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Occurrence of the Invasive Spanish Slug in Gardens

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Occurrence of the Invasive Spanish Slug in Gardens Dörler et al. BMC Ecol (2018) 18:23 https://doi.org/10.1186/s12898-018-0179-7 BMC Ecology RESEARCH ARTICLE Open Access Occurrence of the invasive Spanish slug in gardens: can a citizen science approach help deciphering underlying factors? Daniel Dörler1* , Matthias Kropf2, Gregor Laaha3 and Johann G. Zaller1 Abstract Background: The Spanish slug (Arion vulgaris, also known as A. lusitanicus) is considered one of the most invasive species in agriculture, horticulture and private gardens all over Europe. Although this slug has been problematic for decades, there is still not much known about its occurrence across private gardens and the underlying meteorological and ecological factors. One reason for this knowledge gap is the limited access of researchers to private gardens. Here we used a citizen science approach to overcome this obstacle and examined whether the occurrence of Arionidae in Austrian gardens was associated with meteorological (air temperature, precipitation, global solar radiation, relative humidity) or ecological factors (plant diversity, earthworm activity). Occurrence of the invasive A. vulgaris versus the similar-looking native A. rufus was compared using a DNA-barcoding approach. Results: Slugs were collected from 1061 gardens from the dry Pannonian lowland to the wet alpine climate (altitu- dinal range 742 m). Slug abundance in gardens was best explained and negatively associated with the parameters “sum of the mean air temperature in spring”, “number of frost days in the previous winter” and “mean daily global solar radiation on the day of data collection”. Precipitation, plant diversity and earthworm activity were also related to slug abundance, but positively. Out of our genetic sampling of collected slugs, 92% belonged to A. vulgaris. Conclusions: Our study showed that citizen science (i) is a feasible approach to record species occurrence in restricted areas across a wide geographical range and (ii) could be more widely employed in order to identify underly- ing environmental factors of species occurrence. Keywords: Arion vulgaris, Arion lusitanicus, Participation, Pest slugs, Weather, Neobiota, DNA barcoding Background dispersal occurs are often among the frst to notice this Invasive alien species have been recognized as a threat change in their environment [2, 3]. As a consequence, to biodiversity, human health and economy by many many environmental protection agencies, research facili- countries [1]. Trough global trade routes organisms are ties and municipalities use citizen science as a method of transported both deliberately and accidentally around choice to detect invasive species at early stages [4, 5]. Cit- the globe, sometimes fnding a new home in areas they izen science describes a method where citizens and sci- never could have reached on their own. In many cases entists work together in scientifc projects. Te citizens these species remain unnoticed until they establish viable usually collect data, analyze data or are even involved in populations, spread quickly and outcompete native spe- the whole scientifc process [6]. cies, or become pestiferous in agriculture, horticulture or In the current study we tested the citizen science private gardens. At this stage residents of areas where the approach to assess the occurrence of the Spanish slug Arion vulgaris Moquin-Tandon 1855 (formerly known *Correspondence: [email protected] as A. lusitanicus auct. non-Mabille) in private gardens in 1 Institute of Zoology, University of Natural Resources and Life Sciences, Austria. Urban biota can host a variety of native and non- Vienna, Vienna, Austria native species [7] and gardens are particularly interesting Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat​iveco​mmons​.org/ publi​cdoma​in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Dörler et al. BMC Ecol (2018) 18:23 Page 2 of 11 areas, because they are ‘designed’ by humans [8] and Participants were undergraduate students at the Uni- therefore species numbers often vary from one garden versity of Natural Resources and Life Sciences, Vienna. to the next. In Austria A. vulgaris was described for the All participants got 1 h training explaining the goal of frst time in 1971 in a village near Vienna [9]. Te origin this project and the sampling protocol. Tis method of this slug is still controversial [10, 11], but it is never- allowed us to get data on slug and plant diversity from theless listed among the 100 most invasive species in private properties. To enable people to collect scientif- Europe [12]. In the meanwhile it has become one of the cally sound data, we designed a simple protocol. Te most common pest slugs in private gardens, horticulture participants used a cardboard quadrat (20 × 20 cm) and agriculture in central Europe [13–15]. Te Spanish that they randomly placed in their garden. Tis quad- slug feeds on many vegetables and ornamentals as well rat served as an artifcial shelter for slugs during the as dead plant material [16, 17] and can survive low tem- day. No baits where used to attract slugs. Te quadrats peratures and droughts [18, 19]. Under normal circum- were left undisturbed on the same spot for 2 days, after stances, most Spanish slugs die after oviposition at the which the slugs under the quadrats where counted, end of the year [20], but can live up to 3 years if they are photographed and collected. Additionally, data were unable to breed [21]. Tey can adapt to a variety of envi- collected on altitude of the collection site, on the num- ronmental factors and therefore compete with native slug ber of plant species within a radius of 2 m around the species [22]. Te activity of A. vulgaris is strongly corre- quadrat, number of earthworm casts under the quad- lated to humidity [19, 23, 24] and temperature [18, 21]. rat as a measure for earthworm activity [37] and pre- Additionally, the time of day [25, 26] and the availabil- vious and current control methods against molluscs ity of suitable shelters afect slug activity [25, 27]. Some employed in the garden. studies also observed that earthworms [28, 29] or plant In spring 2014 participants used the smartphone app diversity [30] afected the extent of herbivory by slugs. Epicollect and Epicollect+, respectively [38]. Epicollect In many areas, A. vulgaris co-occurs with two similar and Epicollect+ are open source smartphone applica- looking native Arion species (the red slug A. rufus and tions available for Android and iOS for data collection the black slug A. ater). Recent studies have shown that no in the feld. Te collected data were stored in a central clear mating barrier exists between these three species database and can be exported in various formats for fur- and that fertile hybrids occur [31–34]. Tis makes tradi- ther analyses. In our study participants used the apps to tional species identifcation difcult and genetic analyses submit pictures of slugs and data on location, altitude, a useful addition [35, 36]. number of plant species, number of earthworm casts Hence, the goals of the current study was (I) to test a and slug management methods. In 2015 the participants citizen science approach in order to determine the occur- entered the data for the same parameters in a spread- rence and abundance of slugs in particular across gardens sheet (Microsoft Excel) and uploaded it together with the in Austria, (II) to determine any association of slug abun- associated photographs at the university’s online learn- dance with meteorological factors, plant diversity and ing platform based on Moodle (https ://learn .boku.ac.at/). earthworm activity in these gardens, and (III) to investi- Te number of slugs was deduced from the spreadsheet gate the occurrence of the invasive A. vulgaris versus the and the photographs uploaded via app or on the Moo- native A. rufus by using DNA sequencing. dle platform, respectively, in the year 2015. In 2014 slugs were collected by the participants and preserved in 80% Methods ethanol for further inspection by us. Slug numbers were Study area and data collection then obtained by counting of the preserved slugs. All data Tis study focused on private gardens across Austria. were validated using the photographs the participants Tese gardens were distributed across all Austrian fed- sent or the slug samples, respectively. Inconsistent or eral states, but most of them were located in the highly incomplete data sets were discarded and not included in urbanized regions of Vienna and the greater Vienna further analyses. area. Although the study covers a broad range of geo- In addition, we procured data on weather conditions graphical conditions, there is more weight to the land- from the nearest weather stations from each location scapes of the Vienna region: hilly terrains and fatlands of the year before the collection and the collection year with meadows, forests and cultivated areas. We chose from Austrian Federal meteorological and geophysical a citizen science approach to independently assess the data provider (Zentralanstalt für Meteorologie und Geo- abundance and occurrence of slugs in Austrian gardens dynamik ZAMG). From these data we extracted various in the spring seasons 2014 and 2015. In 2014 the assess- measures for vapour pressure (hPa), air temperature (°C), relative air humidity (%), precipitation (mm) and global ment took place from the 2nd of April to the 12th of 2 June, in 2015 from the 3rd of April to the 15th of May.
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