88 UDK 574.58

ALIEN SPECIES IN THE REPUBLIC OF MOLDOVA: A REVIEW OF THEIR ORIGIN AND MAIN IMPACT

© 2014 Munteanu N.1, Moldovan A.1, Bacal S.2, Toderas I.1

1 Laboratory of Systematics and Molecular Phylogeny, Institute of Zoology, Moldova Academy of Sciences, MD 2028, Chisinau, Academiei 1, Republic of Moldova, e-mail: [email protected] 2 Laboratory of Entomology, Institute of Zoology, Moldova Academy of Sciences, MD 2028, Chisinau, Academiei 1, Republic of Moldova

Received September 15, 2013

A list of considered to be of alien origin in the Republic of Moldova has been set up, with data on their origin, habitat, trophic range and economic impact. Altogether, 75 alien beetle species have been revealed, which represents 2.98% of local coleopteran fauna. The most numerous taxonomic groups are (30 species), Staphylinidae and Chrysomelidae (by 11). The majority of non-native beetles originates in Europe, Asia and Mediterranean region, while comparable less number of species originates in Africa and North America. From the total number of the investigated alien beetles 26.67% are agricultural, forest and storage pests. Key words: alien species, beetles, Republic of Moldova.

Introduction [Kenis, 2005], Israel [Roll et al., 2007], Invertebrates, and among them Albania, Bulgaria and Macedonia [Tomov , represent the greatest part of et al., 2009], and Russia [Maslyakov, alien and are of pronounced Izhevsky, 2011]. importance in agriculture, horticulture and The geographical position of the forestry, with a major economic impact. Republic of Moldova at the crossing point Their activity can alter ecosystems of three biogeographical zones (Central structure and functioning and eventually European, Eurasian and Mediterranean) lead to the extinction of native species, along with the intense human activities inducing biodiversity losses [Elton, 1958; makes it especially prone to alien species Nentwig, 2008; Hulme et al., 2009]. entry. Despite this, the problem of alien Vulnerability of ecosystems to alien species on the investigated territory was species is probably one of the least studied not treated in the scientific literature. and most difficult questions. Knowledge of Available information contains some data alien species effects and potential threats is on certain taxa or groups of beetles, their still insufficient being crucial for managing trophic preferences and distribution but the risks related to species transfer. it does not always contain information on Establishment of first alien arthropods their origin. checklists in Europe started in 2002 and The main goal of this study was to covered Austria [Essl, Rabitsch, 2002], determine which alien beetle species Germany [Geiter et al., 2002], the entered, spread and/or established in Netherlands [Reemer, 2003], the Czech natural transitional, forest and agricultural Republic [Šefrová, Laštůvka, 2005], the ecosystems of the Republic of Moldova, its United Kingdom [Hill et al., 2005, Smith origin and impact, in order to better et al., 2007], Serbia and Montenegro understand how to manage non-native [Glavendekić et al., 2005], Switzerland beetles. Only in this manner the most

Российский Журнал Биологических Инвазий № 1 2014 89 Table 1. Composition of alien beetle species in individual families; S – eusynanthropic, C – casual, N – naturalized non invasive, *N – naturalized post invasive, I – invasive. Taxon Spp. Aliens % of S C N *N I RM all Staphylinidae 321 11 3.42 – – – 11 – Scarabaeidae 124 1 0.8 – – – 1 – Dermestidae 14 1 7.1 – – – 1 – Ptinidae 22 1 4.54 – – – 1 – Coccinellidae 33 1 3.03 – – – – 1 Tenebrionidae 52 5 9.61 5 – – – – Meloidae 26 1 3.84 – – – 1 – Cerambycidae 125 2 1.6 – 1 – 1 – Chrysomelidae 197 11 5.58 2 1 3 4 1 Brentidae 90 8 8.88 – – 3 5 – Dryophthoridae 5 3 60 2 1 – – – Curculionidae 510 30 5.88 – 7 16 6 1 Total Coleoptera 2512 75 2.98 9 10 22 31 3 efficient methods to prevent new arrivals The of the beetle species and/or disseminations, and reduce their is based primarily on the works of impacts, can be proposed and implemented. Kryzhanovskij [1965] and Bouchard et al. [2011]. Biological and geographical Material and methods classification was done according to To initiate the first list of non-native concepts of Darlington [1966] and beetle species in the Republic of Moldova, Banarescu [1970]. we reviewed professional published and unpublished information and available Results and discussions reports, particularly checklists of Miller, In the Republic of Moldova about 2512 Zubowsky [1917], Medvedev, Shapiro beetle species are known [Bacal et al., [1957], Adashkevich [1972], Poiras [1991, 2013]. From the total number, 75 ones 1994, 1998, 2006], Neculiseanu, Matalin (2.98%) represent alien species. Among [2000], Neculiseanu, Bacal [2005], them, 9 species (12%) create short or long- Munteanu [2006], Bacal, Stan [2006], term populations only in heated spaces, Bacal, Derunkov [2010], Derunkov, Bacal with the ability to survive outside only [2011]. Also, museum specimen collection during warm periods of the year, but not of the Institute of Zoology, Academy of under winter conditions. A group of Sciences of Moldova and alien invasive 10 species (13.33%) creates occasionally species inventories websites were used. short-term populations in outdoor Data were compiled into a preliminary environments. The populations of these list of non-native beetles documented species are usually decimated by adverse in the country (either currently or weather conditions, surviving winter with historically). For each species we included difficulty or gradually disappearing for information about its origin, first report, other reasons. Another 56 species (74.66%) habitat, trophic preferences and host. can be considered naturalized; their Further, based on evidence in the literature, populations survive for long time tolerating we identified a number of non-native easily the local climatic conditions. species known as pests of agricultural Between these species, 22 (29.33% of crops, fruit trees, forests, ornamental aliens) ones remain non-invasive, other 31 and storage products. Distribution in alien (41.33%) species are post-invasive at species categories (eusynanthropic, casual, present, and 3 species (4%) are invasive. naturalized non invasive, naturalized post The categories of aliens with the numbers invasive and invasive) was performed of species are shown in the Table 1. [Šefrová, Laštůvka, 2005; Nentwig, The greatest number of identified alien Josefsson, 2010]. species (30) belongs to Curculionidae Российский Журнал Биологических Инвазий № 1 2014 90 family, followed by Staphylinidae, species. Invasive species originate from Chrysomelidae, Brentidae and Tenebrionidae. North America (2) and Asia (1). Detailed The largest proportion of species of alien information on each species is presented in origin is in Dryophthoridae (60%) and the Table 2. Tenebrionidae (9.61%), while for the rest From the total number of non-native it varies between 0.8–8.88 percent. By beetles the majority originates in Europe, contrast, no alien species were documented Asia and Mediterranean region and spreads in other 57 coleopteran families which with the progress of human civilization, occur in the Republic of Moldova. expansion of agricultural crops and for The majority of revealed other various reasons. Comparable less eusynanthropic alien species (5) are number of species originates in America; naturally found in tropical and subtropical their dissemination is partly due to regions; other two species are cryptogenic the human travel and trade activity, and by one are from North America and spontaneous spreading of those species is Asia. The group of casual species is being almost impossible (the geographical represented by four European, three Asian barrier is difficult to pass without human and three Mediterranean species. Among intervention). 22 naturalized non-invasive species 8 ones Alien species impact on economy and originate in Eurasia and Mediterranean environment is a result of trophic and region, 5 species are Mediterranean, by habitat preferences. Concerning habitats three European and Eurasian, two Euro- around 41.33% of the established alien Mediterranean and one North American beetle species colonize cultivated habitats. species. Concerning naturalized post- The second most populated are urban invasive species the most of them (8) settlements (38.66%). Grasslands are also derive from Eurasia and Mediterranean frequent habitats (28%). Woodlands and region, five are Eurasian, four Asian, three forest habitats are occupied by 20% of the European, by two African and non-native beetles. Heathlands, hedgerows Mediterranean, and one from America. and shrubs are populated by 5.33% of the This group also contains six cryptogenic species and only 4% occur in wetlands.

Table 2. Characteristics of alien beetle species in the Republic of Moldova. Status of alien species and their occurrence: S – eusynanthropic, C – casual, N – naturalized non invasive, *N – naturalized post invasive, I – invasive; Habitats: B – coastal habitats; E – grasslands; F – heathlands, hedgerows and shrub plantations; G – woodlands and forests; H – cultivated habitats; J – urban settlements, N/A – data non available; Trophic range: Pr – Predator, De – Detritivorous, Ph – Phytophagous (herbiphagous (her), spermatophagous (spe), leaf/stem browser (lbw), root browser (rbw), root borer (rbo), phloeophagous (phl), saproxylophagous (sxp), xylomycetophagous (xmp), Un – Unknown. Species Origin Status Habitat Trophic Host Reference range Staphylinidae Cilea silphoides Cryptogenic *N J Pr Cattle dung Mihailov, 2012 (Linnaeus, 1767) Atheta oblita Northern *N G, J Pr Fungus, Adashkevich, (Erichson,1839) Europe cattle dung 1972 Carpelimus corticinus Cryptogenic *N B, E Ph Floodplains, Adashkevich, (Gravenhorst, 1806) river banks, sand 1972 C. gracilis Cryptogenic *N B, E Pr Floodplains, Adashkevich, (Mannerheim, 1830) river banks, sand 1972 C. pusillus Cryptogenic *N B, E Pr Floodplains, Adashkevich, (Gravenhorst, 1802) river banks, sand 1972 Lithocharis nigriceps Asia-Tropical *N H, J Pr Compost Neculiseanu, Kraatz, 1859 1984 L. ochracea Eurasia *N J Un Dried vegetals Miller, (Gravenhorst, 1802) Zubowsky, 1917

Российский Журнал Биологических Инвазий № 1 2014 91 Gabrius nigritulus Eurasia *N J Un Fungus Yatsentkovsky, (Gravenhorst, 1802) 1912 Philonthus concinnus Eurasia *N J Pr Fungus, Adashkevich, (Gravenhorst, 1802) cattle dung 1972 P. discoideus Northern Africa, *N J Pr Dung Adashkevich, (Gravenhorst, 1802) Eurasia 1972 P. longicornis Eurasia *N J Pr Dung Miller, Stephens, 1832 Zubowsky, 1917 Scarabaeidae Pleurophorus caesus Eurasia, *N E De Dung Miller, (Creutzer, 1796) America Zubowsky, 1917 Dermestidae Dermestes ater Cryptogenic *N J De Necrophagous Miller, De Geer, 1774 Zubowsky, 1917 Ptinidae Ptinus fur Cryptogenic *N J De Waste, Miller, (Linnaeus, 1758) dried vegetals Zubowsky, 1917 Coccinellidae Harmonia axyridis Asia I H Pr Polyphagous, Iazlovetchi, (Pallas, 1773) predator mainly Sumenkova, aphids and coccids 2013 Tenebrionidae Tribolium castaneum Cryptogenic S J De Stored products Neculiseanu, (Herbst, 1797) Bacal, 2005 T. confusum Africa S J De Stored products Medvedev, Jacquelin du Val, 1868 Shapiro, 1957 T. destructor Tropical S J De Stored products Neculiseanu, Uyttenboogaart, 1933 Bacal, 2005 Alphitobius diaperinus Tropical, S J, G Pr, De Residues, Neculiseanu, (Panzer, 1797) Subtropical inhabitant of Bacal, 2005 chicken houses, on faeces and wastes Alphitophagus Cryptogenic S J, G De Residues, compost, Neculiseanu, bifasciatus rotten fruits, under Bacal, 2005 (Say, 1823) bark old stumps Meloidae Mylabris variabilis Eurasia *N E Pr, Adult floricolous, Miller, (Pallas, 1781) Ph (her) larvae parasite of Zubowsky, 1917 Acrididae Cerambycidae Rosalia alpine Central Europe, C G, H, J Ph (sxp) Fagus, and other Miller, (Linnaeus, 1758) Alps deciduous trees Zubowsky, 1917 Monochamus sutor Northern and *N G Ph (sxp) Picea, Pinus Baban, 2006 (Linnaeus, 1758) Central Europe Chrysomelidae Callosobruchus Asia-Temperate C H, J Ph (spe) Stored legumes Munteanu, chinensis 2006 (Linnaeus, 1758) Bruchus pisorum Asia-Temperate S H, J Ph (spe) Lathyrus, Pisum, Medvedev, (Linnaeus, 1758) Vicia Shapiro, 1957 B. rufimanus Africa *N H, J Ph (spe) Phaseolus, Medvedev, Boheman, 1833 Lathyrus, Lupinus, Shapiro, 1957 Pisum, Lens, Cicer, Vicia B. signaticornis Mediterranean *N H, J Ph (spe) Lathyrus, Lens, Munteanu, Gyllenhal, 1833 region Vicia seeds 2009 Bruchidius Mediterranean *N H Ph (spe) Genistea, Ononis, Munteanu, lividimanus region Cytisus seeds 2006 (Gyllenhal, 1833) Acanthoscelides America S H, J Ph (spe) Phaseolus seeds, Medvedev, obtectus wild and cultivated Shapiro, 1957 Say, 1831 legumes outdoors Российский Журнал Биологических Инвазий № 1 2014 92 A. pallidipennis North America N H, J Ph (spe) Fabaceae Munteanu, (Motschulsky, 1874) 2006 atrata Central, South N H Ph (her) Calestru, 2003 Fabricius, 1787 East Europe Crioceris asparagi Europe, Central N H, J Ph (her) Asparagus Medvedev, (Linnaeus, 1758) Asia Shapiro, 1957 Leptinotarsa Northern and I H Ph (her) Solanum Vorotyntseva, decemlineata Central America tuberosum, 1971 Say, 1824 other Solanaceae Gonioctena fornicate Eastern Europe *N H Ph (her) Medicago Medvedev, (Brüggemann, 1873) Shapiro, 1957 Brentidae Aspidapion validum Asia-Temperate *N H, F Ph (spe) Alcea rosae Miller, (Germar, 1817) Zubowsky, 1917 A. radiolus Asia, Europe, *N N/A Ph (her) Malvaceae Medvedev, (Marsham, 1802) Mediterranean Shapiro, 1957 region Alocentron Asia-Temperate *N H, F Ph (spe) Alcea rosae Solodovnikova, curvirostre Talitskii, 1972 (Gyllenhal, 1833) Squamapion Mediterranean N E Ph (spe) No data Solodovnikova, leucophaeatum region Talitskii, 1972 (Wencker, 1864) Taeniapion rufulum Europe, N E, F Ph (her) Urtica dioica Poiras, 1994 (Wencker, 1864) Mediterranean region Rhopalapion Asia-Temperate *N H Ph (spe) Alcea rosae Miller, longirostre Zubowsky, (Olivier, 1807) 1917 Trichopterapion Asia, Europe, N G Ph (spe) Carpinus betulus, Poiras, 1998 holosericeum Mediterranean C. orientalis (Gyllhenal, 1833) region Ischnopterapion Asia, Europe, *N N/A Ph (her) Trifolium Poiras, 1994 virens Mediterranean (Herbst, 1797) region Dryophthoridae Sitophilus oryzae Asia-Tropical S J Ph (spe) Grain Poiras, 1998 (Linnaeus, 1763) S. granarius Africa S J Ph (spe) Stored grains, Miller, Linnaeus, 1758 Secale Triticum, Zubowsky, 1917 Zea mays Acentrus histrio Mediterranean C E Ph (her) Glaucium Medvedev, Boheman, 1845 region Shapiro, 1957 Curculionidae Lignyodes bischoffi North America I G, H Ph (spe) Fraxinus, Syringa Poiras, 1987 (Blatchley, 1916) Tychius caldaria Mediterranean N E Ph (her) Dorycnium Medvedev, Dieckmann, 1986 region suffruticosum, Shapiro, 1957 D. pentaphyllum Rhynchaenus sparsus Mediterranean N G Ph (lbw) Quercus robur, Poiras, 1991 Fahraeus, 1843 region Q. pubescens Baris janthina Asia, Europe, N E Ph (lbw) Caradaria draba Medvedev, Boheman, 1836 Mediterranean Shapiro, 1957 region Baris prasina South Europe C Ph (lbw) Brassicaceae Poiras, 1998 (Boheman, 1836) Rhinoncus Asia, West *N E, H Ph (rbo) Rumex, Miller, pericarpius Mediterranean Medicago, Zubowsky, 1917 (Linnaeus, 1758) region, Europe Melilotus Thamiocolus Asia, Europe, N E Ph (her) Phlomis pungens Poiras, 1998 uniformis Mediterranean (Gyllenhal, 1837) region Российский Журнал Биологических Инвазий № 1 2014 93 Ranunculiphilus Mediterranean N E Ph (her) No Data Poiras, 1998 kuntzei region (Smreczynski, 1957) Otiorhynchus albidus Asia, West *N E, H Ph (lbw) Cerasus, Juglans, Ruscinski, 1937 Stierlin, 1861 Mediterranean Populus, region, Europe Tamarix, Tilia Trachyphloeus Europe, Asia C N/A Ph (rbw) Cynodon Poiras, 1998 spinimanus Germar, 1824 Phyllobius canus Mediterranean C G, H Ph (lbw) Rosaceae, Plugar, 1963 Gyllenhal, 1834 region, Asia Quercus robur Cycloderes Mediterranean C E Ph (lbw) Plantago Poiras, 1998 canescens region (Rossi, 1792) Sitona lineatus Asia, Europe, *N H, J Ph (rbw)Fabaceae Medvedev, (Linnaeus, 1758) Mediterranean Shapiro, 1957 region S. macularius Asia, Europe, *N H, J Ph (rbw) Trifolium Medvedev, (Marsham, 1802) Mediterranean Shapiro, 1957 region S. puncticollis Asia, Europe, *N H Ph (rbw) Trifolium, Ruscinski, 1937 Stephens, 1831 Mediterranean Melilotus region Aparopion costatum Europe, C E Ph (her) No data Arnoldi et al., Fahraeus, 1843 Mediterranean 1965 region Hypera nigrirostris Asia, Europe, N E, J Ph (lbw) Ononis, Trifolium Medvedev, (Fabricius, 1775) Mediterranean Shapiro, 1957 region H. postica Asia, Europe, *N H, J Ph (lbw) Fabaceae Antonova, 1977 (Gyllenhal, 1813) Mediterranean region H. pastinacae Asia, Europe, N G, H Ph (lbw) Pastinaca sativa, Medvedev, (Rossi, 1790) Mediterranean Daucus carota Shapiro, 1957 region H. contaminata Europe N E Ph (lbw) Lathyrus Ruscinski, 1937 (Herbst, 1795) tuberosus Rhabdorhynchus East N E Ph (her) No data Poiras, 2001 menetriesi Mediterranean Gyllenhal, 1842 region Lachnaeus horridus Asia C E Ph (her) Inula Poiras, 1998 Reitter, 1890 Lixus astrachanicus Asia C E Ph (her) No data Poiras, 1998 Faust, 1883 Pissodes castaneus Asia, Europe, N G Ph (phl) Pinus Poiras, 1991 (De Geer, 1775) Mediterranean region Scolytus laevis Europe N G, H Ph (phl) Ulmus Poiras, 2001 Chapuis, 1873 S. rugulosus Asia, Europe, N H Ph (phl) Rosaceae trees Miller, (Ratzeburg, 1837) Mediterranean Zubowsky, 1917 region Xyleborinus Asia, Europe, N H Ph (xmp) Laurus, Pinus, Miller, saxesenii Mediterranean Castanea Zubowsky, 1917 (Ratzeburg, 1837) region Pteleobius kraatzii Europe, West N H, G, F Ph (phl) Ulmus Miller, (Eichhoff, 1864) Mediterranean Zubowsky, 1917 region Hylastes angustatus South Europe, N G Ph (phl) Pinus Stark, 1952 (Herbst, 1793) Asia H. ater Europe, Asia N G, H Ph (phl) Pinus Miller, (Paykull, 1800) Zubowsky, 1917

Российский Журнал Биологических Инвазий № 1 2014 94 According to larvae trophic preferences earlier release of this species for 54 species of investigated beetles are introduction in Ukraine [Katsoyannos et phytophagous, 12 are predators and 7 al., 1997]. Published data regarding detritivorous; adults of Alphitobius establishment of H. axyridis in the diaperinus and Mylabris variabilis are Republic of Moldova appeared recently, being detritivorous and phytophagous, [Iazlovetchi, Sumenkova, 2013; Timus, respectively. For remaining 2 species Stahi, 2013]. Within H. axyridis information on their diet is not available. populations five forms were identified: Most of the phytophagous H. axyridis var. novemdecimsignata, H. a. beetles (29.09%) are herbiphagous. var. siccoma, H. a. var. succinea, H. a. var. Spermatophagous is the second most spectabilis and H. a. var. conspicua important feeding group (27.27%), [Timus, Stahi, 2013]. Iazlovetchi and followed by leaf/steam browsers (18.18%), Sumenkova [2013] mention that the phloeophagous (10.9%), root browsers species represented 42% of all coccinellids (7.27%) and saproxylophagous (3.63%). recorded in 2011, the proportion has The remaining (by 1.81%) are root borers reached 86% in 2012, and 90% in and xylomycetophagous. From the total 2013, successfully eliminating autochthon number of the investigated alien beetles coccinellids Coccinella septempunctata L. 26.67% are agricultural, forest and storage and Adalia bipunctata L. pests. All non-native species occurring The effects of an alien species entry in in closed spaces (9) are storage pests. a new ecosystem can be diverse. Most Depending on their food bonds and significant is a direct competition with population dynamics, post-invasive and native species for food and space, an invasive species have various degrees of increasing abundance in the new importance, among them Leptinotarsa environment until a complete replacement decemlineata, Sitona lineatus and of native residents occurs. Despite that a Rhopalapion longirostre cause the large amount of attested alien beetles does biggest losses in agricultural crops not produce economic damages, it should yield [Vorotyntseva, 1971; Poiras, 2006; not be ignored because non-invasive status Munteanu et al., 2012], while Lignyodes does not mean that it will not become bischoffi is one of the most dangerous invasive. It could be just a matter of time forest pest [Poiras, 1987, 2006]. Of the and circumstances (biotic and abiotic alien species living under outdoor conditions that may change) until it conditions, the species of casual becomes invasive. That’s why knowledge occurrence and naturalized non-invasive of species peculiarities and behavior in a species do not have great significance, new environment is extremely important because they are active only in short-terms for determining the factors that can lead to or inhabit a very small territory. an alien species uncontrollable expansion Revealed alien predators belong to and invasive statute modification. Staphylinidae and Coccinelidae families. Unfortunately, the hazards caused by Detritivorous species belong to alien species did not cause that much Tenebrionidae, Ptinidae, Dermestidae concern among scientists, nor did it attract and Scarabaeidae. Their influence on public awareness as much as would have environment can be considered beneficial been expected [Hulme et al., 2009]. or neutral as long as they occur in small Conducted researches comprise too large numbers and do not affect native species. regions and cannot solve the problems A representative case of alien species of restricted areas. In the Republic of expansion in the Republic of Moldova is Moldova, for example, this is the first Harmonia axyridis (Pall., 1773). The first study highlighting alien species. The unpublished information on this species, location of the republic at the interference according to Timus and Stahi [2013], dates of biogeographical zones causes a from 1970, which could be related to the continuous pressure of alien species that

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