarius (Cocquempot 2007).

Biogeographic patterns of the cerambycid species alien to Europe
Alien species established in Europe mostly originated from Asia, followed by Africa (Figure 8.1.3).Th e region of origin appears to depend on the major trade routes developed by each country.Some North African species have colonized Mediterranean countries such as Spain, France, and Malta for example.Other African species have often been intercepted but only Phryneta leprosa has established in Malta where the climate is favourable for development (Mifsud and Dandria 2002).Long-established trade routes between Iberian countries and South American countries have resulted in some historic, isolated establishments in the Spanish and Portuguese Atlantic Islands but with a limited risk of further expansion (Lemos-Perreira 1978, Méquignon 1935).With the numerous interceptions in the U.K (Duff y 1953a) together with the colonial trade routes with African and Asiatic countries, it is surprising that only Trinophylum cribratum has established to date (Gilmour 1948); the incompatible climate may negate the development of tropical and subtropical species.Two species native to North America, Parandra brunnea and Neoclytus acuminatus, also colonized Europe at the beginning of the last century.Th e fi rst species is well established but restricted to Dresden (Germany) (Nüssler 1961).Th e second is widely established in the Mediterranean area but its populations appear to be declining (Brustel et al. 2002).Beside these two species, there have been no further establishments originating from North America; the pathway of transported material is mainly in the reverse direction, from Europe to America.Some Australian species have reached Europe but only those using Eucalyptus (Phoracantha spp.) have successfully established (Cocquempot and Sama 2004) and only in areas newly planted with these fast-growing tree species.Th e large diff erences in species composition between the fl oras of Australia and Europe probably accounts for the failure of Australasian longhorn beetles such as in Bardistus cibarius on Xanthorrhoea sp.(Cocquempot 2007) to establish.
Recent increases in commercial traffi c from Asia (especially China) to Europe has accounted for the introduction of a number of new species of cerambycids.Striking examples are Callidiellum rufi penne which has recently established in Spain (Bahillo de la Puebla and Iturrondobeitia-Bilbao 1995) and Italy (Campadelli and Sama 1988), Anoplophora glabripennis and A. chinensis which can be considered as established or not eradicated in several countries (Hérard andRoques 2009, Maspero et al. 2007a), Psacothea hilaris (Pascoe, 1857) under eradication in Italy (Cocquempot 2007, Jucker et al. 2006), and Monochamus alternatus Hope, 1842 intercepted a number of times in Germany (Cocquempot 2007) and France (Cocquempot Unpubl.)but not yet established.A fi nal case, Xylotrechus stebbingi, is less clear.It is believed that an initial introduction from its native area of central Asia to Asia Minor was followed by a step-wise expansion into southern Europe and North Africa (Cocquempot and Debreuil 2006, Sama 2002, Šefrová and Laštůvka 2005).
Alien cerambycid species are not evenly distributed throughout Europe.Large differences in the number of aliens are apparent between countries, France, Italy and Spain being by far the most invaded (Figure 8.1.4).

Main pathways of introduction to Europe of alien cerambycid species
All alien longhorn beetles established in Europe have been introduced accidentally; there are no examples of a successful, deliberate introduction.Th e principal pathways of arrival have been identifi ed and presented by Frank 2002 and each relates to the import of immature stages that subsequently emerge as adults.Th ere are relatively few records of living adults imported with vegetables or fruits although Eucalyptus beetles, Phoracantha recurva, were found in a cluster of bananas (Bosmans 2006).
Th e longest established pathway is timber importation for house construction (Hylotrupes bajulus) or building furniture (e.g.Trichoferus spp., Stromatium spp.and Chlorophorus annularis arriving with bamboo-made objects (Cocquempot 2007)).Species A third, more recent, pathway concerns wood packages, palettes and other wood-derived products (e.g., for Anoplophora glabripennis) (Hérard and Roques 2009).Th e fi nal pathway is the importation of plants for planting in nurseries, including the bonsai industry, which has resulted in the arrival of species such as Anopolophra chinensis (Cocquempot 2007, EPPO 2006, van Rossem et al. 1981, Schembri and Sama 1986), Callidiellum rufi penne and Bardistus cibarius.
All pathways are still prevalent but they vary in importance.Most recent interceptions (from the end of the 20 th Century) have related to wood-manufactured products (e.g.Chlorophorus annularis and Trichoferus campestris).Importation of Eucalyptus wood for pulp has also resulted in the introduction of a second species of Phoracantha, P. recurva (Miquel 2008).If such importations continues a number of additional species of this genus, which are mainly related to Eucalyptus (Wang 1995), are expected to arrive.
Since their fi rst usage, wood packaging and palettes have constituted an important introduction pathway.Th e source material spends suffi cient time as logs without sanitary controls to be colonized by longhorn beetles.When the wood is turned into packages or palettes, infestation occurs mainly as unnoticed early stages (eggs or fi rstinstar larva).Development continues in the woody material during importation and emergence of adults occurs often unnoticed in warehouses, weeks or months after arrival.Th is is the case for A. glabripennis, P. hilaris and M. alternatus which may already complete their entire lifecycle before the source wood is processed or destroyed.Wood package is often produced using low quality timber often colonized by longhorn beetle species, which is increasing its potential as a vector.
Other, less signifi cant, introduction pathways have also been identifi ed, yet they typically only transported one or a few individuals which fail to establish.Th e introduction route is unknown for other species such as Acanthoderes jaspideus (Méquignon 1935), Oxymerus aculeatus (Alluaud 1935), Deroplia albida, and Phryneta leprosa (Mifsud and Dandria 2002) but they may be related to the uncontrolled importation of wild plants.Natural range expansion cannot be ruled out for a few species which have a nearby native range, e.g.Lucasianus levaillantii (Mayet 1905, Pellegrin andCocquempot 2001) and Xylotrechus stebbingi (Šefrová and Laštůvka 2005) originating from North Africa and the Middle East, respectively.

Ecosystems and habitats invaded in Europe by alien cerambycid species
Although all natural or artifi cial terrestrial ecosystems and anthropogenic areas which contain trees, bushes or wood products are potentially occupied by alien longhorn beetles, establishment in Europe is concentrated in man-made habitats to date, especially in parks and gardens (Figure 8.1.5).To date, only the two clytine beetles, Neoclytus acuminatus and Xylotrechus stebbingi, have colonized natural habitats.X. stebbingi is very common on Eucalyptus cut wood in Crete (Sama 2002) for example and may be related to the polyphagous nature of these two species.Other polyphagous species such as Anoplophora spp.also have the potential to live in urban areas, in cultivated lanes (e.g.planted with poplars) as well as in natural forests where potential host plants occur.However, dispersal from man-made habitats to natural forests appears to be a slow process.For the fi rst twenty-two years since its arrival in North America, A. glabripennis has been restricted to trees in urban areas until 2008 when it was found in natural forests dominated by Acer trees (Haack et al. 2010).Although such a process has not yet been observed in Europe, there is a strong risk that Anoplophora spp.will spread to naturally-forested landscapes, if the ongoing eradication attempts in Austria, Germany, France and Italy are unsuccessful.
Th e expansion of oligophagous species is inevitably more dependant on the presence of suitable host plants.Th ose using largely-planted trees can spread more easily.
Th us, Phoracantha spp. that live only in eucalypt trees have colonized ornamental tree plantations in urban areas as well as old plantations such as those found on the Mediterranean islands and in neighbouring countries, and industrial plantations created for paper pulp.Other established species mostly have a distribution restricted to Mediterranean and Atlantic islands.In these areas, anthropogenic ecosystems are mainly colonized.A species of considerable concern with conifer forests is Monochamus alternatus, which could potentially become established in coniferous plantations and forests and subsequently transfer the pine wood nematode (Bursaphelenchus xylophilus Steiner & Buhrer, 1934).

Ecological and economic impact of alien cerambycid species
Although there is concern about the potential ecological impact of the invasive longhorn beetles N. acuminatus and X. stebbingi, there is no measure of their impact on trees or any estimation of possible competitive displacement of the native fauna.Th e ecological impact of Anoplophora species may also be important if they establish in European forests.Anoplophora could compete with other arthropods occupying the same niche, but they also create niches for other arthropods that live in tunnels in decaying wood or compete with other saproxylic beetles.Th e joint introduction and establishment of the Citrus longhorn beetle, A. chinensis, and its parasitoid, Aprostocetus anoplophorae Delvare, 2004, exemplifi es the potential risk of adaptation of imported parasitoids which themselves might not specialise on the native fauna (Delvare et al. 2004).
Although the ecological niche occupied by an alien species may be vacant there remains a risk of secondary infection resulting from their damage.For example, secondary infestation by the pine wood nematode vectored by Monochamus spp.(Evans et al. 2008, Kawai Miho et al. 2006) may cause serious impacts to coniferous trees in all landscapes.M. alternatus has only been intercepted in Germany and France (Cocquempot 2007, Cocquempot (Unpubl.));yet the pine wood nematode which it vectors was recorded from Portugal in 1999 (Mota et al. 1999).After having been contained for several years in a limited area, the nematode has spread throughout Portugal, as well as being eradicated following incursions into Spain in 2008 and Madeira in 2009.A novel association with the native species, M. galloprovincialis (Villiers 1967) has also been reported.Th e expansion as well as new introductions of the pine wood nematode could potentially have a substantial level of economic impact in all areas of coniferous cultivation in Europe.
Other economic impacts are mainly associated with ornamental trees in urban areas, cultivated trees such as poplars and eucalypts and nurseries, including these for bonsai production.Studies of Anoplophora glabripennis in North America and A. chinensis in China indicate the possible scale of economic damage following establishment of these species in a new country or in a plantation, especially of poplar or Citrus trees (Cocquempot et al. 2003, Haack et al. 2010, MacLeod et al. 2002).As a control measure, ornamental trees colonized by invasive longhorns must be eliminated without consideration of their aesthetic value.Eradication measures entail high costs to be borne by local communities or private owners.Special attention is paid to A. chinensis necessitating complete removal of trees, including the rootstock (Haack et al. 2010).
Poplars or eucalypt plantations can be highly aff ected as has already been the case in China (A. glabripennis on poplars) and in Spain (Phoracantha spp.), where infested trees become unsuitable for pulp and wood exploitation.Th e Citrus longhorn beetle is also considered as an important risk for all Citrus fruit production in the Mediterranean area and its islands.
Th e nursery industry is already concerned.Th ere are several examples of introductions or establishments of potentially invasive species such as Callidiellum rufi penne and Anoplophora chinensis, with the imports of nursery plants.Nurseries can themselves be vectors of aliens when they dispatch their products.
Th e eradication process established for quarantine species aims to limit introductions although only a few eradications have been offi cially reported in Europe, e.g. as for Anoplophora chinensis in France (Hérard et al. 2006, Hérard andRoques 2009).Phytosanitary interceptions at borders are likely to have prevented a number of introductions and further establishments (e.g., Monochamus alternatus, Trichoferus campestris in France, Anoplophora glabripennis and A. chinenis in several countries) (Cocquem- pot 2007) whilst at the same time, several non-quarantine species not submitted to importation controls have become established (e.g., Xylotrechus stebbingi, Phoracantha semipunctata, Neoclytus acuminatus).Th is illustrates the importance of quarantine species lists, which should be preventive and not only curative to be most eff ective.
Human-mediated dispersal should also be tightly controlled during the eradication process.Without due respect for control obligations, eradication can fail.For example, the long delay by Italian authorities in applying control measures and strong management measures against Anoplophora chinensis (EPPO 2009, Jucker et al. 2007) or inadvertent movement of untreated wood material for A. glabripennis in New-York (Haack et al. 1997) are examples of ineff ective eradication effi cacy.Th e combination of increasing volumes of trade, the increased speed of import of potential vectors, the diversity of sources and sites for introduction is likely to result in increasing invasion risk (Cocquempot 2007).All recently established species alien to Europe have been intercepted too late after their introduction and have been outside offi cial institutional controls.Th ese factors make it increasingly diffi cult for rapid eradication after initial arrival.Eff ective monitoring of each point of possible entry is unfeasible when the key pathways identifi ed here have diff erent vectors and locations of arrival (e.g.airports, harbours, stations, lorry parks), and there are major diff erence in the quality of phytosanitary controls between European countries, particularly following the enlargement of the EU.Th e risk depends on volume and diversity of vector material imported, and subsequently there is greatest risk in countries such as the UK, France, Spain, Italy, Netherlands, Belgium and Germany.Th e case of Anopolophora glabripennis in North America and Europe clearly demonstrates the possibility of spread in our continent; such detailed assessment is required for all potentially invasive longhorn beetles (MacLeod et al. 2002).

Figure 8
Figure 8.1.1.Relative importance of the subfamilies of Cerambycidae in the alien and native entomofauna in Europe.Subfamilies are presented in a decreasing order based on the number of alien species.Species alien to Europe include cryptogenic species.Th e number over each bar indicates the number of species observed per family.

Figure 8
Figure 8.1.2presents the temporal changes in the records of Cerambycid species alien to Europe from 1492 to 2007.Cerambycids have tracked trade routes since the beginning of overseas communications.Th e fi rst species to have moved are those which live in dry wood and undergo a long stage of larval development.Th ese species have become cosmopolitan (e.g.Hylotrupes bajulus) or nearly so (e.g.Stromatium spp.).With the increased speed of international transport from 1850 to 1925, species with shorter life cycles were able to reach Europe alive and become established, e.g.Neoclytus acuminatus(Reineck 1919, Sama 2002, Tassi 1969).Later, only two species were introduced from North America to Europe via the US eff ort to supply extra furniture and increase military material after the 1 st World War (i.e., Parandra brunnea, Neoclytus acuminatus).Subsequently, 50 years passed until a second wave of introduction arrived alongside with the rapid development of international exchange of goods and transportation after the 2 nd World War.During the recent period, two further species have been detected in the wild -Anoplophora chinensis in 2000 in Italy(Colombo and Limonta 2001) and A. glabripennis in 2001 in Austria(Dauber and Mitter 2001).Th e number of interceptions of Cerambycids is still increasing throughout Europe.However, more eff ective control at borders is like to have reduced establishments following interception or introductions.Th e importation of exotic plants also off ers opportunities for introduction but also constraints the establishment of some alien species.For example, Phoracantha spp.could not have been introduced without the importation and mass cultivation of its host plants, Eucalyptus spp. in the Mediterranean basin.In south-eastern France, an Australian cerambycid, Bardistus cibarius (Newman, 1841) could survive only on its original host plant, an introduced grass tree (Xanthorrhoea sp., Xanthorrhoeaceae); the beetle population disappeared immediately after the infested host plants were removed(Cocquempot 2007).Th e case of Batocera

Figure 8
Figure 8.1.2.Temporal changes in the mean number of new records per year of Cerambycid species alien to Europe from 1492 to 2007.Th e number over each bar indicates the absolute number of species newly recorded per time period.

Figure 8
Figure 8.1.3.Origin of the Cerambycidae species alien to Europe

Figure 8
Figure 8.1.5.Main European habitats colonized by the established alien longhorn beetles.Th e number over each bar indicates the absolute number of alien longhorn beetles recorded per habitat.Note that a species may have colonized several habitats.

Family Species Status Regime Native range 1st record in Europe Invaded countries Habitat Hosts References
List and characteristics of the Cerambycidae species alien to Europe.Status: A: Alien to Europe; C: cryptogenic species.Country codes abbreviations refer to ISO 3166 (s ee appendix I).Habitat abbreviations refer to EUNIS (see appendix II).