Alien leaf beetles (Coleoptera, Chrysomelidae) of European Russia and some general tendencies of leaf beetle invasions

Invasions of leaf beetles can cause tremendous economic consequences because some of these insects become major pests in invaded territories. We present the first inventory of alien Chrysomelidae of European Russia that appeared in the region in the 20th and 21st centuries (9 species) with analysis of the history of their invasions and detailed maps of distribution. This case study revealed some general tendencies of invasions of leaf beetles: (1) Recently, a dramatic increase in the rate of Chrysomelidae invasions is observed, which reflects the increase in international trade of living plants; (2) Alien leaf beetles can spread quickly, occupying almost all of Europe within several decades; (3) When the range of some leaf beetle species is quickly expanding, or when the species has been recorded established somewhere outside the native range, this species should be regarded as a potential invader worldwide. and (4) Alien leaf beetles usually occur on alien or cultivated plants, but some become naturalized in native communities. The specific information was the following. Two species native to the Mediterranean region, Chrysolina americana (feeds on Rosmarinus and Lavandula) and Leptomona erythrocephala (feeds on Lotus corniculatus) were recorded in European Russia for the first time. A polyphagous pest of floriculture Luperomorpha xanthodera native to China and Korea and a pest of soybeans Medythia nigrobilineata native to east Asia have been in the region since 2016. A pest of tobacco Epitrix hirtipennis native to North America has occurred since 2011. A pest of corn Diabrotica virgifera was intercepted at the border of Russia in 2011 but has not established. Three alien species have been in the region since the 20th century: Zygogramma suturalis introduced from North America for control of Ambrosia, Phyllotreta reitteri native to Afghanistan and Tajikistan and feeding on Lepidium latifolium, and the Colorado potato beetle Leptinotarsa decemlineata.


Introduction
Major gaps in knowledge occur in regional alien floras and faunas, and data availability varies among regions [1]. In particular, alien insects of European Russia are poorly studied. Most of subfamilies of Chrysomelidae, except seed beetles (Bruchinae), because seed beetles are very different from other Chrysomelidae in biology and ecology and have different vectors and trends of invasions [6]. Megalopididae and Orsodacnidae are also leaf beetles, but we did not consider these families because no alien species of these groups occur in European Russia. The species below are presented in reverse chronological order of their first records in European Russia.
Leptomona erythrocephala differs from other species of the genus by the shape of the aedeagus (Fig 2) and by the following characters: punctation of elytra entirely confused; pronotum covered with punctures that are slightly smaller than those on elytra; head, pronotum, prosternum, coxae, femora, tibiae and antennomeres 1-3 reddish, mesosternum brown, elytra blue, labrum, tarsi, metasternum, abdominal tergites and sternites black; hind wings reduced. Identification of specimens collected in Sochi (see S2 Appendix) was confirmed by their comparison with specimens of L. erythrocephala from ZIN collected in Spain.
Biology. This species in its native range feeds on Polygonum and is also recorded on Fragaria and Potentilla reptans [26,27]. However, L. russica and representatives of the closely related genus Monolepta feed primarily on Fabaceae [28]. Based on our observations in nature, L. erythrocephala feeds on Lotus corniculatus (Fabaceae), which is a common ruderal plant in the city. Based on observations in a cage, we confirmed feeding on this plant. Ten specimens were placed in cage with the following Fabaceae plants collected in the same biotope: Trifolium repens, Trifolium aureum, Gleditsia triacanthos and Lotus corniculatus. The beetles fed only on L. corniculatus, gnawing on margins of leaves and petals.
Invasion status. Obviously, Leptomona erythrocephala is established in the region. First, many specimens were collected in the wild in two localities in 2017 and 2018. Second, the beetle feeds on a native plant.
Vector of dispersal. Sochi is more than 2000 km distant from the native range of the species; thus, natural spread was impossible. Unintentional introduction with planting material or soil was the most likely dispersal vector. The distance between the two localities in which L. erythrocephala was found in the Caucasus is 28 km. Because L. erythrocephala is a flightless beetle and its natural dispersal ability is restricted, the dispersal of L. erythrocephala in the region was likely connected with an unintentional introduction by man.
Economic impact. Leptomona erythrocephala is not regarded as a pest in its native range. However, special attention should be paid to trophic specialization of this species in the Caucasus, particularly if it becomes abundant. Note that L. erythrocephala is recorded to feed on Fragaria leaves [26], the representatives of the genera Leptomona and Monolepta feed on Fabaceae, and one of them, Monolepta quadriguttata (Motschulsky, 1860), is a serious pest of soybean [28, 29].   [50]; before 1950 in Romania, Austria and Germany (examined specimens from MTD); and in 1963 in the United Kingdom [51]. However, these findings most likely reflected only temporary populations. When Ch. americana was again recorded from the United Kingdom in the 1990s, MacLeod [52] supposed that it would not establish because of the cold climate. However, notably, Ch. americana Alien leaf beetles (Coleoptera, Chrysomelidae) of European Russia established and began to spread quickly and is now common throughout the United Kingdom and Ireland [50]. Introduction of the beetle was also reported in several other European countries and Israel (Table 1).
At present, the species has spread and is established throughout the Netherlands; however, not on native plants. Chrysolina americana thrives in gardens on rosemary and lavender and on cultivated Salvia but has not been recorded on native Salvia species in the wild [56]. Records of Ch. americana from Poland, Romania, Germany and Switzerland are supposedly questionable because of the Mediterranean origin of the species [49, 53,57]. We suppose that these records indicated cases of introduction of the species outside the native range. It is difficult to determine which records indicate establishment of species and which represent translocations or temporal populations.
Record in Crimea. Chrysolina americana has not been recorded from Russia or the Ukraine until now. Here, we present the first record of Ch. americana on the Crimean Peninsula: 13 specimens of this species were collected in Crimea in 2013 (Yalta, Bakhchisaray highway, sanatorium "Uzbekistan," 225 m a.s.l., on Rosmarinus officinalis, 01.06.2013, leg. N.V. Okhrimenko).
Vector of dispersal. Because Rosmarinus and Lavandula are popular garden plants throughout Europe, Ch. americana has been translocated outside the native range along with its host plants [6]. Opinions about natural dispersal abilities of Ch. americana are contradicting. MacLeod [52] states that Ch. americana is flightless and therefore is restricted in its dispersal abilities. However, Beenen and Roques [6] indicate that this species has good flight capacities and disperses naturally by flight. Webster et al. [58] suppose that expansion of the rosemary beetle to the United Kingdom has been expedited by climate change.
Invasion status. Whether Ch. americana is established in Crimea or only a temporal population was recorded is not clear. Further observations are necessary to answer this question, because the example of the population in the United Kingdom shows that this species is able to establish quickly and become a serious invasive pest.
Economic impact. Rosemary beetle is a garden pest and damages the foliage and flowers of various aromatic plants including lavender, rosemary and sage [55]. These plants are widely cultivated in Crimea. Thus, if Ch. americana becomes abundant, the beetle can cause negative economic consequences in the region.
Invasion history. Epitrix hirtipennis began to spread outside the native range at the end of the 19th century (Figs 6 and 7; Table 2). First, the beetle was introduced to islands in Atlantic and Pacific oceans: Hawaii, Bermuda, Tahiti, Fiji and Azores, and has become common there.
In 1983, this species was found in Europe for the first time in northern Italy [62] and was the first alien flea beetle introduced to Europe. The beetle then spread to south and central Italy, Greece, Turkey, Spain, Macedonia, Bulgaria, Syria, European Russia and Georgia. In 2011, E. hirtipennis was found to be common on Honshu (Japan) [90]. In some reviews, records from Sri Lanka [61], the Philippines [95,75] and Tanzania [96] are mentioned; however, these records are doubtful, because no references to the source of information are given.
Records in European Russia. In 2011, E. hirtipennis was first recorded in Russia, namely, on a tobacco plantation in Krasnodar City (south in European Russia) [92]. In 2013, 2016 and 2018, we found E. hirtipennis on the Black Sea coast, namely, in Tuapse and Sochi (Khosta District and Adler District, Imereti Resort) [11]. We collected five specimens in these localities in ruderal vegetation (see S1 Appendix).
Biology. Adults feed on leaves of plants of the family Solanaceae. Larvae develop on roots. Bieńkowski and Orlova-Bienkowskaja [97] review the host plants of E. hirtipennis in different regions. In Italy, E. hirtipennis has been observed to shift onto native Solanaceae [5].
Vector of dispersal. Since E. hirtipennis was the first alien flea beetle introduced to Europe, its record on the continent puzzled experts in Chrysomelidae. Epitrix hirtipennis was assumed to have arrived in Europe as aerial plankton with easterly trade winds blowing from the New World to Europe [98]. However, we believe that the most likely vector of dispersal is an unintentional introduction of larvae in soil with imported planting material.  Table 2. Database on localities of Epitrix hirtipennis is provided in S1 Appendix. https://doi.org/10.1371/journal.pone.0203561.g006 Alien leaf beetles (Coleoptera, Chrysomelidae) of European Russia  Table 2. Database on localities of Epitrix hirtipennis is provided in S1 Appendix.

Invaded regions
Years of records

Sources of information
Hawaii 1892, 1893,1927,1942,1960,1961,1962,1967 Economic impact. This species is known primarily as a pest of tobacco but can also feed on eggplant, potato, tomato and many other solanaceous plants [99].
Remark. The representatives of the genus Epitrix are particularly prone to invasions. Five species are established outside their native ranges in other continents and on islands. One additional representative of the genus, Epitrix setosella (Fairmaire, 1888), was reportedly introduced outside the native range, namely, from east Asia to Georgia [93]. However, our examination of the specimens identified as "E. setosella" from the collection of G.O. Japoshvili showed that the identification was incorrect and that those specimens belonged to E. pubescens (Koch, 1803).

-Diabrotica virgifera LeConte, 1868 (Galerucinae)
Native range. The western corn rootworm Diabrotica virgifera originates from the New World. The initial range is Mexico or Central America [100]. Now, the range in the Americas includes Canada, Costa Rica, Guatemala, Mexico, Nicaragua and the USA [4].
Invasion history. Man has greatly increased the range of this species in the Americas by the cultivation of corn [100]. In Europe, D. virgifera was first observed near the Belgrade airport, Serbia, in 1992 [101]. After several introduction events to different regions of Europe [102], the species has become widespread. Now, the beetle is recorded in at least 22 European countries (Fig 8) [4].
Record in European Russia. In 2011, D. virgifera was captured with a pheromone trap at the border of Russia in the Rostov Region near the international highway [10].
Biology. Adults of Diabrotica virgifera feed on leaves, silks, pollen, and young kernels of corn, and larvae develop on roots [103]. Alien leaf beetles (Coleoptera, Chrysomelidae) of European Russia Vector of dispersal. Diabrotica virgifera has been translocated from North America to Europe several times in aircraft laden with goods and materials [102]. The beetles fly well, and therefore, they spread in Europe both by hitchhiking and naturally [104].
Invasion status. Diabrotica virgifera has apparently not established in Russia yet, because it was intercepted only once in 2011.
Economic impact. Diabrotica virgifera is a major pest of cultivated corn. Feeding on the root system, larvae cause most of the damage. The species is included on the A2 List of quarantine pests of EPPO [4].

-Phyllotreta reitteri Heikertinger, 1911 (Alticinae)
Native range. We believe that the native range of Ph. reitteri is in central Asia (Fig 9), because the primary host plant Lepidium latifolium originates from that region [105]. Before the 1980s, Ph. reitteri was recorded in Kazakhstan and Uzbekistan only [106][107][108]. Most likely the recent record from west China [109] also belongs to the native range.
Invasion history. In 1984, Ph. reitteri was first found outside the native range, namely, in Crimea [110]. Then, in 1986-2012, the beetle was found in four regions in the south of European Russia (Table 3) and in 2002 in Turkey [111].
Distribution in European Russia. Phyllotreta reitteri occurs in Kalmykia, Saratov Region, Astrakhan Region and Krasnodar Territory (see Table 3).
Biology. Experiments conducted in cages and in the field show that the primary host plant of Phyllotreta reitteri is the perennial pepperweed Lepidium latifolium [112]. Adults feed on leaves, and larvae mine petioles and shoots. This plant of Asian origin has been cultivated as a spice and vegetable since the twelfth century [113]. Now, pepperweed is widespread in Asia and Europe, has been recorded on all continents and has become an invasive weed in North America [112]. In European Russia, Ph. reitteri occurs in moist habitats, such as on the banks of rivers and ponds and in irrigated parks.
Vector of dispersal. Unknown. Invasion status. We believe that Ph. reitteri is alien in European Russia. The species meets at least four criteria of alien beetle species [97] as follow:  Table 3. 2. Disjunction of the range, which cannot be explained by disjunction of suitable landscapes or host plant ranges. The range of Ph. reitteri consists of two parts: one is in central Asia, and the second is in the south of European Russia, the Crimean Peninsula and Turkey. The distance between these two parts is more than 1500 km.

Expansion of a part of the range isolated from the main part. Records in Turkey and Astrakhan and Saratov regions in the 2000s most likely indicate the expansion of the range.
4. Feeding on an alien host plant. Lepidium latifolium originates from central Asia [105].
It is unlikely that the species occurred in the region but remained unnoticed for a long time, because this beetle is large for the genus Phyllotreta and has characteristic bright coloration. No collected specimens of Phyllotreta reitteri from the south of European Russia were found in the rich collection of the Zoological Institute of the Russian Academy of Sciences, although the collection contains thousands of specimens of other Phyllotreta species collected in this region at the end of the 19th and the first half of the 20th century.
Economic impact. Phyllotreta reitteri is regarded as a potential biological control agent of perennial pepperweed [105].

-Zygogramma suturalis (Fabricius, 1775) (Chrysomelinae)
Native range. Ragweed leaf beetle is native to the USA and the south of Canada [59]. Invasion history. Zygogramma suturalis (Fig 10) was introduced to the USSR from Canada and the USA for control of one of the most noxious invasive weeds Ambrosia artemisiifolia [114]. The beetles were released in 16 provinces of the USSR: in European Russia, the Ukraine, Georgia, Kazakhstan and the Far East. The most intensive work was performed in the south of European Russia, primarily in the Rostov Region and in Stavropol and Krasnodar territories [114]. The first release (1500 specimens) was performed in the vicinity of Stavropol in 1978. In 1981-1983, Z. suturalis became abundant and began to spread quickly. Now, the beetle is relatively widespread in the south of European Russia and occurs also in the southeast of the Ukraine and in Georgia [115]. In 1985, one specimen was found in Turkey, but the species did not establish, with no other further records [116,117].
Zygogramma suturalis when introduced to the south of European Russia showed rapid evolutionary changes in flight capacity (development of flight ability and morphological changes) within only five generations [118]. The morphological changes were so significant that the new subspecies Zygogramma suturalis volatus Kovalev, 2002 was described [118]. Table 3. Records of Phyllotreta reitteri outside the native range.

Invaded regions
Years of records In 1982-1985, beetles from Stavropol Territory were released in Primorje (Far East). In the 1990s, the population of Z. suturalis in the Far East had supposedly disappeared. However, in 2010, this species was re-discovered in the region, although it was not abundant [119]. Zygogramma suturalis was also released in Croatia and Australia but failed to establish, whereas releases of Z. suturalis in China in 1985 resulted in establishment in some locations [109]. Record of Z. suturalis from Kazakhstan [109] most likely refers to the releases rather than to established populations. There are no current records of Z. suturalis from this country [120].

Sources of information
Distribution in European Russia. Now, Z. suturalis occurs in five provinces in the south of European Russia: Stavropol Territory, Krasnodar Territory, Adygea, Rostov Region, Karachay-Cherkessia [121,122] and Kabardino-Balkaria (see S1 Appendix).
Biology. Larvae and adults feed on leaves, shoots and inflorescences of Ambrosia artemisiifolia [8]. The species is very abundant in some localities, occurs in river valleys, on the fringes of forests, and in saline areas [123].

Vector of dispersal. The beetle was intentionally introduced for biological control of Ambrosia artemisiifolia.
Invasion status. Zygogramma suturalis is established in European Russia. Economic impact. Soon after the introduction of Z. suturalis to the Caucasus, the density of some populations was as high as 100 million specimens per km 2 . Zygogramma suturalis completely destroyed Ambrosia in some locations. However, 10 years after the introduction, surveys revealed that although Z. suturalis remained abundant in some places, the beetle did not significantly affect the general density of the host plant. The "plant-phytophagous" system reached an equilibrium [122,124]. The same situation is observed in the Far East [119].
Invasion history. From the beginning of the 19th to the beginning of the 20th century, L. decemlineata colonized all of North America [7,125]. In 1922, L. decemlineata was found established in Bordeaux (France) and began to spread in Europe. Now, it is distributed almost throughout Europe and northern Asia [4,9,19,125]. Presently, the Colorado potato beetle damages potato crops all over Europe, Asia Minor, Iran, central Asia, and western China [125]. The general distribution of Leptinotarsa decemlineata is well known [4]; thus, we present the map of distribution of this species in Russia only (Fig 11).
Expansion to Russia. In 1958, expansion of the pest range reached the western border of the USSR [9]. Now, the Colorado potato beetle is common all over European Russia, even in the north: in the Leningrad Region [9] and the Republic of Komi [126]. The range has expanded to most parts of Siberia. The northern boundary of the area passes through Karelia, Arkhangelsk Region, Republic of Komi, Tumen Region, Tomsk Region and Krasnoyarsk Territory. Since 2000, an isolated part of the range is also in the Far East in Primorsky Territory [9].
Vector of dispersal. This pest enters new territories primarily because of unintentional transportation with potato and self-dispersal of beetles sometimes aided with the winds [7].
Economic impact. Leptinotarsa decemlineata is the most devastating pest of potato and other cultivated plants of the family Solanaceae [125].

Discussion
Analysis of invasions of leaf beetles to European Russia revealed some general tendencies. First, recent translocations and establishment of Chrysomelidae species outside their native ranges are obviously much more common than previously. Only three alien leaf beetle species were recorded in European Russia in the 20th century: Leptinotarsa decemlineata, Phyllotreta reitteri and intentionally introduced Zygogramma suturalis. However, in 2000-2017, as many as six alien species were found in the region. This situation corresponds to the general tendency of exponential increase in the rate of invasions of leaf beetles to Europe [6] and the increase in invasions of beetles feeding on living plants [128]. The current situation reflects the increase in international trade, particularly the trade of living plants and the increase in air transport. In most cases, leaf beetles are translocated to remote regions with imported plants or (as in the case of Diabrotica virgifera) by hitchhiking in airplanes [102,104]. Most of the alien leaf beetles are associated with agricultural plants, but some species (for example, Phyllotreta reitteri) develop on weeds.
After establishment outside their native ranges, leaf beetles can quickly spread by unintentional introduction by man and natural dispersal. For example, Diabrotica virgifera was first recorded in Europe in 1992 but has now spread to at least 21 countries becoming a major pest of corn in some regions [4]. Luperomorpha xanthodera has occupied all of Europe from Spain to Russia in only 15 years. Therefore, the records of new alien pest leaf beetles are very important and should be published quickly.
In some cases, invasions of leaf beetles are unpredictable. For example, establishment of Leptomona erythrocephala native to Spain in the Caucasus is rather surprising. However, in other cases, emergence of alien species is easy to predict. For example, it was obvious that Epitrix hirtipennis could appear in the south of European Russia, because the range in Europe was expanding to the east. Similarly, in the early 20th century, it was obvious that Leptinotarsa decemlineata would appear in Europe because of its outbreak and quick range expansion in North America. In general, when the range of some leaf beetle species is quickly expanding, or when the species has been recorded established somewhere outside the native range, this species should be regarded as a potential invader worldwide. For example, global invasion of Epitrix hirtipennis began from its establishment in Hawaii at the end of the 19th century [65].
Leaf beetles can be potentially translocated from any part of the world. Four species alien to European Russia originate from North America, two from the Mediterranean region and three from Asia. Recently, the invasions of beetles of east Asia are becoming more important [128]. Establishment and quick spread of Luperomorpha xanthodera in Europe reflects this current tendency.
The Black Sea region is more prone to invasions of leaf beetles than other regions of European Russia. The many records of alien species in this region could not be explained by more intensive survey, because we have the database of localities of leaf beetles collected in all regions of European Russia (approximately 30 000 localities) [129]. The many invasions in the Black Sea region correspond to the general tendency of many invasions of leaf beetles in territories with a warm and wet climate. For example, Italy occupies first place in Europe for the number of alien leaf beetles [6].
However, predicting whether an introduced species can become established based on a simple comparison of climate in native and invaded ranges is difficult (or even impossible), because the establishment of a species depends on a complex of interacting abiotic, biotic and anthropogenic factors. For example, when Ch. americana was recorded for the second time in the United Kingdom in the 1990s, MacLeod [52] supposed that the beetle would not establish because of the cold climate; however, Ch. americana has established and become a common pest.
Alien leaf beetles can spread to native communities and become naturalized. For example, Zygogramma suturalis also occurs in native, undisturbed communities of nature reserves [130,131]. Usually, alien leaf beetles remain strictly related to their original, alien plants [5,6]. This relation is also true for the Chrysomelidae of European Russia. However, some species can also feed also on native plants or cultivated plants from other regions. In particular, Leptinotarsa decemlineata feeds not only on cultivated plants but also on S. dulcamara and Hyoscyamus niger. When a species is established in native communities and feeds on native plants, it is fully naturalized, i.e., ecologically undistinguishable from native species. Because of full naturalization, the distinction between native species and those established before the 20th century is difficult.
Because the invasions of leaf beetles can cause tremendous economic consequences, and because of the exponential increase in the rate of invasions recently observed, special attention should be paid to the study of these invasions. Monitoring is necessary to reveal the cases of emergence of species outside their native ranges. General trends of invasions of leaf beetles should be examined and analyzed carefully.