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Ann. appl. Biol. (2004), 145:139-144
Printed in UK

139

Autumn, winter and spring dynamics of aphid Sitobion avenae and parasitoid
Aphidius rhopalosiphi interactions
By M A LEGRAND1*, H COLINET1, P VERNON2 and T HANCE1
1

Unité d’Écologie et de Biogéographie, Biodiversity Research Centre, Université catholique de Louvain,
Croix du sud 4-5, 1348 Louvain-La-Neuve, Belgium
2
Université de Rennes 1, UMR 6553 CNRS, Station Biologique de Paimpont, France
(Accepted 26 February 2004; Received 19 November 2003)
Summary
The potential of parasitoids for aphid control during summer has been well documented. Few results
are available on the impact of parasitoid populations on aphid hosts during autumn and winter and on
the dynamics of their interactions during this period. The population development of Sitobion avenae,
in Belgium, is analysed, from October to April, in the presence and absence of the parasitoid Aphidius
rhopalosiphi. In the presence of parasitoids in winter, aphid populations decreased markedly and
remained low at the beginning of spring. Induction of winter diapause in A. rhopalosiphi was observed
during November at a mean temperature of 6.3°C and a decreasing photoperiod from 9.5-8.5 h of day
light. A large range of A. rhopalosiphi mummy colourations, between dark and light, was noticed. This
range of colouration did not allow a clear-cut distinction between diapausing and non-diapausing
individuals of A. rhopalosiphi. The influence of seasonal weather and particularly temperature conditions
on parasitoid mortality, strategy for overwintering and aphid population dynamics are discussed.
Key words: Sitobion avenae, Aphidius rhopalosiphi, winter survival, diapause induction, mummy
colourations
Introduction

Several authors have analysed the consequence
of low temperatures on the survival of cereal aphids
(Dedryver & Gellé, 1982; Leather, 1993; Hutchinson
& Bale, 1994; Zhou et al., 1995; Butts et al., 1997).
The overwintering strategy of Sitobion avenae
Fabricius (Hemiptera: Aphididae) has been
investigated in an attempt to forecast aphid outbreaks
in summer (Vickerman, 1977; Dewar & Carter,
1984; Walters & Dewar, 1986; Entwistle & Dixon,
1989). Most forecasting systems do not consider the
effects of low temperatures on the survival of natural
enemies such as parasitoids, although such
information might improve their precision.
Both aphid and parasitoid population dynamics
are influenced by winter conditions. For example,
low temperatures are a major factor affecting aphid
development and survival (Walters & Dewar, 1986;
Leather, 1993; Sømme, 1996). Cold is the most
important winter mortality factor for the aphid S.
avenae (Knight et al., 1986). When temperatures are
above the activity threshold of parasitoids, they may
attack overwintering virginoparae and thus their
activity in autumn and winter may reduce aphid
spring density (Powell, 1982; Vorley, 1986). To
overcome stressful periods and to remain in
synchrony with their biotic requisites, parasitoids
*Corresponding Author E-mail: legrand@ecol.ucl.ac.be
© 2004 Association of Applied Biologists

have evolved adaptations such as diapause and
quiescence (Tauber et al., 1983). In field
observations, Vorley (1986) and Langer et al. (1997),
showed that in temperate climates (as in England
and Belgium) parasitoids of wheat aphids are still
active during the winter months. In Belgium, Langer
& Hance (2000) observed that a part (less than 65%)
of the parasitoids population of anholocyclic S.
avenae enters diapause, with the remaining
population undergoing quiescence. If climatic
conditions allow these quiescent parasitoids to
complete their development and emergence, they
may become active during winter.
Sitobion avenae is an important pest of cereals
worldwide (Vickerman & Wratten, 1979; Carter et
al., 1989). In France and in England, it is considered
to be the most harmful species in spring, especially
after mild winter conditions (Dedryver & Gellé,
1982; Dewar & Carter, 1984). Aphidius rhopalosiphi
De Stefani Perez is one of its most abundant
parasitoids (Hymenoptera: Braconidae) (Stary, 1981;
Krespi et al., 1987; Sigsgaard, 2002; Legrand et al.,
2001). The aim of this study was to analyse the
population development of S. avenae under winter
conditions in relationship with presence or absence
of A. rhopalosiphi and to study the impact of winter
conditions on the activity of A. rhopalosiphi.

140

M A LEGRAND ET AL.

Materials and Methods
Rearing started with individuals collected during
the previous summer. S. avenae was reared on winter
wheat Triticum aestivum L. variety Windsor, at 20°C,
60% r.h. and 16 h of light. The parasitoid A.
rhopalosiphi was reared under the same conditions
on S. avenae. Experiments were carried out using
pots of wheat plants, under outdoor conditions, at
Louvain-la-Neuve, Belgium (50.3°N latitude). The
winter wheat was sown in the laboratory and kept at
20°C-16 h light until germination of the grain. Four
batches of 30 pots were formed with c. 10 seedlings
pot-1 and placed in cages (80 cm × 80 cm × 120 cm).
The front doors of the cages were made of
transparent plastic whereas the sides were composed
of fine mesh net. The experiments started on 22
October 2001 and ended on 8 March 2002.
To investigate the potential of A. rhopalosiphi for
controlling aphid populations, the density of aphids
was chosen in relation to the economic injury level
estimated by Latteur (1985). This author has shown
that a density of five aphids and 10 aphids per tiller
induces respectively a yield loss of 70 kg ha-1 and
180 kg ha-1. The pots of wheat plants were infested
with 100 second or third aphid instars, which makes
an average of 10 aphids per tiller. In October 2001,
all batches of pots were placed in a cage under
outdoor conditions. Temperature and photoperiod
inside cages were recorded every hour using a
Hobo®, model H8. Two batches received only S.
avenae (control treatment: “Sa1” and “Sa2”) and two
others S. avenae plus 20 pairs of A. rhopalosiphi of
maximum 48 h old (parasitoid treatment: “Sa+Ar3”
and “Sa+Ar4”). Stilmant (1997) has shown that the
average fecundity of A. rhopalosiphi is at least 105
per female (Langer, 1999). Therefore, with a density
of 20 active females, the aphid population should
have fallen below the economic injury level.
The ability of A. rhopalosiphi to control aphid
population under autumn, winter and spring
conditions was measured every 3 wk. Five pots were
randomly removed from each batch at each sampling
date and all aphids and mummies were counted.
After an acclimation period during which
temperature was raised by 5°C every 2 h to avoid
thermal shocks (Levie, 2002), living aphids were
incubated at 20°C and 16 h of light until mummies
formed. Total parasitism levels were calculated as
number of mummies divided by the number of live
aphids + mummies recorded. Mummies were kept
until emergence and development time was
calculated on a day-degree (°D) time scale as: °D =
DT (T-To) for T > To, where T is the temperature in
°C, DT is the observed developmental period in days
and To is the lower thermal threshold (Campbell et
al., 1974). According to Ruggle & Holst (1994), the
thermal threshold of A. rhopalosiphi is 6.5°C for egg

to adult development. Colours of mummies sampled
on 23 November 2001 and 14 December 2001 were
ranked in three categories: light brown, intermediary,
and dark brown. Mummies that had not emerged
after 21 days at 20°C were dissected to determine if
the parasitoid inside was dead or still alive
(diapausing). Under normal conditions, development
time between mummy and adult stages should last
at least 70°D (Sigsgaard, 2000); living parasitoid
larvae that had not emerge after 21 days at 20°C
(i.e. 283.5°D) were considered to be under diapause.
To evaluate the impact of winter conditions on the
development of parasitoid population, mortality of
mummies was analysed in relation to cold conditions
Numbers of aphids and mummies were log
transformed and effects of “treatment”, “date” and
“batch” on the number of S. avenae were tested using
a three-way analysis of variance (Dagnelie, 1975).
After arcsin-square-root transformation, percentages
of parasitism were analysed using two-way analysis
of variance. When significant differences were
found, further analyses were carried out using the
Student-Newman-Keuls test (SNK). Percent
mortality and colour of mummies were analysed with
a Chi-squared test (Wonnacott & Wonnacott, 1991).
All analyses were carried out with SAS version 6.12
(Anon., 1989).
Results
Aphid population
Population growth curves of S. avenae between
October 2001 and March 2002, in the absence or
presence of A. rhopalosiphi are shown in Fig. 1.
Aphid populations generally grew until mid
December, a period during which the mean
temperature declined but remained well above 0°C
(Fig. 2). From December to February, the
populations declined in all replicates. The aphid
populations increased rapidly from late February to
April, in control treatments (Sa1 and Sa2). In the
presence of parasitoids (Sa+Ar3 and Sa+Ar4), aphid
populations decreased from November to December
as in the control treatment, but they did not show
the subsequent increase in spring (Fig. 1). The three
way analyses of variance on the number of aphids
showed that there were no batch effects in the same
treatment (Table 1). The number of aphids varied
significantly between sampling date and between
treatments.
Parasitoid population
The two-way analysis of variance on the
percentage of parasitism (Fig. 3.) indicates a
significant effect of the factor “date” (F = 8.59; P =
0.017). The SNK test confirmed that the percentage
observed on 15 February 2002 was significantly
different from the other dates (Table 2). The

141

Overwintering dynamics of aphid-parasitoid interactions

Fig. 1. Sitobion avenae population growth in absence
[“Sa1” (") and “Sa2” (!)] or in presence [“Sa + Ar3”
(#) and “Sa + Ar4”($)] of A. rhopalosiphi, between
22 October 2001 and 8 March 2002.

25/2

11/2

28/1

14/1

31/12

17/12

3/12

19/11

5/11

22/10

Temperature (°C)

18
14
10
6
2
-2
-6
-10

Date
Fig. 2. Mean diurnal temperature between 22 October
2001 and 8 March 2002.
Table 1. Three-way analyses of variance of the
number of aphids for each sampling date, batches
and treatment. NS: non-significant effect; *:
significant α = 0.05; *** : significant α = 0.001

Date
Batches (treatment)
Treatment
Date * treatment
Date*batches*treatment

df

F value

P

5
2
1
5
10

42.54
1.56
83.27
8.42
0.92

< .0001
0.2153
0.0118
0.0023
0.5188

% parasitism

40
35
30
25
20
15
10
5
0
23/11 6/12 19/12 1/1 14/1 27/1 9/2 22/2 7/3
Date

Fig. 3. Percentage parasitism of Aphidius rhopalosiphi
on Sitobion avenae, between 23 November 2001 and
8 March 2002. SaAr3 = ! ; SaAr4 = ".
% mortailty of parasitoid mummies

200
180
160
140
120
100
80
60
40
20
0
22/10 23/11 14/12 04/01 25/01 15/02 08/03
Date

Diapause
As mummies collected on 23 November 2001 did
not emerged after 21 days at 20°C, they were
dissected, all contained a living larva, indicating
diapause. November conditions seems thus to induce
A. rhopalosiphi diapause: mean temperature of 6.3°C

35
30
25
20
15
10
5
0

23/11 14/12

04/01 25/01 15/02
Date

08/03

Fig. 4. Percentage of mummy mortalities between 23
November 2001 and 8 March 2002. Mummies were
sampled in outdoor conditions, on pots of wheat plant
infested with Sitobion avenae.
50

***
NS
*
*
NS

Table 2. Analyses of date effect on parasitism % by
Student-Newman-Keuls test (SNK)
Date

Group

Mean

N

15 Feb
25 Jan
23 Nov
14 Dec
08 Mar
04 Jan

A
B
B
B
B
B

0.32
0.22
0.15
0.15
0.13
0.09

10
10
10
10
10
10

% mummies

No. of live aphids

parasitoid mummy mortality between November
2001 and March 2002 is presented in Fig. 4. It
differed significantly between 14 December 2001
and 4 January 2002 (Chi-squared = 2.67, P = 0.009)
but not between 4 January and 15 February 2002.

40
30
20
10
0

Dark

Intermediate
Date

Light

Fig. 5. Percentage colour morphs for diapausing (grey
bars; n = 27) and non-diapausing (black bars; n = 47)
individuals of Aphidius rhopalosiphi (dark brown,
intermediate and light coloured mummies). Mummies
were sampled on 23 November 2001 and 14 December
2001 under outdoor conditions, on pots of wheat plant
infested with Sitobion avenae.

142

M A LEGRAND ET AL.

and a decreasing photoperiod from 9.5-8.5 h of day
light. When ranked by colour classes, most
diapausing mummies were dark while most nondiapausing mummies were light although these
differences were not significant (Chi-squared = 2.98,
P = 0.225) (Fig. 5).
Discussion
Aphid and parasitoid population growth in winter
Winter cereals are currently sown in October in
Belgium and the level of aphid survival during winter
will determine the rapidity of aphid population
growth in spring (Langer, 1999). The decline of the
aphid population in winter occurred during the
second half of December and corresponded to a clear
decrease in temperature. The mean temperature in
this period was 0.8°C with a minimum of -6.3°C.
The threshold temperature for aphid development
are in the range from 4 to 5°C and according to Bale
(1996), lethal temperature (LT50) for adult S. avenae
is -7 ± 0.4°C. Powell & Parry (1976) and Knight et
al. (1986) showed that, at these low temperatures,
aphids were not able to feed and died of dehydration
and starvation. Knight et al. (1986) observed a
continual decline in the S. avenae population after a
short period at -8.1°C. This observation may explain
why aphid population did not grow directly when
the temperature rose.
A significant increase in A. rhopalosiphi mortality
was observed during the second half of December.
For another parasitoid species, Rivers et al. (2000)
showed that larvae of Nasonia vitripennis (Walker)
(Hymenoptera: Pteromalidae) were killed by chilling
at temperatures well above their supercooling point.
Previous studies (Legrand et al., 2001) have shown
that the emergence rate of mummies of A.
rhopalosiphi, stored for 3 wk at 3°C or 0°C, is only
21% and 25%. The low temperatures recorded (8
days of frost were measured) during the period
ranging from 14 December 2001 to 3 January 2002
might, therefore, explain the high mortality observed.
In spring, after a mild winter, rapid aphid
population growth was observed in the control
treatment. However, when parasitoids were present,
S. avenae populations were reduced to just a few
individuals and were maintained at a very low level,
suggesting that parasitoid activity in winter and
spring is an important factor in maintaining aphid
populations at low densities during spring. Indeed,
in early sown fields, the presence of aphids
throughout winter ensures the presence of natural
enemies that reduce the growth rate of the cereal
aphid population (Vorley & Wratten, 1987). In our
experiment, the development of the parasitoid
showed that the first mummies were formed on 7
November 2001. Moreover, the percent parasitism
on 15 February was at a very high level. This

precocity of the parasitism could explain the low
aphid densities observed in spring 2002.
Diapause
In our experiment, actual development time from
first oviposition is not known. However, when
mummies collected in the cages did not emerge after
21 days at 20°C and contained living larvae, the
development time took more than 283.5°D. On 23
November 2001, 100% of mummies did not emerge
and were considered to be in diapause. The
temperature and photoperiod observed at this period
are known to induce diapause in some parasitoids
(Polgar & Hardie, 2000; Tauber et al., 1983; Leather,
1993; Saunders, 1965).
Krespi et al. (1994) reported that diapausing last
instar of A. rhopalosiphi formed darker mummies
and thicker cocoons than those of non-diapausing
individuals. Schlinger & Hall (1960) also remarked
that diapausing individuals of Trioxys utilis
Muesebeck (Hymenoptera: Braconidae) have a dark
brown colour and a much thicker cocoon. Similar
differences have been observed in a number of
Aphidiinae by Stary (1970). In our experiment, no
significant difference in colour was found between
diapausing and non-diapausing individuals. It seems
that mummy colour in itself is not a sufficient and
effective criterion to determine the diapausing status
of A. rhopalosiphi.
Conclusion
This work points out how weather conditions can
affect aphid and parasitoid population levels. The
cold temperatures recorded during this experiment
were revealed to be a winter mortality factor for the
aphids and their parasites. Surviving virginoparae
aphid may be attacked by parasitoids in autumn,
winter and spring. Indeed, in our study the presence
of parasitoids has affected spring aphid increase.
Temperature and photoperiod can influence the
diapause induction and the time of parasitoid
emergence and thus the effect on the spring aphid
population. The effects of these weather conditions
on natural enemies such as parasitoids should be
more considered in forecasting systems in order to
improve their precision.
Acknowledgements
This study was supported by the «Fonds pour la
Formation à la Recherche dans l’Industrie et dans
l’Agriculture (FRIA)», the « Fonds National de la
Recherche Scientifique (FNRS) (Belgium) » and by
the « Centre National de la Recherche Scientifique,
Direction des Relations Internationales (France) ».
The authors are grateful to C Pels for technical
assistance. We also thank G Boivin and R

Overwintering dynamics of aphid-parasitoid interactions

Wesselingh for their very constructive advice. It is
publication number BRC0051 of the Biodiversity
Research Center, UCL.
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