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The Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Central Germany: Surveillance in its northernmost distribution area
Accepted Manuscript Title: The Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Central Germany: Surveillance in its northernmost distribution area Authors: Cornelius Kuhlisch, Helge Kampen, Doreen Walther PII: DOI: Reference:
S0001-706X(18)30649-1 https://doi.org/10.1016/j.actatropica.2018.08.019 ACTROP 4755
To appear in:
Acta Tropica
Received date: Revised date: Accepted date:
30-5-2018 17-8-2018 17-8-2018
Please cite this article as: Kuhlisch C, Kampen H, Walther D, The Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Central Germany: Surveillance in its northernmost distribution area, Acta Tropica (2018), https://doi.org/10.1016/j.actatropica.2018.08.019 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
The Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Central Germany: surveillance in its northernmost distribution area Cornelius Kuhlischa*, Helge Kampenb, Doreen Walthera a
Leibniz Centre for Agricultural Landscape Research, Eberswalder Str. 84, 15374 Müncheberg, Germany b
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Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Suedufer 10, 17493 Greifswald - Insel Riems, Germany * Corresponding author
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E-mail addresses: [email protected] (C. Kuhlisch) [email protected] (H. Kampen) [email protected] (D. Walther)
Highlights
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Northernmost population of Aedes albopictus observed in Central Germany Local winter temperatures allow long-term establishment of Aedes albopictus Introduction possibly through plants from Italy
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Abstract
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The invasive Asian tiger mosquito Aedes albopictus has recently been observed in southern Germany for the first time to reproduce and even overwinter north of the Alps. After the accidental capture of adult specimens in Jena, German federal state of Thuringia, in mid-2015, regular inspections brought forth developmental stages until autumn 2015, indicating local reproduction. Surveillance activities implemented in 2016 showed larvae already in early May, suggesting overwintering, and throughout the season until late October, although population densities remained low. Further sporadic specimens found in 2017 argue for establishment. Jena is located in Central Germany, north of all known distribution areas of Ae. albopictus, with the area of the municipality affected by the tiger mosquito characterised by a relatively mild climate. To check the suitability of the local climate for Ae. albopictus, winter temperatures, measured in a cemetery of Jena where larvae had regularly been found in 2015 and 2016, were analysed and compared with two sites of establishment in southern Germany. The conditions were similar at all three locations, suggesting that the Jena population might also be able to survive in the long term. While the municipality authorities have been informed and education of the Jena citizens to avoid producing potential breeding places has started, insecticidal control has not yet been implemented. Keywords: Aedes albopictus; cold hardiness; Germany; invasive species; northernmost distribution; overwintering
1. Introduction The Asian tiger mosquito Aedes (Stegomyia) albopictus (Skuse, 1895) is an efficient potential vector of numerous human and animal pathogens, such as dengue virus, chikungunya virus, West Nile virus, Rift Valley fever virus and dirofilarial nematodes (Gratz, 2004; Paupy et al., 2009) and is therefore of paramount public and veterinary health concern. In Europe, it was made responsible for recent outbreaks of dengue and chikungunya (Schaffner et al., 2013; Calba et al., 2017; Succo et al., 2017; Venturi et al., 2017).
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Originating from the Asian-Pacific region, Ae. albopictus was first reported in Europe from Albania in 1979 (Adhami and Reiter, 1998). Only some ten years later, it was discovered in Italy (Sabatini et al., 1990), from where it spread over large parts of the Mediterranean and beyond (Medlock et al., 2015). While both intercontinental and continental displacement is through transportation of eggs or larvae by the trade with used tyres and ornamental plants (e.g. Dracaena sp.), adults entering vehicles contribute to continental spread (Becker et al., 2017; Eritja et al., 2017; Hofhuis et al., 2009; Knudsen et al., 1996; Reiter, 1998; Walther et al., 2017). Since 2007, the species has been found on service stations along South German motorways (Becker et al., 2013; Kampen et al., 2013; Pluskota et al., 2008; Werner et al., 2012), and in 2014 and 2015, extended local reproduction was observed in the German cities of Freiburg, Heidelberg and Jena (Pluskota et al., 2016; Werner and Kampen, 2015; Walther et al., 2017). While in Freiburg and Heidelberg Ae. albopictus quickly developed alarming population densities which had prompted the implementation of control activities (Becker et al., 2017), detections of specimens in Jena remained sporadic.
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Aedes albopictus is a thermophilic mosquito species which is adapted to both tropical and temperate climates, depending on its origin (Benedict et al., 2007; Hawley, 1988). Populations of temperate strains are known to have a higher cold hardiness than tropical ones which, in contrast, cannot overwinter as diapausing eggs (Hanson and Craig, 1994; Hawley et al., 1989). According to studies by Delatte et al. (2009), larval development does not take place below 10 °C and is optimal at temperatures between 25 and 30 °C. Larval survival rates are highest at 15 °C, and gonotrophic cycles are shortest at about 30 °C. In regions with relatively high summer temperatures, populations develop quickly, and densities reach their peaks early in the season, whereas in regions with low summer temperatures population growth is slow but steady, with a maximum later in the season (Alto und Juliano, 2001).
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Future projection models suggest that climatically suitable areas for the establishment of Ae. albopictus will remain stable or increase until 2040 in western and Central Europe and, with some delay, probably also increase in eastern Europe (Caminade et al., 2012; Fischer et al., 2011, 2014). By contrast, living conditions are expected to deteriorate along the western Mediterranean coast of Spain (Fischer et al., 2014). Considerable discrepancies exist between different models, which predict France, Germany and western parts of the United Kingdom to become either persistently unsuitable or increasingly suitable (Fischer et al., 2014). In this study, we describe the finding and population development of Ae. albopictus in the Central German city of Jena, which, to the best of the authors’ knowledge, represents the northernmost area colonised by this invasive mosquito species. Temperature profiles of the winter seasons 2015/2016 and 2016/2017 between locations with Ae. albopictus occurrence in Jena and in the Southwest German towns of Heidelberg and Freiburg, where the species is considered established, were compared.
2. Methods 2.1 Mosquito collection
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In the framework of the German citizen science project ‘Mueckenatlas’ (mosquito atlas), where mosquitoes are routinely submitted for identification by private persons from all over Germany (Walther and Kampen, 2017), two Ae. albopictus specimens were received from the City of Jena (N50.8890, E11.6085, altitude 165 m), German federal state of Thuringia, in July 2015 (Fig. 1). As a reaction, all cemeteries in the municipality of Jena were monitored for Ae. albopictus developmental stages from mid-July to late October 2015. After the repeated detection of larvae in the cemetery of Jena-Lobeda, the surveillance continued at this site and was extended to nearby construction markets, garden centres and allotment gardens from 11 May to 8 November 2016 and from 1 May to 26 October 2017 by checking all water-holding containers on a biweekly basis. In addition, 10 standard ovitraps (440 ml), equipped with wooden spatulas (150 x 30 mm2) as oviposition supports, were distributed over the surveillance area according to the ECDC guidelines for monitoring invasive mosquito species (ECDC, 2012), i.e. placement of one ovitrap per 2,500 m2. Further ovitraps were placed 20 metres apart in the Jena-Lobeda cemetery (n=15), and 100 metres apart around that cemetery (n=25) and in both garden centres (n=5, each) in 2017. Also, ten gravid Aedes traps (BGGAT, Biogents, Germany) were placed to catch adult Ae. albopictus individuals in the Jena-Lobeda cemetery (n=5) and both garden centres (n=2+3). One BG-Sentinel 2 trap (Biogents) each, equipped with BG-Lure (Biogents) and a carbon dioxide tank as attractants, was operated with mains supply for 72 hours at protected and hidden sites in the Jena-Lobeda cemetery and two further cemeteries in Jena, characterised by similar climatic conditions (Hoffmann et al., 2014), in August 2017.
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If larvae were found in water containers (ovitraps, flower vases, plant pots, dishes, etc.), they were brought into the laboratory in jars containing water from their breeding sites and fed with fish food flakes (Guppy, Tetra, Germany) until adult emergence. The wooden spatulas of the ovitraps were collected every two weeks to be checked for eggs. Both eggs and larvae dying before completion of development were genetically identified to species by CO1 barcoding according to Ibáñez-Justicia et al. (2014). Adult mosquito specimens were determined morphologically using the key by Becker et al. (2010). To determine a container index in the Jena-Lobeda cemetery, all containers with eggs, larvae or pupae of Ae. albopictus were counted on 24 August 2016, a date considered representative for the period of highest population density.
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Fig. 1.
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Relief map of Jena showing Ae. albopictus findings in 2015 (yellow), 2015 & 2016 (green), 2016 (red) and 2017 (blue). Dots encircled in black indicate submissions to the ‘Mueckenatlas’. © GeoBasis-DE / BKG 2017.
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2.2 Climate data collection and analysis
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Temperatures were measured by HOBO Pro v2 data loggers (Onset Computer Corporation, MA, USA) every hour from December 2015 to May 2016 and from November 2016 to May 2017, both in the Jena-Lobeda cemetery and at known sites of Ae. albopictus establishment and hibernation in Heidelberg and Freiburg (Becker et al., 2017; Walther et al., 2017). The loggers were located close to known Ae. albopictus breeding places at weather-protected sites at heights of 1.5 to 2.0 metres, as standard for climate measurements.
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As the survival of diapausing eggs does not only depend on the temperature minimum, but also on the duration and the frequency a temperature threshold is exceeded, we defined a ‘frost period’, in which the measured temperatures dropped below a specific threshold. For all thresholds between the local minimum temperatures measured during the two winter seasons and 0 °C, the frequency of frost periods, their durations and minimum temperatures were analysed in Jena, Heidelberg and Freiburg, following the Peak-Over-Threshold (POT) approach: ''The idea is to keep, from recorded series, ... values above a predefined threshold ... . The advantage of the POT approach is that more than one extreme value can be considered.'' (Mailhot et al., 2012). The approach was applied on the additive inverse of the frost temperatures with the R package POT (Ribatet and Dutang, 2016; R Core v3.3.2, 2016).
3. Results 3.1 Collection of Aedes albopictus Two female Ae. albopictus specimens were submitted to the ‘Mueckenatlas’ citizen science project from the Lobeda district of the municipality of Jena, Thuringia, in mid-July 2015 (Fig. 1). During subsequent on-site inspections, eggs (n=141) and larvae (n=51) were continuously found in the JenaLobeda cemetery until 26 October 2015 (Table 1). No Ae. albopictus were found in 20 further cemeteries of the municipality checked in mid-August 2015.
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In 2016, 138 larvae, 3 pupae and 6 adults of Ae. albopictus were collected during inspections of known and new locations in Jena between 11 May and 21 October (Fig. 1, Table 1). On 24 August, the container index in the Jena-Lobeda cemetery was almost 19 % (with developmental stages present in 10 out of 54 water-filled flower vases and ovitraps checked). Moreover, 150 eggs of Ae. albopictus were detected sporadically, and sometimes repeatedly, on the oviposition supports of eight ovitraps operated in this cemetery between 11 August and 5 October.
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In the surroundings of about 300 to 700 metres away from the Jena-Lobeda cemetery, 47 larvae and an attacking female were collected between end-June and mid-September 2016. Furthermore, two females collected on 28 August and 25 September 2016 at a location ca. 400 metres south of the Jena-Lobeda cemetery were submitted to the ‘Mueckenatlas’. Twenty-five eggs and two larvae of Aedes albopictus were identified in early September 2016 in one ovitrap placed 160 metres away from the Jena-Lobeda cemetery. No Ae. albopictus specimens were found between 21 October and the end of the observation period on 8 November 2016.
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Between 1 May and 26 October 2017, neither eggs, nor larvae or adults of Ae. albopictus could be identified during inspections of the Jena-Lobeda district. Instead, three kilometres north of this area, two females and four larvae were collected in the cemeteries of Jena-North and Jena-East in midAugust and late September 2017 (Fig. 1, Table 1).
3.2 Climate data analysis
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Both in Jena and in the other two Ae. albopictus population areas in southern Germany, Heidelberg and Freiburg, where temperature data loggers were operated, monthly mean temperatures stayed above 2 °C in the winter season 2015/2016 (Table 2). By contrast, the monthly mean minimum temperatures (Table 2) and the daily mean temperatures (Fig. 2) in Jena were slightly below freezing point in January, only showing negligible differences to Freiburg and Heidelberg. Also, the general daily temperature profile showed no relevant differences between the three locations (data not shown).
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Fig. 2.
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Daily mean temperatures in the Jena-Lobeda Ae. albopictus distribution area, from December 2015 to May 2016 (red) and from December 2016 to May 2017 (blue). The arrow marks the beginning of the Ae. albopictus detection period in 2016.
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In the winter season 2016/2017, the monthly mean temperatures were lower in December and January in Freiburg than in Heidelberg and Jena (January: -3 °C vs. -1 °C) (Table 2), but the daily mean temperatures in these months reached considerably higher levels in Jena than in Freiburg and Heidelberg (data not shown). In Jena, they increased gradually from 0 °C in late January to above 10 °C in early April, before falling again below 3 °C at the end of April (Fig. 2).
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On average, the measured temperatures in Jena were approximately 4 Kelvin lower between 19 December 2016 and 14 February 2017 (Fig. 3A) but 3 to 4 Kelvin higher between 15 February and 3 April 2017 (Fig. 3B) than in the same time periods of the winter season 2015/2016. After these periods, the courses of the temperatures were similar to the year before until the end of May (Fig. 3C).
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Fig. 3.
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Difference of daily mean temperatures between 2016 and 2017 from December to May in Jena. The sections A (1 December to 15 February), B (16 February to 3 April) and C (3 April to 1 June) show periods of different temperature profiles.
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The hourly measured data of both winter seasons in Jena-Lobeda show that for thresholds between -6 °C and 0 °C, frost periods occurred more frequently during the winter 2016/2017 than during the winter 2015/2016 (Fig. 4). At a threshold temperature of -6 °C, however, frost periods longer than ten hours occurred equally often in both winter seasons. By contrast, at a threshold temperature of -5 °C, more frost periods longer than ten hours were observed in 2016/2017 compared to 2015/2016. At threshold temperatures between -3 °C and 0 °C, frost periods were considerably longer in 2016/2017 than in 2015/2016 (Fig. 4).
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Fig. 4.
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Absolute temperatures [°C] per hour in Jena, Heidelberg and Freiburg from November to March during the cold seasons 2015/2016 and 2016/2017. Temperature measurements in Jena started 24 November 2015 and in Heidelberg and Freiburg 19 December 2015.
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Two cold spells occurred in Jena in January 2016 (Fig. 4), with the first one from 2 to 7 January, reaching a minimum of -2.6 °C on 6 January, and the second one from 17 to 23 January, reaching a minimum of -10.7 °C on 22 January. The duration and frequency of frost periods in Freiburg and Heidelberg were similar to Jena. From 3 November to 30 April of the winter season 2016/2017, there were several periods in each of the three locations, during which the temperature dropped below freezing point. In Jena, ten frost periods were observed for a threshold of -5 °C, which took at least 5 hours, while in Freiburg even 23 such frost periods were registered. The longest frost period in Jena lasted 18 hours, in Freiburg 21 hours. Of three cold spells in Jena in the winter season 2016/2017, the one from 15 to 23 January was extreme in that temperatures dropped below freezing point twice and for a considerable time each, reaching minima of -8.2 °C on 20 January and -9.5 °C on 23 January.
By means of the POT approach, the -3 °C threshold was selected from all possible thresholds for the comparison of the temperature profiles between the three locations and the two winter seasons because the parameters of the Pareto distribution changed between -2 and -4 °C in a qualitative manner. Using the 95 % confidence interval for the mean excess, significant differences at an alphalevel of 5 % could be shown between Jena/Freiburg and Heidelberg in 2015/2016, between Jena/Heidelberg and Freiburg in 2016/2017, and between the two winter seasons in Jena (Table 3).
4. Discussion
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The first report of Ae. albopictus from Jena-Lobeda, due to a submission to the ‘Mueckenatlas’ surveillance scheme, represents one of the first findings of specimens of this species in Germany north of the Upper Rhine Valley (Walther et al., 2017). During initial local inspections in 2015, larvae and eggs were found exclusively in a cemetery close by the collection site of the submitted specimens. Their moderate number suggested a relatively low population density. Collections in the very same cemetery and relatively early in the mosquito season 2016 (May) indicated overwintering. The onset of development in May agrees with the first seasonal findings of larvae in the southern German towns of Heidelberg and Freiburg where Ae. albopictus has been shown to overwinter (Becker et al., 2017; Pluskota et al., 2016; Walther et al., 2017).
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With the population increasing, a higher number of larvae was encountered in the Jena-Lobeda cemetery in August and September 2016. Subsequently, specimens appeared to disperse from the relatively individual-rich centre of the population to the periphery, a behaviour also described by Mori (1979). Thus, outside of the cemetery, eggs were detected in an ovitrap and adults captured in September (Fig. 1).
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Of particular interest regarding the possible mode of introduction of Ae. albopictus to Jena is the report of employees of the affected garden centre about a huge number of mosquito larvae in the water in which lotus plants (Nelumbo sp.) had been delivered in 2014. The plants had been transported from Italy via way-stations in the Netherlands and the German Upper Rhine Valley before they arrived in Jena. The time these plants were imported would well explain the first detection of Ae. albopictus in 2015, supporting the assumption that the garden centre might be the origin of proliferation and dispersal, instead of the Jena-Lobeda cemetery where the first developmental stages were found.
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Eventually, it was not possible yet to find out, where the mosquitoes came from and whether all individuals sampled in Jena resulted from the same initial introduction event or from separate importations. A genetic analysis of the populations in Jena related to other German and European populations is under way. Of course, the high number of larvae collected in late June and September 2016 in the garden centre could have also been caused by the local reproduction of Ae. albopictus specimens introduced from other, previously colonised areas of Jena (e.g., Jena-Lobeda cemetery) or new introductions from areas in southern Germany or southern Europe where high population densities already exist early in the year. The fact that no individuals of Ae. albopictus could be found in Jena-Lobeda in 2017 may be a result of the relatively cold winter season 2016/2017 but also of countermeasures of authorities and citizens sensitised to prevent propagation. Such countermeasures were realised in the cemetery since 2016, where the majority of unused flower vases were turned over and the wells emptied in order not to provide mosquito breeding places. In addition, citizens were publicly requested to empty and clean all water containers in their gardens and on their balconies and to cover water-filled containers. Because of the consistently low abundance of Ae. albopictus individuals, there was no possibility to evaluate the success of the measures quantitatively.
Jena, Heidelberg and Freiburg are located in regions with continental climates, but due to geographical and geological peculiarities, these cities are relatively warm, with a pronounced continental climate in Jena. Therefore, the establishment of Ae. albopictus in Jena may have been facilitated by the following specifics of the affected area: Jena is located in a weather-sheltered region in the Saale Valley where a heat-island effect can occur. The ground consists of Bunter sandstone (Röt formation) with shell-bearing limestone-slopes which are able to heat up excessively and store and reflect the warmth over a considerable period of time (Hoffmann et al., 2014).
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Our findings of Ae. albopictus in Jena agree with some models which show that Germany is a potential distribution area for this species, although the thermal suitability of Europe north of the Alps has generally been considered low (Mogi et al., 2012; Kraemer et al., 2015; Proestos et al., 2016). In its native distribution range of East and Southeast Asia, the northernmost areas of occurrence are located in China and Japan (Hanson, 1995; Kobayashi, 2002; Mogi, 2012; Wu et al., 2011). As a prerequisite for the establishment of Ae. albopictus, various variables have been determined. For Europe, an annual mean precipitation of at least 200 to 250 mm, an annual mean temperature of at least 8 °C and a January mean temperature not lower than -4 to 0 °C has been suggested to be necessary (Waldock et al., 2013). With respect to the January mean temperature, the northern distribution limit in Europe is estimated to correspond to the climatic situation in China (January mean -5 °C; Nawrocki and Hawley, 1987; Wu et al., 2011) rather than in Japan (January mean -2 °C; Kobayashi et al., 2002). In northeastern China, Ae. albopictus was found to permanently occur in areas, where the January mean temperature can be as low as -5 °C, and to expand its summer distribution northwards into regions with even colder average temperatures (Wu et al., 2011). However, according to the Köppen-Geiger climate classification (Kottek et al., 2006), the temperate oceanic and continental regions in western Europe are distributed over a much larger area of land than in Northeast China and may make it more difficult for this mosquito to spread to less favourable climatic regions than in China.
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Consequently, a crucial factor determining the spread of this thermophilic species in temperate Europe is the temperature (Delatte et al., 2009). In addition to other climatic or population-dynamic factors, temperature basically influences population growth during the vegetative season and survival of diapausing eggs during wintertime. At all three locations where temperatures had been measured in this study (Jena, Heidelberg, Freiburg), January mean temperatures were 2 °C or higher in the winter season 2015/2016. Furthermore, long-term annual mean precipitations (period 1980 to 2010) were 610 mm, 732 mm and 934 mm, and annual mean temperatures 9.9 °C, 11.4 °C and 11.4 °C, respectively (Hoffmann et al., 2014; German Weather Service, 2017; Groß, 2015). According to these data, all three locations fall within the climatic requirements for survival during the winter diapause and, thus, for possible establishment of Ae. albopictus (Waldock et al., 2013). The specific temperature conditions in Jena were similar to Heidelberg and Freiburg, where Ae. albopictus proliferates well. This also suggests that other localities with similar data should be thoroughly surveyed for Ae. albopictus establishment in the future. Diapausing eggs of cold-acclimated Ae. albopictus from Rimini, Italy, have been shown to be able to survive temperatures of -10 °C for 24 hours or -12 °C for 1 hour (Thomas et al., 2012). Based on this and the fact that temperatures in Jena, the coldest one of the observed locations, reached -10 °C to -11 °C only once for a period of 4 hours during the winter season 2015/2016, eggs would have been likely to survive the cold season at all three locations. This would explain the early emergence of specimens in Jena in 2016. The winter season 2016/2017 might have influenced the survival of Ae. albopictus and caused no findings in Jena-Lobeda in 2017. In fact, significant differences in the temperature profiles existed in Jena between the two investigated winter seasons 2015/2016 and 2016/2017. Such differences were
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found in the frequency in which temperatures dropped below a certain threshold, the duration of such periods, the minimum temperatures reached and mean excess temperatures below a certain threshold. If the frequency of temperature dropping affected the survival of Ae. albopictus, the eggs may have not survived the winter season 2016/2017 because hourly measured temperatures dropped too often below a threshold between -5 °C and 0 °C. If the duration of the frost periods was relevant, the eggs may have not survived because temperatures dropped below a threshold between -3 °C and 0 °C for too long. Minimum temperatures, however, were lower in 2015/2016 than in 2016/2017 and, therefore, could have not exclusively been responsible for Ae. albopictus not being found in Jena-Lobeda in 2017. Thus, critical conditions may indeed have existed in the winter season 2016/2017 with regard to a higher frequency and a longer duration of low temperature events, causing a reduction in egg survival and no findings of Ae. albopictus in Jena-Lobeda during the monitoring in 2017. This assumption is based on the significant difference in the mean excess for the -3 °C threshold.
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No temperature data for the various districts of Jena where Ae. albopictus emerged in 2017 are available, but due to the specific landscape structure of the municipality, considerable climatic differences are conceivable on a small-scale (Hoffmann et al., 2014), allowing the tiger mosquito to survive in some areas but not in others.
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Furthermore, the cold period in late April 2017 might have had a negative impact on the survival of developing larvae in Jena-Lobeda after a relatively warm period in late March (Fig. 2). While in late March, daily mean temperatures of 11.8 °C to 14.7 °C were recorded for six days following a period of precipitation for two days, suggesting larval hatching (c.f. Lacour et al., 2015; Medlock et al., 2006; Thomas et al., 2012; Toma et al., 2003; Waldock et al., 2013), temperatures dropped again below 10 °C for five days and sometimes even below 5 °C by late April. The findings of Ae. albopictus in Central Jena and Jena-North in August 2017 as well as in Jena-East in September 2017 probably originated from individuals which had been displaced the year before from Jena-Lobeda and overwintered somewhere else or, less likely, were newly introduced in 2017.
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Aedes albopictus succeeded in overwintering in Freiburg from 2014 to 2015 and in Jena, Heidelberg and Freiburg from 2015 to 2016. In Jena, the cool and long spring 2016 might have impeded a quick recovery of the population after the winter (Fig. 2). In addition to the winter and summer conditions (Pluskota et al., 2016), the spring conditions therefore seem to have a decisive impact on the development of Ae. albopictus in temperate Europe and should obtain more attention in future analyses. Thus, in a suboptimal environment such as Europe north of the Alps, the entire course of the year can be expected to influence the distribution and population density of Ae. albopictus.
5. Conclusions
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The findings of Ae. albopictus in Jena from 2015 to 2017 as well as the majority of the climate data demonstrate that the species has the potential to establish in Jena. Indeed, eggs may even survive colder winters at sheltered spots and develop considerable population densities during the following summer. Problems may arise after larval hatching in spring through late frosts and low temperatures, which - due to the continentality - are more likely to occur in Jena than in Heidelberg and Freiburg, resulting in negative effects on population development. Jena currently harbours the northernmost known Ae. albopictus population. This, however, has to be considered with respect to comparable climatic conditions which are not necessarily found at identical latitudes in different regions of the world. The investigations demonstrate the detection of Ae. albopictus in Jena-Lobeda in 2015, following possible introduction in 2014, population growth in 2016, and simultaneous lack of findings in Jena-Lobeda and emergence in other city districts in 2017.
The detailed temperature measurements indicate that the climatic conditions in Jena might be suitable for long time persistence, although - according to the low population density - the species appears to struggle for survival. It remains to be awaited whether Ae. albopictus will become extinct or will firmly establish in the future. Sporadic findings of larvae and adults in Jena-North, Jena-East and Jena-Lobeda in June and July 2018, during the review process of this contribution, suggest a high probability for the latter.
Author contributions
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Conceived and designed the experiments: DW, HK, CK. Collected and identified the mosquitoes: CK, DW, HK. Collected and analysed climate data: CK. Contributed reagents/materials/analysis tools: DW, HK. Wrote the paper: CK, DW, HK. All authors read and approved the final version of the manuscript.
Conflict of interest
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There is no conflict of interest.
Funding
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This work was financially supported by the German Federal Ministry of Food and Agriculture (BMEL) through the Federal Office for Agriculture and Food (BLE) [grant number 2819104615].
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Acknowledgements
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The authors thank the City of Jena for productive collaboration and Jutta Falland and Juliane Horenk for technical support in the laboratory.
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Medlock, J.M., Avenell, D., Barrass, I., Leach, S., 2006. Analysis of the potential for survival and seasonal activity of Aedes albopictus (Diptera: Culicidae) in the United Kingdom. J. Vector Ecol. 31, 292-304. DOI: 10.3376/1081-1710(2006)31[292:AOTPFS]2.0.CO;2 Medlock, J.M., Hansford, K.M., Versteiert, V., Cull, B., Kampen, H., Fontenille, D., Hendrickx, G., Zeller, H., Van Bortel, W., Schaffner, F., 2015. An entomological review of invasive mosquitoes in Europe. Bull. Entomol. Res. 105, 637-663. DOI: 10.1017/S0007485315000103 Mogi, M., Armbruster, P., Fonseca, D.M., 2012. Analyses of the northern distributional limit of Aedes albopictus (Diptera: Culicidae) with a simple thermal index. J. Med. Entomol. 49, 1233-1243. DOI: 10.1603/ME12104 Mori, A., 1979. Effects of larval density and nutrition on some attributes of immature and adult Aedes albopictus. Trop. Med. 21, 85-103.
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Sabatini, A., Raineri, V., Trovato, V.G., Coluzzi, M., 1990. Aedes albopictus in Italia e possibile diffusione della specie nell’area Mediterranea. Parassitologia 32, 301-304.
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Schaffner, F., Medlock, J.M., Van Bortel, W., 2013. Public health significance of invasive mosquitoes in Europe. Clin Microbiol Infect 19, 685-692. DOI: 10.1111/1469-0691.12189
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Succo, T., Leparc-Goffart, I., Ferré, J.B, Roiz, D., Broche, B., Maquart, M., Noel, H., Catelinois, O., Entezam, F, Caire, D., Jourdain, F., Esteve-Moussion, I., Cochet, A., Paupy, C., Rousseau, C., Paty, M.C., Golliot, F. 2016. Autochthonous dengue outbreak in Nîmes, South of France, July to September 2015. Euro Surveill. 26, pii=30240. DOI: 10.2807/1560-7917
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Toma, L., Severini, F., Di Luca, M., Bella, A., Romi, R., 2003. Seasonal patterns of oviposition and egg hatching rate of Aedes albopictus in Rome. J. Am. Mosq. Control Assoc. 19, 19-22.
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Venturi, G., Di Luca, M., Fortuna, C., Remoli, M.E., Riccardo, F., Severini, F., Toma, L., Del Manso, M., Benedetti, E., Caporali, M.G., Amendola, A., Fiorentini, C., De Liberato, C., Giammattei, R., Romi, R., Pezzotti, P., Rezza, G., Rizzo, C., 2017. Detection of a chikungunya outbreak in Central Italy, August to September 2017. Euro Surveill. 22, pii=17-00646. DOI: 10.2807/1560-7917.ES.2017.22.39.17-00646 Waldock, J., Chandra, N.L., Lelieveld, J., Proestos, Y., Michael, E., Christophides, G., Parham, P.E., 2013. The role of environmental variables on Aedes albopictus biology and chikungunya epidemiology. Pathog. Glob. Health 107, 224-241. DOI: 10.1179/2047773213Y.0000000100 Walther, D., Kampen, H., 2017. The citizen science project ‘Mueckenatlas’ helps monitor the distribution and spread of invasive mosquito species (Diptera: Culicidae) in Germany. J. Med. Entomol. 54, 1790-1794. DOI: 10.1093/jme/tjx166.
Walther, D., Scheuch, D.E., Kampen, H., 2017. The invasive Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Germany: local reproduction and overwintering. Acta Trop. 166 186-192. DOI: 10.1016/j.actatropica.2016.11.024 Werner, D., Kampen, H., 2015. Aedes albopictus breeding in southern Germany, 2014. Parasitol. Res. 114, 831-834. DOI: 10.1007/s00436-014-4244-7 Werner, D., Kronefeld, M., Schaffner, F., Kampen, H., 2012. Two invasive mosquito species, Aedes albopictus and Aedes japonicus japonicus, trapped in south-west Germany, July to August 2011. Euro Surveill. 17, pii=020067. DOI: 10.2807/ese.17.04.20067-en
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Wu, F., Liu, Q., Lu, L., Wang, J., Song, X., Ren, D., 2011. Distribution of Aedes albopictus (Diptera: Culicidae) in northwestern China. Vector Borne Zoonot. Dis.11, 1-6. DOI: 10.1089/vbz.2010.0032
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Table 1.
June 17 LL
-
-
1 FH
Aug 45 EE 27 LL 2 PP 1 FG 1 FM
-
44 LL
-
-
-
-
-
subtotal
141 EE 51 LL 1F
7 LL
61 LL
4 LL 1F 1M
total
141 EE 51 LL 1F
141 EE 51 LL
JenaLobeda
1 FM
garden centre Jena-City Jena-East Jena-North
-
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JenaLobeda cemetery
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2016 May 7 LL
A
2015
M
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Numbers of Aedes albopictus with developmental stages (E: egg, L: larva, P: pupa, F: female, M: male) collected in the various parts of Jena from 2015 to 2017. All eggs were collected from ovitraps, all larvae and pupae from artificial water containers (ovitraps, flower vases, plant pots, dishes, etc.). Adults were trapped by a BG-Sentinel 2 (B), a BG-GAT (G), or by hand (H). ‘Mueckenatlas’ submissions are specifically indexed (M). July 4 LL 1 MG
Sept -
total -
-
-
-
Oct 30 EE 5 LL
-
Sept 75 EE 29 LL 1P 1 FH 25 EE 2 LL 1 FM 3L
-
47 LL
-
-
-
-
-
-
-
1 FM -
100 EE 34 LL 1P 2 FF
30 EE 5 LL
-
1 FH 4 LL 1 FB 4 LL 2 FF
1F 1F 4 LL 1F -
45 EE 27 LL 2 PP 2 FF 175 EE, 138 LL, 3 PP, 5 FF, 1 M
-
total 89 LL 3 PP 2 FF 1M 2 LL 4 FF
2017 Aug -
1F
4 LL, 2 FF, 1 F
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Table 2.
A
Dec
Jan
2017 Mar
2.0
4.5
5.1
9.1
14.8
4.5
M
Feb
Apr
May
Nov
Dec
Jan
Feb
Mar
Apr
May
2.9
-1.4
3.5
8.2
8.8
15.1
Heidelberg
7.6
3.6
5.2
6.1
10.1
14.1
6.1
2.6
-1.0
6.2
10.5
11.1
17.2
Freiburg
8.3
4.0
5.4
6.5
10.6
15.9
5.3
0.2
-3.0
5.3
9.7
10.5
17.2
Jena
4.9
-0.3
2.1
2.6
5.0
10.4
2.5
0.7
-3.5
1.0
4.1
5.3
10.3
Heidelberg
3.6
1.1
2.8
1.9
6.1
9.5
3.6
0.3
-3.4
2.9
5.7
6.0
12.5
Freiburg
5.4
1.6
2.6
2.3
5.7
11.2
1.3
-3.7
-6.9
0.7
3.0
2.8
9.2
ED
7.2
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mean minimum temperature (°C)
2016
Jena
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monthly mean temperature (°C)
2015
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Monthly mean temperatures and mean minimum temperatures in Ae. albopictus distribution areas in Jena, Heidelberg and Freiburg as calculated from December 2015 to May 2016 and from November 2016 to May 2017.
Table 3. The mean excesses and their 95 % confidence intervals (95 % CI) for the -3 °C threshold in the winter seasons 2015/2016 and 2016/2017 in Jena, Heidelberg and Freiburg.
Heidelberg
mean excess -2.89 -1.90 -1.64 -1.94 -2.69 -3.48
95 % CI [-3.48, -2.30] [-2.06, -1.73] [-1.88, -1.40] [-2.14, -1.74] [-3.10, -2.29] [-3.73, -3.24]
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ED
M
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Freiburg
2015/2016 2016/2017 2015/2016 2016/2017 2015/2016 2016/2017
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Jena
S0001-706X(18)30649-1 https://doi.org/10.1016/j.actatropica.2018.08.019 ACTROP 4755
To appear in:
Acta Tropica
Received date: Revised date: Accepted date:
30-5-2018 17-8-2018 17-8-2018
Please cite this article as: Kuhlisch C, Kampen H, Walther D, The Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Central Germany: Surveillance in its northernmost distribution area, Acta Tropica (2018), https://doi.org/10.1016/j.actatropica.2018.08.019 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
The Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Central Germany: surveillance in its northernmost distribution area Cornelius Kuhlischa*, Helge Kampenb, Doreen Walthera a
Leibniz Centre for Agricultural Landscape Research, Eberswalder Str. 84, 15374 Müncheberg, Germany b
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Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Suedufer 10, 17493 Greifswald - Insel Riems, Germany * Corresponding author
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E-mail addresses: [email protected] (C. Kuhlisch) [email protected] (H. Kampen) [email protected] (D. Walther)
Highlights
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Northernmost population of Aedes albopictus observed in Central Germany Local winter temperatures allow long-term establishment of Aedes albopictus Introduction possibly through plants from Italy
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Abstract
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The invasive Asian tiger mosquito Aedes albopictus has recently been observed in southern Germany for the first time to reproduce and even overwinter north of the Alps. After the accidental capture of adult specimens in Jena, German federal state of Thuringia, in mid-2015, regular inspections brought forth developmental stages until autumn 2015, indicating local reproduction. Surveillance activities implemented in 2016 showed larvae already in early May, suggesting overwintering, and throughout the season until late October, although population densities remained low. Further sporadic specimens found in 2017 argue for establishment. Jena is located in Central Germany, north of all known distribution areas of Ae. albopictus, with the area of the municipality affected by the tiger mosquito characterised by a relatively mild climate. To check the suitability of the local climate for Ae. albopictus, winter temperatures, measured in a cemetery of Jena where larvae had regularly been found in 2015 and 2016, were analysed and compared with two sites of establishment in southern Germany. The conditions were similar at all three locations, suggesting that the Jena population might also be able to survive in the long term. While the municipality authorities have been informed and education of the Jena citizens to avoid producing potential breeding places has started, insecticidal control has not yet been implemented. Keywords: Aedes albopictus; cold hardiness; Germany; invasive species; northernmost distribution; overwintering
1. Introduction The Asian tiger mosquito Aedes (Stegomyia) albopictus (Skuse, 1895) is an efficient potential vector of numerous human and animal pathogens, such as dengue virus, chikungunya virus, West Nile virus, Rift Valley fever virus and dirofilarial nematodes (Gratz, 2004; Paupy et al., 2009) and is therefore of paramount public and veterinary health concern. In Europe, it was made responsible for recent outbreaks of dengue and chikungunya (Schaffner et al., 2013; Calba et al., 2017; Succo et al., 2017; Venturi et al., 2017).
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Originating from the Asian-Pacific region, Ae. albopictus was first reported in Europe from Albania in 1979 (Adhami and Reiter, 1998). Only some ten years later, it was discovered in Italy (Sabatini et al., 1990), from where it spread over large parts of the Mediterranean and beyond (Medlock et al., 2015). While both intercontinental and continental displacement is through transportation of eggs or larvae by the trade with used tyres and ornamental plants (e.g. Dracaena sp.), adults entering vehicles contribute to continental spread (Becker et al., 2017; Eritja et al., 2017; Hofhuis et al., 2009; Knudsen et al., 1996; Reiter, 1998; Walther et al., 2017). Since 2007, the species has been found on service stations along South German motorways (Becker et al., 2013; Kampen et al., 2013; Pluskota et al., 2008; Werner et al., 2012), and in 2014 and 2015, extended local reproduction was observed in the German cities of Freiburg, Heidelberg and Jena (Pluskota et al., 2016; Werner and Kampen, 2015; Walther et al., 2017). While in Freiburg and Heidelberg Ae. albopictus quickly developed alarming population densities which had prompted the implementation of control activities (Becker et al., 2017), detections of specimens in Jena remained sporadic.
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Aedes albopictus is a thermophilic mosquito species which is adapted to both tropical and temperate climates, depending on its origin (Benedict et al., 2007; Hawley, 1988). Populations of temperate strains are known to have a higher cold hardiness than tropical ones which, in contrast, cannot overwinter as diapausing eggs (Hanson and Craig, 1994; Hawley et al., 1989). According to studies by Delatte et al. (2009), larval development does not take place below 10 °C and is optimal at temperatures between 25 and 30 °C. Larval survival rates are highest at 15 °C, and gonotrophic cycles are shortest at about 30 °C. In regions with relatively high summer temperatures, populations develop quickly, and densities reach their peaks early in the season, whereas in regions with low summer temperatures population growth is slow but steady, with a maximum later in the season (Alto und Juliano, 2001).
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Future projection models suggest that climatically suitable areas for the establishment of Ae. albopictus will remain stable or increase until 2040 in western and Central Europe and, with some delay, probably also increase in eastern Europe (Caminade et al., 2012; Fischer et al., 2011, 2014). By contrast, living conditions are expected to deteriorate along the western Mediterranean coast of Spain (Fischer et al., 2014). Considerable discrepancies exist between different models, which predict France, Germany and western parts of the United Kingdom to become either persistently unsuitable or increasingly suitable (Fischer et al., 2014). In this study, we describe the finding and population development of Ae. albopictus in the Central German city of Jena, which, to the best of the authors’ knowledge, represents the northernmost area colonised by this invasive mosquito species. Temperature profiles of the winter seasons 2015/2016 and 2016/2017 between locations with Ae. albopictus occurrence in Jena and in the Southwest German towns of Heidelberg and Freiburg, where the species is considered established, were compared.
2. Methods 2.1 Mosquito collection
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In the framework of the German citizen science project ‘Mueckenatlas’ (mosquito atlas), where mosquitoes are routinely submitted for identification by private persons from all over Germany (Walther and Kampen, 2017), two Ae. albopictus specimens were received from the City of Jena (N50.8890, E11.6085, altitude 165 m), German federal state of Thuringia, in July 2015 (Fig. 1). As a reaction, all cemeteries in the municipality of Jena were monitored for Ae. albopictus developmental stages from mid-July to late October 2015. After the repeated detection of larvae in the cemetery of Jena-Lobeda, the surveillance continued at this site and was extended to nearby construction markets, garden centres and allotment gardens from 11 May to 8 November 2016 and from 1 May to 26 October 2017 by checking all water-holding containers on a biweekly basis. In addition, 10 standard ovitraps (440 ml), equipped with wooden spatulas (150 x 30 mm2) as oviposition supports, were distributed over the surveillance area according to the ECDC guidelines for monitoring invasive mosquito species (ECDC, 2012), i.e. placement of one ovitrap per 2,500 m2. Further ovitraps were placed 20 metres apart in the Jena-Lobeda cemetery (n=15), and 100 metres apart around that cemetery (n=25) and in both garden centres (n=5, each) in 2017. Also, ten gravid Aedes traps (BGGAT, Biogents, Germany) were placed to catch adult Ae. albopictus individuals in the Jena-Lobeda cemetery (n=5) and both garden centres (n=2+3). One BG-Sentinel 2 trap (Biogents) each, equipped with BG-Lure (Biogents) and a carbon dioxide tank as attractants, was operated with mains supply for 72 hours at protected and hidden sites in the Jena-Lobeda cemetery and two further cemeteries in Jena, characterised by similar climatic conditions (Hoffmann et al., 2014), in August 2017.
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If larvae were found in water containers (ovitraps, flower vases, plant pots, dishes, etc.), they were brought into the laboratory in jars containing water from their breeding sites and fed with fish food flakes (Guppy, Tetra, Germany) until adult emergence. The wooden spatulas of the ovitraps were collected every two weeks to be checked for eggs. Both eggs and larvae dying before completion of development were genetically identified to species by CO1 barcoding according to Ibáñez-Justicia et al. (2014). Adult mosquito specimens were determined morphologically using the key by Becker et al. (2010). To determine a container index in the Jena-Lobeda cemetery, all containers with eggs, larvae or pupae of Ae. albopictus were counted on 24 August 2016, a date considered representative for the period of highest population density.
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Fig. 1.
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Relief map of Jena showing Ae. albopictus findings in 2015 (yellow), 2015 & 2016 (green), 2016 (red) and 2017 (blue). Dots encircled in black indicate submissions to the ‘Mueckenatlas’. © GeoBasis-DE / BKG 2017.
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2.2 Climate data collection and analysis
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Temperatures were measured by HOBO Pro v2 data loggers (Onset Computer Corporation, MA, USA) every hour from December 2015 to May 2016 and from November 2016 to May 2017, both in the Jena-Lobeda cemetery and at known sites of Ae. albopictus establishment and hibernation in Heidelberg and Freiburg (Becker et al., 2017; Walther et al., 2017). The loggers were located close to known Ae. albopictus breeding places at weather-protected sites at heights of 1.5 to 2.0 metres, as standard for climate measurements.
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As the survival of diapausing eggs does not only depend on the temperature minimum, but also on the duration and the frequency a temperature threshold is exceeded, we defined a ‘frost period’, in which the measured temperatures dropped below a specific threshold. For all thresholds between the local minimum temperatures measured during the two winter seasons and 0 °C, the frequency of frost periods, their durations and minimum temperatures were analysed in Jena, Heidelberg and Freiburg, following the Peak-Over-Threshold (POT) approach: ''The idea is to keep, from recorded series, ... values above a predefined threshold ... . The advantage of the POT approach is that more than one extreme value can be considered.'' (Mailhot et al., 2012). The approach was applied on the additive inverse of the frost temperatures with the R package POT (Ribatet and Dutang, 2016; R Core v3.3.2, 2016).
3. Results 3.1 Collection of Aedes albopictus Two female Ae. albopictus specimens were submitted to the ‘Mueckenatlas’ citizen science project from the Lobeda district of the municipality of Jena, Thuringia, in mid-July 2015 (Fig. 1). During subsequent on-site inspections, eggs (n=141) and larvae (n=51) were continuously found in the JenaLobeda cemetery until 26 October 2015 (Table 1). No Ae. albopictus were found in 20 further cemeteries of the municipality checked in mid-August 2015.
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In 2016, 138 larvae, 3 pupae and 6 adults of Ae. albopictus were collected during inspections of known and new locations in Jena between 11 May and 21 October (Fig. 1, Table 1). On 24 August, the container index in the Jena-Lobeda cemetery was almost 19 % (with developmental stages present in 10 out of 54 water-filled flower vases and ovitraps checked). Moreover, 150 eggs of Ae. albopictus were detected sporadically, and sometimes repeatedly, on the oviposition supports of eight ovitraps operated in this cemetery between 11 August and 5 October.
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In the surroundings of about 300 to 700 metres away from the Jena-Lobeda cemetery, 47 larvae and an attacking female were collected between end-June and mid-September 2016. Furthermore, two females collected on 28 August and 25 September 2016 at a location ca. 400 metres south of the Jena-Lobeda cemetery were submitted to the ‘Mueckenatlas’. Twenty-five eggs and two larvae of Aedes albopictus were identified in early September 2016 in one ovitrap placed 160 metres away from the Jena-Lobeda cemetery. No Ae. albopictus specimens were found between 21 October and the end of the observation period on 8 November 2016.
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Between 1 May and 26 October 2017, neither eggs, nor larvae or adults of Ae. albopictus could be identified during inspections of the Jena-Lobeda district. Instead, three kilometres north of this area, two females and four larvae were collected in the cemeteries of Jena-North and Jena-East in midAugust and late September 2017 (Fig. 1, Table 1).
3.2 Climate data analysis
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Both in Jena and in the other two Ae. albopictus population areas in southern Germany, Heidelberg and Freiburg, where temperature data loggers were operated, monthly mean temperatures stayed above 2 °C in the winter season 2015/2016 (Table 2). By contrast, the monthly mean minimum temperatures (Table 2) and the daily mean temperatures (Fig. 2) in Jena were slightly below freezing point in January, only showing negligible differences to Freiburg and Heidelberg. Also, the general daily temperature profile showed no relevant differences between the three locations (data not shown).
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Fig. 2.
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Daily mean temperatures in the Jena-Lobeda Ae. albopictus distribution area, from December 2015 to May 2016 (red) and from December 2016 to May 2017 (blue). The arrow marks the beginning of the Ae. albopictus detection period in 2016.
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In the winter season 2016/2017, the monthly mean temperatures were lower in December and January in Freiburg than in Heidelberg and Jena (January: -3 °C vs. -1 °C) (Table 2), but the daily mean temperatures in these months reached considerably higher levels in Jena than in Freiburg and Heidelberg (data not shown). In Jena, they increased gradually from 0 °C in late January to above 10 °C in early April, before falling again below 3 °C at the end of April (Fig. 2).
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On average, the measured temperatures in Jena were approximately 4 Kelvin lower between 19 December 2016 and 14 February 2017 (Fig. 3A) but 3 to 4 Kelvin higher between 15 February and 3 April 2017 (Fig. 3B) than in the same time periods of the winter season 2015/2016. After these periods, the courses of the temperatures were similar to the year before until the end of May (Fig. 3C).
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Fig. 3.
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Difference of daily mean temperatures between 2016 and 2017 from December to May in Jena. The sections A (1 December to 15 February), B (16 February to 3 April) and C (3 April to 1 June) show periods of different temperature profiles.
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The hourly measured data of both winter seasons in Jena-Lobeda show that for thresholds between -6 °C and 0 °C, frost periods occurred more frequently during the winter 2016/2017 than during the winter 2015/2016 (Fig. 4). At a threshold temperature of -6 °C, however, frost periods longer than ten hours occurred equally often in both winter seasons. By contrast, at a threshold temperature of -5 °C, more frost periods longer than ten hours were observed in 2016/2017 compared to 2015/2016. At threshold temperatures between -3 °C and 0 °C, frost periods were considerably longer in 2016/2017 than in 2015/2016 (Fig. 4).
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Fig. 4.
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Absolute temperatures [°C] per hour in Jena, Heidelberg and Freiburg from November to March during the cold seasons 2015/2016 and 2016/2017. Temperature measurements in Jena started 24 November 2015 and in Heidelberg and Freiburg 19 December 2015.
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Two cold spells occurred in Jena in January 2016 (Fig. 4), with the first one from 2 to 7 January, reaching a minimum of -2.6 °C on 6 January, and the second one from 17 to 23 January, reaching a minimum of -10.7 °C on 22 January. The duration and frequency of frost periods in Freiburg and Heidelberg were similar to Jena. From 3 November to 30 April of the winter season 2016/2017, there were several periods in each of the three locations, during which the temperature dropped below freezing point. In Jena, ten frost periods were observed for a threshold of -5 °C, which took at least 5 hours, while in Freiburg even 23 such frost periods were registered. The longest frost period in Jena lasted 18 hours, in Freiburg 21 hours. Of three cold spells in Jena in the winter season 2016/2017, the one from 15 to 23 January was extreme in that temperatures dropped below freezing point twice and for a considerable time each, reaching minima of -8.2 °C on 20 January and -9.5 °C on 23 January.
By means of the POT approach, the -3 °C threshold was selected from all possible thresholds for the comparison of the temperature profiles between the three locations and the two winter seasons because the parameters of the Pareto distribution changed between -2 and -4 °C in a qualitative manner. Using the 95 % confidence interval for the mean excess, significant differences at an alphalevel of 5 % could be shown between Jena/Freiburg and Heidelberg in 2015/2016, between Jena/Heidelberg and Freiburg in 2016/2017, and between the two winter seasons in Jena (Table 3).
4. Discussion
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The first report of Ae. albopictus from Jena-Lobeda, due to a submission to the ‘Mueckenatlas’ surveillance scheme, represents one of the first findings of specimens of this species in Germany north of the Upper Rhine Valley (Walther et al., 2017). During initial local inspections in 2015, larvae and eggs were found exclusively in a cemetery close by the collection site of the submitted specimens. Their moderate number suggested a relatively low population density. Collections in the very same cemetery and relatively early in the mosquito season 2016 (May) indicated overwintering. The onset of development in May agrees with the first seasonal findings of larvae in the southern German towns of Heidelberg and Freiburg where Ae. albopictus has been shown to overwinter (Becker et al., 2017; Pluskota et al., 2016; Walther et al., 2017).
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With the population increasing, a higher number of larvae was encountered in the Jena-Lobeda cemetery in August and September 2016. Subsequently, specimens appeared to disperse from the relatively individual-rich centre of the population to the periphery, a behaviour also described by Mori (1979). Thus, outside of the cemetery, eggs were detected in an ovitrap and adults captured in September (Fig. 1).
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Of particular interest regarding the possible mode of introduction of Ae. albopictus to Jena is the report of employees of the affected garden centre about a huge number of mosquito larvae in the water in which lotus plants (Nelumbo sp.) had been delivered in 2014. The plants had been transported from Italy via way-stations in the Netherlands and the German Upper Rhine Valley before they arrived in Jena. The time these plants were imported would well explain the first detection of Ae. albopictus in 2015, supporting the assumption that the garden centre might be the origin of proliferation and dispersal, instead of the Jena-Lobeda cemetery where the first developmental stages were found.
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Eventually, it was not possible yet to find out, where the mosquitoes came from and whether all individuals sampled in Jena resulted from the same initial introduction event or from separate importations. A genetic analysis of the populations in Jena related to other German and European populations is under way. Of course, the high number of larvae collected in late June and September 2016 in the garden centre could have also been caused by the local reproduction of Ae. albopictus specimens introduced from other, previously colonised areas of Jena (e.g., Jena-Lobeda cemetery) or new introductions from areas in southern Germany or southern Europe where high population densities already exist early in the year. The fact that no individuals of Ae. albopictus could be found in Jena-Lobeda in 2017 may be a result of the relatively cold winter season 2016/2017 but also of countermeasures of authorities and citizens sensitised to prevent propagation. Such countermeasures were realised in the cemetery since 2016, where the majority of unused flower vases were turned over and the wells emptied in order not to provide mosquito breeding places. In addition, citizens were publicly requested to empty and clean all water containers in their gardens and on their balconies and to cover water-filled containers. Because of the consistently low abundance of Ae. albopictus individuals, there was no possibility to evaluate the success of the measures quantitatively.
Jena, Heidelberg and Freiburg are located in regions with continental climates, but due to geographical and geological peculiarities, these cities are relatively warm, with a pronounced continental climate in Jena. Therefore, the establishment of Ae. albopictus in Jena may have been facilitated by the following specifics of the affected area: Jena is located in a weather-sheltered region in the Saale Valley where a heat-island effect can occur. The ground consists of Bunter sandstone (Röt formation) with shell-bearing limestone-slopes which are able to heat up excessively and store and reflect the warmth over a considerable period of time (Hoffmann et al., 2014).
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Our findings of Ae. albopictus in Jena agree with some models which show that Germany is a potential distribution area for this species, although the thermal suitability of Europe north of the Alps has generally been considered low (Mogi et al., 2012; Kraemer et al., 2015; Proestos et al., 2016). In its native distribution range of East and Southeast Asia, the northernmost areas of occurrence are located in China and Japan (Hanson, 1995; Kobayashi, 2002; Mogi, 2012; Wu et al., 2011). As a prerequisite for the establishment of Ae. albopictus, various variables have been determined. For Europe, an annual mean precipitation of at least 200 to 250 mm, an annual mean temperature of at least 8 °C and a January mean temperature not lower than -4 to 0 °C has been suggested to be necessary (Waldock et al., 2013). With respect to the January mean temperature, the northern distribution limit in Europe is estimated to correspond to the climatic situation in China (January mean -5 °C; Nawrocki and Hawley, 1987; Wu et al., 2011) rather than in Japan (January mean -2 °C; Kobayashi et al., 2002). In northeastern China, Ae. albopictus was found to permanently occur in areas, where the January mean temperature can be as low as -5 °C, and to expand its summer distribution northwards into regions with even colder average temperatures (Wu et al., 2011). However, according to the Köppen-Geiger climate classification (Kottek et al., 2006), the temperate oceanic and continental regions in western Europe are distributed over a much larger area of land than in Northeast China and may make it more difficult for this mosquito to spread to less favourable climatic regions than in China.
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Consequently, a crucial factor determining the spread of this thermophilic species in temperate Europe is the temperature (Delatte et al., 2009). In addition to other climatic or population-dynamic factors, temperature basically influences population growth during the vegetative season and survival of diapausing eggs during wintertime. At all three locations where temperatures had been measured in this study (Jena, Heidelberg, Freiburg), January mean temperatures were 2 °C or higher in the winter season 2015/2016. Furthermore, long-term annual mean precipitations (period 1980 to 2010) were 610 mm, 732 mm and 934 mm, and annual mean temperatures 9.9 °C, 11.4 °C and 11.4 °C, respectively (Hoffmann et al., 2014; German Weather Service, 2017; Groß, 2015). According to these data, all three locations fall within the climatic requirements for survival during the winter diapause and, thus, for possible establishment of Ae. albopictus (Waldock et al., 2013). The specific temperature conditions in Jena were similar to Heidelberg and Freiburg, where Ae. albopictus proliferates well. This also suggests that other localities with similar data should be thoroughly surveyed for Ae. albopictus establishment in the future. Diapausing eggs of cold-acclimated Ae. albopictus from Rimini, Italy, have been shown to be able to survive temperatures of -10 °C for 24 hours or -12 °C for 1 hour (Thomas et al., 2012). Based on this and the fact that temperatures in Jena, the coldest one of the observed locations, reached -10 °C to -11 °C only once for a period of 4 hours during the winter season 2015/2016, eggs would have been likely to survive the cold season at all three locations. This would explain the early emergence of specimens in Jena in 2016. The winter season 2016/2017 might have influenced the survival of Ae. albopictus and caused no findings in Jena-Lobeda in 2017. In fact, significant differences in the temperature profiles existed in Jena between the two investigated winter seasons 2015/2016 and 2016/2017. Such differences were
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found in the frequency in which temperatures dropped below a certain threshold, the duration of such periods, the minimum temperatures reached and mean excess temperatures below a certain threshold. If the frequency of temperature dropping affected the survival of Ae. albopictus, the eggs may have not survived the winter season 2016/2017 because hourly measured temperatures dropped too often below a threshold between -5 °C and 0 °C. If the duration of the frost periods was relevant, the eggs may have not survived because temperatures dropped below a threshold between -3 °C and 0 °C for too long. Minimum temperatures, however, were lower in 2015/2016 than in 2016/2017 and, therefore, could have not exclusively been responsible for Ae. albopictus not being found in Jena-Lobeda in 2017. Thus, critical conditions may indeed have existed in the winter season 2016/2017 with regard to a higher frequency and a longer duration of low temperature events, causing a reduction in egg survival and no findings of Ae. albopictus in Jena-Lobeda during the monitoring in 2017. This assumption is based on the significant difference in the mean excess for the -3 °C threshold.
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No temperature data for the various districts of Jena where Ae. albopictus emerged in 2017 are available, but due to the specific landscape structure of the municipality, considerable climatic differences are conceivable on a small-scale (Hoffmann et al., 2014), allowing the tiger mosquito to survive in some areas but not in others.
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Furthermore, the cold period in late April 2017 might have had a negative impact on the survival of developing larvae in Jena-Lobeda after a relatively warm period in late March (Fig. 2). While in late March, daily mean temperatures of 11.8 °C to 14.7 °C were recorded for six days following a period of precipitation for two days, suggesting larval hatching (c.f. Lacour et al., 2015; Medlock et al., 2006; Thomas et al., 2012; Toma et al., 2003; Waldock et al., 2013), temperatures dropped again below 10 °C for five days and sometimes even below 5 °C by late April. The findings of Ae. albopictus in Central Jena and Jena-North in August 2017 as well as in Jena-East in September 2017 probably originated from individuals which had been displaced the year before from Jena-Lobeda and overwintered somewhere else or, less likely, were newly introduced in 2017.
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Aedes albopictus succeeded in overwintering in Freiburg from 2014 to 2015 and in Jena, Heidelberg and Freiburg from 2015 to 2016. In Jena, the cool and long spring 2016 might have impeded a quick recovery of the population after the winter (Fig. 2). In addition to the winter and summer conditions (Pluskota et al., 2016), the spring conditions therefore seem to have a decisive impact on the development of Ae. albopictus in temperate Europe and should obtain more attention in future analyses. Thus, in a suboptimal environment such as Europe north of the Alps, the entire course of the year can be expected to influence the distribution and population density of Ae. albopictus.
5. Conclusions
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The findings of Ae. albopictus in Jena from 2015 to 2017 as well as the majority of the climate data demonstrate that the species has the potential to establish in Jena. Indeed, eggs may even survive colder winters at sheltered spots and develop considerable population densities during the following summer. Problems may arise after larval hatching in spring through late frosts and low temperatures, which - due to the continentality - are more likely to occur in Jena than in Heidelberg and Freiburg, resulting in negative effects on population development. Jena currently harbours the northernmost known Ae. albopictus population. This, however, has to be considered with respect to comparable climatic conditions which are not necessarily found at identical latitudes in different regions of the world. The investigations demonstrate the detection of Ae. albopictus in Jena-Lobeda in 2015, following possible introduction in 2014, population growth in 2016, and simultaneous lack of findings in Jena-Lobeda and emergence in other city districts in 2017.
The detailed temperature measurements indicate that the climatic conditions in Jena might be suitable for long time persistence, although - according to the low population density - the species appears to struggle for survival. It remains to be awaited whether Ae. albopictus will become extinct or will firmly establish in the future. Sporadic findings of larvae and adults in Jena-North, Jena-East and Jena-Lobeda in June and July 2018, during the review process of this contribution, suggest a high probability for the latter.
Author contributions
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Conceived and designed the experiments: DW, HK, CK. Collected and identified the mosquitoes: CK, DW, HK. Collected and analysed climate data: CK. Contributed reagents/materials/analysis tools: DW, HK. Wrote the paper: CK, DW, HK. All authors read and approved the final version of the manuscript.
Conflict of interest
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There is no conflict of interest.
Funding
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This work was financially supported by the German Federal Ministry of Food and Agriculture (BMEL) through the Federal Office for Agriculture and Food (BLE) [grant number 2819104615].
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Acknowledgements
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The authors thank the City of Jena for productive collaboration and Jutta Falland and Juliane Horenk for technical support in the laboratory.
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ED
M
A
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U
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I N U SC R
Table 1.
June 17 LL
-
-
1 FH
Aug 45 EE 27 LL 2 PP 1 FG 1 FM
-
44 LL
-
-
-
-
-
subtotal
141 EE 51 LL 1F
7 LL
61 LL
4 LL 1F 1M
total
141 EE 51 LL 1F
141 EE 51 LL
JenaLobeda
1 FM
garden centre Jena-City Jena-East Jena-North
-
CC E
PT
JenaLobeda cemetery
ED
2016 May 7 LL
A
2015
M
A
Numbers of Aedes albopictus with developmental stages (E: egg, L: larva, P: pupa, F: female, M: male) collected in the various parts of Jena from 2015 to 2017. All eggs were collected from ovitraps, all larvae and pupae from artificial water containers (ovitraps, flower vases, plant pots, dishes, etc.). Adults were trapped by a BG-Sentinel 2 (B), a BG-GAT (G), or by hand (H). ‘Mueckenatlas’ submissions are specifically indexed (M). July 4 LL 1 MG
Sept -
total -
-
-
-
Oct 30 EE 5 LL
-
Sept 75 EE 29 LL 1P 1 FH 25 EE 2 LL 1 FM 3L
-
47 LL
-
-
-
-
-
-
-
1 FM -
100 EE 34 LL 1P 2 FF
30 EE 5 LL
-
1 FH 4 LL 1 FB 4 LL 2 FF
1F 1F 4 LL 1F -
45 EE 27 LL 2 PP 2 FF 175 EE, 138 LL, 3 PP, 5 FF, 1 M
-
total 89 LL 3 PP 2 FF 1M 2 LL 4 FF
2017 Aug -
1F
4 LL, 2 FF, 1 F
I N U SC R
Table 2.
A
Dec
Jan
2017 Mar
2.0
4.5
5.1
9.1
14.8
4.5
M
Feb
Apr
May
Nov
Dec
Jan
Feb
Mar
Apr
May
2.9
-1.4
3.5
8.2
8.8
15.1
Heidelberg
7.6
3.6
5.2
6.1
10.1
14.1
6.1
2.6
-1.0
6.2
10.5
11.1
17.2
Freiburg
8.3
4.0
5.4
6.5
10.6
15.9
5.3
0.2
-3.0
5.3
9.7
10.5
17.2
Jena
4.9
-0.3
2.1
2.6
5.0
10.4
2.5
0.7
-3.5
1.0
4.1
5.3
10.3
Heidelberg
3.6
1.1
2.8
1.9
6.1
9.5
3.6
0.3
-3.4
2.9
5.7
6.0
12.5
Freiburg
5.4
1.6
2.6
2.3
5.7
11.2
1.3
-3.7
-6.9
0.7
3.0
2.8
9.2
ED
7.2
CC E
mean minimum temperature (°C)
2016
Jena
PT
monthly mean temperature (°C)
2015
A
Monthly mean temperatures and mean minimum temperatures in Ae. albopictus distribution areas in Jena, Heidelberg and Freiburg as calculated from December 2015 to May 2016 and from November 2016 to May 2017.
Table 3. The mean excesses and their 95 % confidence intervals (95 % CI) for the -3 °C threshold in the winter seasons 2015/2016 and 2016/2017 in Jena, Heidelberg and Freiburg.
Heidelberg
mean excess -2.89 -1.90 -1.64 -1.94 -2.69 -3.48
95 % CI [-3.48, -2.30] [-2.06, -1.73] [-1.88, -1.40] [-2.14, -1.74] [-3.10, -2.29] [-3.73, -3.24]
A
CC E
PT
ED
M
A
N
U
SC R
Freiburg
2015/2016 2016/2017 2015/2016 2016/2017 2015/2016 2016/2017
IP T
Jena