РАСТЕНИЕВЪДНИ НАУКИ, ГОД. LI, No. 6 PLANT SCIENCE, VOL. LI, No. 6 София. 2014. Sofia

BIOLOGICAL INVASION IN TERRESTRIAL ECOSYSTEMS OF SUBTROPICS OF RUSSIAN FEDERATION

NATALIA KARPUN*, YEVGENIA IGNATOVA, YELENA MIKHAILOVA The State Research Institution All-Russian Scientific and Research Institute of Floriculture and Subtropical Crops of the Russian Academy of Agricultural Sciences, Sochi, Russia *E-mail: [email protected]

Abstract In recent decades, as a result of active uncontrolled of ornamental woody plants import from abroad, a threat that new pests and diseases might penetrate to Russian Black Sea coast appeared, which led to the extent of an environmental problem. The given paper provides information about the new species detected on fruit, flower and ornamental crops in Sochi (Russia) in the period from 1995 to 2013, which has not been earlier recorded in the region. Among the pests Plurivorous species of Ceratitis capitata Wied. mostly represents danger for fruit plantations and Frankliniella occidentalis Perg. – for flower crops. In 2013, the massive shrinkage of boxwood was noted, which was caused by damage from caterpillars Cydalima perspectalis Walker. This species appeared in the region presumably in 2011 – 2012. The five following species of powdery mildews fungi were recorded for the first time in the study area: Erysiphe azalea (U. Braun) U. Braun & S. Takam. on leaves of Rhododendron luteum Sweet, E. betae (Vaňha) Weltzien – on leaves of Hydrangea macrophylla Ser., E. syringae, Schwein. – on leaves of Syringa vulgaris L., E. tortilis (Wallr.) Link – on leaves of Cornus sp. Golovinomyces sparsus (A. Braun) V. P. Heluta – on leaves of Viburnum opulus L. Because of the emergence of new pests and diseases there is a tendency of expansion of the range of host plants for existing species in the region. Key words: invasion, pests, pathogens, Cydalima perspectalis, terrestrial ecosystems, Black Sea coast of Russia

Carrying out continuous monitoring of specific sive species act as biological contaminants (Igevskii, composition of harmful species in gardens, urban 1995; 2002). Our task was to determine what inva- and natural plantings is one of the main objectives sive species have appeared on the Black Sea coast in plant protection. Early detection of a new object of Russia (Sochi area) for recent years, and to assess enables fast development and application of control the degree of danger from the new pests and patho- measures. This is especially actual for the humid Rus- genes for terrestrial ecosystems. sian subtropics, where favorable climatic conditions are conducive to the development of fruit, subtropical MATERIAL AND METHODS and ornamental woody plants, and mass distribution The research was conducted in fruit, ornamental of pests and pathogens. Analyzing changes in terres- and natural plantings of Sochi from 1995 till 2013. The trial ecosystems due to various exogenous impacts, species diversity was determined applying the meth- the leading ecologists allocated 4 classes of dynami- ods of route investigation with the collection of herbar- cal phenomena that characterize the degree of trans- ium samples and further stationary observations. The formation in ecosystems (Kashmilov, 1974; Budako, quantity and development dynamics were recorded, 1984; Zavadskii, 1984; Kolchinskii, 1977), including using stationary observations on the model plots of loss of biodiversity, replacement of one dominant fruit, ornamental and natural plantings throughout the consument species in ecosystems by others similar in growing period (every two weeks). Model plots were environmental and physiological characteristics; bio- located equally in all administrative districts of the city logical invasions lead to expansion of species ranges, of Sochi. For determining the extent and severity of which is one of the major threats to biodiversity, and the species, generally accepted techniques were used are classified as “biological pollution of ecosystems” (Kosova, Polyakova, 1958; Smolyakova et al., 1999). (Pavlushin, Vilkova and Suhoruchenko, 2013). In re- The population density of the box tree moth on cent decades, as a result of active uncontrolled import boxwood hedges was determined as follows: mea- of ornamental woody plants, a threat that new species suring plate was placed on the upper surface of the may penetrate to the region appeared, which gradu- hedge and the moth number was counted on the en- ally results in extent of an environmental problem. tire height of the hedge. The hedges of boxwood with The invasions are among the main factors leading to an average height of 50 – 70 cm were used for carry- reduction of the regional species diversity. Many inva- ing out the measurements. 82 RESULTS AND DISCUSSION In middle August 2013 as a result of the box tree Over the past 20 years, a number of new pests spe- moth’s damage a strong desiccation of Buxus sempervi- cies and pathogens were established, which had not rens was recorded all over the city of Sochi (from Adler to been spread earlier in humid subtropics of the Russian Lazarevskoye districts). Plants of different ages – from 5 Federation (Table 1) and are potentially dangerous for to 70 years proved to be desiccation prone i.e. in both old plant component of terrestrial ecosystems. plantings and newly landscaped objects. Changes in the From the above listed pest species essential harm colour of leaves and desiccation of plant parts or whole is caused by the box tree moth (Cydalima perspecta- plants were very rapid. Dark green hairy caterpillars, up lis), sycamore lace bug (Corythucha ciliata), western to 4 cm long, with large black heads were detected in flower thrips (Frankliniella occidentalis) and citrus leaf- Buxus sempervirens crowns (Figure 1). The number of miner (Phyllocnistis citrella). these caterpillars reached 60 – 80 individuals/sq. dm

Table 1. Invasion of new species in terrestrial ecosystems of subtropics of Russian Federation

Year № Name of a species Host plant of emergence in the region PESTS Citrus spp., Ziziphus jujuba, Ceratitis capitata Wied. 1. Ficus carica, Diospyrus kaki and more than 2010* (Insecta, Diptera, Tephritidae) 70 other plant species Corythucha ciliata Say 2. Plane tree 1999 (Insecta, Hemiptera, Tingidae) Cydalima perspectalis Walker 3. Buxus spp. 2011 – 2012* (Insecta, Lepidoptera, Crambidae) Prunus persica, Rubus idaeus, Prunus arme- Frankliniella occidentalis Perg. 4. niaca, Rosa spp., Dianthus spp., vegetable 1998 (Insecta, Thysanoptera, Thripidae) cultures, etc. Obolodiplosis robiniae Haldeman 5. Robinia pseudoacacia 2012 (Insecta, Diptera, Cecidomyiidae) Ophelimus maskelli Ashmead 6. Eucalyptus spp. 2013* (Insecta, Hymenoptera, Eulophidae) Parectopa robiniella Clemens 7. Robinia pseudoacacia 2013 (Insecta, Lepidoptera, Gracillariidae) Phyllocnistis citrella Stainton Citrus spp., Eucalyptus spp., 8. 1999* (Insecta, Lepidoptera, Gracillariidae) Salix spp., Philadelphus spp. Polyphagotarsonemus latus Banks Flower, vegetable, fruit, decorative, citrus 9. 2004 (Acari, Trombidiformes, Tarsonemidae) culture and more than 50 other plant species PATHOGENS Erysiphe azaleae (U. Braun) U. Braun & S. 10. Takam. – powdery mildew Rhododendron spp. 2007 (Ascomycota, Leotiomycetes, Erysiphales) E. betae (Vaňha) Weltzien – powdery mildew 11. Hydrangea macrophylla 2009 (Ascomycota, Leotiomycetes, Erysiphales) E. syringae Schwein. – powdery mildew 12. Syringa vulgaris 2005 (Ascomycota, Leotiomycetes, Erysiphales) E. tortilis (Wallr.) Link – powdery mildew 13. Swida sp. 2006 (Ascomycota, Leotiomycetes, Erysiphales) Golovinomyces sparsus (A. Braun) V. P. 14. Heluta – powdery mildew Viburnum opulus 2006 (Ascomycota, Leotiomycetes, Erysiphales) Guignardia aesculi (Peck) V. B. Stewart, anamorphosis Phyllosticta sphaeropsoidea Horse-chestnut 15. Ellis & Everh. – Guignardia leaf blotch 2000 (Aesculus hippocastani) (Ascomycota, Dothideomycetes, Botryosphaeriales) * The species are found in the territory of Russia for the first time. 83 has been in the region for at least 2 years. In 2014, the first generation of the caterpillars was observed at the end of the first ten days of March, which is most likely due to the very warm winter. Thus, under favorable climatic conditions it is possible to expect the devel- opment of the third, and probably forth pest generations in the region. There is concern that, together with the pathogen Cylindrocladium buxicola that has caused desiccation of Buxus sempervirens in the regional ecosystems for recent years, Cy- dalima perspectalis can kill various species of Buxus sempervirens. At the turn of the century, Sycamore lace bug appeared not only in humid subtropics but also in steppe parts of Krasnodar region (Voigt, 2001). At the present time, the pest has multiplied everywhere and causes a Fig. 1. Caterpillar of Cydalima perspectalis Walker change in the color of Platanus leaves from green to bronze by the beginning of August followed by premature loss of foliage. Concerning citrus crops plantings, young growth is substantially damaged by the citrus leafminer and the broad mite. Phyllocnistis citrella mainly causes harm to the following crops in protected grounds: Citrus limon, C. meyeri, C. sinensis and C. paradisi. During the study period the death of shoots reached 70 – 98%. The pest damages C. unshiu and its cultivars to a lesser extent, as during the period of intensive development of the pest, shoots growth of this species was attenu- ating, although within years 2000 – 2010. C. unshiu shoots were damaged on 98 – 100% (Fogel and Ignatova, 2003; 2004). The pest caterpillars penetrate into a sheet and hide in its ribs, and then, eating the leaf parenchyma, they form transparent ribbon- like mines. During pupation, the caterpillar Fig. 2. Powdery mildew on Hydrangea is wrapped in a leaf edge. Damages in fruits of the area of short-haired fences. Adult caterpillars eat were observed too. Up to 6 generations can develop leaves entirely, as well as the bark of branches. during a year: 2 – in spring and 4 – In summer and Homes of the box tree moth are China, Japan, and autumn. The limiting factor of the insect mass repro- Korea, from where the pest came to Western Europe duction is air temperature below +12-16 °C. At higher in 2006, and spreaded there widely. Presumably in temperatures (greenhouse conditions) the propaga- 2011 – 2012 it came to the Black Sea coast of Rus- tion of pests and damage of plants did not stop even in sia. It is known that in European countries the box winter period. This species is especially dangerous for tree moth can develop in 2 – 3 generations (Korycinska, young plants in nurseries. Eyre, 2011). The first detection of the box tree moth The broad mite inhabits axillary shoots and ovaries in Sochi refers to 2012, when it was recorded by N. of fruits and flowers. Heavily infested leaves curl and V. Shiryayeva in the box tree planting material of Im- fall; flower buds withered. Throughout the year this eretinskaya lowland. The caterpillars of the first gen- mite develops up to 30 generations. eration were massively observed in humid subtrop- A dangerous pest of a closed ground western flow- ics in June 2013, of the second – in early and mid- er thrips was observed in the region in flower cultures August (Karpun, Ignatova, 2013).The level of the box in 1998. Frankliniella occidentalis was introduced to tree moth population in 2013 testified that the moth Adler farm so called “Southern cultures” together with

84 rose cuttings from St. Petersburg, where it came from rence in natural and artificial ecosystems. abroad in early 1990s. (Kalishina, 2009). Earlier this In our opinion, invasion of Erysiphe betae (Vaňha) species had not been recorded in Russia. Since the Weltzien, syn. Erysiphe polygoni DC appears most slightest damage can sharply reduce the value of or- clearly. The disease had not been observed in the re- namental flower cultures, the damage at any extent gion before 2009, but at the moment it is a fairly com- has economic significance. mon disease of Hydrangea, which is annually regis- Western flower thrips is equally dangerous for tered while becoming more and more common and flower, ornamental and vegetable crops. Surface penetrating new cultivars of this culture (Figure 2). To of the leaves infested with western flower thrips be- date, the disease is marked by us in 5 cultivars of Hyd- comes discolored as strokes; deepenings appear in rangea macrophylla, including the most common – “Jo- feeding places, followed by necrosis. Full flowers can- seph Banks” and “Madame Faustin Travouillon” (pre- not be formed. In addition, it is a carrying agent of vi- viously wrongly identified as “Hortensia”). The degree ral infections (for example, TSWV – Tomato Spotted of damage from powdery mildew is about the same. Wilt Virus, which has damaged more than 360 species Brown leaf spot of Aesculus hippocastanum has of cultivated plants) (Kalishina, 2009). Hidden way of been developing in humid subtropics of Russia during living, high fertility, short development cycle and high the last 5 years at epiphytoty level. The intensity of resistance to preparations make it extremely difficult to disease development reaches 100 per cent of leaves carry out various protective measures. Consequently, with lesions greater than 50% of the leaf blade. The western flower thrips is widely spread in farms of Rus- disease leads to premature defoliation. For a long sian subtropics of the Black Sea coast. time it was considered that the disease was caused In 2012, in the garden “Tree of Friendship”, we ob- by abiotic factors, which was associated with abjection served massive fruit damage (to 92%) in Ziziphus ju- difficulties. It should be noted that epiphytoty of this juba caused by the Mediterranean fruit fly. Later, the disease is currently observed throughout the whole damages were fixed on the neighbor citrus plantations, European part of Russia. where the damage level did not exceed 18%. Thanks to It was established that a late-blossoming form of timely protective measures, the nidus was eliminated. Aesculus hippocastanum is infected by the disease 10 – As for the black locust gall midge, locust Digitate 14 days later, and it is to a lesser extent. Thus, during Leafminer and Eucalyptus gall wasp, the populations the first ten days period of September (the maximum of these species in the ecosystems of the region is degree of disease development), an affected area of low. The first two species have been observed in Kras- the leaf blade was determined: early form – 77%, late nodar region by the specialists of the Federal State form – 58%. Budget Institution “Roslesozashchita” since 2010 It should be noted that apart from the above men- (Gninenko, 2010; Gninenko et al., 2011; Shturov et al., tioned species, there were also allocated other den- 2013), while Ophelimus maskelli Ashmead has been drotropheus species of fungi in the region for the first recorded in Russia for the first time. Nevertheless, it is time, but they are not widespread or harmful. necessary to closely monitor the populations of these Thus, 13 new pest species and plant pathogens pests as these species have become widespread for have been recorded in the humid subtropics of Russia recent years in Europe, North Africa and the Middle for the last 20 years. East; they are related to invasive species there, caus- Based on the biology of species, all of them can give ing significant damage to host plants and resulting in outbreak in the region and bring significant economic total or partial defoliation (Protasov et al., 2007; Du- damage to agrocenosis and urbocenosis. The greatest rand et al., 2011; Kaptun et al., 2013). harm is caused by the following pests in the region: From the new pathogens identified in the region Phyllocnistis citrella, Cydalima perspectalis, Franklin- over the past 15 years, the most notable are caus- iella occidentalis, Corythucha ciliata; their outbreaks ative agents of powdery mildew. For the first time were recorded in different years of studies. The biggest we observed 5 species (Table 1) for the study area: danger is represented by Guignardia aesculi - brown Erysiphe azaleae on leaves of Rhododendron lute- leaf spot pathogen of Aesculus hippocastanum. Other um Sweet, E. betae on leaves of Hydrangea macro- species should be classified as potentially dangerous. phylla Ser., E. syringae on leaves of Syringa vulgaris The only species which distribution center could be L., E. tortilis on leaves of Cornus sp., Golovinomyces located is Ceratitis capitata. sparsus on leaves of Viburnum opulus L. (Karpun, The emergence of new species with planting mate- 2012). These species are likely to have been deliv- rial, cutting of flowers and fruits requires to organize ered to the region with the planting material of orna- strict control over their dispersal, population size and mental plants. All these species are characterized by development terms in the region, which is necessary annual incidence, increased development intensity to develop measures for protection of fruit trees and of the caused disease and the frequency of occur- ornamental plants.

85 REFERENCES Karpun, N. N. 2012. Representatives of Erysiphaceae Budako, M. I. 1984. [Будыко, М. И. Эволюция биосфе- family on flower-and-ornamental varieties in Sochi. Sofia, ры. Гидрометеоиздат, Ленинград, 488 с.] vol. 28, p. 9-13 Durand, N., Rodrigues, J. C., Mateus, E., Boavida, C. Karpun, N. N., Ignatova, Ye. A. 2013. The First Report and Branco M. 2011. Susceptibility Variation in Eucalyptus about Cydalima perspectalis Walker on Black Sea Coast of spp. in Relation to Leptocybe invasa and Ophelimus maskel- Russia. Education and Science, Vol. 19, 29-32 (Praha) li (Hymenoptera: Eulophidae), Two Invasive Gall Wasps Oc- Kashmilov, M. M. 1974. [Камшилов, М. М. 1974. Пре- curring in Portugal. Silva Lus., vol. 19, n. Especial: 19-31. образование информации в ходе эволюции. Знание, Access mode: http://www.scielo.gpeari.mctes.pt Москва, 64 с.] Fogel, V. A. and Ignatova, E. A. 2003. [Фогель, В. А. Korycinska, A., Eyre, D. 2011. Box tree caterpillar, Cy- и Игнатова, Е. А. 2003. Цитрусовая минирующая моль dalima perspectalis. Plant pest factsheet. – York: The Food (сокоедка). Вестник защиты растений, 1, 70-71] and Environment Research Agency (FERA), 4 p. – Mode Fogel, V. A. and Ignatova, E. A. 2004. [Фогель, В. А. и access: http://www.fera.defra.gov.uk/ Игнатова, Е. А. 2004. Формирование вредной и полезной Kosova, V. V., I. Ya. Polyakova. 1958. (Eds).[В. В. Ко- энтомофауны на цитрусовых культурах в субтропиках сова, И. Я. Полякова. (ред.) 1958. Прогноз появления и РФ. „110 лет в субтропиках России”. –B: Науч. тр. 39, 2. учет вредителей и болезней сельскохозяйственных куль- Сочи, 2004, 418-426] тур. МСХ СССР, Москва, 626 с.] Gninenko, U. I., Glavendekich, M. 2010. [Гниненко, Pavlushin, V. A.Vilkova, N. A. and Suhoruchenko, Ю. И., Главендекич, М. 2010. Рекомендации по выяв- G. I. 2013. [Павлюшин, В. А., Вилкова, Н. А. и Сухоручен- лению белоакациевой листовой галлицы Obolodiplosis ко, Г. И. 2013. Фитосанитарная дестабилизация агроэко- robiniae (Haldeman) (Diptera, Cecidomyiidae). Москва- систем. Родные просторы, Санкт-Петербург, 184 с.] Пушкино, 23 с.] Protasov, A., La Salle, J., Blumberg, D., Brand, D., Gninenko, U. I., Shturov, V. I. and Rakov, A. G. 2011. Saphir, N., Assael, F., Fisher, N. and Mendel, Z. 2007. Biol- [Гниненко, Ю.И., Щуров, В. И. и Раков, А. Г. 2011. Неко- ogy, Revised Taxonomy and Impact on Host Plants of Opheli- торые новые инвазивные виды дендрофильных насеко- mus maskelli, an Invasive Gall Inducer on Eucalyptus spp. in мых в Краснодарском крае. –B: Защита лесов юга России the Mediterranean Area. Phytoparasitica, 35, 1, 50-76 от вредных насекомых и болезней. ВНИИЛМ, Пушкино, Shturov, V. I., Bondarenko, A. S. and Vibe, E. N. 2013. 25-36] [Щуров, В. И., Бондаренко, А. С. и Вибе, Е. Н. 2013. Igevskii, S. S. 1995. [Ижевский, С.С. 1995. Чужеземные Современное распролстранение новых видов-инвай- насекомые как биозагрязнители. Экология, 2, 119-123] деров (Insecta: Homoptera, Heteroptera, Hymenoptera, Igevskii, S. S. 2002. [Ижевский, С. С. 2002. Инвазии: Diptera, Lepidoptera) в древесно-кустарниковых экосис- неизбежность и контроль. Экологическая безопасность темах Северо-Западного Кавказа. VII Чтения памяти О. и инвазии чужеродных организмов. Сборник материалов А. Катаева. Санкт-Петербург, 105-106] Круглого стола Всероссийской конференции по экологи- Smolyakova, V. M. et al. 1999. [Смольякова, В. М. и ческой безопасности России (4-5 июня 2002 г.). – Москва: др. 1999. Методические указания по фитосанитарному и ИПЭЭ им. А.Н. Северцева, IUCN (МСОП), 49-61] токсическому мониторингу плодовых и ягодников. Крас- Kalishina, I. S. 2009. [Калишина, И. С. 2009. Трипсы нодар, 84 с.] в теплицах С-З России. Защита и карантин растений, Voigt, K. 2001. The first Russian record of Corytucha 12, 16-17] ciliata Say from Krasnodar (Heteroptera, Tingidae). Zoosys- Karpun, N. N., Ignatova, E. A. and Mihailova, E. V. tematica Rossica, 1, 10, 76 2013. [Карпун, Н. Н, Игнатова, Е. А. и Михайлова, Е. В. Zavadskii, K. M., Kolchinskii, E. I. 1977. [Завадский, 2013. Новый вредитель робинии лжеакации в субтро- К. М., Колчинский, Э. И. 1977. Эволюция эволюции. пиках Российской Федерации. Научные исследования в Историко-критические очерки проблемы. Наука, Ле- субтропиках России. –B: Тр. мол. ученых, аспирантов и нинград, 236 с.] соиск., ГНУ ВНИИЦиСК, Сочи, 43-53]

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