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ZLATICE (COLEOPTERA: CHRYSOMELIDAE) PLANINE FRUŠKE GORE (VOJVODINA, SJEVERNA SRBIJA), SA PREGLEDOM BILJAKA HRANITELJICA
LEAF BEETLES (COLEOPTERA: CHRYSOMELIDAE) OF MT. FRUŠKA GORA (VOJVODINA PROVINCE, NORTHERN SERBIA), WITH AN OVERVIEW OF HOST PLANTS
Bojan GAVRILOVIĆ, Branka GAVRILOVIĆ, Srećko ĆURČIĆ, Dejan STOJANOVIĆ, Dragiša SAVIĆ
Abstract
Leaf beetles (Coleoptera: Chrysomelidae) have not been sufficiently studied in Serbia so far. The species of the family were investigated in a protected area – the Fruška Gora National Park (Vojvodina Province, Northern Serbia) over the period of 11 years (2001–2011). Mt. Fruška Gora is an isolated island mountain in the Pannonian Plain and is characterized by a complex assembly of forest, meadow, shrubby, grassland, cultivated land, wetland, and aquatic phytocenoses. At total of 99 chrysomelid species from 42 genera and 11 subfamilies were identified from the area. The data on nutritional preference of the found Chrysomelidae species and host plants are given by own observations in nature. Furthermore, economically important leaf beetle species (i.e., forest and crop pests) are identified and briefly discussed as well. The registered species can be classified into seven chorotypes of Holarctic and three chorotypes of Europe according to zoogeographical analysis.
KEY WORDS: Chrysomelidae, Serbia, diversity, trophic associations, distribution
Introduction
Uvod
Family Chrysomelidae is one of the largest phytophagous groups of order Coleoptera. More than 38000 species and 2500 genera have been known so far (Seeno & Wilcox 1982). According to some assumptions their number is far greater, more than 60000 species worldwide (Suzuki 1996). The Catalogue of Palaearctic Coleoptera mentions the existence of 28560 taxa of Chrysomeloidea (Löbl & Smetana 2010). Today, modified classification system proposed by Seeno & Wilcox (1982) is the most utilized, according to which the family Chrysomelidae is composed of 20 subfamilies (Suzuki 1996). Because of the phylogenetic relatedness Bruchinae are sometimes treated as a subfamily within the family Chrysomelidae (Reid 2000; Farrell & Sequeira 2004).

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Chrysomelidae fauna in Serbia is relatively poorly studied. Only a small number of faunistic papers have been published for the group as a whole or some of its subfamilies inhabiting Serbia. Most attention has been paid to leaf beetle species that have a certain economic importance (Živojinović & Tomić 1956; Nonveiller 1960; Jovanić 1962; Živojinović 1963). So far, 415 species of leaf beetles from 74 genera and 13 subfamilies are known to inhabit the territory of Serbia (Gavrilović & Ćurčić 2011, 2013; Stančić 2013). A survey of the leaf beetle fauna of Mt. Fruška Gora was given by Груев (1984, 1986). He noted the presence of 51 species from 18 genera and 4 subfamilies.
Mount Fruška Gora is an imposing orographical element in the relief of Autonomous Province of Vojvodina (Northern Serbia). The area of the entire mountain is around 500 km2, while the area of the region higher than 150 m a.s.l. is around 1160 km2 (Ćurčić 2007). To the north the terrain slopes gently downward toward the Danube River. Since 1960 Mt. Fruška Gora is a national park. Today, the national park covers the area of 25393 ha. The highest part of the mountain range is under primary forest vegetation, while western and eastern regions lack the original natural vegetation. Forests remain intact only in certain areas, but other parts of the mountain are covered by grass and bush vegetation and agricultural fields.
Primary objective of this study is to present the diversity of fauna of the family Chrysomelidae (excluding Bruchinae) of the Mt. Fruška Gora. Given that Serbian leaf beetle fauna is insufficiently surveyed we predict that this locality would yield new taxa and new trophic associations. Observing insect feeding in natural conditions is a good way to improve our knowledge of species biology. Bordering the Pannonian Basin on one side and mountainous region of the central parts of the Balkan Peninsula on the other, it is expected that characteristic position of Mt. Fruška Gora would show a specific species composition from different zoogeographical regions.
Materials and Methods
Materijal i metode
Analysed leaf beetle material had been collected from 2001 to 2011. Insects were collected every year, from the end of March until the beginning of November, depending on weather conditions and outdoor temperature. In order to identify host plant species and to observe the feeding of larvae and imagines collecting was mostly done by hand or using an aspirator. Entomological net was used for collecting of species that can fly or quickly get away. On meadows and fields, where one or several plant species were dominant, sweeping method was used. A beating tray was satisfactory method for collecting tree- and bush-dwelling species.
Insects were killed in killing bottles by ethyl acetate, diethyl ether was also used to a lesser extent. Imagines are stored as dry preparations on entomological pins or glued on sample cards in the private collection of the first author. Stereomicroscope Carl Zeiss STEMI 2000-C with independent lighting Schott KL1500 LCD was used for analysing the material. Material identification was done using the keys by Warchalowski (2003), Bieńkowski (2004), Winkelman & Debreuil (2008) and Debreuil (2010).
Trophical relationships between Chrysomelidae and their host plants were identified on the basis of damages to vegetative and floral parts and the presence of numerous specimens of larvae and imagines. Only host plants from which the insects were collected are presented in this study. Economically important species of Chrysomelidae are particularly singled out. Identification of plants was done using herbarized material and photographs taken in the field. Plant identification was done using the keys by Josifović (1970–1977), Sarić & Diklić (1986) and Sarić (1992).
Leaf beetles were collected from more than 35 localities in the area of Mt. Fruška Gora (Table 1). These localities represent habitats with different types and different composition of vegetation: region along the Danube River, wet meadows, willow (Salix spp.) and poplar (Populus spp.) forests, grasslands with elements of steppe and shrub-steppe plants, a zone of shrubs bordering forests, forests of various compositions, forest clearings, stream valleys, lakes, mountain peaks, numerous agricultural fields and plantations, etc. Using the GPS device Garmin Dakot 20, precise locations were determined on which the insect specimens were collected.
General distributional data are included, together with species distribution details on Mt. Fruška Gora. Using the information on general geographical distribution of each species, the zoogeographical distribution was determined. World distribution and zoogeographical analysis is given for all collected species (Warchałowski 2003; Беньковский 2011; Audisio 2013). Geographical distribution is expressed through chorotype association. Chorotype classification according to Vigna Taglianti et al. (1999) was used. Each species is placed within one of the chorotypes of Holarctic and Europe.
Results
Rezultati
In the area of Mt. Fruška Gora the presence of 99 species from 42 genera and 11 subfamilies from the family of Chrysomelidae have been identified (Table 1). Chrysomelinae are represented by 23 species from 10 genera (23.23% of the total number of registered species), while Alticinae include 22 species from 10 genera (22.22%).

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Sažetak
Zlatice (Chrysomelidae) za sada nisu dovoljno dobro proučene u Srbiji. Vrste ove obitelji istraživane su tijekom razdoblja od 11 godina (2001–2011) u zaštićenom području – Nacionalnom parku "Fruška gora". Planina Fruška gora je izolirana otočna planina u Panonskoj nizini, koju karakterizira kompleksni sklop šumskih, livadskih, žbunastih, travnatih, kultiviranih, močvarnih i vodenih fitocenoza. Kukci su prikupljeni sa 35 lokaliteta, odnosno različitih tipova staništa. Ukupno 99 vrsta zlatica iz 42 roda i 11 podobitelji identificirano je iz ovoga područja. Zajedno s rezultatima Grueva (1984, 1986), koji je vršio ranija istraživanja, fauna zlatica obuhvaća 135 vrsta iz 46 rodova i 11 podobitelji. Podobitelji Chrysomelinae i Alticinae obuhvaćaju najveći broj vrsta. Podaci o ishrani i biljkama hraniteljicama prikupljenih Chrysomelida dobiveni su na osnovi vlastitih zapažanja u prirodi. Zlatice su prikupljene sa 128 vrsta biljaka iz 84 roda i 26 obitelji. Većina je asocirana s biljkama klase Magnoliopsida. Gospodarski važne vrste zlatica (štetnici šuma i usjeva) identificirane su i kratko spomenute. Prema zoogeografskoj analizi registrirane vrste mogu se svrstati u sedam horotipova Holarktika i tri horotipa Europe. Velik broj vrsta ima široku distribuciju u Europi, ali su brojne i zapadnopalearktičke i euroazijske vrste. Zabilježeno je devet vrsta koje se tipično javljaju u brdsko-planinskim regijama.
Ključne riječi: Chrysomelidae, Srbija, bioraznolikost, trofičke asocijacije, distribucija

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Cryptocepha­linae are represented by 15 species from 2 genera (15.16%), Clytrinae include 13 species from 5 genera (13.13%), Cas­si­dinae were present with 10 species from 3 genera (10.10%), Criocerinae contain 6 species from 4 genera (6.06%) and Galerucinae include 6 species from 4 genera (6.06%). Subfamilies Donaciinae, Eumolpinae, Hispinae and Orsodacninae are represented by one species each (1.01% each).
Leaf beetles were collected from 128 plant species from 84 genera and 26 families. Of these plants, 110 species from 69 genera and 19 families belong to class Magnoliopsida, while 18 species from 15 genera and 7 families are from class Liliopsida. From the total number of collected leaf beetles, 90 species from 35 genera and 9 subfamilies were caught on plants belonging to Magnoliopsida, and 9 species from 7 genera and 4 subfamilies were found on Liliopsida (Table 1).
Discussion
Rasprava
In relation to the results by Груев (1984, 1986), who last researched the Chrysomelidae fauna of Mt. Fruška Gora, a far greater number of species, genera and subfamilies were found in our research. Груев (1984, 1986) listed the existence of 51 species from 18 genera and 4 subfamilies. However, presence of 36 of these species (26 species of Alticinae, 3 species of Cassidinae and 7 species of Chrysomelinae) was not confirmed in our study. Together with Груев’s results, leaf beetle fauna of Mt. Fruška Gora incorporates 135 species from 46 genera and 11 subfamilies. Fauna Europaea lists the species Cryptocephalus decemmaculatus (Linnaeus, 1758) as distributed within the territory of the former country Serbia and Montenegro, but without detailed information (Audisio 2013). Records of this species on Mt. Fruška Gora confirm its presence in Serbia.

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The composition of the Chrysomelidae fauna of Mt. Fruška Gora is tightly linked with phytocenoses present in this region. Diversity of habitats and vegetation mostly influence those species that have specialized diets, but also to a lesser extent polyphagous species and those with ecological preferences (e.g., species that feed on aquatic plants). Due to high anthropogenic influence on Mt. Fruška Gora, many habitats are fragmented and leaf beetles are distributed somewhat mosaicly. Agricultural fields are, like isles, suitable for species that otherwise would not occur in the surrounding vegetation.
Among the leaf beetle species collected from Mt. Fruška Gora, a small number of them have an economic importance damaging agriculturally important plants. Chaetocnema tibialis (Illiger, 1807) is a pest of sugar beet (Nonveiller 1960; Sekulić et al. 2002). During this research on the southern slopes of Mt. Fruška Gora during spring imagines were seen to perforate leaves of sugar beet and spinach plants, usually in large numbers. Gonioctena fornicata (Brüggemann, 1873) occurs as a pest of certain fodder crops (György et al. 2007). Species was most often caught on Medicago sativa L. and Trifolium pratense L. Leptinotarsa decemlineata (Say, 1824) is a serious pest of Solanum tuberosum L. Widely distributed in the region of Vojvodina (Gavrilović & Ćurčić 2011), this species was regularly observed mostly on potatoes and other solanaceous plants (Solanum spp.). Oulema melanopus (Linnaeus, 1758) is a pest of cereals (Tanasković et al. 2012). It was found everywhere on Mt. Fruška Gora, doing most damage on fields of Triticum aestivum L., Zea mays L. and Hordeum vulgare L. Lilioceris merdigera (Linnaeus, 1758) occurred only locally on onions (Allium cepa L., A. sativum L.), damaging plant leaves only superficially.
Some species found during this study are known to occur as forest pests. Altica quercetorum Foudras, 1860 damages oak trees of different ages. Infestations have been recorded in central and southern parts of Serbia (Glavendekić 2000; Mihajlović 2008). Chrysomela populi Linnaeus, 1758 and C. vigintipunctata Scopoli, 1763 are one of the most important pests of poplar and willow cultivars in Serbia (Plavšić 1958). Phratora vulgatissima (Linnaeus, 1758) was observed damaging poplar sapling leaves in tree nurseries. Lachnaia sexpunctata (Scopoli, 1763) can inflict negligible damage to new buds and young leaves of Quercus spp., Betula pendula Roth, willows and poplars. Galerucella lineola (Fabricius, 1781) is a pest of willows, poplars, Alnus spp. and Corylus spp. This species normally feeds on plants from the family Salicaceae, but outbreaks or any significant damage to the trees were not observed (Mihajlović 2008).
A great number of the collected species have very wide distribution (Table 1). Most numerous are those whose distribution area encompass Eurasia to Himalayas. Among the analysed species, 11 of them belonging to Holarctic chorotype have an economic importance. Of these 11 species, 7 are treated as pests [Lilioceris lilii (Scopoli, 1763), Oulema gallaeciana (Heyden, 1879), O. melanopus (Linnaeus, 1758), Phaedon cochleariae (Fabricius, 1792), Phratora vulgatissima (Linnaeus, 1758), Phyllotreta striolata (Fabricius, 1803), Galeruca tanaceti (Linnaeus, 1758)], while 4 are used as biocontrol agents [Aphthona flava Guillebeau, 1894, Cassida rubiginosa Müller, 1776, Galerucella calmariensis (Linnaeus, 1767), Gastrophysa polygoni (Linnaeus, 1758)] in various biological control programs against weed plants (Lym 1998; Kok et al. 2000; Ulrich et al. 2004; Grevstad 2006; Petrova et al. 2006; Roditakis & Roditakis 2006; Majka & LeSage 2008; Lee et al. 2011).
Because of its height, Mt. Fruška Gora is a suitable habitat for species that prefer high altitude conditions of hilly and mountainous environments. Nine species found have such a preference (Table 1). Altitude and vegetation cover have a great impact on composition and distribution of leaf beetle fauna in such a way that this area is inhabited by certain hilly and mountainous species, but also the species characteristic to shrub-steppe ecosystems. Wetland vegetation that is distributed along the banks of the Danube River is populated by a specific leaf beetle fauna.
The species of Chrysomelidae identified from Mt. Fruška Gora are classified into 7 chorotypes of Holarctic (Eurasian, Palaearctic, West Palaearctic, Holarctic, Eurosiberian, Centralasian-Euro-Mediterranean and Euro-Mediterranean) and 3 chorotypes of Europe (European, Central European and South European). Two species have a subcosmopolitan distribution each [Leptinotarsa decemlineata (Say, 1824) and Lilioceris merdigera (Linnaeus, 1758)] (Table 1).
In the surveyed area elements of the leaf beetle fauna from different zoographical regions of Europe and Asia come into contact with each other and intertwine. Mt. Fruška Gora represents a northern extension of the Dinarides range, and is positioned in the southern part of the Pannonian Basin. The mountain is a transitional area where different regional relief characteristics, hydrological and climatological patterns combine (Ćurčić, 2007). Numerous species collected during this study typically occur in central and southern parts of Europe and the Mediterranean region. Typical Eastern European species were not found, but there are many species with the distribution in Asia that reach eastern parts of Europe and the Balkan Peninsula.
Conclusions
Zaključci
Number of species and genera of leaf beetles on Mt. Fruška Gora exceeds that found in the former studies. Subfamilies Chrysomelinae and Alticinae contain the greatest number

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