J Insect Behav (2013) 26:120129

DOI 10.1007/s10905-012-9346-4

Long-Distance Wind-Borne Dispersal of Sitodiplosis mosellana

Ghin (Diptera:Cecidomyiidae) in Northern China

Jin Miao & Yu-Qing Wu & Zhong-Jun Gong &

Yun-Zhuan He & Yun Duan & Yue-Li Jiang

Revised: 13 June 2012 / Accepted: 15 June 2012 /

Published online: 27 June 2012
# Springer Science+Business Media, LLC 2012

Abstract Surveys based on the density of the adult wheat midge, Sitodiplosis
mosellana (Ghin) (Diptera: Cecidomyiidae), were conducted at ground level and
at heights between 10 and 75 m in Xushui county (39.02 N, 115.65 E), Hebei
province, China, in 2011. The HYSPLIT-4 model was used to analyze the possible
dispersion trajectories and distances of S. mosellana depending on the experimental
location. The wheat midges were trapped at altitudes from 10 to 75 m a.g.l.
strongly suggest that they might also be present at much higher altitudes,
where potentially, they could take advantage of the fast moving air currents.
6-h backward-trajectories indicate that adult S. mosellana could have come from
both north and south, and the trajectory distances were 25107 Km. 6-h forward-
trajectories indicate that adults most likely migrated to an area located in Tianjin,
Beijing and northern Hebei province, north china, and the trajectory distances were
28195 Km. In this study, no male midges were captured at 10 m or above, which
suggest male midges dont engage in wind borne long distance migration, suggesting
S. mosellana mated before dispersal. The information presented here is helpful to alter
the way we view their migration over limited distances and add to our ability in
outbreak forecasts.

Keywords Sitodiplosis mosellana . wind-borne dispersal . Northern China .

HYSPLIT-4 model . dispersal trajectory

J. Miao : Y.-Q. Wu (*) : Z.-J. Gong : Y. Duan : Y.-L. Jiang

Institute of Plant Protection, Henan Academy of Agricultural Sciences, Zhengzhou 450002,
Peoples Republic of China
e-mail: yuqingwu36@hotmail.com
J. Miao
e-mail: miaojin1977@hotmail.com

Y.-Z. He
College of Plant Protection, Agricultural University of Hebei, Baoding 071001,
Peoples Republic of China
J Insect Behav (2013) 26:120129 121

Introduction

The wheat midge, Sitodiplosis mosellana (Ghin) (Diptera: Cecidomyiidae), is a

chronic wheat (Triticum spp.) pest and is prevalent in Europe, Asia, and North
America (Berzonsky et al. 2003). Currently, financial losses due to grain damage
by this pest exceed several hundredmillion euros worldwide and are more substan-
tial in the years that the pest has thrived (Doane and Olfert 2008; Oakley 2008). In
northern China, two major outbreaks of the wheat midge were recorded in the 1950s
and 1980s, causing an estimated loss of 1000 million Kg per year (Ni and Ding
1994). From 2000 onward, S. mosellana populations have spread further to the east
and north each year in China due to changes in weather conditions and crop
distribution (Wu et al. 2009).
S. mosellana is a cereal specialist, for which wheat is an attractive crop for
oviposition, yet in the absence of a wheat crop at certain growth stages, S.
mosellana either fly to other crops such as rye, triticale, or barley, or complete their
life cycle in weed grasses (Birkett et al. 2004). Female S. mosellana oviposit on
the surface of an inflorescence, commonly referred to as a head, ear, or spike, and the
larvae feed on the developing seeds (Mukerji et al. 1988). Wheat will only
become infested with S. mosellana if it is exposed to ovipositing females from the
time that heads emerge from the flag leaves until anthesis, a process that takes place
in about 7 days (Elliott and Mann 1996). Eggs are laid, either singly or in clusters
of three or four on the florets, on the external surface of the glumes or in the
outer grooves of the florets. The egg stage lasts four to 7 days and depends
strongly on environmental conditions such as temperature. Each larva crawls
into a floret and feeds on the kernel surface for 23 weeks. Once moist
conditions are detected, larvae drop to the ground, burrow into the soil, spin
a larval cocoon and overwinter. Adult S. mosellana emerges from the soil (males
emerging earlier than females) in April and May next year. Females live 37 days and
lay an average of 80 eggs. The adult wheat midge is difficult to detect during the day
because it remains within the crop canopy close to ground level where it is most
humid, while females are more active in the evening (Olfert et al. 2009). S. mosellana
adults are relatively poor fliers, so they need wind assistance to travel a long distance
(Olfert et al. 2009).
Long-distance wind-borne movements are common to a wide range of
insect taxa, including nocturnal moths (Drake and Farrow 1988; Gatehouse
1997; Dantart et al. 2009), aphids (Zhu et al. 2006), ground beetles (Feng et al. 2007)
and planthoppers (Shen et al. 2011). S. mosellana adults were captured at 30 m
above ground level in 1965 (Yuan 2004). Once S. mosellana got into high altitudes,
their transit can be treated as an air parcel for various migration models. We
propose that the geographic source of S. mosellana immigrants can be identified
using meteorological models that calculate the trajectory route of an air parcel. The
aim of this paper was to provide an overview of the long-distance wind-borne
dispersal of S. mosellana in northern China. Backward trajectories and forward
trajectories from the experimental point of view were simulated using the HYSPLIT
atmospheric transport model (Draxler, and Rolph 2003).
122 J Insect Behav (2013) 26:120129

Materials and Methods

Sample Investigation

Surveys that look at the population density of adult S. mosellana on the ground and at
higher altitudes were carried out in Xushui county (39.02 N, 115.65 E), Hebei
province. Yellow sticky traps (10 cm12 cm) were used to provide information about
adult midges at ground level. Ten standard yellow sticky traps were placed at 5 m
intervals and traps were positioned just below the ear of grain. Numbers of adult
midges captured on sticky traps were recorded every 2 days from the 2nd of May to
the 20th of May 2011.
The profile of S. mosellana density at different altitudes were analyzed with a
series of kytoon-supported yellow sticky traps (cylinder: diameter 025 cm,
height 060 cm) located vertically at altitudes 10, 20, 30, 40, 45, 50, 55, 60,
65, 70 and 75 m above ground level. Trap catches were recorded twice
(6:00 AM-18:00 PM and 18:00 PM-next 6:00 AM) every day from the 2nd
of May to the 20th May 2011.

Dispersal Simulation

The possible origin of S. mosellana in experimental location was investigated by

assessing backward-in-time air-mass trajectories. A 6-h back trajectory reaching
experimental location was calculated at 00:00 AM local time for each day between
the 2nd of May and the 20th of May 2011. The theoretical dispersion footprint of S.
mosellana based on each experimental location was simulated by a forward disper-
sion module. A 6-h forward trajectories starting at 18:00 PM local time was calcu-
lated for each day between the 14th of May and the 20th of May 2011.
Backward and forward trajectories were run at 75 ma.s.l. using the Hybrid
Single-Particle Lagrangian Integrated Trajectory (HYSPLIT-4) model of the
National Oceanic and Atmospheric Administration (NOAA) (available at
http://www.arl.noaa.gov/ready/hysplit4.html; Draxler and Rolph 2003). Some param-
eters (Table 1) must to be completed for running the model, and the simulations were
based on the meteorological NCEP/NCAR reanalysis data (global coverage from
1948 to present).

Data Analysis

All data obtained from the studies are presented as means SEM. Statistical analyses
were performed in SPSS 10.0 software (SPSS, Chicago, IL, USA). We tested the
effect of sample date on adult S. mosellana density on field location and at heights
between 10 and 75 m with a repeated-measure mixed-model analysis of variance
(ANOVA), with date repeated within location, which was considered a random effect.
We tested the effect of different altitudes on adult S. mosellana density with ANOVA.
If the ANOVA indicated a significant difference, the means responsible for that
difference were identified using a multiple means test.
J Insect Behav (2013) 26:120129 123

Table 1 The parameters of HYSPLIT model

Results

Density of Adult S. mosellana on the Field and at Altitudes

The means of adult S. mosellana captured on sticky traps varies with the sampling
date on the field (Fig. 1; F015.89; df09, 49; P<0.0001). Adult S. mosellana density

14 18
Density at altitude (numbers/trap)

On field
Density on field (numbers/trap)

12 16
At altitude
14
10
12
8 10
6 8
6
4
4
2 2
0 0
2- 4- 6- 8- 10- 12- 14- 16- 18- 20-
May May May May May May May May May May
Date
Fig. 1 Density of adult S. mosellana on field location and at high altitudes in Xushui on 2nd20th May 2011
124 J Insect Behav (2013) 26:120129

increased from a low of 0 insects per trap on the 2nd of May to a seasonal peak of
10.801.24 per trap on the 12th of May. The density remained high for another 5 d
and declined on the 16th of May.
The means of adult S. mosellana captured by kytoon-supported yellow sticky
traps also varied with sampling date at heights between 10 and 75 m (Fig. 1; F0
12.65; df09, 99; P<0.0001). Adult S. mosellana density increased from a low of
0.090.09 per trap on the 2nd of May to a seasonal peak of 13.732.55 per trap on
the 10th of May, while the density declined following this peak.

Density of Adult S. mosellana at Varying Altitudes

The aerial density of adult S. mosellana (number per trap per time) showed no
stratification according to the altitudes measured above ground level (Fig. 2;
F01.04; df010, 417; P00.4147). The density of adult S. mosellana was greatest at a
height of 10 m, followed by 55 m, 20 m and 70 m. Moreover, almost all S. mosellana
adults were trapped at altitude at night (18:00 PM-6:00 AM), very few were trapped
during the day (6:00 AM18:00 PM) (Fig. 2; F08.02; df01, 18; P00.0111).
An interesting result was found that all midges caught at 10 m or above were all
females full of eggs (Fig 3). The males of S. mosellana will not engage in Long-
distance wind-borne dispersal.

Tracing the Sources of S. mosellana in Xushui in 2011

Back trajectories indicate that adult S. mosellana could have come from both north
and south (Fig. 4). The potential area of adult S. mosellana originated located in the
southern Hebei province, north China, on the 3th, 4th, 7th and 10th of May 2011, the
trajectory distances were 61, 53, 65 and 78 Km, respectively. Similarly, adult S.
mosellana probably migrated from the northern Hebei province on the 5th, 6th, 8th
and 9th of May 2011, the trajectory distances were 59,25, 55 and 107 Km,
respectively.
Population density (numbers/trap/time)

9 Night (18:00 PM-6:00 AM)

8 Day (6:00 AM- 18:00 PM)
7
6
5
4
3
2
1
0
10 20 30 40 45 50 55 60 65 70 75
Heights (m)
Fig. 2 Density of adult S. mosellana at altitudes from 10 to 75 m a.g.l. during the day and night in Xushui
on 2nd20th May 2011
J Insect Behav (2013) 26:120129 125

F i g . 3 Adult S. mosellana
females carrying a full compli-
ment of eggs caught by balloon-
supported yellow traps at alti-
tudes from 10 to 75 m a.g.l.

Forward-Trajectories of S. mosellana in Xushui in 2011

The forward trajectories indicates that adults most likely migrated to an area located
in Tianjin, Beijing and northern Hebei province, north china, on the 14th, 15th, 16th,
19th and 20th of May 2011, the trajectory distances were 195, 28, 177, 107 and 90
Km, respectively (Fig. 5). The population of adult S. mosellana also probably
migrated to an area located in the southern Hebei province on the 17th and 18th of
May 2011, the trajectory distances were 62 and 127 Km, respectively (Fig. 5).

F
D
C

E
H B A

Fig. 4 6-h backward-trajectories at 75 ma.s.l. arriving in Xushui, Hebei province at 00:00 AM local time
on the 3rd10th (A-H red lines, respectively) of May 2011. The site which the green ball marked is Xushui,
Hebei province (39.02 N, 115.65 E)
126 J Insect Behav (2013) 26:120129

G
F
B

Fig. 5 6-h forward-trajectories at 75 ma.s.l. from Xushui, Hebei province at 18:00 PM local time on the
14th20th (A-G red lines, respectively) of May 2011. The site which the green ball marked is Xushui,
Hebei province (39.02 N, 115.65 E)

Discussion

S. mosellana is a chronic wheat pest that is widely distributed throughout the world.
The S. mosellana cocoons were supposedly capable of long-distance dispersal
depending on the water current (Yuan 2004). Gao et al. (2009) reported that the
larvae of S. mosellana insects were transmitted due to the cross-operation of com-
bined harvesting. The dispersal power of the adult insects has likely been under-
estimated, due to S. mosellana being a weak flier that rarely flies long distances (Yuan
2004). Only a primary study has been reported about adult S. mosellana probable
long-distance dispersal with air current (Miao et al. 2011).
As to considerations of the weakness of flight by small insects, it has been
demonstrated that it is best to consider weakly flying as a relative term (Bryne
1999). The wheat midges were captured in yellow sticky traps supported by kytoon
at altitudes from 10 to 75 m a.g.l. (Fig. 1). This indicates a rapid ascension for some
individuals, a behavior indicative of active flight. This information strongly suggest
that they might also be present at much higher altitudes, where potentially, they could
take advantage of the fast moving air currents.
Winds at high altitudes tend to move faster than those nearer the ground (Oke
1987), may be in a different direction, and are much more stable, leading to a possible
overestimate of long-range effects. S. mosellana adults are usually sampled at low
altitudes (Yuan 2004). So, the presented trajectories are the absolute upper limits of
what might be expected, and that the majority of individuals probably came from
J Insect Behav (2013) 26:120129 127

much shorter distances. A recent paper showed that similarly-sized Culicoides midges
moved by long-distance nocturnal windborne transport too, but that only 8 % of move-
ments were over 30 km, and the average movement was 1 km (Sedda et al. 2012).
Although some seasonal migrants take advantage of prevailing air currents for
successfully exploiting temporary breeding habitats (Johnson 1995; Pedgley et al.
1995; Chapman et al. 2008), wind-borne transport also implies that it may lead
insects into areas unfavorable for survival or reproduction (the so-called pied Piper
phenomenon: McNell 1987). For example, adult S. mosellana most probably
migrated to Hengshui (127 km) regions in the southern Hebei province on the
17th of May (Fig. 5). However, the host plant in the region was unfavorable for
oviposition in this time.
Physiological management of the migrationreproduction trade-off often includes
a package of adaptations referred to as the oogenesis-flight syndrome, which was
taken for many years as a fundamental trait of insect migrants (Johnson 1969; Lorenz
2007). However, the oogenesis-flight syndrome is not a universal characteristic of
migratory insects (Jervis et al. 2005; Zhao et al. 2009). There were no significant
correlations between the number of chorionated eggs and flight duration, times of
flight initiation and termination, or flight speed in the migratory moth Agrotis ipsilon
(Hufnagel) (Sappington and Showers 1992). In this study, no male midges were
captured at 10 m or above, which suggest male midges dont engage in wind borne
long distance migration, whilst female midges that were trapped were carrying mature
eggs, suggesting S. mosellana mated before dispersal. Pre-dispersal mating may
increase the risk of inbreeding, but dispersal before mating may decrease the risk of
not finding a sexual partner (Dalecky et al. 2006).
In summary, we think long-distance wind-borne dispersal is a potential movement
of S. mosellana population. The information presented here is helpful to alter the way
we view their migration over limited distances and add to our ability in outbreak
forecasts.

Acknowledgments The authors gratefully acknowledge the NOAA Air Resources Laboratory (ARL) for
the provision of the HYSPLIT transport and dispersion model and READY website (http://www. arl.noaa.
gov/ready.html) used in this publication. We thank Mr Sheng-jie Ke and Ms Ya-nan Hao, Xiao-ling Zhi, Ju
Jin for assistance in field work. This work was sponsored by the China Agricultural Research System
(CARS-03).

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