Cent. Eur. J. Biol. • 8(10) • 2013 • 1032-1047 DOI: 10.2478/s11535-013-0225-6

Central European Journal of Biology

Alien invasive neophytes of the Southeastern part of the Pannonian Plain

Research Article

Goran T. Anačkov1,*, Milica M. Rat1, Boris Dj. Radak1, Ružica S. Igić1, Dragana M. Vukov1, Marko M. Rućando1, Mirjana M. Krstivojević1, Snežana B. Radulović1, Dušanka Lj. Cvijanović1, Dubravka M. Milić1, Biljana I. Panjković2, Klara L. Szabados2, Ranko D. Perić2, Alen M. Kiš2, Vida R. Stojšić2, Pal P. Boža1

1Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, 21000 Novi Sad, Serbia

2Institute for Nature Conservation of Vojvodina, 21000 Novi Sad, Serbia Received 11 December 2012; Accepted 14 June 2013

Abstract: Floristic diversity in the Pannonian Plain is the result of mosaic habitat composition, characterized by steppes, saline meadows, and lowland forests along major rivers. In the last few centuries, the flora has become enriched by species introduced by human activities, such as colonization and industrialization. Presently it consists of nearly 1800 species. As a result of 30 years of field research as well as herbarium and literature searches, a list of invasive alien neophytes has been compiled and is presented here. The list includes 152 species, classified as either naturalized, casual, or unknown. One of the species is listed in Red Bookof Serbian Flora. Eighty species are naturalized, and 61 are casual species. The majority of the introduced flora originates from North America (66) and the Old World (43). Most alien of the Southeastern part of the Pannonian Plain, were introduced accidentally by seed material or deliberately by nursery saplings. The annual and perennial herbaceous , which flower in the summer and summer-autumn periods, are represented in the greatest numbers. The alien flora was further analyzed with respect to , life forms, pollination, and seed dispersal mode. The greatest number of alien species appears in anthropogenic and semi-natural habitats (59). In natural habitats, 45 invasive taxa were recorded, representing a conservation threat to biodiversity.

Keywords: Invasive flora • Species biology • Distribution • Central Europe • Pannonia © Versita Sp. z o.o.

1. Introduction Studies on invasive species in the Pannonian region of Serbia are exceeding the national and local The problem of alien invasive species has become one character from several (geographical, biogeographical) of the most important issues in conservation biology in standpoints. The region occupied by the state of Serbia the last several decades. Invasive species are presently includes several biogeographical units for studying the recognized as the second most important cause of presence, degree of acclimatization, and negative impact biodiversity loss, after habitat destruction [1]. Studies imposed on natural habitats by these species. The region on invasive species, their biology, ecology, and of Pannonian Serbia (Autonomous Province of Vojvodina) distribution, as well as methods of suppression and belongs to the region of Central Europe from geographic, estimates of the negative economic impact and impact historical, and ethnic standpoints. Any analyses of foreign on human health, floristic and vegetation diversity, have plants in Central Europe would be seriously lacking if they been increasingly investigated during the last 40 years fail to include data from Pannonian Serbia. [2]. The first analysis of invasive species in Europe was The latitudinal position of Serbia is one of the main performed in the late 20th century, and included the first reasons for the irregular distribution of alien plant data for the former Yugoslavia with 142 alien species, out species in the Pannonian region of Serbia. The northern of which 108 are of non-European origin [3]. part of Serbia, which is administratively designated as

* E-mail: [email protected] 1032 G.T. Anačkov et al.

the Province of Vojvodina, geographically belongs to The systematic recording of flora in the studied Pannonian Plain region in the southeastern part of area of the southeastern part of Pannonian Plain has Central Europe. It is separated from the southern part a long tradition. The first data are from the 18th century of Serbia, which belongs to the Balkan Peninsula, by [7]. However, until the 1970s the alien species were the large Sava and Danube rivers. The Pannonian often cited as an element leading to “enrichment region of Serbia is geographically situated along the of autochthonous flora”. The first studies where northern border of the Balkan Peninsula, which is allochthonous flora were viewed as having a negative drained by several large rivers (Danube, Sava, Drina, impact on agricultural habitats and yield of cultivated and Morava). These river networks connect Central plants in Serbia were first published during the 1970s Europe with the Adriatic, Aegean, Ionian, and Black [8,9]. seas. This geographic separation correlates with Studies of the phenomenon of “biological invasion” biogeographical units characterized by climate-zonal were initiated in the Pannonian biogeographical region dominant vegetation, which in the region of Pannonian of Serbia during the last decade of the 20th century Serbia belongs to the forest-steppe zone characteristic [10] with the recognition of the impact of allochthonous for the Pannonian Plain [4], dominated by herbaceous flora on natural habitats, gradually leading to changes vegetation of the class Festuco-Brometea. From in composition of plant associations and threats to a historical standpoint, these two areas previously survival of rare edificator species in natural habitats. belonged to different state-historical units until the Considering the importance of understanding and beginning of the 20th century, influencing the everyday systematic monitoring of the spread of invasive life, culture, economics, and agriculture. Pannonian species, the first step toward inclusion of the southern Serbia is a region exclusively oriented toward mass part of the Pannonian Plain into the Pan-European production of cereals and oil-source plant cultures, initiative battling against this type of disruption of industrial plants, and also partially vegetables and fruit. natural assets (this area is not included in international Therefore it has been under intensive anthropogenic lists of invasive species, DAISIE, etc.) is the creation influence for several centuries. It is important to note of a list of invasive alien plant species and recording that in the region of the former Yugoslavia, the end their distribution, degree of adaptation, and period of 20th century was characterized by generally poor of introduction within the study area. However, until economic conditions, and this situation influenced the 2010 there were no lists pertaining exclusively to alien efficiency and degree of agro-technical measures used species. The first set of combined data is coincided at the time in spacious cereal-sown fields. Due to these with the publication of the open access Internet historical factors, our understanding of alien floras in database “List of alien species in Vojvodina”, which Europe includes knowledge on invasive alien species included vertebrates, invertebrates, fungi, algae, and in the current study area as one of the potential starting higher plants. This list was compiled primarily from the points for of their spread of invasive alien species. literature and zoological and herbarium collections. The A challenging factor in the systematic study of invasive first preliminary version of this list was created by 30 species is categorization of species as archaeophytes or national experts, and is available at http://iasv.dbe.pmf. neophytes, as well as categorization into weed species uns.ac.rs. This first version did not include all taxa, and or other species. On the other hand, it has been proven the collected data were not subjected to any analysis. that alien flora is are more similar in different habitats of In the present paper, the previous electronic version of the same biogeographical units than in similar habitats in the list of alien plant species was supplemented with different biogeographical units [5]. A related problem is data for additional species. For the first time, invasive the introduction of Mediterranean and Submediterranean the alien flora of the study area was analyzed from in species into Pannonian Serbia, causing confusion in terms of taxonomy, habitat disturbance, native range, the classification of certain taxa that are autochthonous introduction mode, and biological and ecological species in the hill-mountain area of Serbia (particularly in characteristics. its Submediterranean part), but are alien species in the northern Pannonian area. It is also important to note the problem in categorization of certain taxa in all countries 2. Experimental Procedures (and especially those in the Balkan region) that appear in more than one biogeographical unit. This fact was pointed 2.1 Investigation area out in a similar study that considered invasive species The study area includes the part of the Pannonian in anthropogenic vegetation type in the northwestern Plain eastward from the Danube River (Figure 1). The Balkans [6]. northern boundary is represented by the Subotica-

1033 Invasive neophytes of Pannonian Plain

Figure 1. Location of the study area (green) in Europe and in the Republic of Serbia (https://maps.google.com).

Horgoš Sands, the eastern boundary by the saline flats 2.2 Data collection and list creation of Western Banat, and the extreme southwestern part of This list only includes species introduced by human the Carpathian mountain range (Vršačke Planine), while activity, whether deliberately or accidentally, and the southern boundaries are the Danube and Sava species that spread from other parts of Europe where rivers. This territory has a surface area of 21.506 km² they were introduced by human activity (i.e., Abutilon and is situated between 44°38’ and 46°10’ of northern theophrasti Medik., Elodea nuttallii (Planchon) St latitude and 18°10’ and 21°15’ of eastern longitude. The John.). The invasive taxa for this list is comprised only southern part of the Pannonian Plain ranges in altitude of invasive taxa [12,13] out of 1800 recorded plant between 70 and 641 m above sea level, with almost species in the investigated area (unpublished data). 90% of territory is lowland in altitude range (70-140 m) Naturalized “non-invasive” taxa are not included in [11]. the list. All taxa in this list belong to neophytes - plants The dominant substrate is loess with elements of introduced to the study area after the year 1500, clay, alluvial deposits in valleys of large rivers, and creating stable populations not dependent on humans. two sand flat areas, including the Deliblato Sands in Species of unknown introduction time that are certainly the southern part of the study area, the largest sand invasive alien species are included in the list. The flat area in Europe. As an intensively agrarian region, naturalized species with no known introduction date or the study area was inhabited from the earliest times data for other countries in the region and Europe were and has a long history of being a transit area. It is assumed to be archaeophytes and are not included in characterized by well-developed road and railway the list. Species native to one biogeographical part of networks, as well as by a channel network system Serbia, but alien in the Pannonian part are included connecting two large rivers (Danube and Tisa) with in the list with a note on their “alien region”. Species smaller watercourses. This territory includes a large recorded once, whether still present or now extinct, number of settlements (466) and individual ranch units are included in the list. This list includes data from (homestead) spread throughout the agrarian zone. All the literature for a period of over 150 years as well as these characteristics have greatly contributed to the data from herbarium collections (BUNS Herbarium and introduction and rapid spread of alien species within Herbarium of the Institute for Nature Conservation of the study area. Vojvodina in Novi Sad).

1034 G.T. Anačkov et al.

2.3 Taxonomy, nomenclature, native range, literature based on the investigations in the Pannonian and mode of introduction Plain [12,22,23]. The taxonomic status of each species was matched with DAISIE (Delivering Alien Species Inventories for 2.5 Criteria for determining the current status Europe, the database on invasive species for the wider of species European area) [14], as well as Med-Checklist [15] and The status and degree of invasiveness for each taxon were relevant floras: Flora of Europe and Flora of Serbia determined according to the present distribution, date [16-20]. Data from relevant floras were also used in of introduction(s), pathway, abundance, and frequency. order to define the origin and distribution of each taxon. Invasive neophytes were defined as naturalized, casual, The position of species within certain families was and with insufficient data. The naturalized species were determined according to Takhtajan’s phylogeny system defined as alien plants that reproduce consistently and [21]. Data on modes of introduction were collected sustain populations over many life cycles without direct during several decades of research on flora, including intervention by humans (or in spite of human intervention); literature review [12,18-20,22,23] and herbarium material they often recruit offspring freely, usually close to adult (BUNS). Floristic data for the investigated region were plants [13,27], and do not necessarily invade natural, recorded in many papers and monographs from the 18th semi-natural or human-made ecosystems. Species with and 19th centuries (cc. 800), including data on mode and casual status are alien plants that may flourish and even purpose of introduction of certain species into the region. reproduce occasionally in an area, but which do not form self-replacing populations, and instead rely on repeated 2.4 Biological characterization of species introductions for their persistence [13]. In the casual The biological characteristics of taxa were analyzed taxa are grouped all species which are recorded in the according to the following parameters: growth form, field with observation of intensive adaptation. Intensive life form, life cycle, period of flowering, pollination, adaptation is defined through the following features: and seed dispersal. The growth form types include continuously reported from new habitat types with a shift herbaceous plants, lianas and creeping plants (referred from rural and anthropogenic habitats (firstly inhabitant to as lianas in this study), shrub forms, trees, and the locality) to colonization of semi-natural and non-disturbed transitional form between shrubs and low trees. The life (natural) habitats. These observations were conducted forms were defined according to Raunkier [24], adapted during the last 30 years. All other taxa (recorded only according to Ellenberg and Mueller-Dumbois [25], and once or presently considered extinct in spite of being further for Flora of Serbia by Stevanović [26]. The life previously recorded at one or more localities) have the cycle includes annual, biennial, and perennial plants, status “insufficient data” or “unknown”. as well as plants with a transitional type of life cycle. The flowering periods include following seasons: spring, 2.6 Habitat classifications summer, and autumn, as well as the transitional types: Each species was categorized according to habitat in spring-summer, spring-autumn, and summer-autumn. accordance with the EUNIS list of habitats (available at: For all species data on life cycles, flowering and fruiting http://eunis.eea.eu.int/index.jsp) based on the literature were taken from the literature [12,18-20,22,23]. These data and field observations, up to level 3. For the data were harmonized with data obtained by analyses purpose of this paper and basic analysis, all recorded of herbarium specimens and authors’ field studies. The habitats were grouped as 1) anthropogenic, 2) semi- pollination and dispersal mode data were taken from natural, and 3) natural habitats (Table 1).

Habitats group EUNIS habitats codes*

FA.1, FA.3, FA.4, FB.3, FB.4, G1.C, G1.D, G5.1, G5.2, G5.6, G5.7, G5.8, I1.1, I1.2, I1.3, I1.5, I2.1, I2.2, I2.3, J1.1, J1.2, Anthropogenic J1.3, J1.6, J2.1, J2.2, J2.4, J2.6, J2.7, J3.2, J4.1, J4.2, J4.3, J4.5, J4.6, J4.7, J6.1, J6.2, J6.3, J6.4, J6.5

Semi-natural F3.2, F3.3, F9.2, F9.4, G1.1, G1.2, G1.4, G1.6, G1.7, G1.8, G1.A, C3.4, C3.8, D5.1, D5.2, E1.2, E1.6, E2.6, E2.7, E3.4

Natural C3.1, C3.2, C3.3, C3.5, C3.6, C3.7, E1.1, E1.7, E2.5, E4.2, E6.2

Table 1. Classification of habitat groups in correspondence with EUNIS codes at level 3.

(C – Inland surface waters; D – Mires, bogs and fens; E – Grasslands and lands dominated by forbs, mosses and lichens; F – Heathland, scrub and tundra; G – Woodland, forest and other wooded land; I – Regulary or recently cultivated agricultural, horticultural and domestic habitats; J – Constructed, industrial and other artificial habitats; *http://eunis.eea.eu.int/index.jsp)

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3. Results eight taxa from Eastern Asia and Eurasia (with ranges including Eastern and Southern Europe, and Central, Analysis of literature, herbarium collections, and field Southern, Western, and Southwestern Asia). A group work on the flora of the Pannonian Plain in Serbia has formed by three taxa originated from the Mediterranean revealed the presence of 152 alien invasive neophyte area (parts of Africa, Asia, and Europe), and four taxa had taxa (Supplement). Of this total, there were only 11 Africa origins. For Europe, 22 species were native. These taxa with status unknown, meaning they were either taxa originate from Southern Europe, the Mediterranean recorded only once or are thought to be extinct in the biogeographical region (18), and Southeastern Europe study area. The remaining taxa were either naturalized (4). Two taxa originate from the region of Australia and (80) or casual (61). Oceania. No precise origin could be determined for six taxa, as they have been farmed for centuries in various 3.1 Taxonomic analysis parts of the world and there are no precise data on The alien invasive flora of Pannonian Serbia includes their origins. This group includes cosmopolitan species taxa from three divisions: Polypodiophyta, Pinophyta, belonging to neophytes of the study area. and Magnoliophyta. Division Polypodiophyta is represented by two species of aquatic ferns of genus 3.3 Mode of introduction Azolla L., while the only species of division Pinophyta There were two types of species introduction into the with a status of invasive alien species is Pinus nigra Pannonian Plain by human interference. Most species Arnold. The remaining taxa (149) belong to division were introduced by seed material and nursery saplings Magnoliophyta, with 128 taxa in the class Dicotyledones (Table 2). The taxon Abutilon theophrasti Medik. (84% of analyzed taxa) and 21 taxa in the class was not brought directly by human activity, but was Monocotyledones. Together, all taxa spanned 49 first introduced to Western Europe and then spread families and 103 genera (Supplement). spontaneously into other areas. Most deliberately Families with the greatest number of represented introduced species have the status of naturalized taxa were: Asteraceae (31), Poaceae (14), species (41), similar to accidentally introduced species (10), (9), and Amaranthaceae (8). The (13) and species with an unknown way of introduction greatest number of naturalized taxa were found in the (26). Alien plants with casual status are of the great families Asteraceae (16) and Poaceae (7). Certain importance in this study, since they were extensively families (Azollaceae, Convolvulaceae, Oenotheraceae, represented both by deliberately introduced speces (28) Oleaceae) had a greater number of recorded taxa, and species with unknown modes of introducion (30). all of which were naturalized. Other families were From a conservation point of view, these groups pose a represented by a smaller number of taxa. Of these less potential threat to natural habitats. diverse families, 25 were represented by single taxon each, and are here combined into the group “other” 3.4 Biological characteristics (Figure 1), but most of them were naturalized (13) and The annual and perennial plants flowering in the summer there were only two with unknown status. Genera with and in summer-autumn periods were represented the greatest number of recorded taxa were Amaranthus Introduction Number L. (8), Chenopodium L. (5), Oenothera L. (4), and Introduction pathway mode of species Symphyotrichum Nees (4). accidentally other part of Europe* 1

3.2 Native range accidentally most probably with other seed material 59 Alien species of the flora of Pannonian Serbia have intentionally escaped from gardens, parks, yards 50 originated from all continents except Antarctica (Supplement). The greatest numbers of alien species intentionally planted for industry 3 have American origins. There were 66 taxa that originate intentionally feed 5

from North America (USA and Canada), while a much intentionally food, medicine, honey plant 7 smaller number of were taxa native to South and Central intentionally forestry 6 America (7 and 4, respectively). Only one taxon was native to the broader region of the American continents not known 20 (North, Central, and South America). The Old World took second place regarding the origination points of alien Table 2. Introduction and pathway modes of alien invasive neophytes flora. There were 28 taxa from Asia, half of which have a in Pannonian Serbia (*species is alien for Europe; it was introduced as a garden plant in western Europe, and natural distribution in a wider continental area. There were spread “naturally” from those areas into Serbia).

1036 G.T. Anačkov et al.

in the greatest numbers. Annual plants were also the A significant number of taxa may be pollinated both most common among naturalized species, followed by by anemophily and autophily. Hydrophily is a type of perennial taxa. A similar situation was present for taxa pollination observed in aquatic taxa. Of the total number with a status of casual. Biennial plants and taxa with of analyzed taxa, there were 30 taxa with two types of transitional life cycles (annual to perennial and annual pollination: entomophily and autophily (16), entomophily to biennial) were represented by a very low percentage, and anemophily (11), myrmecophily and autophily (2), including equal numbers of naturalized and casual and anemophily and autophily (1) (Table 4). species. Seeds are most commonly dispersed by zoochory The flowering period for most taxa was either during (animal activity), which was observed in 80% of the summer season or from the beginning of summer to analyzed taxa. Recorded zoochorous types of the end of autumn. There was a smaller number of taxa dispersal were endo- and epizoochory. A subgroup that flower only in spring, while there were also some of endozoochory is dispersal by activity of birds and taxa that flower from spring to autumn. There was only small mammals, feeding on fruits of these species and a single taxon (Bidens frondosa L.) that flowers solely in dispersing them to greater distances. Although all the the autumn period (Supplement). species are considered to be introduced and spreading Most of the alien species recorded as invasive and by assistance of humans, after the introduction into neophyte in the Pannonian Plain were herbaceous plants. There was a significantly smaller number of Naturalized Casual Unknown species classified as trees, shrubs, and transitional forms (shrub/tree). Ligneous representatives were all herb 57 45 10 either naturalized or casual species. Creeping plants climber 6 5 1 and lianas were classified as a separate group, and most were naturalized. Taxa with unknown status were Life form shrub 5 3 0 mostly herbaceous plants (Table 3). tree 10 4 0 Of the Raunkier’s life forms, therophytes were the shrub/tree 5 1 0 most well represented (54%) in all groups: naturalized, casual, and with unknown status. Among the species of naturalized status, the next most abundant group annual 39 34 8 were hemicryptophytes, followed by phanerophytes, while in species with casual status the pattern was bienial 4 0 0 reversed. Scandentophytes and hydrophytes were Life cycle perenial 35 21 3 mostly naturalized, while only a single representative annual/ 2 2 0 of Chamaephyta was recorded (Salvia reflexa Hornem) bien (Supplement). ann/peren 1 3 0 Types of pollination and seed dispersal are important determinants of spreading range. In the analyzed taxa, Table 3. Review of life forms and life cycles of alien invasive the majority were pollinated by insects (106 taxa). neophytes in Pannonian Serbia compared with species status (naturalized, casual, unknown).

Number of Pollination mode Number of species Seed dispersal mode species

Anemophily 33 Anemochory 22

Entomophily 79 Antropochory 10

Myrmecophily 2 Zoochory 63

Autophily 3 Autochory 5

Hydrophily 5 Hidrochory 5

Anemophily/Entomophily 11 Anemochory/Zoochory 22

Autophily/Entomophily 16 Hidrochory/Zoochory 7

Autophily/Myrmecophily 2 Autochory/Anemochory 1

Autophily/Anemophily 1 Autochory/Zoochory 17

Table 4. Pollination and seed dispersal modes of alien invasive neophytes in Pannonian Serbia.

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the flora of an area and establishment of a population These species are either considered “extinct” in the human activity still remained an important form of seed study area or there is only a single data entry on their dispersal in 70 taxa. Dispersal by wind and autochory presence in Pannonian Serbia. were present in alien species, definitively contributing to range expansion and habitat invasion. Comparing seed dispersal in contrast to pollination, two or three 4. Discussion modes of seed dispersal in a single taxon were much more common (in 100 taxa). Anemochory appeared in In Pannonian Serbia there are presently more than 1800 14 taxa as the only mode of pollination, while in 31 taxa recorded taxa of species and subspecies level (BUNS it was an alternative means of pollination. Zoochorous Herbarium, unpublished data). Alien neophytes with pollination was the only pollination mode in 18 out of the invasive potential for Pannonian Serbia (152) comprise 152 recorded taxa (Table 3). less than 10% of the total number of taxa, while for Europe alien neophytes represent 22% of the total 3.5 Analysis of invasiveness and threat/ number of taxa. It was previously reported that 13% of disruption of certain habitat types taxa in the flora of Europe are alien in origin, with only Alien invasive species appeared primarily in 5% having originated outside of the European continent anthropogenous and semi-natural habitats (59 species). [4]. However, after a more detailed approach during There was a high number of species in natural habitats the DAISIE project this number was determined to be (43), while 39 taxa inhabited all three habitat types. For much higher for the European region: 5789 alien taxa 46 taxa, the anthropogenic habitats (streets, alleys, were recorded, including 2483 from other continents. cities, villages, abandoned gardens, ranches, railroad The DAISIE project did not include the study area of this tracks, roads, levees along rivers and channels, parks, paper [28]. While Flora of Croatia [29] included 64 taxa cultivated fields, and stubble fields) were the only which of invasive alien species status, this number is much they inhabit. The presence of taxa with casual status greater in the present study area. However, the Flora in anthropogenic habitats stresses the importance of of Croatia list included only the naturalized species, monitoring further spreading and invasion into other which are represented by 78 species in our sample. In types of habitats. For nine taxa listed in literature as contrast, there are 709 species of neophytes recorded present in anthropogenic and semi-natural habitats, in Hungary, 145 of which are naturalized. In the study there were no data on invasiveness status. These area, there are 63 taxa of casual status, while in Hungary species are either “extinct” in the study area or there is there are 564. The differences are even greater when only a single record of their presence in Serbia (Table 5). other countries in Europe are compared, such as Austria The species that have occupied natural habitats, (276 naturalized, 810 casual), Czech Republic (229 which are under the lowest anthropogenic impact and naturalized, 817 casual), Greece (112 naturalized), and defined as casual by species status, have the greatest Romania (113 naturalized, 271 casual) [28]. According potential for mass destruction of natural habitats and all to Flora of Europe, there were 142 species considered other species appearing in these habitats. There were to be alien for the region of the former Yugoslavia, 108 11 such species in our database (Pinus nigra, Ulmus of which originated outside of Europe [4]. pumila, Impatiens parviflora, multiflorus, Cytisus This list includes only three species of vascular plants grandiflorus, Bryonia dioica, Bidens frondosa, Centaurea that are not flowering plants. Flora of Europe included diffusa, Cytisus scoparius, Impatiens glandulifera, 12 species of ferns [4] where only four were naturalized, Vallisneria spiralis). For nine taxa, which according to and only two species of the genus Azolla (A. caroliniana the literature inhabit anthropogenic and semi-natural and A. filicuolides) have been recorded in Serbia so far habitats, there were no data on invasiveness status. and both are naturalized. Among the gymnosperms, the

Anthropogenic Seminatural An/SN/N An/SN An/N SN/N

Naturalized 11 1 30 36 2 0

Casual 29 0 9 20 2 1

Unknown 6 2 0 3 0 0

Table 5. The ranking of habitat groups by alien invasive neophyte diversity (An=Anthropogenic, SN=Semi-natural, N=Natural habitats).

1038 G.T. Anačkov et al.

only species recorded as an alien invasive neophyte was recorded in 2007 and 2008 at the locality Bašaid for the study area was Pinus nigra Arnold. Pinus nigra (Serbia) in weed vegetation [36]. According to the has been deliberately planted in the specific biotope of DAISIE electronic database, this species was recorded European sand flats (Deliblato Sands) since the mid- as an alien species with casual status in Hungary and 20th century in order to increase forest areas [30], and with unknown status in Bulgaria (http://www.europe- later spread and to become invasive, as in Hungary aliens.org/speciesFactsheet.do?speciesld=5179), while [31]. Other recorded species of gymnosperms alien to according to the most recent data it has casual status in the study area do not have any naturalized populations, the study area. appearing exclusively as planted forests or in parks, The deliberately introduced species (47%) had home gardens, and botanical gardens. All the remaining greater representation than those accidentally species belong to divisions of flowering plants and introduced (39%), while mode of introduction may not these are mostly Dicotyledones (127 taxa). Families be precisely determined for the remaining group. Most with the greatest number of recorded taxa (Asteraceae, of the purposefully introduced species were originally Poaceae, Fabaceae, Brassicaceae) match the profile ornamental and horticultural species (68%) that in time of families best represented in both Serbia and Europe have “escaped” from the initial habitats. This group [32]. Comparisons with the invasive floras of Croatia was also represented in Europe by a slightly lower [29], Czech Republic [33], Greece [34], and Europe [28] percentage (52.2%), while in Austria this group includes show that representation of the richest families is very the greatest number of neophytes [28]. Deliberately similar, and that these are mostly global plant families. introduced species are cited as an important introduction The alien invasive species were classified into 104 vector for other groups of organisms such as terrestrial genera. The genera with the greatest number of species invertebrates [37]. The ornamental species, introduced were Amaranthus, Chenopodium, and Oenothera, which as decorative plants in parks, home gardens, and are also the most speciose genera in the broader area botanical gardens and then spread to surrounding of Europe [4,28]. The genera Ambrosia and Helianthus, habitats, are presently the greatest risk for biodiversity from America, were also important due to the number [38,39]. In the European region, 76.6% of accidentally of species and presence in the study area, as well as introduced alien species were introduced with seed two genera originating from Southern Europe, Cytisus material and soil (mineral materials) [28], while in the and Vicia. study area this percentage is 40%. As the primary use of The neophytes of Pannonian Serbia primarily have the study area is agriculture, it is impossible to precisely American and Asian origins, similarly to other countries pinpoint the number of species that were introduced but in this region including Croatia [29], Hungary [31], and survived only for one or a few vegetation seasons. Latest Greece [34]. The present list is supplemented with analysis of species spreading (Ambrosia trifida L.) from species native to the Balkan Peninsula and introduced agricultural to natural habitats shows that it is important to the Pannonian Plain by human activities, for the to study it in more detail. Ambrosia trifidaL. was recorded needs of forestry management or as ornamental plants. in Serbia for the first time in 1981 in the town of Čoka One of the best examples is Syringa vulgaris L., a relict [40] but in the following period it disappeared from this species in the Balkan Peninsula where it is native in regularly visited locality. Ambrosia trifida was recorded certain localities in Serbia, introduced as an ornamental again in Serbia in 1995, at the locality Despotovo, about species in the Pannonian Plain. Due to very fast and 150 km away. At this locality the species has formed a straightforward propagation by vegetative means, stable population and had started to spread very quickly. this species is spreading to natural habitats, primarily Presently it may be recorded in a wider area in a phase steppe near settlements. On the other hand, species of active spreading. This species and other species of such as Veronica persica Poiret are considered native genus Ambrosia L. were introduced accidentally, with species for Serbia, were introduced to the Pannonian seed material and mineral matter. part of the country. The lack of tradition in studying The greatest percentage of recorded therophytes flora from the perspective of biological invasion and is similar to the alien floras of other countries in the alien flora has caused the species region [23,33]. On the other hand, such high presence (Pall) DC. to be recorded in the Red Book of Flora of of therophytes also matches their dominance in the Serbia as a taxon extinct in the territory of Serbia and autochthonous flora. The flora of Serbia has a bipolar the former Yugoslavia [35]. The Red Book includes Hemicryptophyta-Therophyta character, with a greater only one site for this taxon, from of the Deliblato Sands number of therophytes in the northern part (including area, and lacks any herbarium data and is based only the study area), which belongs to the Pontian-South on oral reports and literature citations. This species Siberian floristic region [41]. The increased percentage

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of participation by phanerophytes when compared to unit as the study area. Semi-natural habitats such as the autochthonous flora of Serbia was also recorded in forested meadows, pastures, and levees are corridors other countries [34,42]. The presence of phanerophytes for the spread of alien species (http://iasv.dbe.pmf. as well as scandentophytes is connected with significant uns.ac.rs). At the same time these habitats are green introduction of ornamental and cultivated species corridors (B. Panjković, unpublished data) in the study of trees and shrubs, while most therophytes were area. Therefore these corridors connect the natural introduced with seed material and mineral matter, which habitats and facilitate not only for migration of species is not controlled. Other life forms such as chamaephytes, but also the spread of alien species. The alien species hemicryptophytes, and geophytes were represented are having a negative impact on corridors as well with much smaller percentage values, again reflecting [B. Panjković, unpublished data]. the situation in other countries of this region. In natural habitats, 45 invasive taxa were recorded, Annual and perennial plants had equal representing a conservation threat for biodiversity, representation. A perennial life cycle in alien species including: Robinia pseudoacacia L., Pinus nigra Arnold, indicates the presence of vegetative reproduction [43], Asclepias syriaca L., Acer negundo L., Ailanthus while in annual plants two or three cycles of flowering altissima (Mill.) Swingle, Amorpha fruticosa L., Datura and fruit-bearing have been recorded during a single stramonium L., Oenothera spp., Solidago spp., Syringa calendar year. The most intensive flowering period vulgaris L., Elodea canadensis Michx, Impatiens spp., of invasive species in the study area included either Populus x canadensis, etc. Participation of these summer or both summer and autumn, matching the species varies within the region, with 17 species were general trend for these species in the region and Europe recorded in Austria [28] and about 40 in Hungary [31]. as a whole. This period was also followed by entomophily Number of recorded alien invasive neophytes in as a dominant type of pollination. Autophily appeared as the region of the Pannonian Plain in Serbia comprises an “alternative” type of self-pollination, indicating that less than 10% of total flora of this area. However, these species with a tendency of expansion also have their abundance, distribution, and population density various ways of coping with changing environmental are not negligible as a negative influence on natural factors. Anthropochory was an alternative mode of habitats and accompanying wildlife, as well as having seed dispersal that appeared as a secondary mode an important socio-economic influence. Knowledge of in a significant number of analyzed species. Although these species and their behavior is crucial to ensure these species definitively have developed mechanisms timely reaction and create prevention plans. Lists of for spreading their propagules, almost all of them have alien invasive species are also a foundation for defining developed a secondary mechanism for spreading, the forms of biological invasion at various levels, both certainly a remarkable adaptation that allows for regional and local [45]. During the long history of floristic successful invasion of new habitats and increase in studies in the Pannonian Plain, these species were range. This is supported by the fact that a significant once characterized as new for the area and enriching percentage of the territory in the study area is situated the native flora. For many species there are no data on very fertile soils. on “first records” so they were classified as naturalized Anthropogenic habitats were most susceptible archaeophytes. For certain species such as Robinia to biological invasion. They include streets, parks, pseudoacacia L., Asclepias syriaca L., and Populus x gardens, industrial areas, settlements, and road and canadensis it is too late to plan an economically sound railway networks, as in the other neighboring countries suppression program, as they are now distributed in [29,31,34] and the whole of Europe and other regions wide areas, represent economically important species, [28,44]. At the same time they represent habitats where and their populations form particularly dense stands. species were first recorded and are at the starting point Conservation of native habitats and habitats with for spread to other habitats. Particularly important are low human impact are equally important at global and railway stations, where several species (Ambrosia national levels. The areas with a significant percentage trifida L., Solanum eleagnifolium Cav.) were recorded of vulnerable ecosystems (swamps, marshes, steppe, in Serbia for the first time [40]. The anthropogenic saline flats), including Pannonian Serbia, are most habitats of agricultural type have also been inhabited threatened by spread of invasive species. These in significant numbers by alien species, primarily species form their centres of distribution and spread appearing at fringe areas that are not chemically systematically in neighboring areas with disturbed treated and often not mechanically altered. These habitats, and later into semi-natural and natural sites. habitats are important invasion centres in neighboring The economic challenges experienced by Serbia in Hungary [31], which is part of the same biogeographical recent years have led to a lack of systematic agro-

1040 G.T. Anačkov et al.

technical measures in this intensively agrarian region. spreading into the northern areas. Combined with the The end result is that this part of the Pannonian Plain is fact that this is an agrarian area with partially outdated definitively one of the areas from which invasive species and inefficient methods of suppressing such species may spread. This situation has resulted from the lack in ecosystems, this characteristic is the foundation of of knowledge on alien invasive flora and exclusion of recognizing this region as the hotspot for spreading this area (and certainly some others) from all Pan- invasive species in this part of Europe. European project initiatives that recognize invasive species as a threat to natural habitats. Therefore this analysis of invasive higher plant species in Pannonian Acknowledgements Serbia was designed to increase knowledge on invasive species in southern territories of Central Europe and This work was supported by the Ministry of Education, Europe in general. The results indicate the particular Science and Technological Development of the importance of this transitional region between Central Republic of Serbia, projects 173030 and III43002, and and the Southern Europe as an important border area, the Provincial Secretariat for Science and Technological where many species of southern origin are presently in Development of Vojvodina (grant no. 114-451- the phase of adaptation and developing strategies for 2056/2011-01).

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