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Exotic in Europe

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Available from: Andreas Martens Retrieved on: 13 September 2015 Exotic Odonata in Europe 1st June 2014125

Exotic Odonata in Europe

Gerold Laister1, Gerhard Lehmann2 & Andreas Martens3

1 Hans-Hofmann-Ring 3, 4470 Enns, Austria; 2 Haunfeldstraße 14, 6330 Kufstein, Austria; 3 University of Education Karlsruhe, Bismarckstraße 10, 76133 Karlsruhe, Germany;

Received 2nd February 2014; revised and accepted 24th March 2014

Abstract. Between 1991 and 2011, more than 1,000 adults of exotic odonate species were recorded from glasshouses of a wholesaler dealer of aquarium plants near Wels, Austria. Twenty-three species could be identified to species level. All species were accidentally introduced as eggs or larvae. The majority are widely distributed and common south- eastern Asian species. About 17 taxa are first recorded from Europe bringing the list of exotic Odonata in Europe to 41 taxa. These odonates are mainly introduced via aquarist trade and many species have emerged from home aquaria and glasshouses. Currently, tropical plants for aquarists are mainly imported to Europe from Singapore, Indonesia and Thailand, which suggests that the exotic Odonata originated in those countries. So far, the introduction of exotic Odonata species into Europe is not ecologically relevant because none of the introduced species have become established in the wild. However, this study will improve understanding of the significance of trading connections in establishing exotic species which could become invasive. Key words. , neobiota, check-list, aquaristic trade, incidental introduction, dispersal, invasive species, long-term study

Introduction Invasive species are one of the major threats to biodiversity (CBD 2000). In freshwater habitats, one of the most important factors triggering biological invasions is the pet and aquarium trade (Duggan 2010; Chucholl 2013). Non-indigenous ornamental fish and crayfish, in particular, have been in- troduced and become established in the wild (Duggan et al. 2006; Chu- choll 2013). In addition to traded species, several other species are intro- duced incidentally (Duggan 2010), including Odonata. Non-indigenous species can be divided into ‘invasive species’ (i.e. alien species, neobiota), which are able to establish new populations in a new area, and those which do not, termed ‘exotic species’.

Odonatologica 43(1/2) 2014: 125-135 126 G. Laister, G. Lehmann & A. Martens

In Europe, the knowledge of exotic Odonata is based on small studies (e.g. Valtonen 1985; Brooks 1988) and reports of single observations (e.g. Wasscher & Groutbeek 1998; Martens & Schiel 2009). Until now, 25 exotic odonate taxa are known from Europe (Wasscher & Bos 2000; Bos et al. 2007; Martens & Griese 2009; Seehausen 2012a). The last review was by Kipping (2006). Several species were found as adults in tropical glass- houses or aquarium trading shops; others were reared from larva to adult in home aquaria. There is a more or less constant flow of eggs and larvae of exotic odonates into Europe with trading of aquarium plants. Living Odo- nata are not traded. So far, in Europe, odonates have not become invasive species. The data presented here are from the first long-time study of exotic odonate species found in a glasshouse. An overview of all published records in Europe so far is also presented. The results demonstrate the principal role of the world-wide aquarium trade in the incidental introduction of exotic Odonata to Europe.

Study site and methods The study was conducted at two glasshouses of a wholesale dealer of aquari- um plants near Wels, Austria (48.08°N, 14.00°E). Both glasshouses together had a total size of ca 650 m². Aquatic plants were cultivated in long rows of 1.2 m wide tanks on the ground as well as in 0.3 m wide containers hanging from the roof above these containers. Both glasshouses had vents for ther- mal regulation. The climate was humid and tropical throughout the year. Outside, additional small containers of 1 m² were used for cultivation in the summer.

Between 1991 and 2011 the first author visited the glasshouses more than 80 times. All odonate imagines seen were collected. The imagines were taken with a small net (24 cm diameter). Additionally, in the first few years of the study the small water containers outside were checked in summer. The imagines were stored dry. They were identified to species level by the second author. Native species which entered the glasshouses via vents were also recorded. Exuviae were also collected, but so far have not been identi- fied.

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Table 1. Exotic Odonata taxa and number of imagines recorded in glasshouses of a plant trader near Wels, Austria. Species recorded in one year only are given bold.

Taxon 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2009 2010 2011 total Aciagrion sp. 1 1 Agriocnemis femina 165 43 2 210 A. cf. nana 2 2 A. pygmaea 24 2 1 27 rubescens 1 1 Ceriagrion cerinorubellum 3 2 3 1 1 4 14 C. chaoi 34 34 Ischnura senegalensis 11 1 2 4 5 14 9 46 Pseudagrion austrialasiae 2 2 P. microcephalum 2 142 2 11 10 11 1 10 19 208 Ictinogomphus rapax 4 3 1 2 10 Epophthalmia vittigera 1 1 Brachydiplax chalybea 4 4 Crocothemis servilia 67 2 1 8 21 1 2 3 105 Diplacodes trivialis 1 1 croceus 3 1 1 1 3 9 fluctuans 128 101 4 5 16 8 262 Orthetrum chrysis 2 2 O. sabina 26 4 1 4 5 14 2 4 2 61 O. testaceum 1 1 2 Rhyothemis p. phyllis 7 7 Tholymis tillarga 5 5 Tramea transmarina 3 3 Trithemis aurora 1 8 2 3 14 Urothemis signata 2 2 total 296 470 20 1 28 1 49 37 1 56 7 33 35 1034 No. of visits 10 27 9 2 4 1 13 3 2 7 1 3 2 84

Results Between 1991 and 2011, more than 1,030 imagines of exotic Odonata were collected. Most Zygoptera and nearly all Anisoptera were taken freshly emerged or immature. Some fully mature individuals of Neurothemis fluc­

Odonatologica 43(1/2) 2014: 125-135 128 G. Laister, G. Lehmann & A. Martens tuans were netted outside. Twenty-three taxa were identified to species level and two to level (Tab. 1). Some species, such as N. fluctuans, Agrio­ cnemis femina, Pseudagrion microcephalum and Crocothemis servilia, were collected in large numbers. Some species occurred regularly in low num- bers, others were recorded only in one year sometimes as a single individual.

Discussion This study significantly extends the list of exotic Odonata known in Europe, to 41 taxa (Tab. 2). The high number of records from glasshouses shows that large numbers of exotic odonates derive from eggs or larvae in or on traded aquatic plants. Other forms of introduction, especially the import of imagines in banana boxes or on ships (Kipping 2006; Corbet et al. 1960; Tab. 2) are comparatively rare. The majority of species are of south-east- ern Asian origin (Fig. 1) from where aquatic plants for home aquaria were mainly imported from countries, such as Singapore, Indonesia and Thai- land (Gueudre & Tison 2007). Annual differences in the species composi- tion and number of individuals (Tab. 1) suggest that there are large changes in the composition of imported material within a short time.

Figure 1. Origin of exotic Odonata in Europe.

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Table 2. Check-list of exotic Odonata taxa in Europe.

Taxon Distribution Remarks References Aciagrion sp. Asia, Africa Austria, glasshouse. This study First record for Europe Agriocnemis femina Asia The Netherlands, Wasscher & Goutbeek (Brauer, 1868) aquarium, Austria, 1998; glasshouses this study A. cf. nana Asia Austria, glasshouse. This study Laidlaw, 1914 First records for Europe A. pygmaea Asia Germany, aquarium Martens & Griese 2009; (Rambur, 1842) trader, Austria, this study glasshouses Argia fumipennis North UK, glasshouse Brooks 1988; (Burmeister, 1839) America this study Argiocnemis rubescens Asia Austria, glasshouse. This study Selys, 1877 First records for Europe Ceriagrion Asia UK, glasshouse; Brooks 1988; cerinorubellum Germany, vicinity of Kipping 2006; (Brauer, 1865) glasshouse; this study Austria, glasshouse C. chaoi Asia Austria, glasshouse. This study Schmidt, 1964 First records for Europe Enallagma signatum North UK, glasshouse Brooks 1988 (Hagen, 1861) America Ischnura posita North UK, glasshouse Brooks 1988 (Hagen, 1861) America I. ramburii North Germany, aquarium Seehausen 2012a (Selys, 1850) America trader I. senegalensis Asia, Africa Finland, aquarium trader; Valtonen 1985; Brooks (Rambur, 1842) UK, glasshouse, fish 1988; Kipping 2006; tanks and garden ponds; Parr 2010; Benken Germany home aquaria & Kommander 2011; and aquarium trader; Lambertz & Schmied Austria, glasshouses 2011; Seehausen 2012b; this study Mecistogaster sp. Central Poland, first record of an Rudow 1898 and South exotic sp. in Europe America Pseudagrion SE Asia Austria, glasshouse. This study austrialasiae First record for Europe Selys, 1876

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Taxon Distribution Remarks References Pseudagrion SE Asia, Finland, aquarium trader; Valtonen 1985; microcephalum Australia Germany, aquaria; Martens & Schiel (Rambur, 1842) Austria, glasshouses 2009; Seehausen & von Blanckenhagen 2012; this study Anax guttatus Asia, UK, glasshouse Brooks 1988 (Burmeister, 1839) N Australia, Pacific A. gibbosulus Asia, UK, glasshouse Brooks 1988 Rambur, 1842 N Australia Ictinogomphus Asia The Netherlands, Lieftinck 1978 decoratus (Selys, 1854) aquarium I. rapax Asia Austria, glasshouse. This study (Rambur, 1842) First records for Europe Epophthalmia vittigera Asia Austria, glasshouse. This study bellicosa Lieftinck, 1948 First record for Europe Brachydiplax chalybea Asia Austria, glasshouse. This study Brauer, 1868 First records for Europe Celithemis eponina North The Netherlands, Bos et al. 2007; (Drury, 1773) America glasshouse near Den M. Wasscher in litt. Haag in 1988 Crocothemis servilia Asia UK, glasshouse and fish Agassiz 1981; Brooks (Drury, 1773) tanks; 1988; Waning Vos The Netherlands, 2005; Wasscher & aquarium; Ruiter 2005; Raab et Austria, glasshouses; al. 2007; Parr 2010; Germany, aquaria; Seehausen & von Poland, aquarium trader Blanckenhagen 2012; Seehausen 2012b; Buczyński & Bielak- Bielecki 2012; this study Diplacodes trivialis Asia Austria, glasshouse. This study (Rambur, 1842) First record for Europe Erythemis simplicicollis North UK, glasshouse Brooks 1988 (Say, 1840) America SE Asia Austria, glasshouse. This study (Brauer, 1867) First records for Europe Neurothemis fluctuans SE Asia Finland, aquarium trader; Valtonen 1985; (Fabricius, 1793) The Netherlands, Wasscher & Goutbeek glasshouse and 1998; aquarium; Waning Vos 2007; Austria, glasshouses this study

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Taxon Distribution Remarks References Orthetrum chrysis Asia Austria, glasshouse. This study (Selys, 1891) First records for Europe O. japonicum E Asia Finland, aquarium trader Valtonen 1985 (Uhler, 1858) O. sabina Asia, UK and Austria, Brooks 1988; Raab et (Drury, 1770) North Africa glasshouses al. 2007; this study O. testaceum Asia Austria, glasshouse. This study (Burmeister, 1839) First record for Europe Pantala flavescens tropics and UK, imagines on board Ford 1954; (Fabricius, 1798) sub­tropics, of ships; Corbet et al. 1960; cosmo­poli­ Germany, imago in Kipping 2006 tan banana box Rhodothemis rufa Asia UK, glasshouse Agassiz 1981; (Rambur, 1842) Brooks 1988 Rhyothemis p. phyllis SE Asia Austria, glasshouse. This study (Sulzer, 1776) First records for Europe Sympetrum eroticum E Asia Lithuania, one young Stanionyte 1989; (Selys, 1883) male caught in the wild Bernard 2005 S. infuscatum E Asia Nousty, France, 09-viii- J.-P. Boudot in litt. (Selys, 1883) -2006; photo taken by J. Deffarges in a garden. First record for Europe Tholymis tillarga Asia, Africa, Austria, glasshouse. This study (Fabricius, 1798) N Australia, First records for Europe Pacific Tramea transmarina SE Asia UK, Austria, glasshouses Agassiz 1981; Brauer, 1867 Brooks 1988; this study Trithemis aurora Asia Austria, glasshouse. This study (Burmeister, 1839) First records for Europe Urothemis bisignata Asia UK, glasshouse Agassiz 1981; Brauer, 1868 Brooks 1988 U. signata Asia Austria, glasshouse. This study (Rambur, 1842) First records for Europe

Many of the imported species, such as Anax guttatus, Ceriagrion cerino­ ru­bellum, Diplacodes trivialis, Neurothemis fluctuans, Orthetrum sabina, Pseud­agrion microcephalum, and several others, breed in disturbed, de- graded areas in their native range and are common in areas with dense hu- man settlement (Orr 2001). In most cases typical habitats are paddy fields, ditches, canals, and open ponds. In primary forests these species are rare or absent (Orr 2001).

Odonatologica 43(1/2) 2014: 125-135 132 G. Laister, G. Lehmann & A. Martens

So far in Europe, there is no case of an exotic odonate becoming established in the wild. This is in contrast to other parts of the world. One odonate spe- cies, Crocothemis servilia, has successfully invaded the subtropics and trop- ics outside its native range. So far the species is established in Florida (Paul- son 1978; Daigle & Rutter 1984; first record 1975), Cuba (Flint 1996; first record 1994), and O’ahu, Hawaii (Polhemus 1995; first record 1994). The biggest number of established introduced Odonata species have been found in Hawaii, where about eight species have been recorded (Englund 2005). In Japan, the occurrence of Pseudagrion australasiae is thought to be as a result of an accidental introduction (Karube et al. 2011). Some cases are ambiguous. Pantala flavescens is a casual migrant in Eu- rope (Buczyński et al. 2014). Therefore records in the wild are hard to in- terpret. Another case is Pachydiplax longipennis (Burmeister). In early Sep- tember 1999, a female of that North American species was found dead on the oil rig Sedco 706 in the North Sea at 60°38’N, 01°39’E (Parr 2000a). It is not clear if the reached the oil rig alive. It could have been carried on board a helicopter or on the jet stream. Because there is no evidence that the individual reached Europe alive it has not been included on the Euro- pean list.

Prospect The increase in exotic odonates illustrates the globalization of the aquarium trade and its significance in the dispersal of neobiota.

(1) A new trend is aquatic plant breeding in North Africa for the European market. This will reduce the risk of tropical Asian being -in troduced into Europe. However, this increases the risk of an introduc- tion and establishment of tropical Asian dragonfly species in those parts of Africa, which belong to the same thermal area. (2) The picture could change rapidly if South American plants and odo- nates begin to be imported into Europe. (3) So far none of the introduced species have established populations in the wild. In the temperate part of Europe there is no risk when plants origi- nate from tropical regions. However, the introduction of plant material from other temperate regions, such as North America or China could

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pose a risk. In Mediterranean Europe, especially on islands, the estab- lishment of a subtropical south-eastern Asian species could be possible. Islands are especially at risk because of their relative small number of species, less diverse genotypes of the inhabitants, and open niches be- cause of isolation effects. (4) Further unidentified species, especially and , will probably be found. There are several reports of unidentified Pseud­ agrion specimens (Brooks 1988; Schmidt 1990; Seidenbusch 1996; Seehausen 2012b) which might belong to P. microcephalum. Special re- quests in aquarist journals and forums (Seehausen 2012b), photo guides from south-eastern Asia (Tang et al. 2010), national checklists (Bos et al. 2007; Parr 2000b; Martens 2014) as well as book chapters (Wilder- muth & Martens 2014) will improve knowledge of imported Odonata.

Acknowledgements We would like to thank Adolf Niederhumer, Aquarium Linden company, for allowing the first author access to the glasshouses. Martin Schorr pro- vided hard to obtain literature. Many thanks to Sónia Ferreira and Vincent Kalkman, for their request for a review on exotic dragonflies at the 1st Euro- pean Congress of Odonatology in Vila do Conde, Portugal, which prompted a closer look at this topic and the analysis of unpublished findings. Finally, many thanks to Steve Brooks and Marcel Wasscher, for their very useful comments on the manuscript.

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