Leaf and Seed Beetles ( Coleoptera , Chrysomelidae ) Chapter 8 . 3

Abstract Th e inventory of the leaf and seed beetles alien to Europe revealed a total of 25 species of which 14 seed beetles (bruchids) and 11 leaf beetles mostly belonging to the subfamilies Alticinae and Chrysomelinae. At present, aliens account for 9.4% of the total fauna of seed beetles in Europe whereas this percentage is less than 1% for leaf beetles. Whilst seed beetles dominated the introductions in Europe until 1950, there has been an exponential increase in the rate of arrival of leaf beetles since then. New leaf beetles arrived at an average rate of 0.6 species per year during the period 2000–2009. Most alien species originated from Asia but this pattern is mainly due to seed beetles of which a half are of Asian origin whereas leaf beetles predominantly originated from North America (36.4%). Unlike other insect groups, a large number of alien species have colonized most of Europe. All but one species have been introduced accidentally with either the trade of beans or as contaminants of vegetal crops or stowaway. Most aliens presently concentrate in man-made habitats but little aff ect natural habitats (<6%). Highly negative economic impacts have been recorded on stored pulses of legumes and crops but very little is known about possible ecological impact.


Introduction
Th e family Chrysomelidae is one of the largest Coleopteran families, including ca. 37 000 described species in the world and perhaps the same number as yet undescribed (Jolivet and Verma 2002).Bruchidae, or seed beetles, is a relatively small family.Kingsolver (2004), referring to the most recent world catalogue, mentions 1,346 valid bruchid species.Although there are good arguments to treat Bruchidae as a subfamily of Chrysomelidae and raise some leaf beetle subfamilies to family rank (Reid 1995), this is still not common practice among leaf beetle researchers.We treat Bruchidae and Chrysomelidae in this contribution as families, merely for practical reasons.According to Fauna Europaea, the fauna presently observed in Europe includes 1532 leaf beetles and 145 seed beetles.
Except for important agricultural pests such as the Colorado potato beetle, Leptinotarsa decemlineata, and more recently, the western corn rootworm, Diabrotica virgifera virgifera, little was known about introductions of alien leaf beetles until Beenen (2006) revealed that 126 species have been translocated at least once from one continent to another.More information on alien seed beetles has been available in the literature mainly because of their potential impact on stored products (Southgate 1979).In the present work, we will show that 25 non-native species of leaf and seed beetles of which one is of unknown origin (cryptogenic) have already established in Europe (Table 8.3.1).Th us, aliens still represent only a very small proportion (1.5%) of the total fauna of leaf and seed beetles in Europe.By comparison, approximately 71 alien leaf beetle species have been recorded from North America (Beenen 2006, Beenen, unpubl.).
Within Europe, changes in the distribution of native leaf beetles have also been noticed which can be partly associated either to human activity or to natural trends such as delayed post-glacial expansion and global warming.For example, the recent northwards expansion of a fl ea beetle, Longitarsus dorsalis, seems to result from both the introduction of a rapidly expanding invasive plant originating from South Africa, Senecio inaequidens DC., on which L. dorsalis thrives (Beenen 1992), and from increasing temperatures during the past years.However, the role of human activity is often diffi cult to ascertain in such observed range expansions of native species.We will essentially consider the species alien to Europe, a summary of the species alien in Europe (Table 8.3.2) and will present their characteristics at the end of the chapter.

Taxonomy
A total of 25 alien species of which 14 seed beetles and 11 leaf beetles have been recorded as established in Europe (Table 8.3.1).Th us, bruchids represent more than a half (56.0%) of the alien species whereas they account for only 8.1% of the native fauna of seed and leaf beetles (Figure 8.3.1).Th is arrival of alien seed beetles has signifi cantly modifi ed the composition of the total fauna of seed beetles observed in Europe, where aliens account for 9.4% at present.Th e pattern is rather diff erent for Chrysomelidae.Although this family includes 13 subfamilies in Europe the alien entomofauna is only distributed among fi ve of these subfamilies.Large diff erences are observed in the contribution of each subfamily without any apparent correlation to its numerical importance in the native fauna.Th e recent arrival in France of an alien palm hispine beetle, Pistosia dactylifera (Drescher and Martinez 2005), largely modifi ed the composition of the Hispinae subfamily which includes only three native species (Fauna Europaea 2009).However, aliens represent much less so for the two major subfamilies of leaf beetles, Alticinae fl ea beetles (four species-0.7% of the total) and Chrysomelinae (four species-1.3% of the total).Other alien species include one skeletonizing leaf beetle (Galerucinae) and one tortoise leaf beetle (Cassidinae).Th e same subfamily pattern is observed for translocations of leaf beetles at world level but Beenen (2006) also noticed other species belonging to Hispinae (e.g.Brontispa palm leaf beetles) and Criocerinae.It is noticeable that representatives from some important subfamilies such as Cryptocephalinae and Donaciinae have never been introduced, or never established at least.
Leaf beetles and seed beetles largely diff er in biological traits that may be involved in the relative success of seed beetle invaders compared to other groups.Seed beetles have several ways of egg-laying.Most species deposit their eggs on mature pods of legumes (Fabaceae), the eggs being cemented to the pod or dropped in a self-made hole in the pod wall.Other species lay eggs on mature seeds that are still attached to the inside of a partly opened pod.A third group of species oviposit on mature seeds that have fallen to the ground from a fully dehisced pod.However, some species such as Acantoscelides obtectus use diff erent life history strategies.Early in the season in this species, oviposition occurs on green pods of Phaseolus, while later in the season, the eggs are deposited on mature seeds that have fallen to the ground.Th ese biological features make A. obtectus fully capable of completing cycle after cycle on naked seeds in storage (Kingsolver 2004).Th e larvae of seed beetles entirely develop within the seeds until pupation and their presence cannot be recognized before adult emergence, unless the seed is X-rayed.
In contrast, leaf beetles show a large variety of reproductive traits.Many Galerucinae (e.g., Diabrotica species) and Alticinae larvae (e.g., Epitrix species) develop in or at the roots of plants and adults feed from leaves of a specifi c host plant or a wide variety of plant species.Other Chrysomelidae feed both as larva and adult externally on leaves of their host plants.Although practically no plant species is free of leaf beetles, most leaf beetles need fresh plant products in all or at least in the adult stage.Stored dry plant products are not suitable for leaf beetles to complete their life cycle.

Temporal trends
Chrysomelids probably began to be introduced thousands of years ago.It is likely that leaf beetles associated with crops have taken the same route as herbs associated with cereals which are supposed to have entered Europe from the Near East (Pinhasi et al. 2005).Beenen (2006) argued that the combination of Buglossoides arvensis (L.) Johnston and Longitarsus fuscoaeneus Redtenbacher 1849 might have taken the route from southwest Asia where they spread with agriculture to large parts of the temperate parts of the Northern hemisphere.Th us, a number of species which are at present considered as native may indeed be originally alien.Bruchidae must have infested pulses grown by man since the dawn of agriculture.Southgate (1979) also mentioned infestations of lentils from the Egyptian Ptolemaic period (305 BC -30 BC).Relatively little is known of these ancient introductions.More recent ones are much better documented as in the case of the potato Colorado beetle (Leptinotarsa decemlineata) (see factsheet 14.10).
From a global point of view, new records of alien species in Europe were relatively important during the 2 nd half of the 19 th century, due to seed beetle species.Th e most important being Acanthoscelides obtectus, Callosobruchus chinensis and C. maculatus.However, these species may have been introduced well before their fi rst record.Since ca.1900, the rate of seed and leaf beetle introductions severely decreased until 1975 when it began to increase again with globalization, essentially through the arrival of leaf beetles.Th e last seven years since 2000 corresponded to an acceleration of introductions, with an average of 0.8 new species of Chrysomelidae per year, again mostly leaf beetles (Figure 8.3.2)

Biogeographic patterns
Asia supplied the major proportion of the alien seed and leaf beetles that have established in Europe (Figure 8.3.3).However, this pattern is mainly due to seed beetles of which a half are of Asian origin whereas leaf beetles predominantly originated from North America (36.4%).No seed and leaf beetle species of Australasian origin have yet established in Europe.
Alien species are not evenly distributed in Europe, and leaf and seed beetles do not show the same pattern of expansion.Half of the alien seed beetles have colonized more than ten countries with four of them present in more than 50 countries and the main islands of Europe.In contrast, 63.6% of the alien leaf beetles have not yet spread out of the country where they have been initially introduced.Only two species, Leptinotarsa decemlineata and Diabrotica virgifera, are presently encountered in 38 and 20 countries respectively (EPPO 2009, Gödöllo University 2004, Grapputo et al. 2005, Purdue University 2008) (see maps in the spreadsheets 8 and 10).Owing to climate change, L. decemlineata may extend its range to Finland (Valosaari et al. 2008).
Alien seed and leaf beetles appear to be concentrated in southern Europe with 18 species observed in mainland Italy and more than 10 species in continental France

Main pathways and vectors to Europe
All alien species of seed and leaf beetle except one (i.e., 95.7%) have been introduced accidentally to Europe.Unlike North America and South Africa, where a number of alien species were released for biological control of weeds (Beenen 2006), only the ragweed leaf beetle, Zygogramma suturalis, has been intentionally introduced from North America for the biological control of common ragweed, Ambrosia artemisifolia L., since 1978 in Russia (Reznik et al. 2004) and several countries of southeastern Europe, and subsequently established in the wild especially in the Caucasus (Kovalev 2004).A fl ea beetle native of Continental Europe, Altica carduorum (Guérin-Méneville), has also been introduced in Britain and Wales in 1969-1970 to control creeping thistles, Cirsium arvense (L.) Scop.but none apparently established (Baker et al. 1972, Cox 2007).Although it is diffi cult to ascertain the exact pathway of introduction for most of the  (Böhme 2001, Kingsolver 2004).However, the arrival of other seed beetles of the genera Bruchidius, Caryedon, Megabruchidius and Mimosestes seems to be more related to the trade in legume tree seeds of Mimosoideae (Albizzia, Acacia) and Caesalpinoideae (Cassia, Cercis, Tamarindus) used as ornamentals in parks and gardens.Megabruchidius tonkineus was at fi rst suspected to have been introduced from Vietnam to Germany with white beans (Wendt 1980) but it was later found to be associated with pods of honey locust trees, Gleditsia triacanthos L. (Papilionoideae), and not capable of complete development in beans (Guillemaud et al. 2010).Similarly, Acanthoscelides pallidipennis was probably introduced with seeds of false indigo bush (Amorpha fructicosa L., Papilionoideae) (Tuda et al. 2006) and Bruchidius siliquastri with these of redbuds (Cercis; Caesalpinoideae) from China (Kergoat et al. 2007).Seeds imported for ornamental purposes may also serve as the vector of seed beetles.Specularius impressithorax (Pic) sustained several generations indoors in the Netherlands after having been introduced from South Africa along with seeds of Erythrina (Papilionoideae) used for decoration, but did not eventually establish (Heetman and Beenen 2008) (Figure 8.3.7).
Most alien leaf beetles are associated with vegetable crops (Solanaceae, Brassicaceae, Gramineae including maize).With both larvae and adults feeding on foliage, these species probably entered Europe as plant contaminants (eggs, larvae) or crop contaminants (adults).Th e Colorado potato beetle has frequently been intercepted with potato plants and tubers, but also in all forms of packaging and transport.For example, it usually arrived to Great Britain with commercial freight among vegetable crops such as lettuce, Lactuca sativa L., or on ships, aircraft or private cars traveling from the continent (Cox 2007).Indeed, fresh vegetables grown on land harbouring overwintering beetles are common means of beetle transport in international trade (Bartlett 1980).Th e African tortoise beetle Aspidimorpha fabricii (= A. cincta Fabricius) was believed to be imported in Italy as a contaminant of bananas in the late 1950s but it became a problem in cultures of Beta vulgaris L. (Zangheri 1960).A hispine palm leaf beetle, Pistosia dactyliferae was also probably introduced as a contaminant of palms imported for ornamental purposes (Drescher and Martinez 2005).
Th e means of introduction appears diff erent when larvae are root-feeding as in Diabrotica and Epitrix species.Unless soil infested with larvae has been imported with host plants, which is usually prohibited, these species probably travel as stowaways.Th e western corn rootworm, Diabrotica virgifera virgifera, proved to have been translocated from North America to Europe at least three times in aircraft laden with goods and materials, but probably not with maize plants (Ciosi et al. 2008, Miller et al. 2005).Th e outbreaks in Northwestern Italy and Central Europe probably resulted from introductions of individuals originating in northern USA (Delaware) (Guillemaud et al. 2010).
However, another pest species related to tobacco, Epitrix hirtipennis, is assumed to have arrived in Europe as aerial plankton with easterly trade winds blowing from the New World to Europe (Döberl 1994b).Similarly, Jolivet (2001) reported the translocation of the Sweet potato fl ea beetle, Chaetocnema confi nis Crotch, from the USA to several tropical destinations by hurricanes.Adults of Colorado potato beetle are also assumed to be capable of migrating across the Channel although this beetle does not fl y strongly (Cox 2007) or from Russia (the St Petersburg region) to Finland (Grapputo et al. 2005).
Th e collection and trade of orchids for greenhouses has also resulted in the arrival of several species which caused severe damage without persisting such as a fl ea beetle, Acrocrypta purpurea Baly, a species from Southeast Asia which was accidentally introduced with plant collections into a greenhouse of Leiden University in the Netherlands (Döberl 1994a).Likewise, larvae of a criocerine species, the yellow orchid beetle Lema pectoralis Baly, were imported to the Netherlands with an orchid collected in 1988 in Th ailand (Beenen, unpubl.).Originating of the Peninsula Malaysia and Singapore (Mohamedsaid 2004), L. pectoralis is a major pest ('orchid lema') of orchid cultures, particularly Vanda and Dendrobium, in the Philippines (de la Cruz 2003).
Pathways within Europe are a source of particular concern because of the waiver of formerly routine phytosanitary inspections on goods transported within the European Union.Th us, alien species once introduced into one European country along with alien plants or seeds, can freely move to other European countries.Spread may combine long-distance, human-mediated dispersal and natural dispersal by adult fl ight, as it is the case for Leptinotarsa decemlineata (Grapputo et al. 2005).Another signifi cant example is the present northwards expansion of a species alien in Europe, Chrysolina americana.Th is leaf beetle originates from the Mediterranean Basin where it is associated to Rosmarinus and Lavendula.Because both plants are popular garden plants throughout Europe, C. americana has been translocated outside its native range along with its host plants, e.g. to the Netherlands along with potted Lavendula plants imported from Italy (Beenen, unpubl.).Once introduced, this species, which has good fl ight capacities, disperses naturally by fl ight.

Most invaded ecosystems and habitats
All alien Chrysomelidae are phytophagous.As expected from the numerical importance of Bruchidae within aliens, seeds constitute the most important larval feeding niche (56.0%), far more important than leaves (24.0%) and roots (20.0%).Almost all these species are only present in man-made habitats which represent 94.1% of the colonized habitats, essentially agricultural lands, parks and gardens, glasshouses, and warehouses for seed beetles (Figure 8.3.5).Natural and semi-natural habitats have been very little colonized yet.
In addition to these strong habitat trends, about 40% of the alien chrysomelid species remain strictly related to their original, alien plants.Th is is especially true for leaf beetles, where only Epitrix hirtipennis out of the 11 alien species has been observed to shift onto native Solanaceae in Italy (Beenen 2006).In contrast, most alien seed beetles found outdoors have already switched to seeds of native plants, for example Bruchidius siliquastri on the native redbud, Cercis siliquastrum, in France (Kergoat et al. 2007), and Acanthoscelides obtectus and Callosobruchus chinensis on wild legumes (Tuda et al. 2001).Under outdoor conditions, a strict dependency to the original alien host was only observed for two Megabruchidius species, M. tonkineus and M. dorsalis, associated with seeds of honey locust tree, Gleditsia triacanthos, in parks and gardens.However, a number of seed beetle species still confi ned to greenhouses and warehouses only develop on alien hosts of tropical origin, such as Caryedon serratus associated with groundnuts (Arachis hypogaea L.), tamarind (Tamarindus indica L.) and other seeds of alien Caesalpinioideae (Kingsolver 2004).Such species still cannot establish outdoors because none of their alien hosts can survive in the wild at the present time.

Ecological and economic impact
Th reats due to alien chrysomelid species were fi rst pointed out by Linnaeus in a lecture in 1752, referring to his observation of asparagus plants (Asparagus offi cinalis L.) that were heavily infested in the vicinity of Hamburg by Crioceris asparagi, a species introduced from Russia at this time (Aurivillius 1909).
Alien chrysomelid species are better known for their economic impact than for their ecological impact.Indeed, possible ecological impacts on native fl ora and fauna are very little documented.Positive impact can be appreciated for only one alien species, Zygogramma suturalis, a strict monophagous species deliberately introduced to Europe for the control of the invasive ragweed (cf above).
Negative economic impacts have been recorded in seven of the alien seed beetle species which may severely aff ect stored pulses of economically-important legumes ( Acanthoscelides obtectus, A. pallidipennis, Bruchus pisorum, B. rufi manus, Callosobruchus chinensis, C. maculatus, C. phaseoli, and Zabrotes subfasciatus; see (Borowiec 1987, Hoffmann et al. 1962)).Most of them are capable of re-infesting stored legumes until the food reserves are exhausted.In leaf beetles, large economic impacts have been shown for the Colorado potato beetle, L. decemlineata, aff ecting potato crops (see factsheet 14.10) and the western corn rootworm, D. virgifera virgifera aff ecting maize roots and foliage (see factsheet 14.8).However, It must be stressed that economic damage has only been seen on maize in Serbia, and in some bordering areas in Croatia, Hungary, Romania, and small areas in Bosnia-Herzegovina and Bulgaria (EPPO 2009).In the United Kingdom, yield losses to be expected from the arrival and spread of D. virgifera virgifera have been estimated to range from 0.9 to 4.1 million € over 20 years in absence of obligatory campaign to prevent spread of western corn rootworm but the costs of such a campaign could also range from 3.7 to 10.5 million € (Central Science Laboratory 2007).Epitrix hirtipennis may also impact tobacco crops (Sannino et al. 1984, Sannino et al. 1985) as well as E. cucumeris these of potato and tomato (Borges and Serrano 1989), and Phaedon brassicae the cabbage crops (Limonta and Colombo 2004).Alien foliage-feeding chrysomelids may also act as vectors for plant diseases, for example D. virgifera which transmits several cowpea virus strains in North America (Lammers 2006).However, little is yet known in this fi eld (Jolivet and Verma 2002).Besides such economic damage, aesthetic impacts are recorded on ornamental plants, such as these of the leaf beetle Pistosia dactylifera on palm trees in southern France (Drescher and Martinez 2005).

Expected trends
Introduction of alien chrysomelids is still an ongoing process, especially through the trade of ornamentals via garden centers.For example, an alien species of the genus Luperomorpha was recently imported to Europe.L. xanthodera, originating from China, was fi rst found in Great Britain feeding in fl owers of several plant species in garden centers (Johnson and Booth 2004).Later it was observed in Switzerland (F.Köhler, personal communication), Germany (Döberl and Sprick 2009) and the Netherlands (Beenen et al. 2009), and also in garden centers, especially on rose fl owers (Figure 8.3.6).Other alien specimens of Luperomorpha observed in Italy (Conti and Raspi 2007) and France (Doguet 2008) were fi rst identifi ed as L. nigripennis, from India and Nepal, but fi nally identifi ed as L. xanthodera (Döberl and Sprick 2009).Plants cultivated in the Mediterranean area, then transported without severe pest control and sold in Central, Western and Northern Europe also constitute a serious threat for the expansion of species alien in Europe.Th e risks associated to this pathway were estimated for Norway (Staverløkk and Saethre 2007).
Species originating from subtropical and tropical regions have also been translocated such as Aspidimorpha nigropunctata (Klug) from tropical Africa to Th e Netherlands and Macrima pallida (Laboissière) from the Himalayan region to Cyprus.Th ese introductions usually have not led to establishment (Beenen 2006).However, they do indicate a potential risk, especially in the context of global warming which may facilitate establishments of such species in the near future.Th e arrival in southern Europe of additional species associated with ornamental palms such as the hispine leaf beetle, Brontispa longis- sima (Gestro), already invasive in other parts of the world (Nakamura et al. 2006), is thus probable, considering the current increase in alien pests related to palms (see Chapter X).
Finally, it is diffi cult to make serious predictions about the results of future translocations because the species may react diff erently to the new habitats and hosts when compared with the situation in their native environment.Furthermore, translocations may enhance evolutionary changes partly because of founder eff ects and genetic bottlenecks and partly because of the triggering of evolution by new environmental factors (Whitney and Gabler 2008).Zygogramma suturalis when introduced to the Northern Caucasus for biological control of ragweed, showed rapid evolutionary changes in fl ight capacity (development of fl ight ability and morphological changes) within only fi ve generations (Kovalev 2004).and other legumes Borowiec (1983), Borowiec (1988), Migliaccio and Zampetti (1989), Szentesi (1999)

Figure 8
Figure 8.3.1.Comparison of the relative importance of the subfamilies of Chrysomelidae and Bruchidae in the alien and native entomofauna in Europe.Subfamilies are presented in a decreasing order based on the number of alien species.Th e number right to the bar indicates the number of species per family.

Figure 8
Figure 8.3.2.Temporal changes in the mean number of new records per year of seed and leaf beetle species alien to Europe from 1800 to 2009.Th e number right to the bar indicates the total number of seed and leaf beetle species recorded per time period.

Figure 8
Figure 8.3.3.Comparative origin of seed and leaf beetle species alien to Europe

Figure 8
Figure 8.3.4.Colonization of continental European countries and main European islands by seed and leaf beetle species alien to Europe.

Figure 8 .
Figure 8.3 5. Main European habitats colonized by the established alien species of Chrysomelidae and Bruchidae.Th e number over each bar indicates the absolute number of alien species recorded per habitat.Note that a species may have colonized several habitats.

Table 8 .3.1.
List and characteristics of the established Chrysomelidae species alien to Europe.Status: A Alien to Europe C cryptogenic species.Country codes abbreviations refer to ISO 3166 (see appendix I).Habitat abbreviations refer to EUNIS (see appendix II).Last update 1 February 2010.

Table 8 .3.2.
RS AT, BA, BE, BG, CH, CZ, DE, FR, GB, HR, HU, IT, MO, NL, PL, RO, RS, SI, SK, UA.List and characteristics of the Chrysomelidae species alien in Europe.Country codes abbreviations refer to ISO 3166 (see appendix I).Habitat abbreviations refer to EUNIS (see appendix II).Last update 1 February 2010.