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M.J. Orlova-Bienkowskaja. 2015. Cascading ecological effects... establishment... Agrilus planipennis...


М.Я. Орлова-Беньковская



M.J. Orlova-Bienkowskaja. 2015.
Cascading ecological effects caused by the establishment of the emerald ash borer Agrilus planipennis (Coleoptera: Buprestidae) in European Russia
[Каскадный экологический эффект, вызванный вселением ясеневой изумрудной узкотелой златки Agrilus planipennis (Coleoptera: Buprestidae) в европейскую часть России].
Eur. J. Entomol., 2015, 112 (4): 778-789.
doi: 10.14411/eje.2015.102
ISSN 1210-5759 (print), 1802-8829 (online)

Файл PDF: orlova-bienkowskaja_2015_cascading_effects_agrilus_planipennis.pdf


Материалы препринта статьи (опубликованы на этом сайте 28 мая 2015 г.)


Текст препринта - в файле формата MS Word Orlova-Bienkowskaja_cascad.doc

Перевод заголовка и резюме:

Каскадный экологический эффект, вызванный вселением ясеневой изумрудной узкотелой златки
Agrilus planipennis (Coleoptera: Buprestidae) в европейскую часть России (препринт)


Ясеневая изумрудная узкотелая златка Agrilus planipennis - один из самых вредоносных жуков-ксилофагов в Северной Америке и европейской части России. Ее ареал в европейской части России быстро расширяется. По-видомому вредитель будет скоро обнаружен и в других европейских странах. Цель данного исследования - проанализировать экологические последствия вселения вредителя в европейскую Россию и ответить на следующие вопросы:
(1) Какие другие ксилофильные жесткокрылые развиваются на ясенях, атакованных A. planipennis?;
(2) Насколько обычен паразитоид Spathius polonicus, развивающийся на златке, и насколько высок уровень паразитизма?;
(3) Повреждает ли златка местный, европейский вид ясень обыкновенный (Fraxinus excelsior)?
Обследование приблизительно 1000 деревьев Fraxinus pennsylvanica, поврежденных A. planipennis в 13 пунктах, показало, что на них обычны Hylesinus varius (Coleoptera: Curculionidae: Scolytinae), Tetrops starkii (Coleoptera: Cerambycidae) и Agrilus convexicollis (Coleoptera: Buprestidae). Spathius polonicus встречается часто и убивает около 50% личинок последнего возраста A. planipennis. На основе анализа 84 литературных источников, а также собственных сборов составлены карты ареалов T. starkii (205 пунктов находок), A. convexicollis (480 пунктов находок) и S. polonicus до и после вселения A. planipennis. Выдвинута гипотеза о том, что эти виды распространились в центр европейской России после вселения A. planipennis. Ясеневая изумрудная узкотелая златка повреждает не только пенсильванский ясень, но и местный ясень обыкновенный Fraxinus excelsior. Поэтому вредитель представляет опасность для широколиственных лесов европейской России и Европы в целом. Вселение ясеневой изумрудной узкотелой златки вызвало каскадные экологические эффекты, в том числе вспышку численности других ксилофильных жесткокрылых на деревьях, пораженных A. planipennis. Развитие этих жесткокрылых приводит к дальнейшему ухудшению состояния деревьев. С другой стороны, массовое размножение паразитоида S. polonicus снижает численность ясеневой изумрудной узкотелой златки и уменьшает негативные последствия ее вселения.



Cascading ecological effects caused by establishment of the emerald ash borer
Agrilus planipennis (Coleoptera: Buprestidae) in European Russia     (preprint)

Marina J. Orlova-Bienkowskaja

A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninskiy Prospect, Moscow 119071, Russia;

e-mail: marinaorlben@yandex.ru


Key words. alien species, biological invasion, common ash, EAB, Agrilus planipennis Tetrops starkii, Agrilus convexicollis, Spathius polonicus


Abstract. Emerald ash borer, Agrilus planipennis, is a destructive invasive forest pest in America and European Russia. The range in European Russia is expanding quickly, so the pest is likely to appear in other countries soon. The aim is to analyze the ecological consequences of establishment of this pest in European Russia and to address:
(1) What other xylophagous beetles develop on ashes affected by A. planipennis?;
(2) How common is the A. planipennis parasitoid Spathius polonicus and is the level of parasitism high?;
and (3) Is Fraxinus excelsior, an ash native to Europe, susceptible to A. planipennis?
Survey of approximately 1000 Fraxinus pennsylvanica trees damaged by A. planipennis in 13 localities has shown that Hylesinus varius (Coleoptera: Curculionidae: Scolytinae), Tetrops starkii (Coleoptera: Cerambycidae) and Agrilus convexicollis (Coleoptera: Buprestidae) are common on them. Spathius polonicus is frequently observed and causes mortality of about 50% of late instar A. planipennis. Maps of the distributions of T. starkii, A. convexicollis and S. polonicus before and after establishment of A. planipennis have been compiled. It is hypothesized that these species native to the West Palaearctic spread to central European Russia after A. planipennis establishment. The native European ash Fraxinus excelsior is susceptible to A. planipennis, heightening the threat posed by this pest. The establishment of A. planipennis has caused cascading ecological effects, such as outbreaks of other xylophagous beetles in A. planipennis-infested trees, which in turn increase stress on the ashes and worsen the situation. Propagation of S. polonicus likely reduces the effect of the A. planipennis outbreak.


INTRODUCTION

The invasion of alien insect species is known to affect the structure of ecosystems through cascading ecological effects (Kenis et al., 2009). In particular, the establishment of one invasive species sometimes makes the ecosystem more likely to be invaded by other alien species (Simberloff & Von Holle, 1999). The example of cascading ecological effects caused by the establishment of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), in European Russia is described in the present article.

Agrilus planipennis is the one of the most destructive forest pests in the world (Aukema et al., 2011). This beetle originates from East Asia: northeastern China, Korea, Japan, Taiwan and Russian Far East (Jendek, 1994; Wei et al., 2007). It was inadvertently introduced to North America in the 1990s (Siegert et al., 2014) and has destroyed tens of millions of ash trees there (Aukema et al., 2011). Agrilus planipennis was firstly collected in Europe in 2003 in Moscow (Izhevskii & Mozolevskaya, 2010). To date, more than 80% of ashes in Moscow have been destroyed by the pest and there are additional infestations in 11 regions of central European Russia (Orlova-Bienkowskaja, 2013, 2014a, 2014b; Baranchikov, 2013; Straw et al., 2013), but our understanding of the ecological impact of A. planipennis there is limited.

Agrilus planipennis in European Russia develops mainly on Fraxinus pennsylvanica Marsh., which was introduced from North America about 100 years ago. It is one of the most common trees in urban plantations. In particular, it comprises about 20% of trees in Moscow (Majorov et al., 2012; Vinogradova et al., 2010). There are interspecific differences in A. planipennis host preference (Wei et al., 2007; Anulewicz et al., 2008). In European Russia, nearly all recorded cases of A. planipennis infestation referred to F. pennsylvanica (Baranchikov et al., 2008), while there were few records of infestation on native Fraxinus excelsior L. (Majorov et al., 2012; Straw et al., 2013). It is important to know if F. excelsior is susceptible to A. planipennis, because F. excelsior is common and plays an important role in biodiversity of European forests (FRAXIGEN, 2005; Mitchell et al., 2014).

Fraxinus excelsior is rare in central European Russia, with only individual trees occurring in urban plantations. The broad-leaved forests with F. excelsior occur in the southern parts of European Russia, in the Kursk region in particular, where A. planipennis has not yet been detected. It has, however, been detected very close to broad-leaved forests in the Tula region (Straw et al., 2013; Orlova-Bienkowskaja, 2014a) though A. planipennis has not been collected nor do the F. excelsior trees exhibit signs or symptoms of infestation.

Fauna of insects encountered on Fraxinus in the center of European Russia, especially in Moscow region, is well-described (Nikitsky et al., 1996; Mozolevskaya et al., 2010). About 20 species of insects (Coleoptera, Lepidoptera, Hymenoptera and Diptera) are common on ashes. Hylesinus varius was the only species of xylophagous beetles known to develop on ashes in the Moscow region before the A. planipennis invasion. After the establishment of A. planipennis, two more species of xylophagous beetles have been recorded: Agrilus convexicollis Redtenbacher (Coleoptera: Buprestidae) (Nikitsky, 2009; Vlasov, 2010) and Tetrops starkii Chevrolat (Coleoptera: Cerambycidae) (Danilevsky, 2012). It has been hypothesized that the range of A. convexicollis, which develops on dry branches of ashes, has expanded as a result of ash canopy decline caused by A. planipennis (Orlova-Bienkowskaja & Volkovitsh, 2014), but the impact of A. planipennis on other xylophagous beetles has not been studied.

The first European parasitoid Spathius polonicus Niezabitowski (Hymenoptera: Braconidae: Doryctinae) was discovered recently (Orlova-Bienkowskaja & Belokobylskij, 2014), but information about its range, phenology and rate of parasitism is scarce.

The aim of this study is to analyze the ecological consequences of establishment of A. planipennis in central European Russia and to answer the questions: (1) What other xylophagous beetles are associated with ashes affected by A. planipennis?; (2) Is S. polonicus widely distributed in the invasive range of A. planipennis and is the level of parasitism high?; and (3) Is F. excelsior susceptible to A. planipennis?

Materials and Methods

574 larvae, pupae and adults of xylophagous beetles and parasitoids were collected from about 1000 trees of F. pennsylvanica severely damaged by A. planipennis in 13 localities of European Russia in 2013 and 2014 (Table 1). Parasitoids were collected from remains of A. planipennis larvae from under the bark in the lower part of stems up to 1.5 m. For this purpose, the lower 1.5 m of trunks of standing trees were debarked by chisel and hammer. Larvae and pupae of xylophagous beetles were collected from under the bark of branches and upper thin parts of stems and preserved in alcohol. Adults were collected from leaves, branches and stems. About 100 trees in Moscow region were regularly surveyed for adults twice a week from 15.05.2014 to 19.07.2014. Dates of additional surveys in other regions are indicated in Tables 3, 4 and 5. Sweep nets and sticky bands were used, but I found that the most effective way of collecting was collecting from leaves by hand. All specimens were examined under the microscope in laboratory. Collected specimens (adults, larvae and pupae) were deposited in the author's collection.

The ranges of T. starkii Chevrolat (Coleoptera: Cerambycidae), A. convexicollis Redtenbacher (Coleoptera: Buprestidae) and S. polonicus Niezabitowski (Hymenoptera: Braconidae: Doryctinae) before and after the establishment of A. planipennis are mapped. The information about findings of these insects have been compiled by examining 84 previously published literature sources and collection data from specimens deposited in Zoological Institute of the Russian Academy of Sciences, St. Petersburg (ZIN) and Moscow State Pedagogical University (MSPU). In addition, I mapped my observations of these insects in Moscow, Yaroslavl and Lipetsk regions in summer 2013 and 2014. Seventy-three localities of A. planipennis, 480 localities of A. convexicollis, 205 localities of T. starkii and 8 localities of S. polonicus are mapped. Maps of recent findings of T. starkii, A. convexicollis, and S. polonicus are compared with the map of the known A. planipennis distribution in European Russia. The program DIVA-GIS Version 7.5 was used to generate maps.

To determine if the native F. excelsior is susceptible to A. planipennis, I examined 37 F. excelsior trees in four cities with known A. planipennis infestations. The sample size was limited because F. excelsior is rare in the central European Russia.

Abbreviations used in figures: AZ - Azerbajan, AD - Adygea, AR - Armenia, BE - Belgium, BY - Belarus, CR - Crimea, CZ - Czech Republic, DA - Dagestan, IR - Iran, IT - Italy, K - Kaluga region, KA - Karachay-Cherkessia, KE - Kemerovo region, KR - Krasnodar territory, L - Lipetsk region, M - Moscow region, NL - Netherlands, O - Orel region, PL - Poland, R - Ryazan region, RO - Rostov region, S - Smolensk region, SE - Serbia, SL - Slovakia, SP - Spain, ST - Stavropol territory, SZ - Switzerland, TA - Tambov region, TD - Tadjikistan, TU - Tula region, TR - Turkmenistan, TVн - Tver region, UK - Ukraine, UZ - Uzbekistan, VL - Vladimir region, VOL - Volgograd region, VOR - Voronezh region, Y - Yaroslavl region.


Results

What other xylophagous beetles develop on ashes affected by A. planipennis?

The survey of ashes affected by A. planipennis revealed that three species of xylophagous beetles are common: T. starkii, A. convexicollis and H. varius. Tetrops starkii is widely distributed in the Western Palaearctic, from Great Britain in the west to Azerbaijan in the east, and from Sweden in the north to Sicily in the south (Table 2, Fig. 1). In European Russia, it has been previously recorded only in the south: Krasnodar region, Rostov region, Voronezh region and Republic of Crimea. In central European Russia, however, it was first recorded only a few years ago, namely in Moscow region in 2012 (Danilevsky, 2012), and in Yaroslavl in 2008 (D. Vlasov, personal communication), so the known range of T. starkii has recently expanded by 700 km to the north. I collected T. starkii in three localities of the Moscow region including Zelenograd, where it has become a common species (Table 3, Fig. 1). In all cases, T. starkii were collected on ashes severely damaged by A. planipennis.

Tetrops starkii is known to feed on F. excelsior (Starzyk & Lessaer, 1978), F. ornus L. (Georgiev et al., 2005) and F. angustifolia Vahl (Bellavista et al., 2009). In all examined localities of central European Russia, adults of T. starkii were collected on F. pennsylvanica. In addition, 18 pupae of T. starkii were collected from the dry branches of F. pennsylvanica, which is a new host record for T. starkii.

In Moscow region, adult T. starkii beetles were collected from late May to mid July (Table 3). Adults are active in daytime and occur on leaves both in sunny and cloudy weather and even when it is rainy. Live hibernating T. starkii pupae were collected in winter and early spring in dry branches of F. pennsylvanica. It is known that in native range T. starkii often occurs on the same trees with A. convexicollis (Starzyk & Lessaer, 1978). In the center of European Russia, these species also coexist on F. pennsylvanica damaged by A. planipennis.

The range of A. convexicollis has been recently described in detail from the examination of 29 museum specimens and 48 literature sources (Orlova-Bienkowskaja & Volkovitsh, 2014). This species occurs in many European and Mediterranean countries, from Spain to Azerbaijan. In European Russia, it was previously recorded only in the south (Adygea, Dagestan, Karachay-Cherkessia, Krasnodar territory, Rostov region, Stavropol territory, Volgograd region and Voronezh region). Before 2007 it was not recorded in central European Russia, but since 2007 specimens of A. convexicollis have been collected in 9 central European Russia localities in Moscow region, Lipetsk region and Yaroslavl region (Fig. 2, Table 4), effectively expanding the northern border of the previously known range by approximately 665 km. In all cases but one, A. convexicollis were collected on ashes with signs of A. planipennis infestation.

In western Europe, A. convexicollis develops mainly in recently dead shoots and branches of ash trees: F. excelsior, F. ornus and F. oxyphylla as well as on some other plants of the family Oleaceae (Brechtel & Kostenbader, 2002). Recently, F. pennsylvanica has been recorded as a host plant (Orlova-Bienkowskaja & Volkovitsh, 2014). All specimens of A. convexicollis in central European Russia were collected on F. pennsylvanica. Fifteen larvae were collected from under the bark of the upper parts of the stems of F. pennsylvanica. In addition, one adult beetle that died in its emergence hole was found. The flying period of A. convexicollis lasts from early June to mid July (Table 4).

Hylesinus varius is a native pest of ash (Stark, 1952). Since 2002, the outbreak of H. varius has been recorded (Izhevskii & Mozolevskaya, 2010). In this study, larval galleries, adults and larvae of H. varius were observed in stems and branches of F. pennsylvanica in seven localities of Moscow region. The percentage of trees damaged by H. varius is estimated to be 10 to 60%. The flying period of adults is in May. New adults occur in the bark from the middle of August to the end of April. Hylesinus varius occurs mainly in the same trees as A. planipennis, but there are also occasionally individual trees severely damaged or even killed by H. varius without sings of infestation by A. planipennis. The portion of such trees in Zelenograd is about 5%.

Is parasitoid of the emerald ash borer Spathius polonicus common and is the level of parasitism high?

Spathius polonicus is an ectoparasitoid of buprestid larvae (Belokobylskij, 2003). It has been recently discovered that it can develop on A. planipennis (Orlova-Bienkowskaja & Belokobylskij, 2014). Spathius polonicus is a widely distributed Western Palaearctic species (Fig. 3). It occurs in Spain, Netherlands, Switzerland, Italy, Poland, Czech Republic, Slovakia, Serbia, Belarus, Ukraine, Russia, Armenia, Azerbaijan, Turkmenistan, Uzbekistan, Tadjikistan, Iran (Belokobylskij, 2003) and Belgium (Belgian Species List, 2014). It was not recorded in the center of European Russia before 2013. The only previously known locality in European Russia is in the southeastern part: in Volgograd region (Belokobylskij, 1989). In 2013-2014, I found S. polonicus at eight localities in Moscow region (Table 5, Fig. 3). The distance between the two extreme localities is about 78 km. So S. polonicus is common and rather widely distributed in the region of the outbreak of A. planipennis.

I have collected 129 specimens (adults in cocoons, larvae and pupae) of S. polonicus associated with late instar A. planipennis under the bark of stems. I found remains of 56 A. planipennis larvae killed by S. polonicus and 51 live late instars larvae. Therefore, the level of parasitism can be estimated by about 50%. Remains of A. planipennis larva killed by S. polonicus typically consist of head capsule, prothorax and a pair of urogomphi connected with thin "thread" (remains of the body) (Fig. 4). Sometimes the dead A. planipennis larvae found with cocoons of S. polonicus were not completely consumed. Up to six specimens of S. polonicus develop on one larva of A. planipennis. They can be on different stages. Sometimes larvae, pupae and adults in cocoons occur simultaneously on the same A. planipennis larva. Cocoons are built close to each other. In winter, hibernating S. polonicus pupae and larvae in cocoons were collected from under the bark (Table 5). Adult S. polonicus were captured on leaves in June-July.

What other insects are connected with F. pennsylvanica affected by A. planipennis?

Adults of Coeloides melanotus Wesmael (Braconinae) are very common on leaves of F. pennsylvanica in Moscow region. Seven adults of this species were reared from pieces of dry branches of F. pennsylvanica collected 16 April 2014. There were larval galleries of T. starkii and H. varius in these branches. It is known that C. melanotus can develop on H. varius (Elton, 1966). Eight larvae of A. convexicollis were killed by unidentified braconid parasitoids. Six pupae and 7 larvae of these parasitoids were found. On 19 July.2014 one pupa of unknown hymenopteran parasitoid was found within the cocoon of S. polonicus. Some insects, in particular Anthonomus pomorum L. (Curculionidae), use the galleries of A. planipennis or space under loose bark of F. pennsylvanica as a shelter. Other species use the larval galleries as a breeding site. For example, the wasp Passoloecus corniger Shuckard (Hymenoptera: Sphecidae) makes nests in larval galleries of A. planipennis in stems of F. pennsylvanica, and the smaller wasp Passoloecus brevilabris Wolf (Hymenoptera: Sphecidae) make nests in larval galleries of A. convexicollis in dry branches.

Is native European ash species Fraxinus excelsior susceptible to A. planipennis?

The survey of 37 trees of landscaped ash F. excelsior in four cities occupied by A. planipennis has shown that 31 of them have emergence holes of A. planipennis (Table 6). All trees with signs of A. planipennis infestation are severely damaged. Many branches and sometimes the upper parts of stems are dry. The larvae of A. planipennis were collected from under the bark of F. excelsior.

Discussion

Invasive plants which change character of ecosystems are termed transformers (Richardson et al., 2000). Agrilus planipennis is an example of transformer species of insects. It significantly changes the community connected with F. pennsylvanica in central European Russia. The scheme of ecological effects connected with establishment of A. planipennis is shown in Fig. 5.

It is known that A. planipennis thrives on F. pennsylvanica (Wei et al., 2007; Anulewicz et al., 2008) and readily colonizes it, causing an outbreak. Outbreaks have occurred in North America where F. pennsylvanica is native and A. planipennis is non-native (Aukema et al., 2011), in China where F. pennsylvanica is non-native and A. planipennis is native (Wei et al., 2007), and in European Russia where both species are non-native (Volkovitsh & Mozolevskaya, 2014). In central European Russia, the native F. excelsior is rare (Gubanov et al., 1992), but mass cultivation of North American F. pennsylvanica created a rich food supply for A. planipennis. It was one of the main factors which predetermined the establishment and quick propagation of this invasive pest. Only few cases of damage of F. excelsior by A. planipennis were known before 2012. It was a hope that F. excelsior might be less susceptible to the pest (Baranchikov et al., 2008; Izhevskii & Mozolevskaya, 2010) but unfortunately it is not so. Many cases of infestation and severe damage of F. excelsior are known (Majorov et al., 2012; Baranchikov et al., 2014 and present study). Fraxinus excelsior is common in the south of European Russia, in the Caucasus, and in central and western Europe. It plays an important role in biodiversity of European forests (Mitchell et al., 2014). Now it is known to be susceptible to A. planipennis, so the ecological consequences of establishment of A. planipennis in Europe could be tremendous.

In the Far East, A. planipennis often affect trees together with Hylesinus chlodkovskyi Berger (Yurchenko et al., 2007). In European Russia, it often affects trees together with the native pest of the same genus: H. varius. The establishment of A. planipennis is accompanied by the outbreak of H. varius (Izhevskii & Mozolevskaya, 2010). This outbreak was recorded since 2002, i.e. before the first specimen of A. planipennis was found (Izhevskii, 2007). I suspect that H. varius began to propagate because A. planipennis weakened the ashes, but it is also possible that establishment of A. planipennis was facilitated by the outbreak of H. varius. It is known that native and alien xylophagous insect species can "help" each other by weakening trees (Kenis et al., 2009). The outbreak of H. varius worsens the situation with ashes and can potentially affect Syringa spp. and other host plants of this species (Stark, 1952).

Examination of ranges and habitats of T. starkii and A. convexicolis has led me to conclude that these West-Palaearctic xylophagous beetles are alien for central European Russia. First, they were not recorded there before the establishment of A. planipennis, but were discovered almost simultaneously after establishment of A. planipennis. Second, they occur only on ashes damaged by A. planipennis. Third, they occur only in developed communities which is typical of newly established alien beetles (Beenen & Roques, 2010). In Western Europe, T. starkii and A. convexicolis develop on dry branches of ashes (Starzyk & Lessaer, 1978; Brechtel & Kostenbader, 2002). I suspect that they spread to the region of European Russia occupied by A. planipennis because of mass weakening of ashes.

Could A. convexicollis and T. starkii have occurred, but remain unnoticed, in central European Russia prior to the arrival of A. planipennis? It is unlikely, though impossible to prove the absence of any insect species in any territory. However, the fauna of xylophagous beetles in Moscow region has historically been intensively surveyed and A. convexicollis and T. starkii were not recorded (Nikitsky et al., 1996). Also, there are no specimens of A. convexicollis and T. starkii collected in central European Russia in rich collections of Zoological Institute (Russian Academy of Sciences), Moscow State Pedagogical University and Zoological Museum of Moscow State University though there are many other specimens from the genera Agrilus and Tetrops and many specimens of beetles collected from ashes, such as H. varius. Additionally, A. convexicollis and T. starkii are easy to notice because they are neither microscopic nor nocturnal. They occur on the leaves of ashes in cities where many professional and amateur entomologists live and where higher and secondary specialized institutions for forest science are located. Finally, A. convexicollis and T. starkii have been detected in hundreds of localities in West and Central Europe before 2007, but have not been detected in the center of European Russia. It is unlikely that they occurred but remained unnoticed in Moscow region since the fauna of beetles of Moscow region is studied as thoroughly as the fauna of Central Europe.

Perhaps more insects were found on ash and their known distribution ranges expanded after A. planipennis detection because people were looking harder and in more places? That is not the case. First, T. starkii and A. convexicollis were found in Yaroslavl region before the data on detection of A. planipennis in central Russia were published (D. Vlasov, personal communication; Vlasov, 2010). Second, the researchers who collected A. convexicollis and T. starkii before 2013 (D. Vlasov, E. Shankhiza, M. Danilevsky) were not engaged in survey of ashes connected with A. planipennis establishment.

Fraxinus pennsylvanica is very common in the center of European Russia, so there is no reason to think that there were less suitable hosts in the center of European Russia than in Europe. In spite of this, in the 20th century, T. starkii and A. convexicollis were found in several hundreds localities in Central and Western Europe but were not found in Moscow region and other regions of Central Russia. There are no reasons to believe that these species were more difficult to find in Moscow region than in Central Europe, so I believe that the absence of these species in collections and lists of fauna is a reliable evidence of the absence of these species before the A. planipennis invasion.

What factors could facilitate expansion of A. convexicollis and T. starkii to central European Russia? First, it is well known that many insects in Europe are now spreading northward because of warming climates (Beenen & Roques, 2010). Second, the introduction of F. pennsylvanica has created the rich food supply for the pest. The main factor is probably the weakening of ashes by A. planipennis because the northern border of the ranges shifts northwards only in the region occupied by A. planipennis. Agrilus convexicollis and T. starkii expanded their known ranges northward by more than 600 km and just in the area recently invaded by A. planipennis. It is unlikely that it is just a coincidence. Larvae of xylophagous beetles can develop faster if the tree is stressed (Tluczek et al., 2011). In stressed trees, they can complete development even if the warm period is short. Therefore, if the shorter warm period was the factor limiting the northern extent of the ranges of T. starkii and A. convexicollis, the appearance of stressed ashes could facilitate the expansion of these species to the north.

It is quite possible that T. starkii and A. convexicollis could weaken F. pennsylvanica and therefore facilitate further propagation of A. planipennis. If this hypothesis is confirmed, the interactions between A. planipennis, A. convexicollis and T. starkii are an example of invasional meltdown, i.e. the process by which a group of alien species facilitate one anotherТs invasion (Simberloff & Von Holle, 1999). Appearance of T. starkii and A. convexicollis, as well as the outbreak of the native pest H. varius, could affect landscape F. excelsior in European Russia. Agrilus convexicollis and T. starkii have been shown to feed on North American F. pennsylvanica, therefore they could potentially become established wherever F. pennsylvanica is present.

Parasitoid S. polonicus could be also alien species which spread to central European Russia shortly after establishment of A. planipennis. It is rather widely distributed in the West Palaearctic, but was not recorded in central European Russia before A. planipennis establishment. It is unlikely that S. polonicus was introduced with A. planipennis because S. polonicus has not been detected in native range of A. planipennis, though less is generally known about the ranges of Braconidae compared to the ranges of many beetles. As a result, it cannot be excluded that S. polonicus may have occurred but remained unnoticed in central European Russia before its recent discovery.

I found S. polonicus under the bark in all localities where I collected larvae of A. planipennis. Obviously this parasitoid has become common in the region occupied by A. planipennis. The level of parasitism by S. polonicus is rather high, so the parasitoid could be an effective biological control agent if propagated and released at A. planipennis infestations, though more precise studies are necessary to evaluate this hypothesis. Spathius polonicus may be suitable for biocontrol of A. planipennis both in Europe and North America, because it is a native to the temperate climate zone. The potential of this parasitoid for biological control needs to be investigated further.

The resulting cascade of ecological effects following A. planipennis invasion may also affect other species, because T. starkii, A. convexicollis and S. polonicus are connected with other insect and plant species in their native ranges. In particular, A. convexicollis feeds on different trees and shrubs of the family Oleaceae (Brechtel & Kostenbader, 2002) and larvae of S. polonicus are known to develop on larvae of many buprestids (Belokobylskij, 2003). In addition, parasitoids have been found both on A. convexicollis and T. starkii. Cascading ecological effects concern not only insects included in food chains connected with ashes,but may affect some insects that use the space under loose bark as a shelter or breeding site.

Cascading direct and indirect effects of the establishment of A. planipennis is described in North America (Smith, 2006; Gandhi & Herms, 2010; Herms & McCullough, 2014). The propagation of A. planipennis causes formation of canopy gaps, changes the woody debris dynamics and biogeochemical cycling, influencing both native and alien plants. In particular, A. planipennis can facilitate the establishment and spread of invasive plants by creating canopy gaps that increase light availability while relaxing interspecific competition for space and resources, thereby igniting an ССinvasional meltdownТТ (Simberloff & Von Holle, 1999).

It is known that invasion of one species could facilitate the invasion of related species (for example, parasites) from the same region (Kenis et al., 2009), but the case considered in the present article is different. The community connected with F. pennsylvanica affected by A. planipennis is "international". The host plant F. pennsylvanica originates from North America, while A. planipennis is from East Asia, T. starkii, A. convexicollis and probably S. polonicus are from European regions west and south to the center of European Russia, and H. varius and other insects are aborigenous. Ecological interactions between the members of this community are anthropogenic, because these are interactions between species that do not occur together in the wild. This case illustrates that the invasion of one alien species could indirectly affect the ranges of other species through cascading ecological effects. In other words, humanity inadvertently creates new complexes of ecologically related species and these complexes have unknown properties.

Acknowledgements. I thank Mikhail Danilevsky (A.N. Severtsov Institute of Ecology and Evolution, Moscow), Aleksander Miroshnikov (Russian Entomological Society, Krasnodar), Dmitrij Vlasov (Yaroslavl State Historical-Architectural and Art Museum-Reserve, Yaroslavl), Vitaly Alekseev (Kaliningrad State Technical University, Kaliningrad) and Georgi Georgiev (Forest Research Institute, Sofia) for valuable information, Sergey Belokobylskij (Zoological Institute, St. Petersburg) for identification of Braconidae, Kirill Makarov (Moscow State Pedagogical University, Moscow) and Mark Volkovitsh (Zoological Institute, St. Petersburg) for the possibility to study specimens from collections deposited in the respective institutes, to Valery Maslyakov (All-Russian Research Institute of Medicinal and Aromatic Plants) for the possibility collect insects in the botanical garden of this institute to Nathan W. Siegert (USDA Forest Service) for linguistic corrections. The study was supported by Russian Foundation for Basic Research (project №15-29-02550).


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Table 1. Sample sites.

Collection localities

Coordinates

Approximatenumber of trees surveyed for adults

Approximatenumber of trees dissected to find larvae and pupae

Number of collected A. planipennis

Number of collected specimens of other species

Zelenograd, 11th district

56.00 N, 37.18 E

300

20

71

179

Zelenograd, 16th district

55.97 N, 37.16 E

100

10

36

29

Zelenograd, Georgievsky prospect

55.98 N, 37.21 E

10

10

1

5

Zelenograd, Panfilova street

55.98 N, 37.17 N

50

10

35

38

Monino

55.84 N, 38.20 E

100

0

1

3

Uzunovo

54.55 N, 38.62 E

50

0

0

3

Yaroslavl

57.63 N, 39.87 E

100

0

1

4

Moscow, VILAR

55.56 N, 37.59 E

100

20

16

13

Staraya Kupavna

55.81 N, 38.18 E

100

10

5

9

Gryazi

52.49 N, 39.93 E

20

0

0

1

Planernaya

55.92 N, 37.38 E

0

50

75

23

Povarovka

56.07 N, 37.07 E

20

10

2

9

Solnechnogorsk

56.19 N, 36.98 E

20

5

3

12

Total number

 

970

145

246

328


Table 2. Localities of Tetrops starkii in its native range.

Region*

Number of mapped localities

Years of collection

Sources of information

Austria

23

1888-2001

Horion, 1974; Holzschuh, 1981; Geiser, 2001, GBIF, 2013

Azerbaijan

1

pre 1928

Danilevsky, 2014

Belarus

0

pre 1997

Danilevsky, 2014

Belgium

3

2012

Drumont et al., 2012

Bosnia Herzegovina

0

pre 2010

Löbl & Smetana, 2010

Bulgaria

6

pre 1931-2005

Horion, 1974; Holzschuh, 1981; Migliaccio et al., 2007; Georgiev et al., 2005; personal communication by G. Georgiev

Croatia

0

pre 2010

Löbl & Smetana, 2010

Czech Republic

8

pre 1929-2007

Roubal, 1929; Holzschuh, 1981; Hoskovec, 2007; Coleoptera Poloniae, 2014 and examined specimens from ZIN**

Denmark

5

1913-1989

Danmarks Fugle og Natur, 2014; Fagdatacenter for Biodiversitet og Terrestrisk Natur, 2007

France

40

pre 1958-2002

Horion, 1974; Schmeltz, 2002; Cocquempot, 2011

Germany

1

pre 1974

Horion, 1974

Great Britain

5

1991-1997

Welch, 2003; GBIF, 2013

Greece

0

pre 2010

Löbl & Smetana, 2010

Hungary

10

pre 1971-2003

Lőkkös, 2010

Italy

7

pre 1927-2009

Roubal, 1929; Horion, 1974; Bellavista et al., 2009; Sama & Rapuzzi, 2011; Hellrigl et al., 2012; GBIF, 2013

Ireland

0

pre 2010

Löbl & Smetana, 2010

Latvia

0

pre 2010

Löbl & Smetana, 2010

Macedonia

1

1971

Holzschuh, 1981

Moldova

1

pre 1927

Roubal, 1929

Netherlands

7

1968-2013

Horion, 1974; Waarneming.nl, 2014

Norway

4

1934-2008

Horion, 1974; GBIF, 2013

Poland

11

pre 1928-2005

Starzyk & Lessaer, 1978; GBIF, 2013; Coleoptera Poloniae, 2014

Romania

5

1895-1965

Holzschuh, 1981; Starzyk & Lessaer, 1978; Serafim, 2010

Russia, Kaliningrad region

1

2014

Personal communication by V. Alekseev

Russia, Krasnodar region

2

1986

Nikitsky et al., 2008; Danilevsky, 2012 and examined specimens from ZIN

Russia, Rostov region

1

1951

Examined specimens from MSPU***

Russia, Voronezh region

1

1960

Examined specimens from MSPU

Russia, Republic of Crimea

1

1910

Examined specimens from ZIN

Serbia

2

pre 1974-2009

Starzyk & Lessaer 1978; Gnjatović & Žikić 2010

Slovakia

5

pre 1929-1991

Roubal, 1929; Holzschuh, 1981; Lamiaires du Monde, 2014 & examined specimens from ZIN

Slovenia

9

1926-1987

Brelih et al., 2006

Spain

1

2002

Sobrino & Sánchez, 2003

Sweden

21

1947-2013

GBIF, 2013

Switzerland

19

1951-2012

CSCF-karch, 2013

Ukraine

4

1911

Personal communication by A. Miroshnikov and examined specimens from ZIN

* Besides these regions T. starkii was recorded in Central Georgia (Starzyk & Lessaer, 1978). But Danilevsky (2014) proved that this record referred to another species. Tamutis et al. (2011) presume, that T. starkii could occur in Lithuania. But there are no documented records.

** ZIN - Zoological Institute of the Russian Academy of Sciences.

*** MSPU - Moscow State Pedagogical University.


Table 3. Localities where Tetrops starkii has been recently found in central European Russia.

Collection localities

Dates

Number of specimens

Source of information

Yaroslavl

21.6.2008, 18.6.2014

4 adults

One examined specimen collected by D. Vlasov and personal communication by D. Vlasov

Bykovo

6.2012

31 adults

Danilevsky (2012)

2013

more than 100 adults

Personal communication by M. Danilevsky

Zelenograd

1.6. -3.7.2013 and 26.5-12.7.2014

57 adults

Specimens collected by the author

19.11.2013, 27.3.2014, 16.04.2014

18 pupae

Monino

21.6.2013

1 adult

Uzunovo

29.6.2013

2 adults


Table 4. Localities where Agrilus convexicollis has been recently found in central European Russia.

Collection localities

Dates

Number of specimens

Was the tree damaged by A. planipennis?

Source of information

Yaroslavl

2007 and 30.6.2013

4 adults

Yes

Vlasov (2010) and specimens collected by the author

Rostov (Yaroslavl Region)

2007

1 adult

Personal communication by D. Vlasov

Manikhino

15.6.2008

1 adult

Yes

Nikitsky (2009)

Zelenograd

1.6.2013-5.7.2013, 2.6-16.7.2014

74 adults, 12 larvae

Yes

Specimens collected by the author

Moscow, Botanical garden of VILAR

19.6.2014

3 adults, 3 larvae

Yes

Staraya Kupavna

21.6.2013

9 adults

Yes

Monino

21.6.2013

2 adults

Yes

Uzunovo

29.6.2013

1 adult

Yes

Gryazi

27.6.2013

1 adult

No

Total number

95 adults, 15 larvae


Table 5. Specimens of S. polonicus collected with the remains of larvae of A. planipennis from under the bark of F. pennsylvanica in Moscow region.

Locality

Date of collection

Collected specimen of S. polonicus

Number of A. planipennis last instar larvae killed by S. polonicus

Number of alive A. planipennis last instar larvae and prepupae

Zelenograd, 11th district

1-2.10.2013

12 larvae in cocoons, 1 pupa

2

8

29.10.2013

4 larvae in cocoons, 1 pupa

1

1

Zelenograd, 16th district

30.10.2013

20 larvae in cocoons

3

4

11.3.2014

9 adults in cocoons

1

2

Zelenograd, Georgievsky prospect

4.5.2014

2 adults in cocoons, 2 larvae in cocoons, 1 pupa

3

1

Zelenograd, Panfilova street

4.6.2014

8 adults in cocoons, 7 larvae

5

6

19.7.2014

9 empty cocoons, 5 adults in cocoons, 2 larvae in cocoons, 4 pupae

13

9

16.6.2014

3 empty cocoons

1

3

Planernaya

9.1.2014

5 larvae in cocoons

1

4

10.3.2014

1 adult in cocoon, 7 larvae in cocoons

2

3

28.4.2014

10 adults in cocoons

12

0

Povarovka

2.5.2014

3 adults in cocoons, 6 larvae in cocoons

6

1

Moscow, Botanical garden of VILAR

19.6.2014

7 adults reared from cocoons

2

9

Solnechnogorsk

21.7.2014

10 adults in cocoons, 2 larvae

4

0

Total number

-

55 adults, 7 pupae, 67 larvae

56

51


Table 6. Results of examinations of trees of Fraxinus excelsior in European Russia.

Localities

Dates

Number of examined trees

Number of trees with emergence holes

Moscow, The Tsytsin Main Moscow Botanical Garden

20.7.2014

3

3

Moscow, Botanical garden of VILAR

19.6.2014

16

16

Voronezh

12.6.2013

1

1

Tula

5.6.2013

3

3

Orel

4-5.6.2013

14

8

Total number

_

37

31


Illustrations:

Fig. 1. The known ranges of Tetrops starkii (Coleoptera: Cerambycidae) and Agrilus planipennis (Coleoptera: Buprestidae) in Europe as of 2014. Left map: the whole ranges, right map: the ranges in the center of European Russia. 1 - findings of T. starkii within native range. 2 - localities where T. starkii was found outside its native range (all findings in 2008-2014). 3 - localities, where A. planipennis was found. Native range of T. starkii is shaded in the left map and invasive range of A. planipennis is shaded in the right map. Sources of information are listed in Tables 1 and 2. The localities of A. planipennis in Figs. 1-3 are given after Orlova-Bienkowskaja (2014) with some new localities. Abbreviations: see in "Materials and methods".


Fig. 2. The known range of Agrilus convexicollis and A. planipennis (Coleoptera: Buprestidae) in Europe as of 2014. Left map represents the whole ranges, right map represents the ranges in the center of European Russia. 1 - findings of A. convexicollis within native range. 2 - localities where A. convexicollis was found outside its native range (all findings in 2007-2014). 3 - localities, where A. planipennis was found. Native range of A. convexicollis is shaded in the left map and invasive range of A. planipennis is shaded in the right map. Abbreviations: see Fig. 1. The range of A. convexicollis is given after Orlova-Bienkowskaja & Volkovitsh (2014) with additional localities (see Table 4).


Fig. 3. The known range of Spathius polonicus (Hymenoptera: Braconidae) and invasive range of A. planipennis (Coleoptera: Buprestidae) in Europe as of 2014. Left map represents the whole ranges, right map represents the ranges in the center of European Russia. 1 - findings of S. polonicus discovered in 2013-2014. 2 - localities, where A. planipennis was found. Countries and regions where S. polonicus was found are shaded in the left map and invasive range of A. planipennis is shaded in the right map. Sources of information are listed in Table 5.


Fig. 4. Remains of larva of Agrilus planipennis with cocoons of ectoparasitoid Spathius polonicus. 1 - head capsule and prothorax, 2 - remains of cuticle with spiracles, 3 - cocoons of the ectoparasitoid, 4 - urogomphi.


Fig. 5. Cascading ecological effects caused by establishment of Agrilus planipennis.