SYNECOLOGICAL CHARACTERIZATION OF THRIP COMMUNITIES (INSECTA, THYSANOPTERA) OF THE UMCS BOTANICAL GARDEN IN LUBLIN

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Teka Kom. Ochr. Kszt. Środ. Przyr. OL PAN, 2015, 12, 5 12 SYNECOLOGICAL CHARACTERIZATION OF THRIP COMMUNITIES (INSECTA, THYSANOPTERA) OF THE UMCS BOTANICAL GARDEN IN LUBLIN Katarzyna Czepiel-Mil, Robert Stryjecki, Danuta Kowalczyk-Pecka Department of Zoology, Animal Ecology and Wildlife Management, University of Life Sciences in Lublin Akademicka str. 13, 20-950 Lublin, kasiamil.mil@gmail.com Abstract. The article presents an ecological characterization of thrips caught in Moericke traps in the Botanical Garden in Lublin. The objective of the research was to study the species composition and abundance of thrips in a man-made environment, where alongside native plants there are also trees and bushes brought in from other parts of the world. A total of 396 adult Thysanoptera individuals belonging to 39 species were caught. This is 17.2% of the thrip fauna in Poland. Among the individuals collected there were 10 dendrophilous species and 3 mycophagous species associated with tree bark and living in rotting wood. This is 25% of the Thysanoptera occurring in Poland with these food preferences. The trap method chosen is effective at catching thrips appearing in the spring and early summer, i.e. Taeniothrips inconsequens, Thrips minutissimus, Oxythrips ajugae and O. bicolor, as well as deeply hidden species that are difficult to capture using other methods. Using the Moericke trap method we collected four species rarely recorded in Poland. Key words: thrips, Thysanoptera, Moericke traps, synecological groups, botanical garden INTRODUCTION Thrips (Thysanoptera) are very small insects, 1 3 mm in size, among which the largest group consists of phytophages feeding on sap, which they extract with their piercing-sucking mouthparts. When these insects feed they mechanically damage plants, deforming them or inhibiting their growth. Thrips also include a group of mycophagous species and zoophages that feed on aphids and the larvae of other insects [Kucharczyk 2004b]. In Poland there is little information concerning thrips occurring in artificial environments such as botanical gardens, which contain plants that do not occur naturally in this country, including trees, shrubs and herbaceous plants [Pobożniak et al. 2008, Łabanowski and Soika 2010, Pobożniak and Sobolewska 2011].

6 Katarzyna Czepiel-Mil et al. Thus far 226 thrip species have been recorded in Poland, of which 51 have a diet associated with trees and shrubs, feeding on their leaves and in their flowers, or as mycophages live on rotting wood [Kucharczyk and Kucharczyk 2013]. Due to their often hidden way of life, Moericke traps are an effective method of collecting them. The aim of the study was a synecological characterization of thrip communities in the man-made habitat of a botanical garden. We analysed the effect of the collection method using Moericke traps on the qualitative composition of the thrips. MATERIAL AND METHODS The Botanical Garden in Lublin is one of the youngest in Poland. It was established in 1965 thanks to the efforts of the administration of the Maria Curie- -Skłodowska University. It was officially made available to the public in May 1974. The garden is located in the western part of the city. It is one of the largest in Poland and one of the most beautiful in terms of landscape. It currently occupies 25 ha. Here one can see plants from all over the world, occurring naturally or obtained by breeding [Chmielewski and Sawicki 1986, Czarnecka et al. 1997]. Research in the UMCS Botanical Garden in Lublin was carried out in the years 2001 2002 at four selected sites. The sites were varied in terms of trees and flowers. Site 1 an open area by a pond, with dominance of grassy vegetation. Site 2 a moist, shaded ravine covered by a dense complex of various species of trees. Site 3 a flat area with dense and varied woody plants penetrated by sunlight. Site 4 sunlit flower beds. The study material was collected using Moericke traps. This method is usually used mainly to catch insects in treetops. Studies show that the largest numbers of insects, including thrips, fall into white traps that reflect ultraviolet light [Kirk 1984, Czepiel and Kucharczyk 1998]. For this reason traps of this colour were suspended among tree branches at a height of about 1.5 m and in the flower beds. They did not contain attractants, but were filled only with glycol diluted with water. Material was collected from them twice a month. The thrips were assigned to 6 ecological groups on the basis of food preferences and habitat [zur Strassen 1993]: graminicolous, floricolous, herbicolous, foliicolous, zoophagous and saprophagous species occurring mainly under tree bark and in litter. To identify Thysanoptera species we used keys by Mound et al. [1976], Schliephake and Klimt [1979], zur Strassen [2003], and Zawirska [1994], and nomenclature according to the list of thrips of Poland [Kucharczyk 2004b].

SYNECOLOGICAL CHARACTERIZATION OF THRIP COMMUNITIES 7 RESULTS AND DISCUSSION At the four sites at the UMSC Botanical Garden in Lublin 396 adult Thysanoptera individuals belonging to 39 species were collected in Moericke traps. This is 17.2% of the thrips fauna occurring in Poland. The species belonged to three families: Aeolothripidae, Thripidae and Phlaeothripidae (Table 1). Two trophic groups were distinguished among the thrips collected phytophages and zoophages. Phytophages were dominant in the material (98.5%, 36 sp.). Only three species were included among zoophages: Aeolothrips intermedius, Aeolothrips melaleucus and Xylaplothrips fuliginosus. Among these predators, Aeolothrips intermedius is very common and abundant throughout Poland. It sucks the larvae of other thrips, aphids, and the larvae and eggs of small insects [Kucharczyk et al. 2006]. Its larvae puncture plant tissues, mainly flower petals, and suck out their contents [Zawirska 1969]. This species, taking in a variety of food, develops more rapidly and produces large numbers of offspring [Trdan et al. 2005]. The dominant species feeding on herbaceous plants were Thrips fuscipennis (26.0%), T. flavus (14.9%), T. major (13.9%), T. tabaci (8.3%) and Frankliniella intonsa (7.8%). Thrips living in flowers account for the largest group, mainly species of the genera Thrips and Frankliniella [Funderburk 2001]. Aided by the wind, these small insects make their way to various flowering plants, including flowering trees, and pollinate them [Sakai 2002]. Polyphages were the most numerous group in terms of food preferences 20 species in this group accounted for 91.4% of the fauna caught in the traps. The quantitative share of the other two groups monophages and oligophages was the same (4.3% each), but considerably more oligophagous species were noted (13 sp.) than monophagous ones (6 sp.). Among the oligophages in the traps, species found on monocotyledonous plants were dominant: Aptinothrips rufus, A. stylifer, Chirothrips manicatus, Frankliniella tenuicornis and Limothrips denticornis. This is indicative of the tendency of thrips towards migratory flight. The most abundant of the monophagous species was Pezothrips dianthi, a thermophilic species found on plants of the genus Dianthus. It was caught in traps placed among flower beds, where the flowers of these plants were present. The other monophagous species were the graminicolous species Chirothrips ambulans (associated with Poa pratensis) and Limothrips consimilis (associated with Bromus sp.), the floricolous Thrips albopilosus (associated with Humulus lupulus), the hygrophilous Hoplothrips ulmi, found under tree bark, and the foliicolous T. calcaratus (associated with Tilia sp.), which having been introduced to South America became a serious pest defoliating American Linden (Tilia Americana) [Werner et al. 2004].

8 Katarzyna Czepiel-Mil et al. Table 1. List of species and ecological structure of thrips (Thysanoptera) collected in UMCS Botanical Garden in Lublin in 2001 2002 Thysanoptera Preferences trophic food Total Aeolothripidae 1. Aeolothrips intermedius Bagnall, 1934 Polyphagous z 3 2. Aeolothrips melaleucus (Haliday, 1852) Oligophagous z 2 Thripidae 3. Anaphothrips obscurus (Müller, 1776) Polyphagous g 2 4. Aptinothrips elegans Priesner, 1924 Polyphagous g 1 5. Aptinothrips rufus Haliday, 1836 Oligophagous g 1 6. Aptinothrips stylifer Trybom, 1894 Oligophagous g 1 7. Chirothrips ambulans Bagnall, 1932 Monophagous g 1 8. Chirothrips manicatus Haliday, 1836 Oligophagous g 2 9. Dendrothrips degeeri Uzel, 1895 Polyphagous fo 12 10. Frankliniella intonsa (Trybom, 1895) Polyphagous h 31 11. Frankliniella tenuicornis (Uzel, 1895) Oligophagous h 1 12. Limothrips consimilis Priesner, 1926 Monophagous g 1 13. Limothrips denticornis Haliday, 1836 Oligophagous g 1 14. Myterothrips albidicornis (Knechtel, 1923) Polyphagous fo 2 15. Mycterothrips latus (Bagnall, 1912) Polyphagous fo 1 16. Neohydatothrips abnormis (Karny, 1909) Oligophagous fl 1 17. Oxythrips ajugae Uzel, 1895 Oligophagous fo 1 18. Oxythrips bicolor (O.M.Reuter, 1879) Oligophagous fo 1 19. Pezothrips dianthi (Priesner, 1921) Monophagous fl 8 20. Riubiothrips sordidus (Uzel, 1895) Oligophagous h 1 21. Taeniothrips inconsequens (Uzel, 1895) Polyphagous fo 19 22. Thrips albopilosus Uzel, 1895 Monophagous fl 2 23. Thrips atratus Haliday, 1836 Polyphagous h 11 24. Thrips calcaratus Uzel, 1895 Monophagous fo 4 25. Thrips flavus Schrank, 1776 Polyphagous h 59 26. Thrips fuscipennis Haliday, 1836 Polyphagous h 103 27. Thrips major Uzel, 1895 Polyphagous h 55 28. Thrips minutissimus Linnaeus, 1758 Polyphagous fo 3 29. Thrips nigropilosus Uzel, 1895 Polyphagous h 3 30. Thrips physapus Linnaeus, 1758 Polyphagous h 13 31. Thrips pillichi Priesner, 1924 Polyphagous fl 6 32. Thrips tabaci Lindeman, 1889 Polyphagous h 33 33. Thrips trehernei Priesner, 1927 Polyphagous h 1 34. Thrips validus Uzel, 1895 Polyphagous fl 2 35. Thrips viminalis Uzel, 1895 Oligophagous fo 2 Phlaeothripidae 36. Haplothrips kurdjumovi Karny, 1913 Polyphagous fo 2 37. Hoplothrips ulmi (Fabricius, 1781) Monophagous m 1 38. Poecilothrips albopictus Uzel, 1895 Oligophagous m 2 39. Xylaplothrips fuliginosus (Schille, 1910) Oligophagous m, z 1 Total 396 Abbreviations: fl floricolous, fo foliicolous, g graminicolous, h herbicolous, z zoophagous, m mycophagous, rare species

SYNECOLOGICAL CHARACTERIZATION OF THRIP COMMUNITIES 9 In terms of food preferences, the largest group in the samples from the Moericke traps comprised herbicolous species (11 sp., 78%). The most abundant of these was Thrips fuscipennis (26%) (Table 1). The material collected contained 10 foliicolous species (11.8%). Leaves are a permanent food source for the larvae of numerous species in the absence of flowers (Sakai 2002). The most numerous was Taeniothrips inconsequens, which feeds on fruit trees and attacks maples, hawthorn and blackthorn [Zawirska 1994]. A smaller group comprised graminicolous species (8 sp.) and floricolous species (6 sp.). The smallest and least abundant group was mycophages associated with tree bark and living on rotting wood: Hoplothrips ulmi, Poecilothrips albopictus and Xylaplothrips fuliginosus. The last of these is also a zoophage and is found in natural forest habitats in Europe. It is little known in Poland [Kucharczyk 2008]. The dendrophilous and mycophagous species caught accounted for 25% of the Thysanoptera of Poland with these food preferences. Dendrophilous species, i.e. Taeniothrips inconsequens, Thrips minutissimus, Oxythrips ajugae and Ox. bicolor, were collected in the Moericke traps only in spring. This is confirmed by numerous studies conducted in a forest environment [Kucharczyk and Sęczkowska 1990, Kucharczyk 2004a, Kucharczyk and Kucharczyk 2011, Lubiarz 2011]. These species have only one generation per year and hibernate in the form of pupae or as adult forms. They are caught in the largest numbers in the spring, when they leave their wintering places and feed on young leaves [Kucharczyk and Kucharczyk 2013]. Fig. 1. Faunistic similarity between study sites where Moericke traps were set up

10 Katarzyna Czepiel-Mil et al. The hygrophilous species Thrips viminalis, found on willow (Salix L.), alder (Alnus Mill.) and poplar (Populus L.), was caught only in autumn. The highest faunistic similarity was found between sites 2 and 3 (35.6%) (Fig. 1). The high similarity between the fauna of these two sites was probably due to habitat similarity, as there were dense complexes of various tree species at both sites. The lowest similarity was noted between sites 1 and 2 (14.2%). Site 1 was an open area near a pond and was covered with grassy vegetation, so the two sites were substantially different. Using the Moericke trap method we caught 4 species that are rare in Poland: Neohydatothrips abnormis (floricolous), Mycterothrips albidicornis (dendrophilous), Xylaplothrips fuliginosus and Poecilothrips albopictus (both mycophages). These mycophages have been caught in Moericke traps at other sites in Lublin and its outskirts [Czepiel-Mil 2006]. CONCLUSIONS 1. A total of 396 adult Thysanoptera individuals belonging to 39 species were collected. This is 17.2% of the thrips fauna occurring in Poland. 2. There were 10 dendrophilous Thysanoptera species and 3 mycophagous species associated with tree bark in the material collected. This is 25% of the Thysanoptera fauna occurring in Poland with these food preferences. 3. Most of the species caught were early-spring species, which are most abundant in the spring and early summer when the leaves and flowers of trees begin to develop. 4. The highest faunistic similarity was noted at the sites with many trees of different species growing in a dense complex. 5. The highest species diversity among the thrips was noted at the site with a trap set up in a flower bed. Here herbicolous species living on various herbaceous plant species were dominant. 6. The Moericke trap method is an effective method for catching deeply hidden species that are difficult to capture using other methods. REFERENCES Chmielewski T., Sawicki R., 1986. Ogród Botaniczny UMCS w Lublinie. Przewodnik. Wojewódzki Ośrodek Informacji Turystycznej, Lublin. Czarnecka B., Dybkowska M., Sawicki R., 1997. Ogród Botaniczny UMCS. Przewodnik dydaktyczny. Wyd. UMCS, Lublin. Czepiel-Mil K., 2006. Rzadkie dla fauny Polski gatunki wciornastków (Thysanoptera) stwierdzone w Lublinie. Wiad. Entomol. 25, Supl. 2, 59 64. Czepiel K., Kucharczyk H., 1998. Liczebność wciornastków (Thysanoptera) na tle innych owadów odławianych do kolorowych pułapek Moericke go w Poleskim Parku Narodowym. Wiad. Entomol. 17 (supl.), s. 163.

SYNECOLOGICAL CHARACTERIZATION OF THRIP COMMUNITIES 11 Funderburk J., 2001. Ecology of thrips. In: Thrips and tospoviruses: Proceedings of the 7 th International Symposium on Thysanoptera, Marullo R., Mound L. (eds.), e-book: www.ento.csiro.au- /thysanoptera/symposium/, 121 128. Kirk W.D.J., 1984. Ecologically selective coloured traps. Ecol. Entomol. 9, 35 41. Kucharczyk H., 2004a. Wciornastki (Insecta: Thysanoptera) jako element monitoringu ekologicznego w Puszczy Białowieskiej. Leś. Pr. Bad. 3, 85 94. Kucharczyk H., 2004b. Wciornastki (Thysanoptera) Polski. W: Fauna Polski. W. Bogdanowicz (red.). Wyd. IZ PAN, Warszawa. Kucharczyk H., 2008. Xylaplothrips zawirskae n. sp. a new species from Poland (Thysanoptera: Phlaeothripidae). Genus 19 (1), 7 13. Kucharczyk H., Kucharczyk M., 2011. Wciornastki (Thysanoptera) lasów bukowych południowo- -wschodniej Polski. Leś. Pr. Bad. 72 (4), 329 337. Kucharczyk H., Kucharczyk M., 2013. Charakterystyka i cechy diagnostyczne wciornastków z rodziny Thripidae (Insecta, Thysanoptera) najczęściej występujących w koronach drzew lasów centralnej Europy. Leś. Pr. Bad. 74 (1), 5 11. Kucharczyk H., Setniewska M., Legutowska H., 2006. Zróżnicowanie fauny wciornastków (Thysanoptera) na roślinach zielarskich w rejonie warszawskim. Post. Ochr. Rośl. 46 (2), 429 432. Kucharczyk H., Sęczkowska K., 1990. Przylżeńce (Thysanoptera) zespołu grądowego (Tilio- Carpinetum) w rezerwacie Bachus (Wyżyna Lubelska). Fragm. Faun. 33(20), 349 360. Lubiarz M., 2011. Thrips (Thysanoptera) inhabiting Quercus robur L. in the town landscape of Puławy and the natural landscape of Poleski National Park. Urban Fauna. Studies of animal biology, ecology and conservation in European cities. Bydgoszcz, 161 170. Łabanowski G., Soika G., 2010. Przylżeńce (Thysanoptera) występujące na trawach ozdobnych. Prog. Plant Prot. 50(3), 1274 1286. Mound L.A., Morison G.B., Pitkin B.R., Palmer J.M., 1976. Handbooks for the identification of British insects. Roy. Entomol. Soc. London, 12 79. Pobożniak M., Bisaga A., Bussler M., 2008. Atrakcyjność kwiatów drzew i krzewów dla wciornastków Thysnoptera w Ogrodzie Botanicznym w Krakowie. W: Fauna miast. Ochronić różnorodność biotyczną w miastach. SAR Pomorze, Bydgoszcz, 373 382. Pobożniak M., Sobolewska A., 2011. Thrips (Thysanoptera) species infesting herbaceous plants in Botanical Garden in Krakow (Poland). Urban Fauna. Studies of animal biology, ecology and conservation in European cities. UTP, Bydgoszcz, 171 179. Sakai S., 2002. A review of brood-site pollination mutualism: plants providing breeding sites for their pollinators. J. Plant Res., Tokyo, 115, 161 168. Schliephake G., Klimt K., 1979. Thysanoptera Fransenflügler. Gustav Fischer Verlag, Jena, 71 477. Strassen zur R., 1993. Fransenflügler (Insecta: Thysanoptera) in Naturschutzgebiet Arschleife Altenahr und in einer benachbarten Weinbergbrachfläche. Beiträge Landespflege Rheinland- Pfalz 16, 359 381. Strassen zur R., 2003. Die terebranten Thysanopteren Europas. Goecke & Evers, Keltern. Trdan S., Andjus L., Raspudić E., Kać M., 2005. Distribution of Aeolothrips intermedius Bagnall (Thysanoptera:Aeolothripidae) and its potential prey Thysanoptera species on different cultivated host plants. J. Pest Sci. 78, 217 226. Werner S.M., Nordheim E.V., Raffa K.F., 2004. Comparison of methods for sampling Thysanoptera on basswood (Tilia americana L.) trees in mixed northern hardwood deciduous forests. Forest Ecol. Manage. 201, 327 334. Zawirska I., 1969. Fauna przylżeńców (Thysanoptera) w kwiatach roślin strączkowych w Polsce. Pr. Nauk. IOR 11(2), 81 89. Zawirska I., 1994. Klucz do oznaczania wciornastków (Thysanoptera). W: Diagnostyka szkodników roślin i ich wrogów naturalnych. SGGW, Warszawa, 145 174.

12 Katarzyna Czepiel-Mil et al. CHARAKTERYSTYKA SYNEKOLOGICZNA ZGRUPOWAŃ WCIORNASTKÓW (INSECTA, THYSANOPTERA) OGRODU BOTANICZNEGO UMCS W LUBLINIE Streszczenie. W artykule zaprezentowano charakterystykę ekologiczną wciornastków złowionych do pułapek Moerickego na terenie ogrodu botanicznego w Lublinie. Celem pracy było zbadanie składu gatunkowego i liczebności wciornastków w środowisku sztucznie stworzonym przez człowieka, gdzie obok rodzimych roślin, drzew i krzewów występują także te sprowadzone z innych części świata. Ogółem zebrano 396 osobników dorosłych Thysanoptera należących do 39 gatunków. Stanowi to 17,2% fauny wciornastków Polski. Wśród zebranych osobników stwierdzono 10 gatunków dendrofilnych Thysanoptera oraz 3 gatunki mykofagiczne związane z korą drzew i żyjące na rozkładającym się drewnie. Stanowi to 25% fauny Thysanoptera Polski o takich preferencjach pokarmowych. Wybrana metoda pułapkowa jest skuteczną metodą do połowu wciornastków pojawiających się wiosną i wczesnym latem, tj. Taeniothrips inconsequens, Thrips minutissimus, Oxythrips ajugae i O. bicolor oraz gatunków głęboko ukrytych, trudnych do schwytania innymi metodami. Metodą pułapek Moerickego pozyskano 4 gatunki rzadko wykazywane w Polsce. Słowa kluczowe: wciornastki, Thysanoptera, pułapki Moerickego, grupy synekologiczne, ogród botaniczny