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Article

Ctenolepisma longicaudatum Escherich (1905) Became a Common Pest in Europe: Case Studies from Czechia and the United Kingdom

1
National Reference Laboratory of Vector Control, National Institute of Public Health, Šrobárova 49/48, 100 00 Prague, Czech Republic
2
Department of Zoology and Fisheries, Czech University of Life Sciences Prague, Kamýcká 129, 165 00 Prague, Czech Republic
3
Killgerm Chemicals Ltd., Wakefield Road, Ossett WF5 9AJ, UK
4
Department of Food, Environmental and Nutritional Sciences (DeFENS), University of Milan, Via Celoria, 2, 20133 Milan, Italy
*
Author to whom correspondence should be addressed.
Insects 2021, 12(9), 810; https://doi.org/10.3390/insects12090810
Submission received: 21 July 2021 / Revised: 5 September 2021 / Accepted: 8 September 2021 / Published: 10 September 2021
(This article belongs to the Section Insect Societies and Sociality)

Abstract

:

Simple Summary

Ctenolepisma longicaudatum, an invasive silverfish species, has high tolerance to low humidity and temperatures and has been passively introduced to the majority of European territory. Its presence may cause stress and discomfort to people inhabiting or working the infested areas. In addition, it may cause damage to organic materials, contaminate food and carry microbes. This paper summarizes the available data on its spreading and current distribution of species in Europe and displayed the species is present throughout the continent including Scandinavia. This northward shift of C. longicaudatum might be explained by use of the insulation and central heating to provide optimal climate for the species to establish. The paper also contains updates on the current status of C. longicaudatum in Czechia, United Kingdom, and Ireland, where its first populations were recently detected. Based on the collected data, the spread in the monitored countries continues rapidly, when the domestic settings were the main habitat. Furthermore, the species is often present in accommodation facilities, warehouses, factories, public institutions, shopping malls, archives, museums, and art galleries. Therefore, the study indicates the species may occur everywhere indoors. The paper also highlights an urgent need for establishment of effective pest management strategy and preventive measures.

Abstract

Synanthropic invasive silverfish, Ctenolepisma longicaudatum, has been recently reported to cause nuisance in the indoor environment in many European countries. To get more details on the species distribution, the species occurrence was monitored by the authors in the countries where establishment of C. longicaudatum has been revealed in the last years. In Czechia, 20 findings from 14 municipalities in eight regions were recorded within the last three years. In the United Kingdom, 49 cases, including the first occurrence in Scotland, were recorded. Five cases were recorded for the Republic of Ireland. Domestic settings were the main habitat in the study countries (50.0% for the Czechia and Ireland and 36.8% for the United Kingdom). Regarding C. longicaudatum control, the standard silverfish strategy fails, and the use of insecticidal baits complemented by dust insecticides was suggested as the most promising approach. To reveal presence of C. longicaudatum in Europe, the search of literature, social platforms and databases on invasive species was conducted. According to these sources, the species is known from majority of European countries, when the high increase of records in recent decade was detected.

Graphical Abstract

1. Introduction

Biological invasions, in general, cause huge global environmental and socio-economic losses [1], when intercontinental traffic is known to be one of the main sources of non-native organisms [2] and anthropogenic activities are the main driver of non-native species introductions. Therefore, the synanthropic species can become invaders in human infrastructure and urban environments, even if their survival in wildlands may be limited by local climatic conditions [3].
Ctenolepisma longicaudatum Escherich (1905) (Zygentoma; Lepismatidae), a wingless primitive insect, whose adults can live for a long time and continue to molt. The species also known under the common names of giant silverfish, gray silverfish, long-tailed silverfish, or paperfish [4,5] is a synanthropic invasive pest from the family Lepismatidae, with uncertain native range [6,7], even though some authors speculate that it may originate from the central parts of America [7]. The species was described by the German entomologist and professor of zoology Karl Leopold Escherich in 1905 based on type material collected in the Orange Free State, Republic of South Africa [8]. Recently, the gender of the genus was shifted from feminine to neuter, and so, the species name should be changed from longicaudata to longicaudatum [9]. The species was synonymized with Ctenolepisma coreana Uchida (1943), Ctenolepisma dives Silvestri (1908), Ctenolepisma pinicola Uchida (1964), Ctenolepisma urbana Slabaugh (1940), and Lepisma corticola Ridley (1890).
Apart from other European synanthropic silverfish species, C. longicaudatum can survive long periods of starvation [4] and tolerate low indoor humidity and temperature levels [10]. The development time in optimal conditions is one and a half years, while it could also reach for up to three years [11]. Then, the lifespan of this silverfish has been reported to be up to seven years [12]. Therefore, it has the potential to inconspicuously become a dominant pest in the indoor environment in future years.
Even though C. longicaudatum is mainly nuisance in homes and pest in museums and archives, some attention from public health point of view has been also paid to silverfish activity. Generally, the crawling insects, including silverfish, are known to be sources of inhalant allergens [13]. From this point of view, tropomyosin was identified as the major allergen of Lepisma saccharinum by Barletta et al. [14], and its presence in other silverfish species is thus probable. Furthermore, several gregarines were found in the intestines of various silverfish species, with Gregarina ctenolepismae and Lepismatophila ctenolepismae associated with C. longicaudatum [15]. Recently, an association of opportunistic bacteria with C. longicaudatum has been reported in unpublished data of F. Boiocchi. Indeed, bacteria of the genus Staphylococcus, Acinetobacter, Bacillus and Kocuria were isolated from both the exoskeleton and internal structures of specimens of C. longicaudatum. Being this insect species commonly found within human dwellings, the carriage of opportunistic pathogens could represent a risk for human health. Despite a direct transmission from the insect to a human host has never been recorded, it is plausible to assume that these insects could mechanically disperse across the household bacterial cells able to cause infections in humans. This risk would be higher for immunocompromised people. Furthermore, pores and mycelial fragments of the fungi were proved to be transmitted by C. longicaudatum [16]. As aggregations of C. longicaudatum usually appear close to their sources [17], food contamination may potentially be another risk factor for humans. Nevertheless, no evidence supporting this hypothesis is currently available. The activity of such pests may generate stress and discomfort to people inhabiting or working in infested buildings [18]. Moreover, the species is considered to be an economic pest [19] due to its feeding on paper, book bindings, books, wallpaper, papier-mâché, photos and plant-based materials such as cellulose and starch [20,21]. In addition, the species can damage fabrics, especially cotton [22,23]. For these reasons, it is listed as a pest among museums and gallery with a possible devastating impact on art paintings, books, and documents [24] and where the damage costs might be incalculable. The costs of damage could be especially high when occurring in heritage sites. For instance, C. longicaudatum was also found on board historic ships in the United Kingdom [25].
Although the presence of C. longicaudatum has already been reported throughout Europe [11,26,27,28], the current range and distribution of this species is considered to be underestimated due to its cryptic behavior, likely misidentification when found and low awareness of the importance of reporting the species occurrence. Therefore, we aimed to present a review of the current status of C. longicaudatum across Europe and to gather information about its occurrence in the Czechia and the United Kingdom three and six years after the first records there of a case of spread of this synanthropic species using citizen science and social media.

2. Materials and Methods

2.1. Data Collection

The records of C. longicaudatum in Europe were collected from the publicly available on-line databases and social platforms (see Table 1). All data from databases were filtered using the categories “species” and “country”.
In Czechia, citizen and pest control service reports of the species were collected and documented by entomologists of the National Institute of Public Health in Prague (NIPH). Moreover, the group objected to the determination of invertebrates on Facebook (https://www.facebook.com/groups/bezobratli, accessed on 29 March 2021) was regularly checked for the presence of suspicious pictures.
In case of the United Kingdom, the records from internal database of Killgerm Chemicals Ltd. insect identification service (https://www.killgerm.com/technical/insect-identification/, accessed on 22 March 2021) and from a 12-month citizen science project carried out in Birmingham (UK), which surveyed the complete household arthropod community, were included. Furthermore, the literature research was performed using online databases, Web of Science, Scopus, and Google Scholar.

2.2. Case Regions

2.2.1. Czechia

In this study, we aimed to gather information on the occurrence of C. longicaudatum throughout Czechia, three years after its first record [26]. The issues of this species invasion and the potential consequences were presented to both academics and professionals using various conferences and local journals, in order to increase awareness and prevent further spread. For the purpose of this study, only photos with clear morphological patterns were used. Selected localities were also inspected personally by employees of the NIPH. The captured specimens (see Figure 1) were determined using entomological keys [6,29], euthanized, and deposited at the National Reference Laboratory of Vector Control at NIPH.

2.2.2. United Kingdom and the Republic of Ireland

In the United Kingdom and the Republic of Ireland, the first record of C. longicaudatum, in a domestic premise, was from 2014 in Reading, England [30]. Killgerm records of C. longicaudatum are provided from, in most cases, insect identification of physical specimens. The remainder was obtained from photographs with clear morphological patterns. The identifications were undertaken by entomologists from the Technical Department of Killgerm Chemicals Ltd. Regarding the citizen science project, volunteers in the Birmingham area were recruited and trained to carry out arthropod collection in their homes using sticky traps for crawling insects and a pooter and spider catcher for active capture. The volunteers collected household arthropods across 12 months, from November 2018 to October 2019, providing a record of the arthropods present within the households. The captures were stored in a domestic freezer (active collection) or in a sticky trap until monthly collection, and the species were then identified by an entomologist. The aim of the citizen science project was to investigate the household arthropods community in the Birmingham area, but also to explore the possible microbiological risks associated with them. Therefore, after the identification, the insects were analysed with microbiological techniques in order to isolate bacterial strains and assess the potential health hazard represented by these arthropods.

3. Results

Based on searches of selected databases and in addition to previously published and confirmed occurrences, the vast majority of the European territory was considered to have been invaded by C. longicaudatum (Figure 2). The oldest verified record is from 1978 in Spain, and the oldest unpublished record is from 1941 in Portugal. Various European countries and regions, including Czechia and the United Kingdom, have been invaded in recent years. By 1999, the species officially occurred in seven countries, mainly from western and southern Europe. In 2000–2021, evidence of C. longicaudatum is available throughout Europe, except in a few eastern European countries (Belarus, Bosnia and Herzegovina, Bulgaria, Kosovo, Latvia, Moldova, Montenegro, North Macedonia, Romania, and Serbia) and mini-states such as Andorra, Liechtenstein, Monaco, San Marino, and the Vatican.
Regarding C. longicaudatum in Czechia, 20 confirmed reports of the species from 14 municipalities in eight regions (Table 2 and Figure 3a) were collected by March 2021. Prague (7) had the highest number of invasions, followed by Moravian-Silesian (4), South Moravian (2), and Central Bohemian (2) regions.
From October 2017 to January 2021, Killgerm reported records from England (14), Scotland (1), and the Republic of Ireland (2). Furthermore, the citizen science research showed the species is present in households in Birmingham (England) from October 2018 to November 2019. A total of 96 individuals of C. longicaudatum were recovered from six out of 20 households surveyed during the year of collection. The National Biodiversity Network records show cases in Northern Ireland (3) from 2016 to 2018. Further records were added from the available social platforms and databases (Figure 3b and Table 3).
As shown in Figure 4 and Table 4, the highest abundance of records was found in Norway, where the pest control services reported more than 5000 interventions against C. longicaudatum. More than 100 cases of gray silverfish have also been documented in Belgium, Netherlands, Spain, and Italy. More than 50 observations were reported from Azores, Denmark, France, Germany, Portugal mainland, Spain mainland, and Sweden. On the other hand, only a single occurrence of the species is known from Iceland, Croatia (Brać Island), Slovakia, and Slovenia. The single record of the species is known from Cyprus; however, the two other surveyed databases reported the presence of C. longicaudatum.

4. Discussion

The assumption that the current distribution of C. longicaudatum in Europe is underestimated was confirmed, when the study revealed growing number of reports throughout the continent from scientific literature, databases of invasive species and social platforms. Although the identification of silverfish from photographs might be sometimes confusing, C. longicaudatum is as different from another European synanthropic species as such identification is possible [27] and the majority of the reports uploaded on the investigated social sites seem to be identified correctly. Anyway, the further collaboration among local entomologists, citizens and pest control services is essential to confirm the distribution area of the species. Additionally, the data collected on social networks indicated that C. longicaudatum is present (and sometimes even abundant) in countries without published reports of C. longicaudatum. The widespread presence of this silverfish was also supported by reports of new localities in countries with known occurrence of the species. Apparently, the frequency of new introductions has been rising in recent years, and further spreading is thus expected. The species is strictly synanthropic and does not occur outdoors; therefore, its spread is not limited by climate. Thus, it has recently become well established, even in northern Europe. For instance, in Norway, the species was officially registered in 2014, and the number of reported infestations escalated from nine to 3433 cases in 2018 [18]. From this point of view, the confirmation of gray silverfish establishments in the up-to-date non-colonized countries are expected very soon. In particular, considering the fact that some of those states are surrounded by areas with common C. longicaudatum nuisance, confirmed cases are rather the tip of the iceberg. It is also possible that the species is present but unrevealed in these areas. In the Faroe Islands, the occurrence of this silverfish pest was not known in 2019, when it was revealed in the Facebook survey conducted by Thomsen et al. [27] that C. longicaudatum is widespread in private houses as well as in public institutions. This is in agreement with the citizen science study from Birmingham, where almost one-third of the monitored sites were proven to be infested by C. longicaudatum. From this point of view, social platforms and citizen science appear to be useful tools to monitor species distribution. On the other hand, the sampling programs should be conducted to reveal the real status of the species in the countries with no confirmed presence of C. longicaudatum. For instance, some of them such as Andorra, Liechtenstein, Monaco, San Marino, and Vatican are surrounded by the countries where the species has been reported abundant for years, and so, their unregistered occurrence there is therefore highly probable.
Ctenolepisma longicaudatum is not exploited by humans and is transported unintentionally as an unseen invader; thus, even if reasonable, it is not possible to simply ban the import of the species. Therefore, its inclusion in the updated list of invasive alien species of European Union concern (Regulation 1143/2014; the so-called Union list) is likely to be totally ineffective. The higher effectiveness of any regulation is not related to increasing knowledge of the general public, as in the case of ornamentals and pets [44]. The focus should be on traders and conveyers who would be trained in mandatory preventive timely treatment of cardboard boxes and similar materials before transport.
In Czechia, the first establishment of the C. longicaudatum population was reported in warehouses and surrounding office buildings in 2017 [26]. Subsequently, within the next three years, the presence of C. longicaudatum was recorded throughout the country. As expected, the flats (nine records) were found to be the main habitats of the species. In contrast, five records of C. longicaudatum were obtained from warehouses. Interestingly, repeated introductions have been reported in the warehouse of a pharmaceutical company in Prague, the capital of Czechia. In 2019, one individual and several exuviae (n < 10) were found in barrels imported from Japan (Sejkora R., pers. comm. 2019), where C. longicaudatum was established in the 1990s [45]. Although museums, libraries, and archives were mentioned as the main habitat of C. longicaudatum in the past [33,46], only one such case was reported in Czechia. In 2018, the presence of C. longicaudatum was revealed by the National Gallery Prague. Fortunately, the staff detected the pest activity relatively soon, when the damage was found on the reverse side of the exhibited paintings where the glue was applied. No serious damage to the paintings was observed. Both room and artworks were then treated with biocides. Despite the early successful eradication, this finding is alarming and underlines previous notes on art collections caused by C. longicaudatum. Moreover, the lack of maintenance during shutdowns of connected to COVID-19 pandemic may result in exponential development of the silverfish populations in such institutions [47].
In the United Kingdom, C. longicaudatum has especially been detected in the domestic environment, but findings of the “What’s Eating your Collection” and “iNaturalist” databases revealed that the species is often present in accommodation facilities, archives, museums, and warehouses. The first evidence of C. longicaudatum in Scotland came from Aberdeen (Table 4), and it was suspected to have been introduced from Norway, via international travel by the resident (G. MacKay., pers. comm. 2021), according to discussions with the pest control operator. Regarding the report from a museum, the background of only a single event from southeast London (Table 4) is known, and the pest control operator reported C. longicaudatum among historical papers/books, paper goods, and clothing, but no damage was observed. In Ireland, two findings of the species in a domestic setting were complemented by one silverfish report from the medical center and two unknown localities (Table 4).
The novel data from the studied countries confirmed households as a major habitat of C. longicaudatum. This phenomenon is known, for instance, in the Faroe Islands, the Netherlands, and Norway, where the species has become a major household species [17,23,27,48]. Additionally, the inhabitants of houses are often unaware of their occurrence due to the hidden activity of silverfish pests. For instance, Witteman et al. [49] reported many homes in which the inhabitants were unaware of the presence of silverfish to contain silverfish antigen concentrations indicative of silverfish exposure. Therefore, the real levels of activity might be even higher than expected. The hypothesis of spreading using cardboard boxes and industrial, manufacturing, and warehouse facilities as one of the primary habitats suggested by Kulma et al. [26] was also supported by records of such species in these facilities in several regions throughout both countries.
The increasing intensity of records throughout the case regions highlighted the urgent need for reliable pest management. The authors recommended eradication at all the investigated localities. Based on the feedback provided by the companies in Czechia, the pyrethroids applied by spraying or smoke generator by the professional control services reduced silverfish abundance for a few months. However, the re-emergence of this species was reported by the employees of infested institutions. The species is considered to be sensitive to conventional pesticides [18,50], but the regular application of biocides containing similar active substances is not recommended because of the risk of resistance development [51]. Moreover, the suitability of commonly used insect control programmes of Integrated Pest Management (IPM) such as nitrogen or anoxia fumigation against giant silverfish due to hidden life is questionable. In view of this, novel approaches to control C. longicaudatum have recently received some attention. For instance, Wilke et al. [24] recommended a warm air eradication technology. The local use of heat treatment in cavities might also be beneficial according to Aak et al. [18], who also pointed out that C. longicaudatum inhabits spots inside walls, where the heat hardly penetrates. In light of this, the use of poisoned baits seems to be the most promising strategy. The laboratory bioassay conducted by Aak et al. [17] showed that baits with indoxacarb, clothianidin, and fipronil killed more than 90% of the insects; however, high secondary toxicity was observed in indoxacarb bait only (>75%). Therefore, same authors [52] also verified the effect of such a substance in the field and reached >90% population decline with minimal bait consumption. Therefore, using baits containing indoxacarb might be an economic and efficient strategy against this target species. Similarly, a field test in the Netherlands revealed that baits containing clothianidin caused a 93% population reduction [53]. Aak et al. [51] also highlighted that proper training in bait placement and improved knowledge of C. longicaudatum bionomy is crucial for achieving efficacy similar to that of commonly used sprayable insecticides.
Maintenance of low humidity is generally recommended to eliminate the risk of silverfish nuisance. However, this measure was designed for L. saccharinum and could not be effective enough for C. longicaudatum because of its low environmental requirements. Therefore, preventing the introduction of this species is difficult. The risk of contamination might be reduced by proper handling of incoming materials and rapid elimination of packages [18,54]. In the case of museums, libraries, and historic buildings, the IPM involves sealing the building against pest entry, adapting the micro-climate, maintaining high hygienic standards, quarantining all new and incoming objects, and regular monitoring of pest infestations with traps [21]. Nevertheless, a 100% reliable prevention will require costly and logistically challenging measures such as heat, cold, or freeze treatment of the entire moving load [18]. Therefore, further campaigns on this invasion, including the development of novel approaches for both prevention and control, are essential. In addition, pest controllers should be educated in order to correctly identify the species and establish proper management.

5. Conclusions

The study proved the monitoring of social platforms and citizen science might be useful tools to monitor the invasion of C. longicaudatum. On the other hand, these records have to be considered carefully due to probability of misidentification in certain cases. The collaboration between pest controllers and entomologists is thus highly needed. Based on the confirmed events throughout the case countries, the invasion of C. longicaudatum in Europe continues. Moreover, the data by citizen science study showed that the species distribution is most likely extremely under-recorded and C. longicaudatum is currently one of the common nuisance indoor pests. Moreover, the insulation and central heating providing a stable dry and warm environment, serving as a perfect environment for C. longicaudatum and is probably a reason of its shift northward. Similar conditions exist in museums and galleries; thus, an increasing number of new records are expected in regions where C. longicaudatum is or will be introduced. It follows from the above mentioned that the early identification and control of pests especially in museums and galleries, including C. longicaudatum, should be given high priority according to the importance of keeping safe art paintings and other valuable materials in collections for the future.

Author Contributions

M.K.: Conceptualization, data curation, funding acquisition, investigation, methodology, project administration, writing—original draft, writing—review and editing; T.B.: data curation, investigation; M.P.D.: data curation, investigation, writing—original draft, writing—review and editing; F.B.: data curation, investigation, writing—original draft, writing—review and editing; J.P.: conceptualization, data curation, methodology, supervision, visualization, writing—original draft, writing–review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

MK and TB were supported by the Ministry of Health CZ-DRO (National Institute of Public Health, NIPH, 75010330) for its financial support. JP was supported by the Technology Agency of the Czech Republic within the project “DivLand” (SS02030018).

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors thank Miloslav Petrtýl for the photos and involved citizens for their help with data collection.

Conflicts of Interest

The authors have no potential conflict of interest concerning the present study. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Vila, M.; Hulme, P.E. Impact of Biological Invasions on Ecosystem Services (Invading Nature—Springer Series in Invasion Ecology, 12); Springer International Publishing AG: Cham, Switzerland, 2017. [Google Scholar]
  2. Sardain, A.; Sardain, E.; Leung, B. Global forecasts of shipping traffic and biological invasions to 2050. Nat. Sustain. 2019, 2, 274–282. [Google Scholar] [CrossRef]
  3. Shochat, E.; Lerman, S.B.; Anderies, J.M.; Warren, P.S.; Faeth, S.H.; Nilon, C.H. Invasion, Competition, and Biodiversity Loss in Urban Ecosystems. Bioscience 2010, 60, 199–208. [Google Scholar] [CrossRef] [Green Version]
  4. Lindsay, E. The biology of the silverfish, Ctenolepisma longicaudata Esch. with particular reference to its feeding habits. Proc. R. Soc. Vic. 1940, 52, 35–83. [Google Scholar]
  5. Hasenfuss, I. A possible evolutionary pathway to insect flight starting from lepismatid organization. J. Zool. Syst. Evol. Res. 2002. [Google Scholar] [CrossRef] [Green Version]
  6. Wygodzinsky, P.W. A review of the silverfish (Lepismatidae, Thysanura) of the United States and the Caribbean area. Am. Mus. Novit. 1972, 2481, 1–25. [Google Scholar]
  7. Zettel, J. Springtails and Silverfishes (Apterygota); BioRisk: Bern, Switzerland, 2010; Volume 4, Chapter 13.5; pp. 851–854. [Google Scholar]
  8. Escherich, K. Das System der Lepismatiden. Zool 1905, 18, 1–164. [Google Scholar]
  9. ICZN. Opinion 2427 (Case 3704)—Lepisma Linnaeus, 1758 (Insecta, Zygentoma, Lepismatidae): Direction 71 (1957) reversed. Bull. Zool. Nomencl. 2018, 75, 209–294.
  10. Lock, K. Distribution of the Belgian Zygentoma. Notes Fauniques Gembloux. 2007, 60, 27–29. [Google Scholar]
  11. Aak, A.; Hage, M.; Magerøy, Ø.; Byrkjeland, R.; Lindstedt, H.H.; Ottesen, P.; Rukke, B.A. Introduction, dispersal, establishment and societal impact of the long-tailed silverfish Ctenolepisma longicaudata (Escherich, 1905) in Norway. BioInvasions Rec. 2021, 10. in press. [Google Scholar] [CrossRef]
  12. Smith, G. A new Australian species of Acrotelsella (Zygentoma: Lepismatidae); could it be an endangered short range endemic? Soil Org. 2015, 87, 169–181. [Google Scholar]
  13. Panzani, R.C.; Ariano, R. Arthropods and invertebrates allergy (with the exclusion of mites): The concept of panallergy. Allergy Eur. J. Allergy Clin. Immunol. Suppl. 2001, 56, 1–22. [Google Scholar] [CrossRef]
  14. Barletta, B.; Felice, G.; Pini, C. Biochemical and Molecular Biological Aspects of Silverfish Allergens. Protein Pept. Lett. 2007, 14, 970–974. [Google Scholar] [CrossRef] [PubMed]
  15. Lindsay, E. Two gregarines from Ctenolepisma longicaudata, with notes on forms in other silverfish. Proc. R. Soc. Vic. 1939, 51, 99–111. [Google Scholar]
  16. Querner, P.; Sterflinger, K. Evidence of Fungal Spreading by the Grey Silverfish (Ctenolepisma longicaudatum) in Austrian Museums. Restaur. Int. J. Preserv. Libr. Arch. Mater. 2021, 42, 57–65. [Google Scholar]
  17. Aak, A.; Hage, M.; Rukke, B.A. Long-tailed silverfish (Ctenolepisma longicaudata) control; bait choice based on primary and secondary poisoning. Insects 2020, 11, 170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Aak, A.; Rukke, B.A.; Ottesen, P.S. Long-tailed silverfish (Ctenolepisma longicadaudata)—Biology and control. In Norwegian Institute of Public Health Report; Norwegian Institute of Public Health: Oslo, Norway, 2019; pp. 1–43. [Google Scholar]
  19. Smith, G.B. The Australian silverfish fauna (Order: Zygentoma) abundant, diverse, ancient and largely ignored. Gen. Appl. Entomol. J. Entomol. Soc. N. S. W. 2017, 45, 9. [Google Scholar]
  20. Van der Weijden, W.; Leewis, R.J.; Bol, P. Biological Globalisation: Bio-Invasions and Their Impacts on Nature, the Economy, and Public Health; KNNV-Uitgeverij: Utrecht, The Netherlands, 2007. [Google Scholar]
  21. Querner, P. Insect Pests and Integrated Pest Management in Museums, Libraries and Historic Buildings. Insects 2015, 6, 595–607. [Google Scholar] [CrossRef]
  22. Mallis, A.; Miller, A.C.; Hill, R.C. Feeding of four species of fabric pests on natural and synthetic textiles. J. Econ. Entomol. 1958, 51, 248–249. [Google Scholar] [CrossRef]
  23. Schoelitsz, B.; Brooks, M. Distribution of Ctenolepisma longicaudatum (Zygentoma: Lepismatidae) in The Netherlands. In Proceedings of the 8th International Conference on Urban Pests, Zurich, Switzerland, 20–23 July 2014; pp. 353–357. [Google Scholar]
  24. Wilke, N.; Sawyer, R.; Junk, O. Application Technology Humidity-controlled and warm-air pest eradication technology with a focus on museum collections and works of art. Int. Pest Control 2018, 60, 80–83. [Google Scholar]
  25. Davies, D. Bringing IPM to historic ships in the, U.K. In Integrated Pest Management (IPM) for Cultural Heritage; Nilsen, L., Rossipal, M., Eds.; Swedish National Heritage Board (Riksantikvarieämbetet): Stockholm, Sweden, 2019; pp. 95–104. [Google Scholar]
  26. Kulma, M.; Vrabec, V.; Patoka, J.; Rettich, F. The first established population of the invasive silverfish Ctenolepisma longicaudata (Escherich) in the Czech Republic. BioInvasions Rec. 2018, 7, 329–333. [Google Scholar] [CrossRef]
  27. Thomsen, E.; í Kongsstovu, S.; Dahl, H.A.; Mikalsen, S.O. Ctenolepisma longicaudata (Escherich, 1905): A common, but previously unregistered, species of silverfish in the Faroe Islands. BioInvasions Rec. 2019, 8, 540–550. [Google Scholar] [CrossRef]
  28. Sammet, K.; Martin, M.; Kesküla, T.; Kurina, O. An update to the distribution of invasive Ctenolepisma longicaudatum Escherich in northern Europe, with an overview of other records of Estonian synanthropic bristletails (Insecta: Zygentoma). Biodivers. Data J. 2021, 9, e61848. [Google Scholar] [CrossRef] [PubMed]
  29. Goddard, M.R.; Foster, C.W.; Holloway, G.J. Ctenolepisma longicaudata (Zygentoma: Lepismatidae) new to Britain. Br. J. Entomol. Nat. Hist. 2016, 29, 33–35. [Google Scholar]
  30. Theron, J.G. The domestic fish moths of South Africa (Thysanura: Lepismatidae). S. Afr. J. Agric. Sci. 1963, 6, 125–130. [Google Scholar]
  31. Christian, E. Die primär flügellosen “Urinsekten” (Apterygota). In Neobiota in Österreich; Essl, F., Rabitsch, W., Eds.; Umweltbundesamt: Wien, Austria, 2002; pp. 301–303. [Google Scholar]
  32. Thomas, L. Ctenolepisma Longicaudata—ny eller Gammel Sølvfisk for Danmark?—Side 1—Artikler—Nyheder—Fugleognatur.dk. 2017. Available online: https://www.fugleognatur.dk/forum/show_message.asp?page=1&MessageID=1669029&ForumID=4 (accessed on 3 March 2021).
  33. Silfverberg, H. Changes in the list of Finnish insects during 2001–2005. Entomol. Fenn. 2007, 18, 82–101. [Google Scholar] [CrossRef] [Green Version]
  34. Paclt, J. Thysanura: Fam. Lepidotrichidae, Maindroniidae, Lepismatidae. Genera Insectorum. 1967, 218, 1–86. [Google Scholar]
  35. Meineke, T.; Menge, K. Ein weiterer Fund des Papierfischchens Ctenolepisma longicaudata Escherich, 1905 (Zygentoma, Lepismatidae) in Deutschland. Entomol. Nachr. Ber. 2014, 58, 153–154. [Google Scholar]
  36. Molero-Baltanás, R.; Fanciulli, P.P.; Frati, F.; Carapelli, A.; Gaju-Ricart, M. New data on the Zygentoma (Insecta, Apterygota) from Italy. Pedobiologia 2000, 44, 320–332. [Google Scholar] [CrossRef]
  37. Schoelitsz, B.; Poortvliet, P.M.; Takken, W. Factors driving public tolerance levels and information-seeking behaviour concerning insects in the household environment. Pest Manag. Sci. 2018, 1478–1493. [Google Scholar] [CrossRef] [Green Version]
  38. Davies, M. The Grey Silverfish/‘Paperfish’ Now Confirmed in Poland as well as the UK|Pest Control News. 2019. Available online: https://www.pestcontrolnews.com/the-grey-silverfish-paperfish-now-confirmed-in-poland-as-well-as-the-uk/ (accessed on 3 March 2021).
  39. Molero-Baltanás, R.; Gaju-Ricart, M.; Bach de Roca, C. Actualización del conocimiento del género Ctenolepisma Escherich, 1905 (Zygentoma, Lepismatidae) en España peninsular y Baleares. Boletín Asoc. Española Entomol. 2015, 39, 365–390. [Google Scholar]
  40. Molero-Baltanás, R.; Gaju-Ricart, M. Los Lepismatidae antropófilos de España. Tomo Extraordin 125 Aniversario Real Soc. Española Hist. Nat. 1996, 12, 178–181. [Google Scholar]
  41. Molero-Baltanás, R.; Gaju-Ricart, M.; Bach de Roca, C.; Mendes, L.F. New faunistic data on the Lepismatidae of Spain. Acta Zool Fenn. 1994, 195, 107–110. [Google Scholar]
  42. Pape, T.; Wahlstedt, U. En silverborstsvans nyinförd till Sverige (Thysanura: Lepismatidae). Entomol. Tidskr. 2002, 123, 149–151. [Google Scholar]
  43. Monteith, R. First record of the Grey Silverfish Ctenolepisma longicaudata Escherich, 1905, (Zygentoma: Lepismatidae) from Northern Ireland. Entomol. Mon. Mag. 2018, 154, 308. [Google Scholar] [CrossRef]
  44. Patoka, J.; Magalhães, A.L.B.; Kouba, A.; Faulkes, Z.; Jerikho, R.; Vitule, J.R.S. Invasive aquatic pets: Failed policies increase risks of harmful invasions. Biodivers. Conserv. 2018, 27, 3037–3046. [Google Scholar] [CrossRef] [Green Version]
  45. Machida, R.; Takashi, O. Thysanurans from the Ogasawara Islands (Zygentoma, Lepismatidae), Ctenolepisma longicaudata and Acrotelsa collaris, new to the Japanese fauna. Jpn. J. Entomol. 1996, 64, 365–366. [Google Scholar]
  46. Nierop, B.M.B.; Hakbijl, T. Ctenolepisma longicaudatum heeft ongemerkt bebouwd Nederland veroverd; met een sleutel voor de Nederlandse Lepismatidae (Thysanura). Entomol. Ber. 2002, 62, 34–42. [Google Scholar]
  47. Brimblecombe, P.; Querner, P. Silverfish (Zygentoma) in Austrian Museums before and during COVID-19 lockdown. Int. Biodeterior. Biodegrad. 2021, 164, 105296. [Google Scholar] [CrossRef]
  48. Buijs, J. Arthropods that annoy Amsterdam people. In Proceedings of the Netherlands Entomological Society Meeting; Bruin, J., Ed.; Nederlandse Entomologische Vereniging: Amsterdam, The Netherlands, 2019; pp. 31–44. [Google Scholar]
  49. Witteman, A.M.; Voorneman, R.; Van Den Oudenrijn, S.; Van Leeuwen, J.; Akkerdaas, J.; Van der Zee, J.S.; Aalberse, R.C. Silverfish protein in house dust in relation to mite and total arthropod level. Clin. Exp. Allergy 1996, 26, 1171–1176. [Google Scholar] [CrossRef] [PubMed]
  50. Mallis, A. Preliminary experiments on the silverfish Ctenolepisma urbani Slabaugh. J. Econ. Entomol. 1941, 34, 787–791. [Google Scholar] [CrossRef]
  51. Zhu, F.; Lavine, L.; O’Neal, S.; Lavine, M.; Foss, C.; Walsh, D. Insecticide resistance and management strategies in urban ecosystems. Insects 2016, 7, 2. [Google Scholar] [CrossRef] [PubMed]
  52. Aak, A.; Hage, M.; Lindstedt, H.H.; Rukke, B.A. Development of a Poisoned Bait Strategy against the Silverfish Ctenolepisma longicaudata (Escherich, 1905). Insects 2020, 11, 852. [Google Scholar] [CrossRef] [PubMed]
  53. BPCA. Silver solver: Control silverfish professionally. Prof. Pest Control. 2020, 8, 23. [Google Scholar]
  54. Mattsson, J.; Kolbjørn Mohn, J. Handling the increasing problem with grey silverfish (Ctenolepisma longicaudata) in archives. In Integrated Pest Management for Cultural Heritage; Swedish National Heritage Board (Riksantikvarieämbetet): Stockholm, Sweden, 2019; p. 21. [Google Scholar]
Figure 1. (a) Head of the captured male of Ctenolepisma longicaudatum, dorsal side; (b) abdomen of the captured C. longicaudatum, ventral side, (scales: (a) 0.1 mm; (b) 2 mm).
Figure 1. (a) Head of the captured male of Ctenolepisma longicaudatum, dorsal side; (b) abdomen of the captured C. longicaudatum, ventral side, (scales: (a) 0.1 mm; (b) 2 mm).
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Figure 2. The distribution of Ctenolepisma longicaudatum in Europe; red: confirmed records; and orange: unverified records. The distribution data from white countries are not available/were not found among the sources.
Figure 2. The distribution of Ctenolepisma longicaudatum in Europe; red: confirmed records; and orange: unverified records. The distribution data from white countries are not available/were not found among the sources.
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Figure 3. The distribution of Ctenolepisma longicaudatum in the United Kingdom, and Ireland (a) and in Czechia (b). Sources: iNaturalist, Observation.org, What’s Eating Your Collection, the Killgerm database and collected citizen reports.
Figure 3. The distribution of Ctenolepisma longicaudatum in the United Kingdom, and Ireland (a) and in Czechia (b). Sources: iNaturalist, Observation.org, What’s Eating Your Collection, the Killgerm database and collected citizen reports.
Insects 12 00810 g003
Figure 4. The abundance of Ctenolepisma longicaudatum in Europe based on citizen reports. Sources: Fauna Europea, Global Biodiversity Information Facility (GBIF), iNaturalist, Killgerm, European Network on Invasive Alien Species (NOBANIS), Observation.org, and Pan-European Species Directories Infrastructure (PESI); “What’s Eating Your Collection”, and available literature sources (see Table 4).
Figure 4. The abundance of Ctenolepisma longicaudatum in Europe based on citizen reports. Sources: Fauna Europea, Global Biodiversity Information Facility (GBIF), iNaturalist, Killgerm, European Network on Invasive Alien Species (NOBANIS), Observation.org, and Pan-European Species Directories Infrastructure (PESI); “What’s Eating Your Collection”, and available literature sources (see Table 4).
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Table 1. The public sources surveyed within monitoring the occurrence of Ctenolepisma longicaudatum in Europe.
Table 1. The public sources surveyed within monitoring the occurrence of Ctenolepisma longicaudatum in Europe.
SourceAbbreviationsAvailable from
European Network on Invasive Alien SpeciesNOBANIShttps://www.nobanis.org, 31 March 2021
Fauna Europea-https://fauna-eu.org/, 6 April 2021
Global Biodiversity Information Facility *GBIFhttps://www.gbif.org, 8 April 2021
iNaturalist *-https://www.inaturalist.org, 12 April 2021
Observation-https://observation.org, 12 April 2021
Pan-European Species directories InfrastructurePESIhttp://www.eu-nomen.eu, 18 March 2021
What’s Eating Your Collection-https://www.whatseatingyourcollection.com, 12 May 2021
* In the case of GBIF, the dataset “iNaturalist” was excluded in order to not double the number of observations gathered from this database.
Table 2. The reported occurrence of Ctenolepisma longicaudatum in Czechia in 2017–2021.
Table 2. The reported occurrence of Ctenolepisma longicaudatum in Czechia in 2017–2021.
LocalityMunicipalityRegionDateLocationSource
1PrahaPraha10/2017Warehouse *NIPH ID
2PrahaPraha06/2018Gallery *NIPH ID
3KroměřížZlín07/2018flatfacebook.com
4PlzeňPlzeň12/2018warehouseNIPH ID
5AdamovSouth Moravian02/2019flatfacebook.com
6PrahaPraha05/2019flatfacebook.com
7OrlováMoravian-Silesian09/2019flatfacebook.com
8PrahaPraha10/2019Warehouse *NIPH ID
9Klášterec nad OhříÚstí nad Labem01/2020flatfacebook.com
10DobrovízCentral Bohemian01/2020warehouseNIPH ID
11PrahaPraha02/2020shopping mallNIPH ID
12PrahaPraha04/2020houseiNaturalist.org
13BohumínMoravian-Silesian07/2020flatfacebook.com
14KlecanyCentral Bohemian07/2020pub. instituteiNaturalist.org
15BrnoSouth Moravian09/2020flatiNaturalist.org
16PrahaPraha11/2020warehouseNIPH ID
17TišnovSouth Moravian01/2021Flat *facebook.com
18OstravaMoravian-Silesian02/2021flatfacebook.com
19JaroměřHradec Králové02/2021factoryfacebook.com
20KopřivniceMoravian-Silesian03/2021factoryNIPH ID
* Personal inspection of researchers from NIPH. NIPH: National Institute of Public Health Prague.
Table 3. The reported occurrence Ctenolepisma longicaudatum in the United Kingdom and Republic of Ireland in 2016–2021.
Table 3. The reported occurrence Ctenolepisma longicaudatum in the United Kingdom and Republic of Ireland in 2016–2021.
LocalityTown/CityCountryDateLocationSource
1LondonEngland06/2016museumwhatseatingyourcollection.com
2AntrimN. Ireland07/2016unknownNBN
3LondonEngland09/2016gallerywhatseatingyourcollection.com
4LondonEngland09/2017museumwhatseatingyourcollection.com
5QuaintonEngland09/2017archivewhatseatingyourcollection.com
6SouthamptonEngland10/2017student acc.Killgerm ID
7CorkIreland10/2017domesticKillgerm ID
8DoncasterEngland10/2017domesticKillgerm ID
9LeedsEngland11/2017flatsKillgerm ID
10CorkIreland12/2017apartmentsKillgerm ID
11LondonEngland01/2018museumwhatseatingyourcollection.com
12BirminghamEngland01/2018museumwhatseatingyourcollection.com
13LondonEngland01/2018storewhatseatingyourcollection.com
14LondonEngland04/2018gallerywhatseatingyourcollection.com
15AntrimN. Ireland05/2018unknownNBN
16GloucesterEngland09/2018archivewhatseatingyourcollection.com
17TemplepatrickN. Ireland09/2018unknownNBN
18–23BirminghamEngland11/2018–10/2019domesticcitizen science reports
24LondonEngland01/2019museumwhatseatingyourcollection.com
25LeedsEngland01/2019domesticKillgerm ID
26AberdeenScotland *02/2019domesticKillgerm ID
27PortsmouthEngland05/2019storewhatseatingyourcollection.com
28AshfordEngland06/2019officeKillgerm ID
29CheltenhamEngland07/2019domesticKillgerm ID
30GalwayIreland09/2019medical centeriNaturalist.org
31LondonEngland09/2019shopping centreiNaturalist.org
32LondonEngland09/2019archivewhatseatingyourcollection.com
33LondonEngland09/2019archivewhatseatingyourcollection.com
34LondonEngland10/2019archivewhatseatingyourcollection.com
35ManchesterEngland12/2019student acc.iNaturalist.org
36BirminghamEngland01/2020student acc.iNaturalist.org
37ChelmsfordEngland02/2020garden centreiNaturalist.org
38GloucesterEngland04/2020domesticiNaturalist.org
39LondonEngland04/2020archivewhatseatingyourcollection.com
40HartleyEngland06/2020domesticKillgerm ID
41BallinaIreland07/2020domesticiNaturalist.org
42IpswichEngland07/2020apartmentsKillgerm ID
43North LondonEngland07/2020domesticKillgerm ID
44Royal Tunbridge WellsEngland07/2020warehouseiNaturalist.org
45TauntonEngland08/2020domesticwhatseatingyourcollection.com
46TotnesEngland10/2020domesticiNaturalist.org
47BrightonEngland11/2020apartments for studentsiNaturalist.org
48PortsmouthEngland12/2020unknowniNaturalist.org
49BrentfordEngland12/2020domesticiNaturalist.org
50South East LondonEngland12/2020museumKillgerm ID
51PeterboroughEngland12/2020domesticKillgerm ID
52ManchesterEngland01/2021domesticiNaturalist.org
53ChiswickEngland01/2021unknowniNaturalist.org
54BalbrigganIreland01/2021domesticiNaturalist.org
55North West LondonEngland01/2021domesticKillgerm ID
56SouthamptonEngland02/2021warehouseiNaturalist.org
57Milton KeynesEngland03/2021warehouseiNaturalist.org
58South East LondonEngland03/2021unknownKillgerm ID
59CanterburyEngland03/2021domesticKillgerm ID
NBN: National Biodiversity Network. * the first record of Ctenolepisma longicaudata in Scotland.
Table 4. The abundance of Ctenolepisma. longicaudatum in Europe based on online databases, namely, iNaturalist, GBIF, Observation.org, Fauna Europea, NOBANIS, and PESI and available literature sources.
Table 4. The abundance of Ctenolepisma. longicaudatum in Europe based on online databases, namely, iNaturalist, GBIF, Observation.org, Fauna Europea, NOBANIS, and PESI and available literature sources.
iNaturalistGBIFObservationFauna EuropeaNOBANISPESILiterature
Albania300present000
Andorra0000000
Austria33100present09 [16,31]
Azores066 *000present0
Belarus0000000
Belgium2966 *00006 [10]
Bosnia and Herzegovina0000000
Bulgaria0000000
Canary Islands400present0present0
Croatia1000000
Cyprus100present0present0
Czechia3000001 [26]
Denmark mainland80000002 [32]
Estonia11 *1 005 [28]
Faroe Islands00000065 [27]
Finland22000001 [33]
France5121present0present1 [34]
Germany6716 *140002 [35]
Greece2304present0present0
Greenland0000000
Hungary2020000
Iceland1000000
Ireland3000000
Italy10502present0present1 [36]
Kosovo0000000
Latvia0000000
Liechtenstein0000000
Lithuania2000000
Luxembourg3010000
Madeira420present0present0
Malta000present000
Moldova0000000
Monaco0000000
Montenegro0000000
Netherlands68134 *00present034 [37]
North Macedonia0000000
Norway632 *00006788 [11,18]
Poland4000001 [38]
Portugal mainland628 *1present0present0
Romania0000000
Russian Federation3000000
San Marino0000000
Serbia0000000
Slovakia1000000
Slovenia1000000
Spain mainland + Balears9527present0present12 [39,40,41]
Sweden591 *00001 [42]
Switzerland11000000
Turkey6000
Ukraine3000000
United Kingdom16000002 [30,43] **
Vatican City0000000
* Records with identical global positioning system coordinates were regarded as a single record.; ** the first record for Scotland was obtained within this study.
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Kulma, M.; Bubová, T.; Davies, M.P.; Boiocchi, F.; Patoka, J. Ctenolepisma longicaudatum Escherich (1905) Became a Common Pest in Europe: Case Studies from Czechia and the United Kingdom. Insects 2021, 12, 810. https://doi.org/10.3390/insects12090810

AMA Style

Kulma M, Bubová T, Davies MP, Boiocchi F, Patoka J. Ctenolepisma longicaudatum Escherich (1905) Became a Common Pest in Europe: Case Studies from Czechia and the United Kingdom. Insects. 2021; 12(9):810. https://doi.org/10.3390/insects12090810

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Kulma, Martin, Terezie Bubová, Matthew Paul Davies, Federica Boiocchi, and Jiří Patoka. 2021. "Ctenolepisma longicaudatum Escherich (1905) Became a Common Pest in Europe: Case Studies from Czechia and the United Kingdom" Insects 12, no. 9: 810. https://doi.org/10.3390/insects12090810

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