Apeer-reviewed open-access journal BioRisk 16: I-13 (2021) agen : doi: 10.3897/biorisk.16.61099 RESEARCH ARTICLE & R Ke) Re IS k https://biorisk.pensoft.net Citizen scientists significantly improve our knowledge on the non-native longhorn beetle Chlorophorus annularis (Fabricius, 1787) (Coleoptera, Cerambycidae) in Europe Matthias Seidel', Maren Liittke', Christian Cocquempot’, Katy Potts?, Wil J. Heeney*, Martin Husemann! | Centrum fir Naturkunde, Universitat Hamburg, Martin-Luther-King-Platz 3, Hamburg, Germany 2 25 Route du Queffleuth, 29600 Plourin-les-Morlaix, France 3 The Angela Marmont Centre for U.K. Bio- diversity, The Natural History Museum, Cromwell Road, SW7 5BD, London, UK 4 105 Withycombe Drive, Banbury, OX16 OSD, Oxon, UK Corresponding author: Matthias Seidel (matthias.seidel@uni-hamburg.de) Academic editor: P. Pygek | Received 24 November 2020 | Accepted 28 January 2021 | Published 9 March 2021 Citation: Seidel M, Liittke M, Cocquempot C, Potts K, Heeney WJ, Husemann M (2021) Citizen scientists significantly improve our knowledge on the non-native longhorn beetle Chlorophorus annularis (Fabricius, 1787) (Coleoptera, Cerambycidae) in Europe. BioRisk 16: 1-13. https://doi.org/10.3897/biorisk.16.61099 Abstract The Asian bamboo borer Chlorophorus annularis is a beetle species that has been introduced in many countries globally. Originating in Southeast Asia, it can now be found in the Americas, South Africa, the Middle East, Australasia and Europe. The literature record of the species in Europe consists of findings of single individuals usually associated with imported bamboo products. A general European effort in sur- veying C. annularis was never undertaken, since the overall scientific consensus was that the species cannot establish here. Yet, recent records in Genk, Torhout (Belgium) and in Hamburg (Germany) do not seem directly associated with a recently imported product and hence may indicate otherwise. Such a shortfall in recording commonly imported, potentially invasive species may be counteracted through citizen sci- ence initiatives, allowing for continuous, high density monitoring. In this paper we present thirteen new records of the species from five European countries, including two new country records, mostly going back to interested citizen scientists. Keywords bamboo, Cerambycidae, Coleoptera, Hamburg, insect, invasion biology, neozoa, pest organism Copyright Matthias Seidel et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 2 Matthias Seidel et al. / BioRisk 16: 1-13 (2021) Introduction Non-native species, accidentally or purposefully introduced organisms, represent one of the big challenges in a globalized world (Kenis et al. 2009; Simberloff et al. 2013; Bellard et al. 2016; Bradshaw et al. 2016), with constantly rising numbers of newly recorded species (Hulme 2009; Seebens et al. 2017). These species, while often barely recognized, may represent severe economic and ecological threats (e.g. as agricultural pests, ecological competitors or predators of native species). However, despite their potentially high importance, surveying non-native species is still only performed for a limited number of highly invasive species, as it is time consuming and expensive. Including the general public in such surveying activities through citizen science initia- tives and projects, or taxonomic interest groups and websites, may be a viable alterna- tive (Gallo and Waitt 2011; Chandler et al. 2017). This approach has been proven to be powerful, for example, in demonstrating the decline of monarch butterflies (Schultz et al. 2017), and changes in ladybird populations (Gardiner et al. 2012) and has also been used to detect and monitor non-native species (Delaney et al. 2008; Crall et al. ZOOS 2OI)s While large invasive species, such as mammals, birds and fish, are detected more easily, smaller arthropod species often remain unspotted for some time after their in- troduction (e.g. Wolter and Rohr 2010; Fischer et. al. 2016). Nevertheless, arthropods, and especially insects have high invasion potential and can often be detrimental pests (Kiritani and Yamamura 2003). Insects are frequently transported with raw materials, and agricultural products, or living plants and plant material. One of the groups spe- cifically commonly introduced with plants and wood are the longhorn wood boring beetles of the family Cerambycidae (Eyre and Haack 2017). The family comprises more than 40,000 described species worldwide, which are all phytophagous, xylophagous or saproxylophagous. Fortunately, only some species are true pests of economic importance. In the past, only species with a long life cycle and species capable of lasting several generations in the same host material could bear the long times of transportation and emerge in the countries of importation to generate a possible invasion. Hylotrupes bajulus (Linnaeus, 1758) (Cerambycinae, Callidiini) and Nathrius brevipennis (Mulsant, 1839) (Cerambycinae, Nathriini) were probably two of these invasive pioneers. A first synthesis of imported beetles in Europe was done by Duffy (1953). The growth of international trade, the reduction of the length of transport and the increase in diversity of potential vectors of longhorn beetles since the 20" century allowed an increase in the number of individuals and species accidentally imported, as shown by the numerous interceptions, introductions and establishments reported by national and international organizations (e.g. EPPO (in European Un- ion), APHIS (in United States of America), AQIS (in Australia) and Biodiversity (in New Zealand), over the past four decades. Despite international sanitary and control measures, many new potential invasive cerambycids reach foreign areas on a regular basis (e.g. Cocquempot 2007; Cocquempot and Lindeléw 2010). While interceptions have become common, sometimes introductions may occur unrecognized, but rarely Non-native Chlorophorus annularis in Europe e) species are able to establish. Within the longhorn beetles, the Asian longhorn beetle (Anoplophora glabripennis (Motschulsky, 1853)) (Lamiinae, Monochamini) is among the most feared. The species originates in Central Asia, but has been introduced in North America and Europe, where it attacks a diverse range of trees (Meng et al. 2015). Other introduced cerambycids include the Citrus longhorn beetle (Anoplophora chinensis (Forster, 1771)), or the Red-necked longhorn beetle (Avomia bungii Falder- man, 1835) (Cerambycinae, Callichromatini). Newly imported cerambycid species are constantly reported (e.g. Friedman et al. 2008; Burmeister et al. 2012; Cocquempot et al. 2015a, b; Sarto i Monteys and Torras i Tutusaus 2018). One of the species of longhorn beetles that is more frequently intercepted is the Bamboo borer Chlorophorus annularis (Fabricius, 1787) (Cerambycinae, Clytini). ‘This beetle originally inhabits temperate to subtropical regions of Southeast Asia (native range: Cambodia, China, India, Indonesia, Japan, Korea Laos, Malaysia, Myanmar, Nepal, New Guinea, Philippines, Singapore, Sri Lanka, Taiwan, Thailand and Viet- nam (Monné 2005; Cocquempot 2007; Friedman et al. 2008). It has been reported to attack species of fourteen different plant families: Aceraceae, Anacardiaceae, Betu- laceae, Dipterocarpaceae, Hamamelidaceae, Juglandaceae, Lamiaceae, Malvaceae, Mi- mosaceae, Paeoniaceae, Poaceae, Rosaceae, Ulmaceae, Vitaceae (for genera and species see Monné 2005). Most notable is the damage the species is causing to bamboo, which is the main product it is contaminating outside of its natural range. So far, it has been intercepted in the Middle East (Israel: Friedman et al. 2008), South Africa (Suma and Bella 2018), South America (Brazil: Monné 2005; Uruguay: Suma and Bella 2018), North America (Unites States: Mattson et al. 1994; Eyre and Haack 2007; Canada: NAPPO 2014), Australasia (Australia: Hanks et al. 1997; New Caledonia: Suma and Bella 2018; New Zealand: MPI 2013) and ten European countries (Cocquempot 2007; Suma and Bella 2018). The first European specimen was captured in the United Kingdom in 1924, followed by records in Finland and Czech Republic in 1936 and subsequently in Germany, Austria, Spain, Hungary, France, Denmark and Italy (for map and references see Fig. 2 and Table 1). So far, the species is only regarded as inva- sive in Spain with the potential to get established in other Mediterranean areas as well (Vives 1995; Cocquempot and Lindeléw 2010). Here we report Chlorophorus annula- ris as newly intercepted to the Netherlands and Belgium, as well as the first traceable record for Denmark. For Czech Republic, France, Germany and the United Kingdom, new records are presented, mostly based on records from citizen scientists. Materials and methods Physical specimens examined One specimen (ZMH 83366): ,aus Tonkin Frithjahr 1953 eingeftihrt, Chlorophorus annularis F. Dr. E. Franz det. 1953“; two specimens (ZMH 833668, ZMH 833668): Aschaffenburg aus Bambus Blumengest[ell], [X.59“; one specimen (ZMH 833670): 4 Matthias Seidel et al. / BioRisk 16: 1-13 (2021) Table |. Records of Chlorophorus annularis in Europe sorted by country and date of introduction. Locality Origin Reference Austria Vienna July 1993 Schillhammer (1994) Judenburg bamboo furniture Adlbauer (2001) Klagenfurt no date Bamboo Steiner (1997) Belgium Genk July 2019 inside car with no host plant hetps://www.inaturalist.org/ob- association servations/39960166 (accessed 27.10.2020); new record (this paper) Torhout December 2020 inside house with no host plant new record (this paper) association Czech Republic Brno 1936 Bamboo Slama (1998) Brno between 1930 to 1951 Bamboo Heyrovsky (1951) Prague between 1930 to 1951 Bamboo Heyrovsky (1951) Horni Poéernice ca. 2000 Bamboo new record (this paper) Obtistvi August 2016 to August bamboo poles imported from new record (this paper) 2018 China via the Netherlands Denmark Denmark Cocquempot (2007) (Com. pers M. Petersen) Hesselager July 2016 bamboo sticks new record (this paper) Finland Helsinki bamboo (ski poles) Saalas (1940) Helsinki no date Bamboo Tuurala (1945) France Saint-Georges-de-Didonne July 1986 on flower of Ligustrum, probably Hengoat (2008) emerged from bamboo lounge furniture Saulx-les-Chartreux August 2001 (date in Ha- | on the street with no host plant Hanot (2006) not (2006) incorrect [pers. association comm. Hanot 2020]) Betton July 2001 inside the house Gouverneur and Guérard (2011) Mesquiers bamboo furniture imported from Cocquempot (2007) Vietnam Besse-sur-Issole April 2008 bamboo furniture imported from new record (this paper) Indonesia Le Crés April 2014 bamboo broomstick new record (this paper) Germany Hamburg spring 1953 imported bamboo (“Tonkinrohr” | Weidner (1954); specimen in ZMH = Arundinaria amabilis) Frankfurt am Main May 1958 bamboo frame Franz (1959) Hildesheim bamboo pieces Schmidt (1962) Stuttgart August 1959 bamboo stick Harde (1959) Aschaffenburg “Blumengestell” Weidner (1982); specimen in ZMH Aschaffensburg-Schweinheim April 1965 Elbert (1969) Hamburg, Billwerder hatched from bamboo railing Weidner (1982) Niederlinxweiler 1967 bamboo Stock (2001), Niehuis (2001) Hamburg August 1991 bamboo sofa imported from Bali | new record (this paper); specimen Roth April 2001 Stock (2001) Karlsruhe October 2004 — May 2005 bamboo furniture Riedel (2005) Schmira October 2005 imported bamboo sticks Kopetz et al. (2008) Hamburg August 2020 on wooden fence in close proxim- new record (this paper) ity to ornamental bamboo plant Hungary Budapest May 2008 bamboo Kovacs (2010) Italy Catania May 2018 bamboo ladder Suma and Bella (2018) Non-native Chlorophorus annularis in Europe 5 Locality Origin Reference Netherlands Wageningen August 2011 bamboo stick hetps://waarneming.nl/obser- | | vation/62023595/ (accessed 30.10.2020); new record (this paper) Spain Sant Cugat del Vallés September 1991 on flowers in an urban area with Vives (1995) planted bamboo United Kingdom Oxford? [=home of the before 1924 bamboo pot imported from Poulton (1924) author] Myanmar London bamboo Fisher (1942) Princes Risboroug October 1940 — October bamboo Fisher (1942) 1941 Buckenham Wood no date Cocquempot (2007) Braintree July 2018 suspected to be from bamboo iRecord, new record (this paper) from horticultural supplier Lincoln September 2019 bamboo sticks https://www.inaturalist.org/ob- servations/33252453 (accessed 27.10.2020); new record (this paper) Stirchley October 2020 bamboo iRecord, new record (this paper) »Herkunftsland: Bali in BS aus Importsofa geschliipft 8.8.1991". All specimens are deposited in ZMH (Zoologisches Museum, Centrum ftir Naturkunde, Hamburg, Germany). Citizen science Firstly, the term ‘Chlorophorus annularis was entered in the search function of the citizen science platforms listed below. Secondly, all Chlorophorus species records were checked to exclude possible misidentifications with similar looking species. iNaturalist (https://www.inaturalist.org/) iRecord (https://www.bre.ac.uk/irecord/) Entomologické Férum (http://www.entoforum.cz/) waarneming.nl (https://waarneming.nl/ [Dutch version of observation.org]) Results Corrections of previous records The occurrence of the species from Romania was reported by Cocquempot (2007), but after further research for this paper, we noticed that it was a misinterpretation of a record from Czech Republic. So far, the species has not been recorded in the country (pers. comm. R. Serafim 2020). The specimen reported by Hanot (2006) in Saulx-les- Chartreux (France) was collected on the 12" of August 2001 and not as stated in the paper on 22™ of July 2002. 6 Matthias Seidel et al. / BioRisk 16: 1-13 (2021) New Records Belgium. A specimen was found alive in a car in Genk on the 31™ of July 2019 and subsequently reported on iNaturalist. An association with a host plant could not be established. A specimen emerged in a house in Torhout (approximately 51.069, 3.101) on the 30" of December 2020 and was collected by Tineke De Blauwe. No apparent connection to a host plant could be established. The specimen was subsequently iden- tified by Koen Verhoeyen (Deinze, Belgium) and Alain Drumont (Brussels, Belgium) and will be deposited in the Royal Belgian Institute of natural Sciences (Brussels, Bel- gium). [hese two finds represent the first records of the species for Belgium. Czech Republic. Multiple specimens (Fig. L[A—C) were found alive in Obftistvi (approximately 50.294, 14.476) between August 2016 and August 2018 and subse- quently posted in the Entomologické Forum (a Czech entomological online forum). Broken bamboo poles inhabited by larvae and adults were found between June and Au- gust. Adults usually hatched in August. Along with Chlorophorus annularis, species of Anthribidae, Bostrichidae and Curculionidae were found (pers. comm. P. Jansa 2020). The specimens are deposited in the collection of Vaclav Hanzlik. A second occurrence of the species was recorded from Horni Poéernice around the year 2000 by a local entomologist (pers. comm. P. Jansa 2020). The specimen came from a company that imports bamboo furniture and sticks and was collected at light in a warehouse window. Both new records are the first of the species in Czech Republic for over 60 years. Denmark. Seven specimens hatched out of bamboo sticks in Hesselager on Funen Island (approximately 55.175, 10.744) between the 15" July and 15 August 2016. They were collected by Henning L. Hansen and identified by Jorn Misser. The find consisted of larvae in bamboo sticks imported from Vietnam out of which seven adults hatched. The specimens are preserved in the collection of Jorn Misser. France. Several specimens hatched out of a bamboo bed inside a home in Besse- sur-Issole (approximately 43.339, 6.197) on the 17" of April 2008 and were collected by Jean-Yves Poirier-Baldovini. The bed was imported from Indonesia and exhibited multiple exit holes (Fig. 1D). A specimen hatched out of a bamboo broomstick from a workshop in Le Crés (approximately 43.643, 3.93) in April 2014 and was recorded by Jéréme Sudre. The broomstick exhibited multiple exit holes, but no more specimens were found. We assume that additional specimens escaped the location. Germany. A specimen hatched out of an imported bamboo sofa in Hamburg on the 8" of August 1991. The specimen was imported from Bali (Indonesia) and subse- quently deposited in the ZMH collection. A specimen (Fig. 1E) was recorded alive on the 23" of August 2020 in a garden in Hans-Dewitz-Ring, 21075 Hamburg (Harburg) (53.4596, 9.9459) by Maren Liittke. The specimen was found on a wooden fence in close proximity to a ca. 15-year-old ornamental bamboo plant. The specimen was not preserved and only recorded with a smartphone camera. This is the third record for Hamburg and the first since 55 years. Netherlands. One specimen (Fig. 1F) was found in Wageningen, Gelderland (51.9877, 5.6673) on the 18" of August 2011 and subsequently reported on waarne- ming.nl. The specimen was found alive under a pile of bamboo sticks that was pur- Non-native Chlorophorus annularis in Europe ie Figure |. Chlorophorus annularis specimens and host plants of new records A=C Objiistvi, Czech Repub- lic (photos by P. Jansa & V. Hanzlik) D Besse-sur-Issole, France (photo by J. Poirier-Baldovini) E Ham- burg, Germany (photo by M. Liittke) F Wageningen, the Netherlands (photo by D. Belgers) G Braintree, United Kingdom (photo by S. Rolls) H Lincoln, United Kingdom (photo by S. Cotter) I Stirchley, United Kingdom (photo by A. Slater) A, B emerging specimen from bamboo stick C, E-I emerged specimens D exit holes in bamboo furniture of Besse-sur-Issole specimens. chased from a garden center (pers. comm. D. Belgers). This represents the first record of the species for the Netherlands. United Kingdom. A specimen (Fig. 1G) was found alive in Braintree (approximately 51.903, 0.569) on the 1* of July 2018 and subsequently reported on iRecord. The speci- men is suspected to have come from bamboo bought from a horticultural supplier. An- other specimen (Fig. 1H) was found alive at Think Tank, Lincoln (approximately 53.228, -0.555) on the 23" of September 2019 and subsequently reported on iNaturalist. The 8 Matthias Seidel et al. / BioRisk 16: 1-13 (2021) Figure 2. Occurrence of Chlorophorus annularis in Europe (red: new records; black: literature records). specimen was found on a window and most likely came from a bundle of bamboo sticks stored in an office (pers. comm. Sheena Cotter). It was released outside after photography. A third specimen (Fig. 11) was found alive in Newlands Road, Strichely (approximately 52.429, -1.913) on the 9" of October 2020 and subsequently reported on the Record App. ‘The specimen was found in a garage, in which bamboo was stored (remark by Rob Tilling). These three records are the first to be recorded in over 13 years for the United Kingdom. Discussion We here present thirteen new records of Chlorophorus annularis from seven European countries including two new country records displaying the wide spread of this com- monly overlooked non-native species. Most records were provided by citizen scientists, clearly displaying the impact of taxonomic interest forums and recording platforms such as iNaturalist, iRecord and waarneming.nl to provide data for rare and non-native species. Other social media platforms, such as Facebook, also provide an invaluable tool in biological recording of invasive species, as many records are sent into entomol- ogy and nature-themed groups, where both amateurs and scientists help in identifying them. The awareness raised by these citizen science tools may, in the future, even help to act as an early warning system for invasive species. Despite custom controls at import sites, like harbors and airports by national plant protection services and despite international standards for the importation of products and wood packaging, more and more invasive species arrive in Europe and are intercepted (see all Pest alerts from European Plant Protection Organization (EPPO/OEPP)). However, Non-native Chlorophorus annularis in Europe 9 even more accidental imports remain undetected or are discovered only years after the in- troduction, potentially facilitating the establishment of detrimental species. This may also be true in the case of C. annularis, which resembles local species across Europe and hence may often be mistaken and not recognized. Therefore, the number of specimens reaching Europe every year likely remains grossly underestimated. This may also explain, why the species so far has not been reported from the Scandinavian Peninsula, Balkan countries and European countries east of Germany (Czechia, Austria and Hungary). Similarly, Por- tugal, Switzerland and Ireland in western and Central Europe currently lack records. Yet, it remains likely that the species is also imported into these countries via the bamboo trade. While the species has been intercepted in many European countries, it is mostly represent- ed by single or a few individuals, which are clearly associated with the substrate they were imported with, and hence are likely not established. However, current records from Genk, Torhout (Belgium) and Hamburg (Germany), where the species was found without direct association to an imported product, may indicate that C: annularis could establish in Euro- pean countries other than Spain. However, due to a lack of data it is currently not predict- able where. Furthermore, climate change may facilitate future establishment, where host plants are available. These conditions could be met in the major cities of southern Europe. Therefore, recent records in Sicily and in the Hérault and Var departments in southern France are concerning and should be further surveyed. One tool to do so may be directed citizen science efforts as recently done in several European countries, for example for the Asian hornet Vespa velutina or for non-native mosquitoes (Walther and Kampen 2017). In order to use the power of citizen science for the monitoring of non-native spe- cies more effectively, two approaches may be specifically promising. On the one hand, specialized platforms introducing non-native species of interest to the general public and providing reporting tools may increase public awareness and also recording activi- ties for these taxa. On the other hand, drawing records of specific non-native species of interest, which are flagged and regularly exported from other citizen science databases and platforms may help to provide a better overview of distributions of these taxa. Both approaches combined may be the most effective way to channel citizen science activities towards a better monitoring of non-native species. Acknowledgements We thank Rodica Serafim (Grigore Antipa National Museum of Natural History, Bu- charest, Romania), Aslak Kappel Hansen (Zoological Museum, Copenhagen, Den- mark), Michael Geiser (Natural History Museum, London, United Kingdom) and Zdenko Lucbauer (Malacky, Slovakia) for information on Chlorophorus annularis. 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