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Physiological Entomology (2006) 31, 234–240

DOI: 10.1111/j.1365-3032.2006.00511.x

The impact of fluctuating thermal regimes on the
survival of a cold-exposed parasitic wasp, Aphidius
colemani
H . C O L I N E T 1 , D . R E N A U L T 2 , T . H A N C E 1 and P . V E R N O N 3
Unite´ d’E´cologie et de Bioge´ographie, Biodiversity Research Centre, Universite´ catholique de Louvain, Louvain-la-Neuve,
Belgium, 2Universite´ de Rennes 1, UMR CNRS 6553 ECOBIO, Rennes, France and 3Universite´ de Rennes 1,UMR CNRS
6553 ECOBIO, Station Biologique de Paimpont, Paimpont, France.
1

Abstract. The impact of fluctuating thermal regimes on the cold tolerance of the

parasitoid Aphidius colemani at the mummy stage is examined. The hypothesis is
tested that, if a cold period is interrupted by a return to a higher temperature for a
short time, a physiological recovery is possible and may lead to higher survival.
Mummies are exposed to a constant temperature of 4 C and, when periodic
sudden transfers to 20 C for 2 h are applied, survival of immature parasitoids is
markedly improved, proportionally to the warming frequency. The time lag
before emergence diminishes with the duration of cold exposure and with warming frequency. The sex ratio of emergent adults after cold exposure indicates that
males may be more susceptible than females to cold-injury. It is suggested that the
transfer to 20 C allows a re-activation of the normal metabolism, leading to
repair and recovery of any injuries caused by prolonged chilling. The study
underlines the importance of cyclic temperature changes on insect survival.
Key words. Aphidius colemani, cold exposures, chill injuries, Myzus persicae,

recovery.

Introduction
Temperature plays an important role in insect population
dynamics, mortality in winter time being a major cause in
regulating population growth (Leather et al., 1993).
Survival of insects exposed to low temperatures has been
studied in many insect species (Denlinger & Lee, 1998;
Sømme, 1999). The underlying mechanisms allowing these
organisms to increase their cold-hardiness have long been a
central theme in the field of thermal biology and have been
extensively reviewed (Sømme, 1999; Bale, 2002; Sinclair
et al., 2003). Studies on insect cold-hardiness are generally
achieved by measuring the capacity to survive at constant
low temperatures for extended periods, and/or by measuring supercooling abilities (Renault et al., 2002).

Correspondence: H. Colinet, Unite´ d’E´cologie et de Bioge´ographie,
Biodiversity Research Centre, Universite´ catholique de Louvain, Croix
du Sud 4-5, 1348 Louvain-la-Neuve, Belgium. Tel.: þ32 10 45 34 91;
fax: þ32 10 45 34 90; e-mail: colinet@ecol.ucl.ac.be

234

However, in nature animals are regularly exposed to
thermal fluctuations, and the importance of measuring survival at both constant and fluctuating temperatures has
previously been stressed by Bale (2002). Surprisingly, subsequent to the pioneer studies of Casagrande & Haynes
(1976) and Bale (1989), very few data are available on insect
survival at fluctuating temperatures. A higher mortality
was found under these conditions by Coulson & Bale
(1996) in the weevil Rhynchaenus fagi. However, because
recent work shows that variable temperatures can improve
cold survival in some species (Leopold et al., 1998; Nedved
et al., 1998; Renault et al., 2004), the necessity of studying
insect cold tolerance under cycling temperature regimes has
been re-emphasized (Renault et al., 2004; Danks, 2005).
Because insect parasitoids and predators are commonly
used in biological control, the possibility of using cold
storage as an aid to mass-release was examined over
70 years ago and there is ample literature dealing with
this topic (Archer et al., 1973; Hofsvang & Hagvar, 1977;
Jarry & Tremblay, 1989; Kostal et al., 2001; Levie et al.,
2005; Colinet et al., 2006). Currently, cold storage of most
of the species used in biocontrol or in integrated pest
# 2006 The Authors
Journal compilation # 2006 The Royal Entomological Society

Survival of a cold-exposed parasitic wasp, A. colemani
management programmes involves chilling at some subambient temperature above 0 C (Leopold, 1998). Low temperatures are known to induce mortality due to chill injury
at temperatures well above the supercooling point
(McDonald et al., 1997; Rivers et al., 2000). However,
causes of death at low temperatures are still not well understood (Denlinger & Lee, 1998; Renault et al., 2002).
Moreover, the possibility of a cold-induced differential
mortality between sexes has been regularly neglected
(Renault et al., 2002), although the proportion of females
is of a great importance in biological control programmes,
with female parasitoids being directly responsible for killing
the pests by oviposition.
To date, no study has been undertaken to analyse the
impact of fluctuating thermal regimes on the survival of
cold-exposed parasitic wasps. In natural cold conditions,
most Aphidiinae arrest their development and enter in
hibernal quiescence (dormancy) inside the cocoon of a
mummified aphid (Stary´, 1970a; Jarry & Tremblay, 1989).
Quiescent mummies are usually used for cold storage in
insectaries for mass production because they are more tolerant to cold exposure than adults (Stary´, 1970b). In the
present study, the hypothesis is tested that, if the cold
exposure is interrupted by a return to a higher temperature
over a short period, a physiological recovery is possible and
may lead to a higher survival when exposed to further cold
periods. Whether detrimental effects of the cold exposure
affect the sexes differentially is also examined
The parasitoid Aphidius colemani Viereck (Hymenoptera:
Aphidiinae) is used as the model. This parasitoid is commercially produced and widely distributed as an aphid
biocontrol agent, targeting primarily Myzus persicae
Sulzer (Homoptera: Aphididae) in glasshouses of several
European countries.

235

mummies were left to develop for 1 day, under the same
rearing conditions before cold exposure. One-day-old
mummies were used in the experiment because young mummies are known to be generally more tolerant to cold
exposure (Hofsvang & Hagvar, 1977; Levie et al., 2005).

Thermal treatments and parameters measured
For aphid parasitoids, low temperatures used for cold
storage depend on the species, and generally are in the
range 0–7 C (Archer et al., 1973; Singh & Srivastava,
1988; Rigaux et al., 2000). In the present study, exposure
to 4 C was chosen as a temperature close to the thermal
threshold (2.8 C) of A. colemani (Elliott et al., 1995).
Batches of 50 randomly chosen 1-day-old mummies were
placed in small plastic Petri dishes (4.5 cm diameter). To
maintain a saturated relative humidity, these Petri dishes
were placed into larger ones (15 cm diameter) containing a
filter paper that was constantly wet. Mummies were then
exposed to low temperature but, to avoid potential coldshock, the temperature was lowered progressively by 5 C
every 2 h, as described by Levie et al. (2005), from 18 to
4 C. Mummies were kept in darkness in a thermoregulated LMSÒ incubator (LMS Ltd., Kent, U.K.); the
temperature and relative humidity were checked using
HoboÒ automatic recorders (Onset Computer, Bourne,
Massachusetts). Batches of mummies were randomly
assigned to each of the four thermal treatments:
Treatment C Constant temperature: 4 C for the entire
duration of the experiment.
Treatment F1 Fluctuating temperature 1: the 4 C
exposure was interrupted daily (every 22 h) by a transfer
to 20 C for 2 h.

Materials and methods
Rearing aphids and parasitoids
The green peach aphid, M. persicae, was used as host for
the parasitoid rearing, and laboratory cultures were established from individuals collected in fields during 2000 at
Louvain-la-Neuve, Belgium (50.3 N latitude). Aphids were
reared in 0.3 m3 cages on oilseed rape [Brassica napus (L.),
var. Mesural] at 18 1 C, 60% relative humidity (RH)
under an LD 16 : 8 h photoperiod. Aphidius colemani, originally from Biobest Co. (Belgium), were subsequently
reared in the laboratory under the same conditions.
To obtain standard mummies, batches of 50 standardized 3-day-old aphids were offered to a mated female parasitoid for 4 h. Aphids were all synchronized at the same age
to avoid host-age effects on parasitoids development
(Colinet et al., 2005). The parasitoid females used were
aged less than 48 h, naı¨ ve, and mated. To ensure mating,
each female was placed with two males for 24 h and fed on
water and honey. Resulting parasitized aphids were then
reared as above, until mummification. Newly formed

Treatment F2 Fluctuating temperature 2: the 4 C
exposure was interrupted every other day (every 46 h) by
a transfer to 20 C for 2 h.
Treatment F3 Fluctuating temperature 3: the 4 C
exposure was interrupted every three days (every 70 h) by
a transfer to 20 C for 2 h.
For each treatment, three batches of 50 mummies were
removed at weekly intervals and kept at 20 C to measure
the survival after 1, 2 and 3 weeks of cold-exposure. The
survival was assessed as the number of adult parasitoids
that successfully emerged from the mummies. A non coldexposed control (i.e. three batches of 50 mummies) was
maintained at 20 C. For each thermal treatment and duration, the time-to-adult emergence, when the mummies were
replaced at 20 C after cold exposure (i.e. the time lag
before emergence), was recorded for each individual, as
well as the sex of emerging wasps. The sex ratio was then
determined and expressed as the proportion of males. It
was assumed that any significant change of sex ratio value
from the control would indicate a differential mortality.

# 2006 The Authors
Journal compilation # 2006 The Royal Entomological Society, Physiological Entomology, 31, 234–240

236 H. Colinet et al.
Statistical analysis
Arcsine square-root transformation was required to normalize the distribution of proportional data (emergence
rate and sex ratio) (Hardy, 2002). Emergence rate and sex
ratio were analysed using two-way analysis of variance
(PROC GLM, SAS Institute, 1990) with thermal treatment
and duration of cold-exposure as fixed factors. For emergence rate, multiple comparisons were then performed on
each factor using the Student–Newman–Keuls test to
describe differences between groups. For the sex ratio,
Dunnett’s pairwise multiple comparison t-test was used to
compare the mean values with the control mean. A significance level of a ¼ 0.05 was used for all tests. Data presented in the figures are untransformed.
For the time lag before emergence, a generalized linear
model based on a gamma distribution and log-link function
was used (PROC GENMOD, SAS Institute, 1990). This statistical method accounts for the fact that the time variable
lacks homoscedasticity and normality.

cold-stored for 1 week was over 90%. After 2 weeks of cold
exposure, the survival of the mummies decreased, especially
for individuals kept at constant 4 C (treatment C). After
3 weeks of cold-storage, the emergence rate for treatment
F1 remained close to 90%, whereas the number of emerging adults in treatment C was drastically reduced and fell
to 45%. Emergence was significantly affected by the duration of cold exposure (F ¼ 80.01; P < 0.001). Multiple
comparisons (Table 1) indicated that survival was the highest for control mummies (no cold-exposure, duration ¼ 0),
and the lowest for mummies cold-exposed for 3 weeks.
Emergence was also significantly affected by the thermal
treatment (F ¼ 14.22; P < 0.001). Multiple comparisons
(Table 1) indicated that survival was highest for mummies
that received a daily warming at 20 C (F1), followed by
treatments that received warming every 46 h (F2) and every
70 h (F3) and, finally, the lowest survival was observed for
mummies exposed to a constant low temperature (C). The
reduction in the emergence rate with cold-exposure duration differed between the treatments (interaction: F ¼ 4.75;
P < 0.001).

Results
Survival

Sex ratio

In all thermal treatments, reduction of parasitoid emergence was observed with the duration of cold exposure
(Fig. 1). The emergence rate of the control and mummies

The sex ratio was female biased in all four thermal treatments (Fig. 2), with the male proportion in the range
0.3–0.4. The sex ratio was significantly affected by the
duration of cold-exposure (F ¼ 8.21; P < 0.001).
Dunnett’s multiple comparison tests (Table 1) indicated
that the proportion of males was the same in the control
and in the 1-week cold-exposed mummies; but the sex ratio
was significantly lower than in the control for mummies
cold-stored for 2 and 3 weeks. The sex ratio (Fig. 2;
Table 1) did not differ significantly between the four treatments (F ¼ 0.81; P ¼ 0.50). The influence of the duration
of cold exposure on the sex ratio was similar for all thermal
treatments (interaction: F ¼ 0.54; P ¼ 0.83).

C

F1

F2

F3

Emergence (%)

100
75
50
25
0

Emergence (%)

100

Table 1. Multiple comparisons performed on the mean exposure
values.

75
50
25
0
0
1
2
3
Cold exposure duration (weeks)

0
1
2
3
Cold exposure duration (weeks)

Fig. 1. Percentage of adults emerging (mean SE) as a function
of the duration of cold-exposure for each thermal treatment: constant 4 C (C, white bars), fluctuating temperatures with daily
warming (F1, black bars), fluctuating temperatures, 4 C for 46 h
and 20 C for 2 h (F2, squared bars) and fluctuating temperatures,
4 C for 70 h and 20 C for 2 h (F3, hatched bars).

Duration of storage (weeks)
0
1
2
3
Thermal treatment
C
F1
F2
F3

Emergence
ratea

Sex
ratiob

Time
lagc

a
b
c
d

a
a
b
b

a
b
c
d

c
a
b
b

a
a
a
a

a
c
b
a

Different letters in a column indicate a significant difference (a ¼ 0.05).
a
Student–Newman–Keuls tests, bDunnett’s t-test and cscale parameters
estimated by maximum likelihood.

# 2006 The Authors
Journal compilation # 2006 The Royal Entomological Society, Physiological Entomology, 31, 234–240

C

F1

Sex ratio (male proportion)

0.4
0.3
0.2
0.1
0.0

F2

F3

Sex ratio (male proportion)

0.4
0.3
0.2
0.1
0.0

0
1
2
3
0
1
2
3
Cold exposure duration (weeks) Cold exposure duration (weeks)

Fig. 2. Sex ratio expressed as male proportion (mean SE) as a
function of the duration of cold-exposure for each thermal treatment: constant 4 C (C, white bars), fluctuating temperatures with
daily warming (F1, black bars), fluctuating temperatures, 4 C for
46 h and 20 C for 2 h (F2, squared bars) and fluctuating temperatures, 4 C for 70 h and 20 C for 2 h (F3, hatched bars)

Lag time before emergence (days) Lag time before emergence (days)

Survival of a cold-exposed parasitic wasp, A. colemani

237

C

F1

F2

F3

0
1
2
3
Cold exposure duration (weeks)

0
1
2
3
Cold exposure duration (weeks)

6
5
4
3
2
1

6
5
4
3
2
1

Fig. 3. Time lag before emergence of adults at 20 C after cold
exposure (mean SE) in relation to duration of cold-exposure for
each thermal treatment: constant 4 C (C, white bars), fluctuating
temperatures with daily warming (F1, black bars), fluctuating temperatures, 4 C for 46 h and 20 C for 2 h (F2, squared bars) and
fluctuating temperatures, 4 C for 70 h and 20 C for 2 h (F3,
hatched bars).

Time lag before emergence
The time required for adults to emerge after the cold
exposure was affected by the duration of cold exposure
(Fig. 3). Control mummies required 5.7 days to emerge
whereas 3-week, cold-exposed insects emerged in less than
half the time (2.4 0.17 days). The time lag before emergence was significantly affected by the duration of coldexposure (w2 ¼ 2389.50; P < 0.001). Multiple comparisons
(Table 1) indicated that the time-to-adult emergence was
longer for controls followed by 1-, 2- and 3-week exposed
insects. The time lag was also significantly affected by the
thermal treatment (w2 ¼ 206.90; P < 0.001): it took longer
for adults to emerge from thermal treatments C and F3
followed by treatment F2, and finally by treatment F1
(Table 1). The reduction of time lag with the duration of
cold-exposure was specific to the thermal treatment applied
(interaction: w2 ¼ 130.59; P < 0.001).
Discussion
As observed in many other studies, exposure to prolonged
constant low temperatures has a detrimental effect on the
survival of parasitic wasps (Hofsvang & Hagvar, 1977;
Jarry & Tremblay, 1989; Langer & Hance, 2000; Levie
et al., 2005; Colinet et al., 2006). As expected, the lethal
effects of the low temperature increases with the duration
of cold-exposure in A. colemani.

Survival at low temperatures is related to the depletion of
energy reserves during starvation, which may progressively
become critical (Renault et al., 2002; Colinet et al., 2006).
In addition, low temperatures may induce injuries, even at
temperatures well above the supercooling point (Rivers
et al., 2000; Carrillo et al., 2005). The level of accumulated
injury is significantly correlated with the duration of exposure at a given low temperature, and probably results from
the accumulation of metabolic wastes such as lactic acid
and nitrogenous substances, cellular damage, enzyme
blockage and/or accumulation of molecules that may be
toxic at high concentrations (Nedved et al., 1998; Renault
et al., 2002). Oxidative stress may also contribute to the
chill injuries occurring during prolonged cold exposure.
Indeed, Rojas & Leopold (1996) provided indirect evidence
for the role of oxidative stress in causing chilling injury.
In the present study, the survival of a parasitic wasp is
improved when the cold-exposed mummies receive short
pulses at a higher temperature. Transferring mummies to
20 C may reduce the speed and the amount of accumulated injuries and may result in an increase of the metabolism activity, facilitating the elimination of a substantial
part of the accumulated toxins.
The mummies that receive thermal treatment F1 survive
better than those that receive treatments F2 and F3, suggesting that the beneficial effect of high-temperature interruptions is cumulative. In F1, chill injury may not

# 2006 The Authors
Journal compilation # 2006 The Royal Entomological Society, Physiological Entomology, 31, 234–240

238 H. Colinet et al.
accumulate from day to day, as they do for wasps kept at
constant temperatures or in the thermal treatments F2 and
F3 (i.e. the daily accumulated injuries may be repaired
every day in F1). Renault et al. (2004) also show that a
daily exposure to 25 C drastically reduces the mortality in
the tenebrionid beetle, Alphitobius diaperinus. Similar
results are seen in the collembolan Orchesella cincata
(Nedved et al., 1998) and the house fly, Musca domestica
(Leopold et al., 1998).
Another interesting aspect that could be raised is the
thermal stress experienced by the wasps. When mummies
are transferred from 4 to 20 C and from 20 to 4 C,
individuals experience a sudden thermal variation at a
rate of approximately 0.8 C min 1 for 20 min. Rapid
temperature variations have long been considered as
stressful conditions, and are assumed to induce high mortality in cold-stored parasitoids (Shalaby & Rabasse, 1979;
Singh & Srivastava, 1988). To reduce potential mortality,
acclimation and postacclimation processes are often performed to avoid the risk of cold shocks associated with
sudden temperature variations (Shalaby & Rabasse, 1979;
Singh & Srivastava, 1988; Rigaux et al., 2000; Levie et al.,
2005). The acclimation refers to the use of a gradual
decrease in temperature. Interestingly, the rapid thermal
variations between storage conditions (4 C) and room
temperature (20 C) do not induce mortality in the present
study but, on the other hand, improve the survival, suggesting that the potential detrimental effects of sudden
thermal variations are much lower than the beneficial
effects on recovery. In many insects, low temperature
exposure is known to induce synthesis of stress proteins
during recovery periods at higher temperature
(Nunamaker et al., 1996; Yocum, 2001). Further experiments should determine whether stress proteins are
expressed and involved in the increased cold resistance of
mummies under fluctuating thermal regimes.
The time lag before emergence after exposure at low
temperature follows the expected patterns: it decreases
with the duration of cold exposure and with warming frequency. This indicates that, even at low temperature, immature parasitoids still develop slowly. Indeed, the
temperature experienced by cold-exposed mummies (4 C)
is above the estimated thermal threshold (2.8 C) of
A. colemani (Elliott et al., 1995). The short pulse at high
temperature also allows parasitoids to develop further.
According to Leopold et al. (1998), the increased survival
of house flies submitted to periodic warming during cold
storage could result from a developmental process where
high temperature interruptions allow a chilling intolerant
stage to develop to a more tolerant stage. This explanation
is improbable for aphid parasitoids because newly formed
mummies are generally known to survive cold-exposure
better than older ones, as reported for Lysiphlebus testaceipes (Archer et al., 1973), Ephedrus cerasicola (Hofsvang
& Hagvar, 1977) and Aphidius rhopalosiphi (Levie et al.,
2005).
Few studies have examined the possibility of a coldinduced differential mortality between sexes (Renault

et al., 2002) and limited information is available on the
effect of low temperature on the sex ratio. The results of
the present study indicate that males may be more susceptible than females to cold-injuries: the proportion of
males is higher in the control and 1-week cold-exposed
mummies than in the two- and 3-week cold-conserved
mummies. Similar results, where females could better
withstand cold exposure than males, have previously
been reported in Lysiphlebus testaceipes (Archer et al.,
1973), Aphelinus asychis (Archer & Eikenbary, 1973) and
Ephedrus cerasicola (Hofsvang & Hagvar, 1977).
However, contrasting conclusions are reached by Jarry
& Tremblay (1989), who show that cold-exposure of
mummies does not affect sexes differentially. The main
differences between sexes are reproductive systems and
size/weight parameters. In A. colemani, as in most parasitoid wasp species, there is a noticeable sexual size
dimorphism, females being larger than males, as a result
of which females may be characterized by higher amounts
of energy reserves. Under low temperatures, insects do
not feed and maintain a low level of metabolism, and so
energy reserves can be critically affected (Renault et al.,
2002, 2003). Thus, it can be hypothesized that males
exhaust their energy stock more rapidly than females
because of reduced initial stores and/or because of differential utilization. In the lesser mealworm Alphitobius diaperinus, females survive better than males at low
temperature (Renault et al., 2003). In the millipede,
Polysonium germanicum, females conserve their fat mass
better than males during starvation (David & Vannier,
1994). In adults of Pseudacteon tricuspis, a phorid fly
parasitoid of ants, nutrient levels and patterns of metabolism appear to be slightly different between the two
sexes (Fadamiro et al., 2005). The sex ratio is very dependent on external factors (King, 1987), so that general
conclusions are difficult to draw, but the study of its
variation must be highlighted because it is a parameter
of paramount importance in population dynamics.
In the present study, the importance of a relative short
stay at a higher temperature on the survival of cold-exposed
parasitic wasps is demonstrated. The high temperature
interruptions may allow a repair of chill injuries even if
the wasps experience repeated sudden thermal changes. It
is important that, in further ecological studies, the ability to
recover and the speed by which species are able to recover
from chill injuries should be taken into account in a wider
range of species.

Acknowledgements
This study was supported by Ministe`re de la Re´gion
wallonne DGTRE Division de la Recherche et de la
Coope´ration scientifique. FIRST EUROPE Objectif 3.
We are also grateful to the Station Biologique de
Paimpont, University of Rennes 1, for facilities. This
paper is BRC 086 of the biodiversity research centre.

# 2006 The Authors
Journal compilation # 2006 The Royal Entomological Society, Physiological Entomology, 31, 234–240

Survival of a cold-exposed parasitic wasp, A. colemani
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Accepted 6 January 2006
First published online 27 March 2006

# 2006 The Authors
Journal compilation # 2006 The Royal Entomological Society, Physiological Entomology, 31, 234–240


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