Nezara viridula ( L .) 361
the overwintering conditions for the species and enhances its survival. This, in turn, allows invaders to
reproduce in the spring, have the advantage of reproducing in early-season on early agricultural crops,
and to become established in newly colonized areas (Musolin 2012).
7.3.2 Europe
The earliest record of Nezara viridula within Europe apparently is the description of Cimex smaragdulus
by Fabricius (1775) from the Macaronesian island of Madeira. The species subsequently was mentioned
in most of the southern European countries with the first continental record from southern France by
Villers (1789). The global distribution map suggested by DeWitt and Godfrey (1972) drew the north-
ern limit of occurrence in Europe along southern France, northern Italy (south of the Alps), Slovenia,
southern Hungary, and along the north coast of the Black Sea, which generally coincides with the
Mediterranean climate or biogeographic region, particularly in the eastern European realm. However,
according to these records, it is suggested that records north of the Alps at the approximate latitude of
46°N should be considered recent immigrations (Rabitsch 2008).
The reasons for the current northward expansion in Europe are unclear. Climate change favors popu-
lation growth via shortened developmental cycle and extended environmentally favorable period in the
summer. These latter factors result in higher population density and increased numbers of annual genera-
tions but also reduced winter mortality due to milder winters (e.g., Musolin and Numata 2003b; Musolin
2007, 2012). A similar pattern was demonstrated for Japan (Yukawa et al. 2007, Tougou et al. 2009). The
suggested threshold for overwintering survival is approximately 5°C mean air temperature of the coldest
winter month, 26 cold days during January and February with daily mean temperature below 5°C, and
mean annual lowest temperature below –3°C (see the case study in Section 7. 3.1. 2), however, this sur-
vival threshold falls short in most western and central European climates. The average January air tem-
perature in Budapest is ≈–1°C, but, nevertheless, the species has become established. The “heat island”
effect within cities and urban habitats may play a crucial role in the establishment process of Nezara
viridula in large parts of Europe and elsewhere (Tougou et al. 2009). It further has to be demonstrated
that populations can survive winters and be sustained for longer periods of time.
Besides active dispersal, the role of passive, short-distance, human-assisted translocations within a
(more or less) contiguous continent without border inspections for goods, particularly plants for transplant-
ing (e.g., greenhouse and ornamentals) or human consumption (e.g., field crops, vegetables, and fruits),
and any other transport vehicles may be equally relevant for the northward expansion. Nezara viridula
regularly is intercepted by plant inspection authorities on a wide range of imported plants and products
of different origin (Reid 2005, Malumphy and Reid 2007). The isolated records in Great Britain can only
be explained from such an independent translocation event from continental Europe or from elsewhere.
7.3.2.1 The Invasion History in Europe
Assuming that records from regions with a Mediterranean climate in southern Europe fall within the
native range of Nezara viridula, the first documented findings outside this area were during the 1920s
from Germany, the 1930s from Great Britain, and the 1950–1960s from Belgium, the European part
of Russia (Crimea), Finland, and Austria, with subsequent, but scattered records in Bulgaria, Hungary,
Switzerland, Romania, Slovakia, and the Netherlands (Table 7.1). Apparently, at least some of these
occurrences did not lead to the immediate establishment of permanent reproducing and overwintering
populations. Some time lag (i.e., the delay between first introduction and establishment in the field) is a
well-known feature of the biological invasion process (e.g., Crooks 2005). The status in Finland, Austria,
Romania, Slovakia, and the Netherlands needs to be monitored further. Most recently, observations of
nymphs have been made in Austria and the Netherlands in house gardens and glass houses, which indi-
cate at least temporarily reproducing populations (Aukema 2016, Rabitsch 2016).
The leading edge distribution range dynamics of Nezara viridula in the eastern European realm are
difficult to disentangle. According to DeWitt and Godfrey (1972), all of Bulgaria and southern Romania
falls within the native range. The first mention for southern Bulgaria was by Strawinski (1959), and we
here consider this geographical area as part of this bug’s native range. However, N. viridula has been