Invasion of the Asian Ladybird Harmonia axyridis (Pallas, 1773) in the European Part of Russia

The natural range of the Asian ladybird Harmonia axyridis (Pallas, 1773) covers the territories of China, Mongolia, Korea, Japan, and Russia (Far East, Southern Siberia, and Altai). Since the early 1980's, the global invasion of H. axyridis began, first on the territory of the United States, from where the Asian ladybird spread to South America, Africa, and Europe. By 2016, this species occupied all of Western Europe with the exception of its northern and southern regions. Penetration of H. axyridis on the territory of the Russian Federation (Kaliningrad) was discovered in 2010, and since 2011, the species has spread to the Black Sea coast. This report presents our data on the distribution of Harmonia axyridis in central Russia, from its western borders, to the Volga River. The occupation of this huge territory by this species occurred mainly in the last 3 years−2018–2020. The rate of movement of the species on the territory of the European part of Russia is about 200 km/year.


INTRODUCTION
The natural range of the Asian ladybird Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) covers the following territories: North-Eastern and Central China, Mongolia, Korea, Japan, Eastern Kazakhstan, and in Russia-the Far East, southern Siberia, Tyva, and Altai (Orlova-Bienkowskaja et al., 2015;Blekhman and Goryacheva, 2017;Andrianov et al., 2018). In the early 1980's, the global invasion of H. axyridis began first in the United States (Koch et al., 2006), from where the Asian ladybird spread to South America, Africa, and Europe where it mixed with populations used in biological protection of greenhouse crops that escaped into the open (Lombaert et al., 2010;Roy et al., 2016). In Europe, invasive populations of H. axyridis were discovered in the early 2000's (Adriaens et al., 2003), and by 2016, this species occupied all of Western Europe except for its northernmost and southernmost regions (Roy et al., 2016).
In the European part of Russia, the occurrence of H. axyridis was observed from 2004 to 2006 in the territory of the Belgorod Region (Binkovskaya, 2004;Orlova-Bienkowskaja, 2013). In 2010, mass reproduction of the species was recorded by one of the authors in Kaliningrad (Zakharov et al., 2011). The presence and reproduction of H. axyridis have been observed since 2011 on the Black Sea coast of the Caucasus (Orlova-Bienkowskaja, 2013;Ukrainsky, 2013) and since 2012-2013 in the Krasnodar Territory (Korotyaev, 2015a,b). During the same period, there were reports of H. axyridis finds in Ukraine [since 2007-(Nekrasova andTytar, 2009;Verizhnikova and Shylova, 2013)], in Belarus [since 2011- (Kruglova, 2015;Kruglova and Sinchuk, 2017)], and in Latvia [since 2009[since -(Barševskis, 2009]. This report presents the authors' data on the distribution of H. axyridis in central Russia, from its western borders to the Volga River. The discussed species captured this huge territory mainly in the last 3 years−2018-2020.

MATERIALS AND METHODS
The presence of H. axyridis was recorded during the implementation of special collections of coccinellids or when collecting other insects. Beetles H. axyridis were collected at the stages of imago, pupae, and last instar larvae. Collections were carried out on various shrubs and trees, in cities-mainly on lime trees (Tilia sp.), as well as during the autumn flight and in wintering areas. Methods of collecting beetles and keeping them in the laboratory are described in Andrianov et al. (2018). In the collections of H. axyridis, where morphs were counted, three phenotypes were distinguished: succinea (yellow or red with a different number of black spots), spectabilis, and conspicua (both are black, with four and two red spots, respectively) and axyridis (black with many red/yellow spots). Among the succinea morphs, the proportion of individuals without spots was taken into account (see Table 2).

RESULTS AND DISCUSSION
Information about the materials collected by the authors of this paper and the collections of other researchers is presented in Table 1 and the map (Figure 1). It can be seen that H. axyridis Frontiers in Conservation Science | www.frontiersin.org  occupied a huge territory-from the western borders of the Russian Federation to the Volga. Almost exclusively the morphs found commonly in Europe-succinea, spectabilis, conspicua-were present in all the collections, with f. succinea dominating. The West Siberian morph axyridis was found only once-in Saransk (one individual). The least number of melanics (spectabilis, conspicua) was in Kaliningrad. The proportion of beetles of the succinea morph without spots was the greatest in Sochi in comparison with other populations ( Table 2). This suggests that the settlement of the Black Sea coast of the Caucasus occurred not only from the west, as in other regions, but also from the south, from Asia Minor.
It is known that in the new territories occupied by H. axyridis, this species successfully competes with the local Coccinellidae, as a result of which the number of the latter decreases  Table 3). These data should be supplemented in subsequent years. The rate of progress of the species was estimated from the findings in Kaliningrad (2010), the first breeding colony in Moscow [2015- (Zakharov, 2015)], and in Saratov [2019- ]. Taking into account the distance from Kaliningrad to Moscow (1,100 km) and from Kaliningrad to Saratov (1,750 km), the propagation speed is about 200 km/year. At this speed, beetles can spread both naturally (Jeffries et al., 2013) and using passing transport. The rate of spread calculated here is the same as that calculated in other parts of Europe (Brown et al., 2011).
Given the wide adaptability of H. axyridis to various environmental and climatic conditions, one can expect the spread of this species in the coming years to the north, at least to St. Petersburg (in 2019, H. axyridis was not there yet) and to the east, to the Urals.
If H. axyridis spreads to the east beyond the Urals, it will be possible to observe an interesting natural experiment, when the populations of two subspecies of H. axyridis, which clearly differ in morphological features [color and pattern on the elytra- (Blekhman and Goryacheva, 2017)] and in mitotypes-variants of mitochondrial DNA (Zakharov et al., 2011), unite in the Tomsk-Novosibirsk area (the western edge of the native range). Given the rate of spread of H. axyridis, one can expect that nature will stage this population-genetic experiment in the next 10 years.

DATA AVAILABILITY STATEMENT
The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding authors.

AUTHOR CONTRIBUTIONS
IZ conceived the project, designed methodology, and led the writing of the manuscript. IZ, AR, LE, DR, and AS contributed to ladybird collection and identification. All authors contributed critically to the drafts and gave final approval for publication.