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Bulletin of Insectology 65 (1): 9-16, 2012
ISSN 1721-8861
Evaluation of flight phenology and number of
generations of the four-spotted sap beetle,
Glischrochilus quadrisignatus in Europe
Sándor KESZTHELYI
Department of Botany and Plant Production, University of Kaposvár FAS, Hungary
Abstract
The study aimed to acquire the widest possible information on the flight phenology and European distribution of the four-spotted
sap beetle, Glischrochilus quadrisignatus (Say) (Coleoptera Nitidulidae). The field investigations were made in 2009 and 2010 in
the outskirts of Csurgó (Somogy county) in Hungary. Glass traps filled with broken maize grain were placed in the maize fields in
order to follow the course of flight. Besides, the number of generations was determined in Europe by accumulated day-degrees,
using threshold temperature available from literature. The results showed the presence of two-generations of G. quadrisignatus in
Hungary. In the experimental plot the second generation proved to be larger. The meteorological elements significantly influenced
the possibility of trapping, but the effect of annual precipitation on the flight phenology was the most decisive. The numerous
trapped individuals in monoculture maize can be explained by its overwintering site. According to the results and to the biblio-
graphic sources the range of this nitidulid presence has extended to many countries in Central Europe, the Balkans and Italy. The
distribution of this species reaches more geographic regions in Europe where one, two and three generations per year may de-
velop.
Key words: four-spotted sap beetle, Glischrochilus quadrisignatus, flight phenology, European generation number.
Introduction
The four-spotted sap beetle, Glischrochilus quadrisig-
natus (Say) is a native species in North and Central
America. Its endemic distribution area is Nearctic and
Neotropic regions of American Continent (Parsons,
1943). Its European invasion began with introductions
via transports of fruits and vegetables for American
army in Europe at the end of World War II. The first
dated confirmation of its presence in Germany was from
1948 (Karnkowski, 2001). Since then the range of its
invasion has extended to other countries of Central and
North Europe, Balkan Peninsula, Apennine Peninsula
and western Russia (Audisio, 1985; Kałmuk et al.,
2008).
Table 1 shows the list of findings of G. quadrisignatus
in Europe. Publications have originated from twenty
countries since the first appearance of the beetle in
Europe (1948) (figure 1). According to the data exam-
ined, the spreading of this invasive species has been
continuous since the second part of the twentieth cen-
tury. Its first invasion extended to the whole territory of
Germany and the Czech Republic (Jelinek, 1984), later
it appeared in Poland (Kałmuk et al., 2008), Hungary
(Audisio, 1980) the Netherlands (Brakman, 1966) and
France (Callot, 2008), then its southward expansion be-
gan at the beginning of the decades preceding the mil-
lennium. So its presence was first confirmed in Serbia in
1983 (Balarin, 1984), in Italy in 1985 and in Moldavia
in 1990 (EPPO, 1994). Due to its good adaptation and
quick spreading, its southward expansion is a phenome-
non of the present decades and the near future.
The G. quadrisignatus is an invasive, polyphagous
saprophage and herbivore of high environmental toler-
ance, which can be appeared both in agri- and horticul-
tural biocoenoses (Šefrová and Laštuvka, 2005). This
insect generally feeds on fruits and other plant parts that
are ripening or decomposing. Its host range may include
tree and small fruits such as peaches, blueberries, rasp-
berries and strawberries, melons, field- and sweet
maize, stored maize and dried fruit products (Audisio,
1980; Bourchier, 1986; Davidson and Lyon, 1979).
G. quadrisignatus has been observed feeding on the
silk and pollen of undamaged maize. It also invades
fields with maize stalks damaged by the European corn
borer (McCoy and Brindley, 1961). It is a secondary, so
called “scavenger” invader in fields where ears are
damaged by other pests. G. quadrisignatus is also asso-
ciated with Fusarium species of maize roots, stalks, and
ears (Windels et al., 1976), and is capable of transmit-
ting conidia and ascospores of Gibberella zea (the
perithelial state of Fusarium graminearum) causing rot
to ears (Attwater and Busch, 1983). Besides, it can ap-
pear as an important maize pest too, where the damage
ratio can reach 30 % in maize acreage (Dowd, 2005;
Foot, 1975; Funt et al., 2004; Westgate and Hazzard,
2005). In North America it can be a serious pest of rip-
ening fruit and vegetables and a nuisance to picnic areas
(Ikin et al., 1999).
G. quadrisignatus develops several generations as a
function of its distribution area (Luckmann, 1963). So it
may have one (Funt et al., 2004), two and even more
generations per year. In the tropics, multiple generations
may occur especially if there is enough food available
throughout the year (Dowd and Nelson, 1994). The
threshold temperature for the development of pest is
10.5 °C (Luckmann, 1963) and its accumulated day-
degrees for the entire development (egg to adult) is
535.9 DD (Mussen and Chiang, 1974). G. quadrisigna-
tus overwinters as an adult and becomes active on warm
10
Table 1. List of the G. quadrisignatus bibliographical sources in Europe (in order of publication date).
Country Sources
Austria (A) Kofler et al., 1989; Kofler and Schmölzer, 2000; Köppl, 2003; Wieser et al., 2004;
Ressl, 2005; Wittenberg et al., 2005; Frauenschuh and Kromp, 2009
Bosnia and Herzegovina (BIH) Balarin, 1984; Audisio, 1985; Kałmuk et al., 2008
Bulgaria (BG) Audisio, 1985; Kałmuk et al., 2008
Byelorussia (BY) Tsinkevich et al., 2005; Alekseev and Nikitsky, 2008
Croatia (HR) Balarin, 1984; Audisio, 1985; Merkl, 1998; Kałmuk et al., 2008
Czech Republic (CZ) Jelinek, 1984, 1997; Sefrova and Lastuvka, 2005
France (F) Brua and Callot 2010; Callot 2008
Germany (D) Adeli, 1963; Lienemann et al., 2003; Kałmuk et al., 2008; Müller et al., 2008
Hungary (H) Audisio, 1980; Rakk et al., 1992; Slipinski and Merkl, 1993; Merkl, 1998, 2001;
Horváth et al., 2004; Merkl and Vig, 2009; Vig et al., 2010
Italy (I) Audisio, 1985; 1990; 1993; Ciampolini et al., 1994; EPPO, 1994; Angelini et al.,
1995; Audisio and De Biase, 2005; Audisio et al., 1990
Lithuania (LT) Tsinkevich et al., 2005; Ferenca et al., 2006; Alekseev and Nikitsky, 2008; Fossestol
and Sverdrup-Thygesonb, 2009
Moldavia (MD) EPPO, 1994; Kałmuk et al., 2008
Poland (PL) Lasoń, 1999; Karnkowski, 2001; Błochowiak, 2004; Boroń and Mrówczyński, 2005;
Przewoźny, 2007; Ruta, 2007; Beres and Pruszynski, 2008; Kałmuk et al., 2008
Romania (RO) EPPO, 1994; Kałmuk et al., 2008; Merkl, 2008
Russia (RUS) Koval, 1987; Kyrejshuk, 1999; Alekseev and Nikitsky, 2008
Serbia (SRB) Balarin, 1984; Audisio, 1985; Glavendekic et al., 2005; Kałmuk et al., 2008
Slovakia (SK) Jelinek, 1984; Kałmuk et al., 2008
Slovenia (SLO) Balarin, 1984; Kałmuk et al., 2008
Switzerland (CH) Wittenberg et al., 2005
The Netherlands (NL) Brakman, 1966; Cuppen and Oude, 1996; Oude, 1999; Reemer, 2003; Oude, 2005;
Cuppen and Drost, 2007
Ukraine (UA) Audisio, 1985; Kałmuk et al., 2008
Figure 1. One of the theoretical spreadings of G. quadrisignatus in Europe (based on Kałmuk et al., 2008).
11
days in late winter or early spring. Most eggs are depos-
ited in May. Females can oviposit up to 400 eggs in
their lifetime. To be suitable for oviposition and larval
development, food material must either be buried in the
soil or be in contact with the soil and must be moist. Ac-
tive adults of the new generation begin leaving the soil
in June. They fly to fields of ripening or damaged ber-
ries, tree wounds and maize. Adults live long time (40-
60 days) and late in June various life stages including
both the new and overwintering generation can be found
together in the soil (Blackmer and Phelan, 1995). Food
source has a significant effect on the development time
of G. quadrisignatus from neonate larvae to adult, with
the shortest mean development time of 41.2 days on
multiple-species rearing diet and the longest mean of
63.4 days on sap beetle diet (Peng and Williams, 1991).
The objective of this study was to know more accu-
rately the flight phenology of the G. quadrisignatus
adults in Hungary and to predict the number of genera-
tions in Europe based on a degree-day model. The re-
sults may also indicate the optimal timing of chemical
control.
Materials and methods
Comprehensive experiments were carried out on the
population number and flight dynamics of G. quadrisig-
natus on the basis of catching data. The places of trap-
ping were in maize fields at Csurgó (Hungary, Somogy
county: 17°5'47"E, 46°15'18"N): 22.3 ha in 2009, and
18.6 ha in 2010. In the experimental fields maize was
grown both in rotation and in monoculture in these
years. After the harvest of the previous year’s sun-
flower, PR37Y12® (FAO 390), maize hybrids were
sown in the fields. Soil disinfection (Force 1.5G®; 14
kg/ha) to control western corn rootworm (Diabrotica
virgifera virgifera LeConte) was carried out in maize
monoculture both in 2009 and 2010. Insecticides were
not applied either in the fields with maize grown in rota-
tion, or during the growing season when different crop-
ping techniques were used.
To determine the G. quadrisignatus yearly appearance
and the flight phenology in Hungary the so called „glass
traps” were used during the growing season of maize in
two years (2009: 9th March - 4th October; 2010: 8th
March - 3rd October). The same numbers of traps were
placed out with both cultivation techniques. The traps
were fixed to stakes at a height of 140-150 cm, then
when the plants reached the right size the traps were
placed above the ear at the same height (figure 2). The
attractant was an alcoholic fermented broken maize
grain, which was replaced weekly. The number of
caught beetles was assessed every week.
The values of abiotic environmental factors (soil and
air temperature, precipitation) were obtained from
March to October for the area concerned at Csurgó
(Monsanto® online website: www.dekalbmet.hu).
Student t-test (P ≤ 0.05) was applied to ascertain the
significant differences among dates and cultivation
practices. The effects of abiotic factors on the trapped
individuals were statistically examined with the regres-
sion and correlation analyses. Statistical examinations
were performed by means of Microsoft Excel 2007 and
SPSS 11.5 for Windows.
In addition to the flight observation, and based on the
European distribution provided by Kałmuk et al. (2008),
the yearly generation number (G) was calculated at dif-
ferent points using the threshold temperature for the de-
velopment (t0 = 10.5 °C) (Luckmann, 1963) and the ac-
cumulated day-degrees (C = 535.9 DD) (Mussen and
Chiang, 1974). The cumulated temperature amount in
the growing season was calculated as [T = Σn × (taver. − t0);
where: Σn = number of days in growing season, taver. =
daily average temperature]. For the calculations of gen-
eration numbers, adults appearance in early April was
taken into consideration after a short maturation feeding
and copulation period (10 days). This calculation based
on the growing season (from 15 April to 30 November)
uniformly, independently of examined areas and times.
G = [Σn × (taver. − t0)]/C
The international temperature data originated from the
online meteorological website, Wounder Underground®
(www.weatherground.com). Besides these, the appear-
ance of this species in Hungary was analysed by using
the average winter and summer temperatures of the last
107 years (from the beginning of the twentieth century
to 2007). These meteorological data were taken from
the publication of the Hungarian Meteorological Service
(Bihari et al., 2008).
Figure 2. The applied glass trap, and the location of these prognostic gears in maize acreage in 2009, 2010.
12
Results
The catching results of the glass traps observed at
Csurgó in 2009 and 2010 can be seen in figures 3 and 4.
The meteorological values are shown together with the
captures.
The flight phenology was more or less similar in the
two years studied. The appearance of the first beetle co-
incided with an increase in soil temperature in the mid-
dle of spring. The appearance of overwintered beetles
and the beginning of their flight can be noticed when the
soil temperature is about 10-11 °C. The flight activity
was gradually intensified by the increasing daily tem-
perature. Warmer, arid periods in the growing season
provide possibility for a more extended flight. The sepa-
ration of two generations is conspicuous in both years.
The escalating of the later generations, the increasing
number of trapped beetles from the middle of summer
and the dominant later flight peaks can be observed in
the phenology diagrams.
The flight periods were a little dissimilar, which can
unequivocally originate from the different climatic fea-
tures. The abundant precipitation especially influenced
and decreased the number of trapped insects in 2010.
The first beetle was trapped on 18th April and the last
one on 4th October in 2009. So the period of flight was
especially long, exactly 170 days. The first beetle was
trapped on 12th April and the last one on 12th September
in 2010. So the period of flight was only 154 days in
that year. The time of appearance for the different gen-
erations was calculated by taking into considerations the
beetles maturation feeding time and the 10 days copula-
tion period. Based on these facts it is confirmed that the
first generation appeared on 6th July in 2009, and on 30th
June in 2010, while the second generation on 25th Au-
gust in 2009 and on 18th August in 2010.
A higher number of trapped individuals can be ob-
served exceptionally well in the case of maize monocul-
ture. The Student-t value (t = 0.012) for the numbers of
trapped individuals was significant in different cultiva-
tion practices.
The tested data to regression and correlation analyses
showed normal distribution. The statistical examination
confirmed a positive linear correlation in the case of the
number of trapped individuals and the average tempera-
tures (p = 0.044; r = 0.363), and a negative linear corre-
lation between the trapped individuals and the precipita-
tion values (p = 0.011; r = −0.450). Besides, this exami-
nation confirms the dominant effect of precipitation, be-
cause this factor influenced the trapped population
number by 20.3% (R2 = 0.203), in contrast to the 13.2%
(R2 = 0.132), value of the effect of temperature.
The number of predicted generations in Europe is
shown in figure 5. G. quadrisignatus presence covers
more geographic regions. The one- (Lithuania, Nether-
land, Germany, France, Czech Republic, Poland, Swit-
zerland, Austria) and two-generation (Belorussia,
Ukraine, Slovakia, Hungary, Romania, Moldavia, Ser-
bia, Bosnia and Herzegovina, in northern parts of Croa-
tia, Slovenia, Bulgaria and Italy) populations are located
in the largest area in Europe, while the three-generation
populations only in a relatively smaller area (in southern
parts of Croatia, Slovenia, Bulgaria and Italy), on the
southern border of the habitat.
Figure 3. Flight diagram of G. quadrisignatus at Csurgó (Somogy county, Hungary) in 2009 correlate with abiotic
factors. The average temperature and the aggregated precipitation were indicated on the vertical axis of Walter-
Lieth climatediagram (1:3) according to weather of Central-Europe.
13
Figure 4. Flight diagram of G. quadrisignatus at Csurgó (Somogy county, Hungary) in 2010 correlate with abiotic
factors. The average temperature and the aggregated precipitation were indicated on the vertical axis of Walter-
Lieth climatediagram (1:3) according to weather of Central-Europe.
Figure 5. Distribution area of G. quadrisignatus in Europe, and the calculated borderline of its different generation
number populations in 2010. Decimal numbers indicate the theoretical generation numbers. Natural integers show
the numbers of the entire developing cycle (from egg to adult).
14
Discussion
The temperature of the growing season has profound
effects on generation number of G. quadrisignatus, but
the amount and distribution of precipitation principally
influence the flight phenology of this insect. As seen
from the figures changes in the population number of G.
quadrisignatus were proportionately followed by a
change in the values of meteorological data in both
years.
The numerous trapped individuals in maize monocul-
ture can be explained with its overwintering site, be-
cause the maize ears found in the soil as G. quadrisig-
natus food can give shelter to the overwintering adults
(Blackmer and Phelan, 1995; Luckmann, 1963). So its
overwintering is more successful.
This insect develops different generation numbers in
its distribution area, with a maximum of three at pre-
sent. Naturally, the borderlines between number of gen-
erations may change depending on the climatic effects
of different years.
In all probability the maximum European northward
expansion is as far as 66-68°N latitude in view of the
thermal requirement of the species. G. quadrisignatus
gradual southward distribution can be forecasted from
its rapid spreading, where four-generation populations
may appear in the future.
In addition, any warming period may quickly and sub-
stantially increase the number of generations as well as
the arrival of adventive, thermophilic insect species
(Kozár, 1997). Hereinafter the global warming could
provide perfect conditions to the European expansion of
this species. Most adventive species originating from
America settled in Southern Europe (e.g. D. virgifera
virgifera), and their northward expansion is continuous
as a function of the yearly average temperature. In con-
trast, G. quadrisignatus appearing in Northern Europe
can be presupposed to have a rapid, quick expansion in
the southern, warmer areas in Europe after the relatively
slower initial spread. Its spreading can be delayed by
relief barriers such as the mountain chains of the Alps,
the Carpathians or Dinarides. In addition, because of the
absence of their natural enemies, the new invader in-
sects can cause serious problems in agriculture through
long term outbreaks.
Acknowledgements
I am indebted to Prof. Ferenc Kozár, research adviser of
Hungarian Plant Protection Institute for useful guidance
in connection with insect ecology.
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Author’s address: Sándor KESZTHELYI (corresponding au-
thor, ostrinia@gmail.com), Department of Botany and Plant
Production, Faculty of Animal Sciences, University of Kapos-
vár, Guba S. str. 40, H-7400 Kaposvár, Hungary.
Received July 1, 2011. Accepted November 21, 2011.
