Research Article |
Corresponding author: Martin Husemann ( martin.husemann@uni-hamburg.de ) Academic editor: Oliver Hawlitschek
© 2022 Viktor Hartung, Martin Heller, Martin Husemann.
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.
Citation:
Hartung V, Heller M, Husemann M (2022) First record of the invasive true bug (Heteroptera) Halyomorpha halys (Stål, 1855) from Hamburg with other records from Northern Germany and possible implications for its range expansion. Evolutionary Systematics 6(1): 57-64. https://doi.org/10.3897/evolsyst.6.80744
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The invasive pentatomid true bug Halyomorpha halys is reported for the first time from the German state of Hamburg, along with records from several other locations in Northern Germany. Specimens collected by scientists were evaluated along with records from citizen science platforms. DNA barcode sequences of several H. halys specimens from Hamburg were evaluated along with 42 sequences of the species from across the world in a haplotype network analysis demonstrating that all specimens studied from Hamburg had the haplotype H3. The present state of distribution of H. halys in Germany, patterns of range extension, invasiveness, and possible economic impacts are discussed.
biological invasions, neobiota, insect pests, accidental introduction, agricultural pest
Hamburg, as one of the main harbor cities of Germany, has long been known as a major hub of non-native and invasive species. Already in 1900, Kraepelin reported almost 500 non-native species in the Hamburg harbor, many of which were insects (
Halyomorpha halys was originally distributed in mainland China, Hainan, Taiwan, Japan, Korea and Northern Vietnam (
In Germany, the first H. halys specimens were found in October 2011 at the port of Bremen in Northern Germany, arriving from the USA with a package of machine parts (
Here, we report the first documented findings of H. halys from Hamburg, corroborated by photos and with voucher specimens deposited in the collection of the Zoological Museum in Hamburg (
In addition to our own collections, records for H. halys on the citizen science platforms iNaturalist.org, naturgucker.de, and neobiota-hamburg.de were evaluated. Colleagues from natural history institutions in Northern Germany were requested to report occurrences of the species. For online platforms, only those records with a voucher photo were considered and only the finds from Northern Germany were included in the present study. We define Northern Germany as the area of Germany north of the 52. parallel (roughly corresponding to the line between the cities of Münster and Magdeburg), which constitutes most of the North German Plain geographical region. Only the records present on the platforms as of 06.11.2021 were considered in the present study. Berlin was excluded from the survey, since H. halys has been known from the city for a longer time already (
For DNA barcoding sensu Hebert and co-authors (2004), six specimens from two locations in Hamburg-Hamm (53°33'25.2"N, 10°03'09.1"E; 53°33'25.5"N, 10°03'13.5"E) were analyzed. Specimens are deposited in the Zoological Museum of Hamburg (
A TCS network was constructed using PopArt (
M. Heller reported three juvenile specimens (ZMH844214–ZMH844216) from a Nasturtium plant on his balcony in Hamburg-Hamm (53°33'25.2"N, 10°03'09.1"E) on the 07.07.2021 at the online portal www.neobiota-hamburg.de. Three additional specimens were collected by the authors on 23.07.2021 (ZMH844217–ZMH844219) and further specimens were recorded on the 25.08.2021 and 13.09.2021 close to the original location (53°33'25.5"N, 10°03'13.5"E) on Rubus fruticosus. Morphological identification was unequivocal, as H. halys is the only pentatomoid species in Germany bearing large spines on the pronotum as nymphs (Fig.
A. Habitat in Hamburg-Hamm; B. Halyomorpha halys nymph in situ on a Rubus fruticosus leaf; C. An older nymphal instar photographed in the lab.
The species identification was further confirmed by DNA barcoding. Five specimens were successfully sequenced. All sequences represented a single haplotype. The sequence was deposited in NCBI Genbank under accession MZ828400. It represents the haplotype H3 from Yan et al. (2021) and
TCS haplotype network generated for COI-sequences of Halyomorpha halys specimens from Hamburg and those available via NCBI and BOLD. Each line represents a single mutational change whereas small black lines indicate missing haplotypes. The diameter of the circles is proportional to the number of haplotypes sampled (see given open circles with numbers). The most common haplotypes H1 and H3 are marked.
In addition, the online citizen science platforms iNatursalist.org and naturgucker.de delivered records of H. halys of which the IDs could be verified by photos. Two reports from Hamburg (one from Schnelsen in Eimsbüttel and another without precise coordinates) were uploaded on iNaturalist in October 2021. There was also a single adult specimen from Bremen (campus of Bremen University, Horn-Lehe) and a single adult from Braunschweig (carpark of Johann Heinrich von Thünen Institute) collected by museum staff. iNaturalist.org and naturgucker.de delivered additional records for other cities in Northern Germany: Osnabrück (1), Hameln (1), Magdeburg (1), Müritz National Park (1), Kaltenweide in the region of Hannover (1), Braunschweig (2) and Hannover (4). All collection information is summarized in Suppl. material
Halyomorpha halys distribution in Northern Germany, own records (dark red) and records from citizen science platforms (white). Berlin is coloured all white due to numerous records that are not shown here in detail. Made with QGis 3.16.10.
Several records from citizen science platforms were not considered valid due to poor quality photos or depicting first nymphal instars that are not easy to distinguish from other species of Pentatomidae): Bremen (https://www.inaturalist.org/observations/63811907), Rehhorst (https://naturgucker.de/?bild=1147003753), Lüneburg (https://naturgucker.de/?bild=231118762), Hannover (https://naturgucker.de/?bild=170137063) . Also, there is a record from Estedt (Saxony-Anhalt) made on 31.03.2019 (naturgucker.de), a record from the vicinity of Wennigsen (Lower Saxony) made on 07.06.2020 and a record from Strausberg (Brandenburg) made on 11.08.2021 (naturgucker.de) that cannot be verified due to the lack of a photo.
The specimens collected or documented in Hamburg provide the first record of the invasive H. halys for this German state. Together with first occurrences in Bremen and Mecklenburg-Western Pomerania (Suppl. material
However, it is interesting to note that predictions of possible geographical occurrence based on ecological niche modelling did not anticipate the arrival of H. halys in Northern Germany in all models. The model applied by
The distribution patterns of H. halys and factors determining its distribution have been subject of many studies (summarized in e.g.
Based on the number and age of the detected specimens in the invasive area and the circumstances of their detection, four relative stages of their range expansion, colonization, and invasion spread can be described. These stages probably do not reflect any biological characters of H. halys, but help to characterize the probable current condition of a local population (Fig.
The question of the possible economic impact of H. halys in Hamburg and neighboring areas is a complicated one. On the one hand, since the species is known to damage fruit (
On the other hand, not every region where this invasive species was established is doomed to suffer serious economic damage. Examples from the USA (
The ecological niche model studies cited above (
All this is of course not a good reason to give up caution, even for Hamburg, since climate change may alter the situation and make the region more suitable for H. halys in the future. Still, the circumstances described above may provide some time to establish a monitoring scheme in the region (probably involving citizen scientists, since such an approach proved to be a valuable tool in the study of the species as e.g.
We thank the Bürgerstiftung Hamburg, the University of Hamburg, and the BUKEA Hamburg for funding for the web portal neobiota-hamburg.de, on which the first specimens of H. halys were reported. Further, we are grateful to all citizen scientists contributing to the portal. We thank Timo Wehrt for generating the sequences. Wolfgang Dorow (Naturmuseum Senckenberg, Frankfurt) provided a specimen from Braunschweig and Volker Lohrmann (Übersee-Museum Bremen) reported one from Bremen. Tim Haye (CABI, Delémont, Switzerland) helped with literature. Ingo Wendt (State Museum of Natural History Stuttgart), Rainer Steinle and Dorothee Steinle (Gardening Consulting Service Gartenbaulicher Beratungsdienst für integrierten Gemüsebau Heilbronn e.V.) provided contact details and/or shared information on the economic impact of H. halys in Baden-Württemberg. Michael Raupach (Bavarian State Collection of Zoology, Munich) and Oliver Hawlitschek (LIB, Hamburg) made many useful suggestions on a previous version of the paper that helped to improve its quality. We finally thank the LIB for funding for the open access publication of this article.
Table S1
Data type: excel file
Explanation note: Records of Halyomorpha halys in Northern Germany
Table S2
Data type: docx file
Explanation note: Sequences used for COI network analysis