Harmonia axyridis (Coleoptera: Coccinellidae) in Asia: a re-examination of the native range and invasion to southeastern Kazakhstan and Kyrgyzstan

First publication on-line:
Marina J. Orlova-Bienkowskaja, Andrey S. Ukrainsky, Peter M. J. Brown.
2015.
Harmonia axyridis (Coleoptera: Coccinellidae) in Asia: a re-examination of the native range and invasion to southeastern Kazakhstan and Kyrgyzstan.
Biological Invasions. DOI 10.1007/s10530-015-0848-9.

M. J. Orlova-Bienkowskaja (Corresponding author)

     A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences,

     33 Leninskiy Prospect, Moscow, 119071, Russia

     e-mail: marinaorlben@yandex.ru

     State Scientific Research Institute of Restoration,

     44/1 Gastello Str., Moscow, 107014, Russia

     Animal & Environment Research Group, Department of Life Sciences, Anglia Ruskin University,

     East Road, Cambridge CB1 1PT, UK

     e-mail: peter.brown@anglia.ac.uk

Abstract Harmonia axyridis (Pallas) is an invasive ladybird spreading in several continents. It is native to East Asia, but its range in Asia has until now been poorly understood. The most complete map of the range of Harmonia axyridis in Asia has been compiled (432 localities). Harmonia axyridis occurs in the south-east of West Siberia, the south of East Siberia, the south of Russian Far East, the east of Kazakhstan, the north of Kyrgyzstan, Mongolia, China, North Korea, South Korea, Japan, and the north of Vietnam. Southeastern Kazakhstan and the north of Kyrgyzstan are not a part of the native range: the large Balkhash Desert is situated between this mountainous region and the nearest part of the native range (Altai mountains). The analysis of dates and places of findings indicates that Harmonia axyridis appeared in southeastern Kazakhstan and Kyrgyzstan after the construction of the Turkestan-Siberian Railway. It is hypothesized that the beetles crossed the desert along this railway.

Keywords Harmonia axyridis; Coccinellidae; Harlequin ladybird; Invasive species; Multicolored Asian lady beetle; Native range

Introduction

Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is an emblematic invasive species. This Asian beetle was released for the biological control of aphids and has become almost cosmopolitan, having negative ecological and economic consequences (Brown et al. 2011). The spread of H. axyridis caused the decline of populations of native ladybird species in some regions (Roy et al. 2012a). In addition, this beetle has become a pest of fruit production and wine production and a nuisance that infests houses in large numbers (Koch and Galvan 2008).

Harmonia axyridis has been recorded in more than 50 countries of Asia, Europe, Africa, North and South America (EPPO 2014). Recently it was recorded in Moldova (Iazloveţchii and Sumencova 2013), European Russia (Zakharov et al. 2011; Orlova-Bienkowskaja 2013; Ukrainsky and Orlova-Bienkowskaja 2014), and the Caucasus (Ukrainsky and Shapovalov 2010; Ukrainsky 2013; Belyakova and Reznik 2013; Orlova-Bienkowskaja 2014). The invaded range of the species is well known (e.g. Brown et al. 2011), but the native range of the species in Asia has until now been poorly understood (Poutsma et al. 2008). Whilst it was mapped by Vorontsov and Blekhman (2001) and by Poutsma et al. (2008), both maps represent the species' range only partially. The first map is focused on localities from Russia, and the second on those from Japan and China. Some parts of the map by Poutsma et al. (2008) are inaccurate, because they are based on previously published verbal descriptions. Some parts of the native range are not presented in either map.

A map of the entire range of H. axyridis in Asia is necessary for several reasons. First, this information is the basis for ecological models and predictions of the future invasive distribution of H. axyridis (Poutsma et al. 2008; Bidinger et al. 2012). Second, knowledge of the native range is important for studying the ecology of the species and its relations with other species in the community. Third, natural enemies of the species co-occur in the native range, and these may be used to control H. axyridis in various ways (Kenis et al. 2008). Thus, we compiled a list of 432 localities of H. axyridis in Asia, made a detailed map of the native range and reconstructed the history of invasion of the species into southeastern Kazakhstan and Kyrgyzstan.

Material and methods

We examined approximately 6000 specimens of H. axyridis: material deposited in ZIN (Zoological Institute of Russian Academy of Sciences, St. Petersburg), ZMMU (Zoological Museum of Moscow State University), BC (collection of A.O. Bienkowski, Moscow), UC (collection of A.S. Ukrainsky, Moscow) and VC (collection of V.D. Vlasov, Yaroslavl) and specimens collected by C.E. Thomas and P.M.J. Brown. We mapped 260 localities indicated in labels of examined specimens, 157 other localities indicated in the literature (Münster 1923; Dobzhansky 1924; Tan 1946; Komai et al. 1950; Komai 1956; Sharova 1962; Savojskaja 1963; Chapin 1965; Bielawski 1965; Beresneva 1967; Bielawski 1968; Filatova 1970; Bielawski 1975; Merkl 1984; Kholin 1990; Vorontsov and Blekhman 2001; Zhao et al. 2002; Kuznetsov and Proshchalykin 2006; Kovář 2007; Hoàng 2007; Kuznetsov and Proshchalykin 2007; Poutsma et al. 2008; Tyumaseva and Guskova 2008; USDA-ROBO 2008; Sato et al. 2008; Krivets and Korovinskaya 2009; Tyumaseva and Zhdanova 2009; Blekhman 2008; Ren et al. 2009; Guoyue 2010; Li et al. 2010; Wang et al. 2011; GBIF 2013; EPPO 2014; Beetles (Coleoptera) and coleopterists 2014; Lombaert et al. 2014) and 15 localities by personal communication by S.V. Kolov and D.A. Milko. The programs ArcView GIS 3.2a and DIVA-GIS 7.5 were used for mapping.

Results and Discussion

Range

The range of H. axyridis in Asia is illustrated (Fig. 1). All mapped localities with grid references and sources of information are listed (Online Resource 1). H. axyridis occurs in the following regions: the south-east of West Siberia, the south of East Siberia, the south of the Russian Far East, the east of Kazakhstan, the north of Kyrgyzstan, Mongolia, China, North Korea, South Korea, Japan, and the north of Vietnam. The most western localities of the species in Asia are in the plain of West Siberia, although H. axyridis is rather rare there. We know of only two findings in that region: in the beginning of the 20th century in Tyukalinsk District (Omsk Region) (Fig. 1a) and in 2009 in Surgut (Khanty-Mansi Autonomous Okrug) (Fig. 1b). H. axyridis is a common species in the upper part of the Ob basin, in the mountains in the south-east of West Siberia, in the south of East Siberia and in the Russian Far East. The most northern known locality of H. axyridis in West Siberia is Surgut (Fig. 1b), in East Siberia is Kirensk (Fig. 1c), and in the Far East is the Shantar Islands (Fig. 1d). H. axyridis also occurs in the south of Sakhalin Island (Fig. 1e) and in the Southern Kurile Islands: Iturup (Fig. 1f) and Kunashir (Fig. 1g). H. axyridis is a very common species in Japan and the Korean peninsular: several thousand findings in these regions are listed in GBIF (2013). H. axyridis occurs in the mountains of Mongolia, but is not recorded from deserts in the south of the country or from adjacent arid regions of China. The east and south of China and the north of Vietnam are also parts of the range. The most southern known locality is the island of Hainan (Fig. 1h). The southern part of the range of H. axyridis in China needs further examination, because H. axyridis was confused with the sibling species Harmonia yedoensis (Takizawa, 1917) (Yu 2010). However, the presence of H. axyridis in southern China (Yunnan Province) (Fig. 1i), was proved by genetic analysis (Lombaert et al. 2014). Dobzhansky (1933) and Vorontsov and Blekhman (2001) showed that H. axyridis populations living west of Baikal Lake (in West Siberia and the western part of East Siberia) significantly differ in coloration and other morphological characters from those living east of Baikal (Fig. 1k). The same result was shown for genetic characters (Lombaert et al. 2011; Lombaert et al. 2014).

Incorrect and questionable records

The analysis of large number of locations has revealed that H. axyridis does not occur in the northern part of Khabarovsk Krai or in most parts of northern Kazakhstan. In the maps by Poutsma et al. (2008) and Bidinger et al. (2012) these regions were indicated on the basis of previously published records from whole administrative regions.

There is a single record of H. axyridis from the middle Ural River (Western Kazakhstan) (Tyumaseva 1981): specimens were collected by Z.I. Tyumaseva in 1976-1978 but neither the locality of collection nor the depository of specimens is indicated. There are no specimens of H. axyridis from West Kazakhstan in ZIN or ZMMU, though there are rich collections of other beetles from this region. Additionally, the region of the middle Ural River is a desert, and H. axyridis is not a species characteristic of arid territory. Therefore this record is doubtful and needs confirmation.

H. axyridis was recorded from Yakutia in the middle of the 19th century by Motschulsky (Dobzhansky 1926). We have seen one specimen with the label "Yakutsk Maak <...> 1854-1859" in ZIN. However, there is no evidence of further findings of H. axyridis in Yakutia (Averensky 2010). Yakutsk is much further north than all other localities of H. axyridis: the distance between it and the nearest locality is more than 1000 km, so it is unlikely that H. axyridis occurs in Yakutia.

The record of H. axyridis from Nepal or Himalaya (Korschefsky 1932) that is cited in some other sources (Iablokoff-Khnzorian 1982; Poorani 2002) is a mistake. This record refers to another species - Coelophora circumvelata (Mulsant, 1850). Korschefsky (1932) presumed that C. circumvelata could be a synonym of H. axyridis, but now C. circumvelata is regarded as a valid species (Poorani 2002). H. axyridis is not recorded for Nepal in the catalogue of Palaearctic beetles (Kovář 2007).

The record of H. axyridis from northern India (Sikkim, Darjeeling District) (Kovář 2007) is questionable. This species is not recorded from northern India in the checklist of Coccinellidae of the Indian subregion (Poorani 2002). Sikkim is 1400 km from the nearest known localities of H. axyridis.

H. axyridis was recorded in the Ryukyu Islands (Poutsma et al. 2008; GBIF 2013), but Noriyuki et al. (2012) report that it does not occur there. It is likely that the records relate to the congener H. yedoensis and not to H. axyridis. Similarly, several sources indicate the presence of H. axyridis in Taiwan (Poorani 2002; Kovář 2007; EPPO 2014), but Sasaji (1982) states that H. axyridis does not occur in Taiwan, and observations and collected specimens concern H. yedoensis. H. axyridis was released in Uzbekistan, in the Tashkent region in 1951-1952, but it failed to establish there (Voronin 1968).

Kazakhstan and Kyrgyzstan

Perhaps the most interesting aspect of H. axyridis in Asia concerns the pattern of its distribution in Kazakhstan and Kyrgyzstan (Fig. 1g and Fig. 2). This part of the range has been partially described by Orlova-Bienkowskaja (2015). In some recent studies the vicinity of Almaty is regarded as part of the native range of H. axyridis (Loiseau et al. 2009; Lombaert et al. 2011; Lombaert et al. 2014). However, this is incorrect. H. axyridis was not recorded in the south-east of Kazakhstan and Kyrgyzstan in the 19th century or in the first half of the 20th century (Savojskaja 1970, 1971; Ovchinnikov 1996). There are no specimens of H. axyridis from southeastern Kazakhstan and Kyrgyzstan collected before 1976 in the collections of ZIN and ZMMU, though there are many other beetle specimens collected from there in the first half of the 20th century.

The most western part of the native range is in the Altai mountains, situated in north-eastern Kazakhstan and West Siberia. In the collection of ZIN there are hundreds of specimens collected there in the 19th century and first half of the 20th century. The large Balkhash Desert is south of the most western part of the native range. The desert occupies about 600 km between the Altai mountains and the Ile Alatau mountains in south-eastern Kazakhstan. Localities and dates of findings indicate that the southerly dispersal of H. axyridis through this arid territory began in the second half of the 20th century (Fig. 2). In 1963 H. axyridis was first recorded south of its natural range in the floodplain of the Ayaguz River (Fig. 2, 1), surrounded by the desert (Savojskaja 1963). Savojskaja (1963) wrote that the finding of the Siberian species was very surprising and stated that the beetles could not disperse through the desert unaided.

In 1976 H. axyridis was found even further south, in the floodplain of the Aksu River (Fig. 2, 2) (Vorontsov and Blekhman 2001). Whilst Iablokoff-Khnzorian (1983) wrote that H. axyridis occurs in Semirechye, this does not add any information because the floodplain of Aksu is in Semirechye.

In later years dispersal to the south continued and by 2007 H. axyridis had become a common species in the city of Almaty and its vicinity (Fig. 2, 3) (Loiseau et al. 2009; Lombaert et al. 2011). We examined specimens of H. axyridis collected there in 2008. Now H. axyridis occurs even further south, in Kyrgyzstan (examined specimen from collection of D.V. Vlasov and personal communication by D.A. Milko).

In 1968-1970 attempts were made to introduce H. axyridis in the vicinity of Almaty, for the biological control of aphids (Savojskaja 1971). About 250,000 specimens from Primorsky Territory (Russian Far East) were released. However, the attempt failed: H. axyridis did not establish (Savojskaja 1983). No beetles were found for many years after the releases. Both morphological and genetic data strongly indicate that the H. axyridis occurring in the vicinity of Almaty now are not descendants of released beetles. First, the only colour form recorded in Kazakhstan is f. axyridis, which is characteristic of West Siberia, but does not occur in Primorsky Territory (Zakharov and Blekhman 2001). Second, according to genetic studies, the beetles from the vicinity of Almaty are related to West-Siberian populations and significantly differ from populations of Primorsky Territory (Lombaert et al. 2011; Lombaert et al. 2014).

H. axyridis dispersed to South-East Kazakhstan from the north, but how could the beetles cross 600 km of desert? Rivers of this region cross the desert from east to west and therefore cannot be the pathways of dispersal from north to south. It is very unlikely that the beetles could disperse through the desert by themselves and it appears that the dispersal must have been human-assisted. The vector of invasion is unknown, but it is hypothesized that the beetles spread along the Turkestan-Siberian Railway, which was constructed in 1931 (Small Soviet Encyclopedia 1959). Dates and localities of H. axyridis findings support this suggestion. The railway passes through the Balkhash Desert from the Altai mountains to Almaty and across the floodplains of the Ayaguz and Aksu rivers. The localities of the first findings of H. axyridis in these regions are situated along this railway in strict chronological sequence from north to the south. Additionally, the only known locality of H. axyridis in western China is in Xinjiang, very close to the China-Kazakhstan border and relatively close to the railway, which crosses the Turkestan-Siberian Railway (Poutsma et al. 2008). The date of this finding is not indicated.

The unintentional transport of H. axyridis via trains and other vehicles is one of the usual dispersal mechanisms of H. axyridis (Brown et al. 2011). For example, observations by Korotyaev (2013) indicate that the beetles, seeking overwintering sites, enter standing vehicles and can then potentially be transported anywhere. Thus we suggest that H. axyridis was probably unintentionally introduced to South-East Kazakhstan via trains. Since a single gravid H. axyridis female can lay hundreds of eggs and potentially establish a new population, this seemingly low propagule pressure may not be a hindrance to such dispersal.

Conclusion

Our study has revealed that the maps of the native range of H. axyridis used for ecological modelling and prediction of the future invasive range, by Poutsma et al. (2008) and Bidinger et al. (2012), need to be corrected and refined in some aspects. First, H. axyridis does not occur in the northern part of Khabarovsk Krai or in most parts of northern Kazakhstan. Second, Nepal and the Ryukyu Islands should not be regarded as parts of the native range, since the records from these regions are likely to refer to another species. Third, northern Vietnam and eastern Kazakhstan should be added to the map of the native range. Finally, the distribution of H. axyridis in Mongolia has been mapped for the first time.

Improving our knowledge of the native ranges of species is an important facet of ecology generally, and of invasion biology specifically. A better understanding of the ecological requirements of a species in its native range may assist both in modelling range expansion, and in the assessment of management options. The information presented here for H. axyridis is especially important because of the high status of this species: it is one of the best studied invasive animals and has been used as a model for understanding a range of invasion processes (Roy and Wajnberg 2008; Roy et al. 2012b). We recommend that similar data be compiled for other invasive species (and for those with a high propensity to become invasive). Such data may currently be available only in museum specimen information and local literature sources, but should be published for an international audience.

Acknowledgements

We would like to thank Sergej Vladimirovich Kolov (Al-Farabi Kazakh National University, Almaty, Kazakhstan), Dmitrij Viktorovich Vlasov (Yaroslavl State Historical-Architectural and Art Museum-Reserve, Yaroslavl, Russia) and Dmitrij Anatoljevich Milko (Institute for Biology and Pedology, National Academy of Sciences of Kyrgyzstan, Bishkek, Kyrgyzstan) for valuable information. The study was supported by Russian Foundation for Basic Research. One of the authors of this article A.S. Ukrainsky died suddenly June 22, 2014.

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Fig. 1 Localities of findings H. axyridis in Asia. Black dots - localities from which the specimens have been examined. Grey dots - localities indicated in the literature. a - the most western locality: Tyukalinsk District, b - the most northern locality in West Siberia: Surgut, c - the most northern locality in East Siberia: Kirensk, d - the most northen locality in the Far East: Shantar Islands, the most eastern localities: e - Sakhalin Island, f - Iturup Island, g - Kunashir Island, h - the most southern locality: Hainan Island, i - the most southern locality confirmed by genetic analysis (Lombaert et al 2014): Shilin, j - invasive occurrences outside the native range are circled, k - border between western and eastern groups of populations differing in coloration and genetic characters.

Fig. 2 Invasion of H. axyridis to southeastern Kazakhstan and Kyrgyzstan. Records of H. axyridis south of the native range: 1 - floodplain of the Ayaguz River (first record in 1963), 2 - floodplain of the Aksu River (first record in 1976), 3 - Almaty and its vicinity (first record in 2007), 4 - Kyrgyzstan (first record in 2009), 5 - Xinjiang (the date of record is not indicated).