Faunistic Study of Ladybirds (Coleoptera: ) in the Banat Region, Romania

Ana – Maria VIRTEIU1* 1, Ramona STEF1, Mihai VLAD1 and Ionela DOBRIN2

1 , Ioana GROZEA

Department of Biology and Plant Protection, Banat’s University of Agricultural Sciences and Veterinary2 Medicine “King Michael I of Romania” from Timisoara 119 Calea Aradului, Timisoara, Romania Department of Plant Sciences,[email protected] University of Agronomic Science and Veterinary Medicine Bucharest 59 Marasti Bvd, Sector 1, Bucharest, Romania *Corresponding author:

Bulletin USAMV series Agriculture 72(2)/2015 Print ISSN 1843-5246; Electronic ISSN 1843-5386 DOI 10.15835/buasvmcn-agr: 11489

ABSTRACT

Ladybirds (Coccinellidae) are a popular, Insectawidely recognizedPterygota and highly regardedColeoptera group duePolyphaga to their bright color Cucujoidea and role in controllingCoccinellidae. insect pests. Worldwide nearly 6000 species are known. From systematic point of view, ladybeetles belonging to Class , Subclass , Order , Suborder , Superfamily anf Family Coccinellids are of interest and importance in agriculture and forestry, since adults and larvae of most species are predators of herbivorous pests such aphids, psyllids, mealy bugs and scale . The aim of this research regarding coccinellid was to explore, identify and also characterize the coccinellid fauna of the Banat region (Romania). The coccinellid beetles were collected from March 2013 to September 2014 from 4 localities at different altitudes in the Banat region. Samples were collected at weekly interval from a wide variety of habitats: agricultural land, gardens and parks, both on herbaceous and Coccinellawoody essences. 5 – punctata In this study Coccinella a total 7 of– punctata15 species belongingCoccinulla to14 11 – pustulata genera and Tythaspis3 subfamilies 17 – werepunctata identified. Adalia In 2the – punctatainvestigated Adaliahabitats 10 from – punctata the entomofaunistic Propylaea 14point – punctata of view, the Subcoccinella coccinelid species 24 – punctata identified were Psylobora as follows: 22 – punctata Hippodamia L., tredecimpunctata AdoniaL., variegate HarmoniaL., axyridis Calvia decimguttataL., Chilocorus L.,bipustulatus ChilocorusL., renipustulatus L., L., L., L., Goeze., Pallas., L., L. and Scriba. Seven species were the most abundant and could be observedKey words: in the Banat investigated region, Coccinellidae, area every year. environmental factors, faunistic study, feeding habits.

INTRODUCTION Scymninae, Chilochorinae, Ortalinae, Sticholotidinae Coccinellidae and Epilachninae

The family is a well- (Vandenberg, 2002). Most of known, abundant and diverse family (Majka & this coccinellids are bright shining colors with a McCorquodale, 2010). From a human perspective pattern of spots or patches against a contrasting ladybirds are one of the most beautifulCucujoidea insects background. Many appear to be distasteful to birds (Gordon, 1985). and their conspicuous appearance is an exemple This family belongs to superfamily of warning coloration (Moreton, 1969). and are aet largeal. family with about 6000 spe­ theirThe use coccinellidaeas biological control are an agent important and in group their liescies of described coccinellidae: worldwide Coccidulinae, (Vandenberg, , 2002; of beetles from both an economic standpoint in Khormizi , 2013). There are seven subfami­ diversity and adaptation to a number of differing 577

Faunistic Study of Ladybirds (Coleoptera: Coccinellidae) in the Banat Region, Romania et al. RESULTS AND DISCUSSION habitats (Debach, 1974; Michels, 1987; Jafari , case Coccinellidae 2013). They are environmentally beneficial and Insect biodiversity research group, in our have been used in different parts of the world to also the changes that family occur is in extremely numbers importantin certain control pests such as aphids, mealybugs, thrips, because it determines not only their number, but scale insects etc (Majerus, 1985, Ansari Pour, 2012).MATERIALS AND METHODS habitats. Ecosystems, namely agro-ecosystems in which they practice intensive agriculture have undergone major changes over the last decade, The coccinellid beetles were collected from thereby affecting the structure of fauna of insects, March 2013 to September 2014 from 4 localities not only insects, but all living organisms. at different altitudes in the Banat region. Samples In this context, our research aim is to highlight were collected at weekly interval from a wide the species of coccinellidae fauna present in Entomologicalvariety of habitats: material agricultural that is theland, subject gardens of andthis different habitats in Timis County (Tab. 1). The parks, both on herbaceous and woody essences. composition in species of coccinellidae fauna is largely determined by climatic factors and can study was collected as follows: Gătaia, the first vary greatly from one locality to another. The locality – the experimental field was located microclimate conditions influence through plant on a family farms, the ladybirds collection was density, density of predators, annual changes in made from alfalfa culture; Timisoara, the second abundance of insect species, and differences in locality – the experimental field was represented the rate and time when the population migration by the green spaces between apartment buildings occurs. and parks in town; Jimbolia, the third locality - Insects collected from Timisoara, Gataia, the experimental fields were represented by the Jimbolia and Faget is a typical example of the fields belonging to SC Westland Company SRL, Coccinellacoccinellidae septempunctata fauna present and in westernAdonia variegata Romania. the wheat crop; and the forth locality, Făget - the SeasonalThe first variation species collected in terms from of the the number field were of experimental field was represented by green areas . and wooded areas surrounding the city. The specimens present on herbaceous plants coccinellid species was affected primarily by were collected using a standard entomological net climatic conditions, the density of crops (we refer (on a plot 25 double sweeps for each repetition to alfalfa and wheat), and the availability of food ofwere tree performed, or shrub theyusing were a used 3 repetitions / resources. umbrellas)experience) and– those present on different species In samples collected in period 2013 – 2014 beating tray (Japanese they were identified a total of 427 specimens the collection procedure was Coccinellabelonging septempunctata to 15 species and (n 3 subfamilies (Tab. marking the location, geographical coordinates 1), of which the most abundant species were (using a GPS device), and the name of the tree or = 113) - representsPropylaea shrub species from which was made the insect quatordecimpunctata26.46% of the total (n number of collected collection; for each location (park, green space, insects. Next dominant species was garden) were randomly selected 5 species of trees Adalia bipunctata= 56) ( -n represents = 55) and 13.11% Adonia and shrubs (depending on the availability of the variegataof the total (n collected insects. Dominant species area) that were collected insects. were also The collected ladybirds were taken to labora­ = 57) - represent 12.88%Harmonia and axyridis,12.41% tory. The adults of each species were carefully Adaliaof all insects decimpunctata, collected. Calvia decemguttata, studied under binocular microscope in order CoccinulaFour species quatordecimpustulata of coccinellids ( ) had an to determine the scientific name of the species. medium abundance (n Gender systematic classification of species was Subcoccinella vigintiquatorpunctata, made using phylogenetic sequence by Gordonet al. Chilocorus bipustulatus, Coccinella= 20 – 37), quinquepuncta, while seven (1985), and also using the superior classification Hippodamiaspecies ( tredecimpunctata, Psyllobora after Vandenberg (2002) and Lawrence vigintiduopunctata, Tytthaspis sedecimpunctata (1995). Bulletin UASVM Agriculture 72 (2) / 2015 578 VIRTEIU et al and Chilocorus renipustulatus n = 1 – Adonia ) were rareChilocoris ( variegatacrops, so their presence in fields from Gătaia renipustulatus,12). Coccinella quinquepunctata and and Jimbolia is solely entitled. Species HarmoniaThe adults axyridis of 3 coccinellids species: was more abundant in the Jimbolia area Hippodamia tredecimpunctata and than in Gătaia. Subcoccinella vigintoquatorpunctata were collected only in Timisoara, Comparing the data with those of the literature while 2 species found that coccinelids species identified in the were found 4 studied areas in western Romania coincides belongingin Gătaia. to During the Coccinellidae the growing season of 2013 largely with those found by other authors who and 2014, the larvae of several species of insects studied nearby in Serbia, Hungary and Romania family were seen Coccinella(Lövei, 1981; septempunctata Thalji, 2006, Lisenchi Murariu, feeding on vegetation inCoccinele the area studied,quinquepunctata but they 2008). In the literature studied, the species are not our goal in this research. was regarded as the It is known that species with the highest abundance and frequency prefer woody essences, so its presence only of coccinellid predatory species, as has also been in Timisoara area is explicable, this species demonstrated in this study. Coccinellidae hibernates underAdonia plant variegata debris or and in Hippodamia the edge of Current knowledge on zoogeographical distri­ tredecimpunctataforests. are characteristic of cereal bution of insect species belonging to The species family in western Romania can be considered Tab. 1. Coccinellidae satisfactory.

The insect species belonging to family and the number of specimens collected from the four locality in western Romania, in 2013 - 2014 period Total number Timisoara Gataia

Family Species 7 - Făget2 Jimbolia- of specimen Chilocorus Chilocorus bipustulatus 1 - - - 91 21 12 1 21 55 renipustulatus 5 4 11 2 22 Adalia bipunctata Calvia decemguttata - 7 5 21 Adalia decimpunctata Coccinella 98 - - - 8 Coccinella quinquepuncta 33 27 35 18 113 Coccinula septempunctata - 11 -

37 - - 9- 2037 quatordecimpustulata Adonia variegata 3 17 5 28 53 Harmonia axyridis - 5 - 3 8 Coccinellidae Hippodamia tredecimpunctata 16 31 5 4 56 Propylaea quatordecimpunctata 2 3 - 2 7 Psyllobora vigintiduopunctata - 2 - 3 5 SubcoccinellaTytthaspis sedecimpunctata - 12 - - 12 Total 427 vigintiquatorpunctata

Bulletin UASVM Agriculture 72 (2) / 2015 579

Faunistic Study of Ladybirds (Coleoptera: Coccinellidae) in the Banat Region, Romania General characteristics of coccinellidae

both phytophagous and mycophagous feeding fauna in the studied area is characterized by regime (Tab. 3). et al. zoogeographic point of view as is shown in table 2. et al.Studies by Pembertonet and al. Vandenberg (1993), The chorological categories were made with Hodek (1973, 1996), Moser (2008), Lundgren direct reference to species level and based on a (2009) and Giorgi (2009) suggest that well-structured classification. Zoogeographical species generally regarded as predaceous may distribution is made after Serafim and Maican regularly supplement their basic diet with small (2004). amounts of leaf material even in the presence of As far as chorology is concerned there are abundant prey and water (zoophytophagy). 9 Palaearctic species, 2 cosmopolitan species, 1 Polyphagy also occurs among at least some South – Palaearctic species, a Eurasian species, 1 mycophagouset coccinellidsal. whichet often al. complement andWest food– Palaearctic source specieshas an and immediate 1 Holarctic effect species. on theirSince diet with insects pollen of (Anderson,1982;Coccinellidae Ricci, 1982, Coccinellids species have specific food habits 1986; Ricci , 1983; Giorgi ,2009). Three major categories of feeding habits family shows development. significant differences regarding diet, they can be a good barometer of biodiversity; the species generally are recognized in the areas under study: richness of this family being in close correlation - predation (zoophagy) - 12 species of coccinellids with the overall diversity of fauna. have a zoophagous food regime, 7 of which Most species collected are zoophagous, the consume aphids (aphidophagous), 4 species most numerous being aphidophagous, and some consume aphids and psyllids (Psylla Tytthaspissp.) and a of them consuming psyllids or scale insects, sedecimpunctatasingle species eat only psyllids; having as host hundreds of species of plants, - fungus feeding (mycophagy) - both herbaceous and woody essences. Only a few have a mycophagousSubcoccinella feeding collectingspecies have of a insectsphitophagous from feedingforests regime.surrounding vigintiquatorpunctata,regime; areasIn (F assessingget) has not the meant number a considerable of specimens, source the - Psyllobora plant feeding vigintiduopunctata (phytophagy) - consume plant tissues; ă Tab. 2. species has of ladybugs thatCoccinellidae colonize plant species. Oviposition

Zoogeographical distribution of insect species belonging to family, collected from the four locality in western Romania, in 2013 - 2014 period (region) Timisoara Gataia Zoogeographical distribution Locality Classification South - Palaearctic * * Făget Jimbolia Palaearctic * Chilocorus bipustulatus * * * * Chilocorus renipustulatus Palaearctic * * * * Adalia bipunctata Cosmopolitan Calvia decemguttata Palaearctic * * * Adalia decimpunctata Palaearctic * Palaearctic * * * * Coccinella quinquepuncta Eurasia * * Coccinella septempunctata West - Palaearctic * Coccinula quatordecimpustulata Adonia variegata Palaearctic * * * * Harmonia axyridis Holarctic * * Palaearctic * * * * Hippodamia tredecimpunctata Palaearctic * * * Propylaea quatordecimpunctata Palaearctic * * Psyllobora vigintiduopunctata * Tytthaspis sedecimpunctata

Subcoccinella vigintiquatorpunctata Cosmopolitan Bulletin UASVM Agriculture 72 (2) / 2015 580 VIRTEIU et al

Tab. 3. Feeding habits Coccinellidae

of insect species belonging to family, collected from the four locality in western Romania, in 2013 - 2014 period Feeding habits Classification Mycophagy Aphids Psyllids Zoophagy * Phytophagy * Chilocorus bipustulatus * Chilocorus renipustulatus * Adalia bipunctata Calvia decemguttata * * Adalia decimpunctata * * * Coccinella quinquepuncta * Coccinella septempunctata * * Coccinula quatordecimpustulata Adonia variegata * * Harmonia axyridis * * Hippodamia tredecimpunctata * * Propylaea quatordecimpunctata * Psyllobora vigintiduopunctata * Tytthaspis sedecimpunctata Subcoccinella vigintiquatorpunctata by the hibernating females and larvae survival Coccinellidae species have not been able to is directly correlated with climate changes and maintain a low population level of aphids, but they availability of food source, so a large population representedREFERENCES the largest group of predators. of aphids can sustain a significant number of coccinelide. So, as a conclusion, the ladybugs in lack of food can migrate long distances in search 1. Anderson JME (1982). Seasonal habitat utilization and food of the ladybirds Scymnodes lividigaster and of it.CONCLUSION Leptothea galbula Coleoptera Coccinellidae. Australian Journal of Zoology 30:59–70. 2. Ansari Pour A, Shakarami J (2012). Recognition of The diversity of the coccinellidae fauna ladybirds fauna (Col: coccinellidae) in the alfalfa fields is largely determinate by the evolution of the of Khorramabad. Journal of & Plant Science 22(4):939–943. environmental factors and feeding habits. belonging to Coccinellidae Coccinella 3. Debach P (1974). Biological control by natural enemies. septempunctataThe most abundant species of insects Cambridge University Press, Cambridge family was 4. Giorgi JA, Vandenberg NJ, McHugh JV, Forrester J, Ślipiński (26.46%). ControlA, Miller 51:215–231 KB, Shapiro LR, Whiting MF (2009). The As far as chorology is concerned there are evolution of food preferences in Coccinellidae. Biological 9 Palaearctic species, 2 cosmopolitan species, 1 South – Palaearctic species, a Eurasian species, 1 5. Gordon R (1985). The Coccinellidae (Coleoptera) of West – Palaearctic species and 1 Holarctic species. PragueAmerica North of Mexico. J. Entomol. Soc. 93(1):1–912 Considering the type of diet, they are 12 6. Hodek I (1973). Biology of In Coccinellidae. Academia, zoophagous species, 1 phytophagous species, 1 7. Hodek I (1996). Food relations. : Hodek I, Honek A (Eds.), mycophagousSince insects species of Coccinellidaeand 1 species feeds both on Ecology of Coccinellidae. Kluwer Academic Publishers, plants and fungus. Dordrecht, 143–238 pp. family shows 8. Jafari R, Fursch H, Zarei M (2013). A checklist of significant differences regarding diet, they can be the Scymninae (Coleoptera: Coccinellidae) of Iran. a good barometer of biodiversity. International Research Journal of Applied and Basic Sciences 4(12):4055–4061 Bulletin UASVM Agriculture 72 (2) / 2015 581

Faunistic Study of Ladybirds (Coleoptera: Coccinellidae) in the Banat Region, Romania Larval feeding on

9. Khormizi Zare M, Biranvand A, Shakarami J (2013). The 18. Moser SE, Harwood JD, Obrycki J (2008). faunistic survey of lady beetles (Coleoptera, Coccinellidae) bt hybrid and non-bt corn seedlings by Harmonia axyridis in the Mehriz region (Yazd Province), Iran. Bull. Iraq nat. 37:525–533(Coleoptera: Coccinellidae) and Coleomegilla maculate Hist. Mus. 12(4):43–51 (Coleoptera: Coccinellidae). Environmental Entomology 10. Lawrence JF, Newton AF (1995).In Families and subfamilies of Coleoptera (with selected genera, notes, references and 19. Pemberton RW, Vandenberg NJ (1993). Extrafloral nectar data on family-group names). : Pakaluk J, Slipinski SA feeding by ladybird beetles (Coleoptera: Coccinellidae). (Eds.), Biology, phylogeny and classification of Coleoptera: Proceedings of the Entomological Society of Washington papers celebrating the 80th birthday of Roy A Crowson. 95:139–151 Volume 2. Museum i Instytut Zoologii PAN, Warsaw, 779- 20. Ricci C (1982). Sulla constituzione e funzione delle 1006 pp. mandible delle mandiboile delle larvae di Tytthaspis 11. Lisenchi Murariu Camelia, Andriev Sorina Octavia (2008). sedecempunctata (L.) e Tytthaspis trilineata (Weise). The biodiversity of ladybirds (Coleoptera: Coccinellidae) Frustula Entomologica 3:205–212 in some alfalfa crops from the north of Moldavia. Analele 21. Ricci C, Fiori G, Colazza S (1983). Regime alimentare Științifice ale Universității „Al. I. Cuza” Iași, s. Biologie dell’adulto di Tytthaspis sedecimpunctataIn: Proceedings XIII (L.) animal, tom LIV (Coleoptera: Coccinellidae) in ambiente a influenza 12. Lövei GL (1981). Coccinellid community in a apple orchard antropica primaria: prato polifita. bordering a Deciduous forest. Acta Phytopathologica Congresso Nazionale Italiano di Entomologia, Instituto di Academiae Scientiarum Hungaricae 16(1-2):143–150 Entomologia Agraria e Apicoltura, Università di Torino, 13. Lundgren JG (2009). Relationships of Natural Enemies Turín, 691–697 pp. and Non-prey Foods. Springer International, Dordrecht 22. Ricci C (1986). Food strategy of Tytthaspis sedecimpunctata 14. Majerus MEN (1994). Ladybirds. Ed. Harper Collins (L.) in different habitats. In: Hodek I (Ed.), Ecology of London, 359 pp. Aphidophaga. Proceedings of a SymposiumContributions held at Zvíkovské Podhradí. Academia, Prague, 211–216 pp. 15. Majka CGIn & McCorquodale DB (2010). Ladybird beetles (Coleoptera: Coccinellidae) of the Atlantic Maritime 23. Serafim Rodica și Maican Sanda (2004). Ecozone. Assessment of Species Diversity in the Atlantic to the knowledge of the coleopterans, from the littoral of Maritime Ecozone. Ed. DF McAlpine and IM Smith. NRC the Black Sea (Romania), Travaux du Musdurn National Research Press, Ottawa, Canada, 436–452 pp. d’Histoire Naturelle ct Grigore Antipa XLVIl:169–210 16. Michels GJ (1987). A checklist of the coccinellidae 24. Thalji R (2006). Composition of Coccinellid Comunities in Suger Beet Fields in Vojvidina. Proc. Nat. Sci. 110:267– (coleoptera) of Wyoming. The Coleopterist BulletinIn: In 41(3):249–255 273, Matica Srpska Novi Sad 17. Moreton BD (1969). Ladybirds and spider mites. 25. Vandenberg NJ (2002). CoccinellidaeEdited by Latreille 1807. Beneficial insects and mites. Her Majesty, Stationary American Beetles. Volume 2. Polyphaga: Scarabaeoidea Office London. Ministry of Agriculture, Fisheries and through Curculionoidea. RH Arnett Jr, MC Food. Bulletin 20:15– 20 Thomas, PE Skelley and JH Frank. CRC Press, Boca Raton, 371–389 pp.

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