Invasive alien species (IAS) are causing a multitude of negative effects on both natural and agricultural ecosystems, leading to serious economic losses and adverse environmental impacts (Simberloff et al. 2013). A recent case of IAS is the Brown Marmorated Stink Bug (BMSB) Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) (Online Resource 3), an extremely polyphagous pest of many agricultural crops. BMSB is also known as a dwelling nuisance because of its massive overwintering aggregations inside buildings (Hoebeke and Carter 2003). Native to Asia, BMSB arrived in North America in the mid- to late 1990s (Hoebeke and Carter 2003) and spread rapidly, causing millions of dollars of losses in fruit orchards. Its management consisting of season-long repeated insecticide treatments has disrupted previous IPM programs (Leskey et al. 2012a). In Europe, the first appearance occurred in Switzerland in 2004, followed by Liechtenstein, Germany, France, Hungary and Greece (Haye et al. 2015). In Italy the first BMSB specimen was captured in 2012 in the province of Modena (Emilia Romagna Region, Northern Italy), where an increasing problem with deformed pears (5–37 % damage at harvest) was initially attributed to mirid species (Heteroptera: Miridae). In northern Switzerland BMSB is univoltine and is mostly a household nuisance, only occasionally damaging vegetable gardens (Haye et al. 2014a). However, in Italy, there is a high concern that BMSB will not be limited to being a dwelling nuisance, because: (a) it was first detected in Emilia Romagna, one of the major European orchards, providing 25 % of the Italian fruit production and exporting fruits for 446 million Euro (Fanfani and Pieri 2012); (b) Emilia Romagna is a strategic, busy crossroads between continental Europe and Centre-Southern Italy; (c) the warmer climatic conditions could support bivoltinism. Together, these factors could favour a fast population increase and facilitate the spread all over the country and beyond, ultimately resulting in a potentially high impact of BMSB on the entire Italian/European agricultural production.

Accurate species identification is crucial to phytosanitary officers, IPM staff and farmers. At the same time, early detection and the ability to rapidly track the spread of IAS are essential to undertake decisions on their management. In the US, a 5 year delay between the likely date of first introduction of BMSB and the date of its correct identification (Hoebeke and Carter 2003) caused a delay in research and management efforts. Thus, the development of easy to use “universal keys” could allow for correct recognition of BMSB among similar stink bugs by non-specialists. Difficulties in tracking the real-time spread of IAS could be overcome with the involvement of many people by means of “citizen science” surveys (Scyphers et al. 2014). Citizen science data, if properly checked and verified by experts, are a potentially valuable source of information on biodiversity and species distribution (Crall et al. 2010).

The aim of this study was to verify the current distribution of BMSB and to obtain data on its phenology, host plants and voltinism, by combining active search and a multimedia citizen science survey.

After the first detection of BMSB in the Province of Modena (Magreta, 13 September 2012), which occurred during an insect collection for educational purposes, we launched an active search campaign in Northern Italy and Southern Switzerland. In the provinces of Modena and Reggio Emilia presence of BMSB was also checked during the weekly monitoring program (May–September 2013) for mirids performed by the local phytosanitary agencies in selected orchards. At the same time, a citizen science survey was initiated by: (a) encouraging the students of the University of Modena and Reggio Emilia (UNIMORE) Entomology classes and the personnel in Canton Ticino schools to actively search for the bug; (b) alerting professional and amateur entomologists/naturalists, using social networks and web forums; (c) alerting the phytosanitary services in Canton Ticino and Lombardy; (d) alerting UNIMORE personnel and general public through the UNIMORE website; (e) alerting farmers and general public through the Emilia Romagna Phytosanitary Service website and its extension magazine; (f) issuing a press-release, published in many newspapers and websites; (g) alerting the local municipalities and sanitary offices by means of extension flyers, published also in the respective websites; (h) organizing public conferences. In all cases, the public was invited to collect or take high quality photographs of any brown-grey marmorated bugs and to send them to the authors, together with details on the collection/sighting. All the records were collected in a database indicating: (a) when (date); (b) where (locality and street); (c) context of detection (open field = crops or uncultivated land; rural = isolated country farmhouses; country village = small residential area in the countryside; urban = cities); (d) place of detection (house/building, terrace, urban green, vegetable garden, crop, means of transport); (e) plant species, if the bug was found on plants; (f) how the bug was collected/detected (hand, photo, type of trap or sampling technique); (g) number and instar of the specimens observed/collected; (h) detector name and category (Researcher = investigator in University or other institution; Mus nat = Natural History Museums personnel; Ento/nat = entomologist/naturalist; Phytosan = phytosanitary services personnel; Student = university student; Cit = citizen not belonging to previous categories); (1) additional observations if any. This work refers to data collected up to November 17, 2013.

As BMSB adults can be confused with similar European pentatomids, e.g. Rhaphigaster nebulosa Poda, Troilus luridus Fabricius, and Arma custos Fabricius, the records were validated by the authors as positive if H. halys was recognized when examining dead/alive specimens and/or digital pictures. Records were considered negative when related to other species or to cases where BMSB was actively searched for but never detected in the considered period. The positive records were categorized, obtaining the percentages of occurrence of BMSB according to: (a) the presence in different regions, in relation to the known bug biology (January–April = overwintering period, May–June = emergence from recovery sites and spread to host plants, July–August = reproductive period, September–November = movement to overwintering sites); (b) the presence in different contexts and places, for each region; (c) the size of the record (total number of individuals detected/record); (d) the method of detection and the category of the survey participants.

Halyomorpha halys is currently one of the most invasive pests in the world and due to international trade and favourable biological features, its spread appears uncontrollable. The first detection of BMSB in Italy elicited a serious concern, as it occurred in Emilia Romagna, a region of primary importance in Europe for fruit and wine production (Fig. 3) (Fanfani and Pieri 2012). The timely activation of an investigation combining active search, performed by experts and purposely trained people (university students, entomologists and naturalists, phytosanitary services personnel) and the citizen science survey resulted in the first distribution map (Fig. 1) of BMSB and provided information on its biology in the newly invaded areas. Our survey consisted of 377 records collected between September 2012 and November 2013 in Northern Italy (87 % of all records), in Canton Ticino (10 %) and in Central and Southern Italy (3 %). A total of 200 records were positively validated as H. halys. The 177 negative records were misidentified native pentatomids, mainly R. nebulosa (15 % of negative records), and/or failure to detect BMSB during active search.

Fig. 1
figure 1

Map of Northern Italy and Southern Switzerland representing the distribution of Halyomorpha halys according to our survey (dots). Dot colours represent the size of each record (number of specimens detected). Coloured dots positive records; white dots negative records, represented by cases of detection of pentatomids other than H. halys or by cases where BMSB was actively searched but never detected in the considered period

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Halyomorpha halys can be easily confused with similar pentatomids in different parts of the world. In Europe, mottled brown-greyish stink bugs resembling BMSB include other phytophagous species, as well as predators of eggs and juvenile instars of plant pests, which are both potentially useful biological control agents. A correct recognition of the species and knowledge of their bio-ecology, are therefore crucial. Thus, we developed a photo-based identification key that allows for an accurate, quick recognition of H. halys adult and immature instars among pentatomids from all over the world (Online Resources 1, 2, 3), by means of a simplified dichotomy.

This study took advantage of the voluntary collaboration by many stakeholders who understood the potential threat of this introduced bug for Italian/European agriculture. Students were the major contributors to this survey (about 1/3 of records), followed by citizens (22 %), researchers (20 %), entomologists/naturalists (17 %), personnel of plant protection services (6 %) and museum personnel (2 %). Other phytosanitary relevant IAS similarly detected in Europe were Leptoglossus occidentalis (Hemiptera: Coreidae) (Taylor et al. 2001) and Aromia bungii (Coleoptera: Cerambycidae) (Burmeister et al. 2012). Our findings confirm that, when verified by competent taxonomy specialists, insect collection performed for educational purposes and/or by entomology amateurs can be crucial for the detection of allochthonous insects. Indeed, an increasing number of aliens are reported in dedicated web forums. We are aware that citizen science data are not reliable in yielding estimates of species distribution (Van Strien et al. 2013), since they are collected without a standardized protocol and explicit sampling design. However, these data are extremely useful for early detection of invasive pests and in tracking their spread in the initial introduction stages.

Our data are not necessarily exhaustive and possibly represent only a partial picture of the actual distribution of H. halys in Italy and Southern Switzerland. The compiled map (Fig. 1) shows three conspicuous apparently isolated nuclei. The most relevant, in terms of number and consistency of records, is centred in the province of Modena (Emilia Romagna, ER) (Online resource 5); the second is the area between Milan (Lombardy, LOM) and Bellinzona (Canton Ticino, TIC); the third is in Piedmont (PIE), where it was recorded also by Pansa et al. (2013). BMSB was detected mostly along main roads and/or railway lines like, in ER, the highway/railway connecting Centre-South Italy with continental Europe, and, in LOM, the lines connecting Italy to Switzerland, where BMSB has been established for 10 years (Haye et al. 2015). The possibility that H. halys colonization is facilitated by “hitchhiking” was directly verified in our study by detecting it inside cars and in train stations (Table 1). A strong association with urban development and railroads occurred also in the initial establishment and dispersal of BMSB in the US (Wallner et al. 2014).

Table 1 Number of records of Halyomorpha halys detected for each context, in each region (ER Emilia Romagna, LOM lombardy, TIC Ticino), according to the place of detection
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The likelihood that the population in the LOM-TIC nucleus derives, at least in part, from the Swiss one, is confirmed by the genetic analysis of specimens collected during this survey (Cesari et al. 2015). Considering the actual presence of monovoltine BMSB population in central Europe, (Haye et al. 2014a), our records and the records from Greece represent (Milonas and Partsinevelos 2014), one of the most southern points of the distribution range for the European continent.

The number and size of our records (Fig. 1; Online resource 5) indicate established breeding populations of low-moderate population levels in the described areas. Combining the data on occurrence relative to season (Fig. 2) with the occurrence related to the context, region and place of detection (Table 1) and the biological observations on individuals reared in semi-field conditions, it is possible to summarize the phenology of H. halys in the investigated areas. During autumn the bugs aggregate inside buildings to overwinter; in April–May they disperse onto host plants and mate until August, developing through two annual generations; immature individuals are detected until mid October. These findings are in agreement with the described biology of the species in the warmer US states (Leskey et al. 2012b). In our study BMSB was mainly detected in urban and country village settings (Table 1; Online resource 5) and most of the records occurred in autumn (with cases of hundreds of individuals: red dots, Fig. 1; Online resource 5) in buildings facing green areas, indicating proximity between host plants and the shelters chosen to overwinter. In urban settings the bugs were frequently found on balcony plants, especially on the highest floors (even the 10th floor). These observations indicate that: (a) autumn is the most favourable period to collect data on BMSB presence, because adult bugs are easily noticed inside buildings in any setting, (b) even the smallest green area in a city can host BMSB; (c) these bugs, already known to prefer the higher parts of plants (Leskey et al. 2012b), are able to fly higher than 25 m. These findings should be taken into account when designing a detection campaign for H. halys presence and the association with a citizen science survey could save time and energy.

Fig. 2
figure 2

Number of Halyomorpha halys records detected in the different regions, according to the bug biology

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Considering the 33 recorded plant species on which BMSB was detected, (Online Resource 4), 7 are new, compared to available literature (Lee et al. 2013; USDA-NIFA SCRI 2016; Haye et al. 2015), further increasing the host range of this extremely polyphagous bug. New hosts include ornamentals (Ageratum houstonianum vs. nana, Myosotis sp., Calycanthus sp., Broussonetia papyrifera) and 3 species typically grown in vegetable gardens (Ocimum basilicum, Thymus sp., Capsicum chinense). Also, we report the first European case of an open field crop infestation by BMSB. This infestation occurred in mid October 2013 on soybean in Canton Ticino (Switzerland), where despite an estimated presence of 500 individuals/ha, no significant yield loss was reported. In addition, BMSB was occasionally detected in ER in vineyards at harvest and in pear/peach orchards during monitoring for other pests, and in PIE on nectarines after last harvest (Pansa et al. 2013). The detection of BMSB in field crops without a specific monitoring program is alarming, especially taking into account that 35 % of the total positive records occurred in the countryside villages surrounded by high value orchards and vineyards in a region of great agricultural relevance such as ER (Fig. 3). BMSB was never detected during the field monitoring program for mirids in 2013, but this is misleading, as BMSB is a typically arboreal species, easier to catch using tree-beating rather than sweep nets as are used for mirid sampling (Nielsen and Hamilton 2009).

Fig. 3
figure 3

Map of Emilia Romagna region (Northern Italy) representing the detection sites of Halyomorpha halys (red dots) and, in brownish green, the distribution and amount (in hectares) of the cultivated crops mostly threatened by this alien species (fruit orchards and grapevine)

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The likelihood that H. halys could become a crop pest in Europe, as well as in the US, depends on factors such as voltinism, type and range of host plants, biotic potential and possibility to overcome geographical barriers. According to the pest risk assessment performed for France (Haye et al. 2014b), the risk of invasion with negative impact on crops is high. Our findings indicate that south of the Alps, BMSB has established breeding populations that can rapidly spread due to bivoltinism, passive transportation and an increased host range. Thus there is a concrete risk that it could become a serious agricultural pest in Southern Europe and along the Mediterranean basin. In Italy, the results of this study led to the development of a specific field monitoring program for H. halys that is currently being performed in ER and other regions, together with a detailed study on the biology and the potential of native antagonists. The citizen science survey is still active, producing real-time data on BMSB spread and acting as an alert system for other regions. The methods used for this survey could serve as a functional example for other introduced species. Moreover, the obtained information and the provided identification keys can be used to spot and track the spread of the invasive pest H. halys all over the world.