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Ecological Entomology (2005) 30, 473–479

Host age and fitness-related traits in a koinobiont aphid
parasitoid
H . C O L I N E T 1 , C . S A L I N 1 , G . B O I V I N 2 and T H . H A N C E 1

Unite´ d’E´cologie et de
Bioge´ographie, Biodiversity Research Centre, Universite´ catholique de Louvain, Belgium and Centre de Recherches et de
de´veloppement en Horticulture, Agriculture, et Agroalimentaire Canada, Saint-Jean-sur-Richelieu, Que´bec, Canada
1

2

Abstract. 1. Trade-offs play a key role in species evolution and should be found
in host–parasitoid interactions where the host quality may differ between host age
categories.
2. The braconid wasp, Aphidius ervi, is a solitary endoparasitoid that allows its
aphid hosts to continue to feed and grow after parasitisation. The hypotheses that
host age influences their quality and that female parasitoids exploit their hosts
based on that quality were tested under laboratory conditions using no-choice
tests.
3. Aphidius ervi females accepted the aphid Myzus persicae for oviposition and
their progeny developed successfully in all host ages. The fitness-related traits of
parasitoids did not increase linearly with the host age in which they developed.
Host quality was found to be optimal at intermediate host ages and the females
preferred to parasitise these hosts. The shortest progeny development time and a
more female-biased sex ratio were observed in hosts of intermediate age.
4. This study suggests the existence of multiple interactive trade-offs occurring
during host–parasitoid interactions according to host age related quality.
Key words. Aphidius ervi, host age, koinobiont, life-history traits, Myzus persicae, quality, trade-off.

Introduction
For insect parasitoids, the host represents the whole nutritional and physiological environment during immature
development. Thus, host quality evaluation by female parasitoids plays a key role, and host choice may result in tradeoffs between lower fitness gain because of host quality and
developmental requirements (Vinson, 1990; Godfray, 1994;
Harvey & Strand, 2002; Beckage & Gelman, 2004).
Parasitoids that paralyse or kill their host, also referred
to as idiobionts, can use host size as an indicator of the
potential resource for their offspring (Godfray, 1994). In

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. E-mail: colinet@ecol.
ucl.ac.be

#

2005 The Royal Entomological Society

contrast, parasitoids that allow the host to continue to feed
and grow after parasitisation, also referred to as koinobionts, have to cope with a higher degree of uncertainty
about the resources for their offspring as host quality varies
during the course of parasitoid development (Mackauer,
1986). Thus the relationship between the host characteristics at oviposition and the fitness gain of the parasitoid is
not obvious and depends on a combination of factors such
as (1) the physiology and behaviour of the host instars (Liu
et al., 1984; Gerling et al., 1990; Weisser, 1994; Jones &
Greenberg, 1998; Chau & Mackauer, 2000; Lin & Ives,
2003), (2) host-plant quality (Kouame´ & Mackauer, 1992;
Stadler & Mackauer, 1996), and (3) the feeding ecology of
the host (Harvey & Strand, 2002).
Parasitoid fitness is usually measured by life-history traits
such as development time, survival, fecundity, sex ratio, and
size (Godfray, 1994; Roitberg et al., 2001). Several host quality
models assume that fitness is related to host size or age at
parasitism (e.g. Nicol & Mackauer, 1999; Chau & Mackauer,
473

474 H. Colinet et al.
2001). Arguments have been based principally, if not exclusively, on the relationship between host size at oviposition and
emerging parasitoid size, whereas the relationship with the
parasitoid’s development time is less well documented
(Harvey et al., 2000). Nevertheless, development time determines generation time, which is inversely related to the growth
rate (rm) of the parasitoid population (Tripathi & Singh, 1990);
it may therefore provide a good index of relative host quality.
When host size and quality vary, parasitoid wasps are
expected to oviposit more females in high quality hosts, because
the fitness of sons suffers less from being small than the fitness of
the daughters, who will have to produce eggs in turn (Charnov
et al., 1981). The size of aphids increases with age, but does this
increase necessarily induce improvement of host quality?
The assumption that host quality varies with age and
influences parasitoid fitness-related traits was tested in
Aphidius ervi Haliday (Hymenoptera: Aphidiidae), which
is a solitary endoparasitoid of the green peach aphid
Myzus persicae Sulzer (Homoptera: Aphididae), by examining the influence of host age on the apparent parasitism,
parasitoid sex ratio, and developmental time.

Materials and methods
Aphid and parasitoid cultures
Laboratory cultures of M. persicae and A. ervi were established from individuals collected in 2000 at Louvain-laNeuve, Belgium (50.3 N, 4.3 E). Aphids were initially
reared on broad beans (Vicia faba L., Fabaceae) before
being used in the experiments. Because aphid development
time and mortality depend on host-plant quality (Kouame´ &
Mackauer, 1991; Stadler & Mackauer, 1996), to remove this
factor from these experiments, both unparasitised and parasitised aphids were reared on an artificial diet. The method
described by Cambier et al. (2001) was used, which allows
cohorts to be synchronised and aphid growth to be standardised. To obtain synchronised cohorts of aphids for nochoice experiments, apterous adults originating from the
laboratory culture were placed on the artificial diet in Petri
dishes and allowed to reproduce for 24 h. The operation was
repeated for a duration of 11 days. Every day, newly born
aphid nymphs were removed from the Petri dishes and
placed on the artificial diet to develop to the desired age.
The diet was replaced every other day in order to avoid
contamination by microorganisms and to ensure a constant
quality. Nine different aphid ages were obtained, from newly
born to adult (1, 2, 3, 4, 5, 6, 7, 9, and 11 days old and
corresponding instars L1, L1, L2, L2, L3, L3, L4, Ad and
Ad). Experiments were conducted in a climate-controlled
room (20 1.5 C, &60% RH and L:D 16:8 h).

Host suitability and parasitoid life-history traits
All replicates were carried out on the same day to
minimise the potential effect of variability in conditions.
#

The parasitoid females used were less than 48 h old, naive,
and mated. Before the experiment, each female was left for
24 h with two males and fed on water and honey. For host
parasitisation, one parasitoid female was released for 4 h in
a plastic Petri dish (4.5 cm diameter) containing 50 aphids
of a given age and feeding on the artificial diet. The number
of aphids was based on a prior experiment and exceeded the
capacity of a female parasitising for 4 h. Thereafter, the
parasitoid female was removed and the aphids were maintained on the artificial diet to continue their development
until mummification. Ten replicates were performed for
each host age. As a control, 20 aphids of each age were
followed for 10 days in order to estimate mortality in the
absence of parasitoids.
After 10 days of incubation, the number of mummies was counted. The parasitisation rate was estimated by the proportion of the total number of hosts
that produced mummies (i.e. secondary parasitisation
rate). Although this measure does not distinguish
between acceptability for oviposition and suitability
for parasitoid development, it provides a useful assessment of the net effect of host characteristics on the
success of parasitism (Li & Mills, 2004). Aphid survival and mortality (in treatment) were also calculated as
the proportion of unparasitised and dead aphids
respectively. Emergences were checked every day, and
the development time and sex of emerging adults were
determined. The sex ratio was expressed as the proportion of males. The mortality in the treatment was
corrected against that in the control for each host
age according to Abbott (1925):
Mcorrected ¼

Mtreatment Mcontrol
100:
100 Mcontrol

ð1Þ

Statistical analysis
Normality was verified using the Shapiro–Wilk statistic (a ¼ 0.05). Arcsin square root transformation was
required (Hardy, 2002) to normalise the distribution of
proportional data (e.g. parasitisation, sex ratio). The
dependence of various measures of parasitoid fitness
on aphid age was analysed using regressions. As the
age increases linearly, simple linear regression was first
used to model the potential relationships between
variables. However, as host quality and its consequences on parasitoid fitness probably do not vary
linearly with age (young nymphs and adults may be
less suitable for development), nonlinear regression
was also applied to model the relationships. F-tests
were used to compare the two models, indicating if a
nonlinear function gives a more accurate fit to the data
(test on the quadratic term). For development time, no
transformation was required for regression analysis,
which is based on mean development time within each
host age class. The development time was compared
between the two sexes using ANOVA. These analyses
were achieved using the Statistical Analysis System
(SAS Institute, 1990).

2005 The Royal Entomological Society, Ecological Entomology, 30, 473–479

Host age quality and parasitoid fitness
Results

Table 1. Control mortality (in absence of parasitoid), treatment
mortality (predicted values calculated from regression model), and
Abbott’s corrected mortality, according to host ages.

Parasitisation rate, mortality, and survival
Aphidius ervi was able to parasitise and to develop up to
the mummy stage in aphids of all ages. Parasitism of young
nymphs and adult aphids produced a lower parasitisation
rate than intermediate host classes (Fig. 1). Regression
analysis revealed that parasitisation rate (i.e. proportion
of mummies) varied significantly with host age at oviposition; a quadratic curvilinear function best fits this relationship (Table 2).
In the control, mortality was not dependent on host age
(Table 2). The mean value was 5.5 2.61% with a maximum of 10% for 5-day-old aphids and a minimum of 0%
for 2-day-old aphids (Table 1). In the parasitised treatment,
mortality varied significantly with host age at oviposition
(Fig. 2) and decreased linearly with age (Table 2); however
a better fit was obtained using a quadratic model (Table 2).
Parasitism did not seem to induce mortality higher than in
the control for older nymphs and adult aphids (from ages 5
to 11) as corrected mortality was closed to zero (Table 1).
Corrected mortality also varied significantly according to
host age and a quadratic curvilinear function best fits this
relationship (Table 2), indicating that newly born aphids
were more prone to die when stung by a parasitoid than
were older individuals.
The aphid survival varied significantly with host age as a
greater proportion of unparasitised hosts was observed in
adult aphids (Fig. 3). Both linear and quadratic models
could explain the relationship but the best fit corresponded
to a quadratic curvilinear function (Table 2).

Host
age

Control
mortality (%)

Treatment
mortality (%)

Corrected
mortality (%)

1
2
3
4
5
6
7
9
11

5
0
5.3
5
10
5
5.9
6.25
7.1

26.87
20.69
15.86
12.23
9.6
7.8
6.67
6.04
7.42

23.02
20.69
11.19
7.61
0.44
2.95
0.84
0.22
0.3

Parasitoid emergence, sex allocation, and development time
Emergence rate was not significantly related to host age
at oviposition (Table 2), and reached on average 80% for
all ages.
The sex ratio of the progeny that emerged was always
female biased. Newly born nymphs and adult hosts produced a greater proportion of males than the intermediate
host class (Fig. 4). Sex ratio did not vary linearly with host
age; however, the addition of a quadratic term to the linear
equation significantly increased the fit to the data
(Table 2).
For both sexes, development time decreased with host
age (Fig. 5); the best fit was obtained using a curvilinear
function (Table 2). The development time of both males
and females was longer in young aphid nymphs, decreased

0.8
Transformed mortality rate (%)

Transformed parasitization rate (%)

1.4

1.2

1.0

0.8

0.6

0.6

0.4

0.2

0.0

0.4
1

2

3

4

5

6

7

8

9

1

10 11

Fig. 1. Parasitisation rate in relation to host age (i.e. proportion of
parasitised and mummified hosts).

2

3

4

5

6

7

8

9

10 11

Host age (days)

Host age (days)

#

475

Fig. 2. Aphid mortality rate in relation to host age (i.e. proportion
of dead hosts).

2005 The Royal Entomological Society, Ecological Entomology, 30, 473–479

476 H. Colinet et al.
Table 2. Result of regression analyses of life-history traits according to host age at oviposition. Linear (b1x þ b0) and quadratic
(b2x2 þ b1x þ b0) models were tested. The F-test compares the significance of the quadratic term. Regression parameters are only reported
for P < 0.05.
Dependent variable

Model

Mortality

Linear
Quadratic
Comparison

F-value

P-value

r2

33.59
26.48
11.69

0.02
<0.001
0.001

0.25
0.38

0.49
0.62

2
1.15

0.2
0.377

0.22
0.27




b0

b1

B2

0.02
0.08

0.005

Control mortality

Linear
Quadratic

Corrected mortality

Linear
Quadratic
Comparison

18.09
20.43
7.07

0.004
0.002
0.03

0.72
0.94

0.48
0.67

0.05
0.14

0.007

Linear
Quadratic
Comparison

3.41
12.13
20.05

0.07
<0.001
<0.001

0.04
0.23


0.75


0.09

0.007

Linear
Quadratic
Comparison

8.21
9.98
7.61

0.03
0.001
0.007

0.08
0.17

0.36
0.45

0.01
0.03

0.003

Linear
Quadratic

2.1
1.17

0.15
0.31

0.02
0.03




Linear
Quadratic
Comparison

0.1
3.24
11.53

0.75
0.02
0.001

0.01
0.09


0.69


0.06

0.005

Linear
Quadratic
Comparison

8.03
124.41
113.27

0.03
<0.001
<0.001

0.53
0.97

18.14
19.7

0.2
0.93

0.06

Linear
Quadratic
Comparison

6.27
83.31
82.63

0.04
<0.001
<0.001

0.47
0.965

17.34
18.55

0.14
0.71

0.05

Parasitisation

Survival

Emergence
Sex ratio

Female development time

Male development time











1.0

0.8
Transformed sex ratio (%)

Transformed survival rate (%)

0.8

0.6

0.4

0.6

0.4

0.2

0.2
0.0
0.0
1

2

3

4

5

6

7

8

9

10 11

1

2

3

4

5

6

7

8

9

10 11

Host age (days)

Host age (days)
Fig. 3. Aphid survival rate in relation to host age (i.e. proportion
of unparasitised hosts).

#

Fig. 4. Parasitoid sex ratio in relation to host age (i.e. proportion
of males).

2005 The Royal Entomological Society, Ecological Entomology, 30, 473–479

Host age quality and parasitoid fitness

Development time (days)

19

18

17

16

1

2

3

4

5

6

7

9

11

Host age (days)
Fig. 5. Development time to adult (mean SE) for male (*) and
female (&) Aphidius ervi in relation to host age.

for middle-aged aphids, and increased again when the
aphids reached the adult stage (Fig. 5). Analyses of variance revealed that females generally took longer to develop
than males (P < 0.05 for host of 1, 2, 3, 5, and 6 days old).

Discussion
Plant effects were avoided by using an artificial diet for growing aphids. Host age at oviposition can therefore be assumed
to be the only host-quality factor investigated. Moreover, the
parasitoids could only accept or reject the host on offer, but
not choose between hosts of different quality.
Aphidius ervi parasitised and developed successfully to
the mummy stage in all host ages from young nymphs to
adults of M. persicae. Host nymphs of intermediate ages
produced the highest parasitisation rate. Differences in
parasitisation rate between host ages may result from several factors such as developmental disruption of the parasitoid larvae, aphid injury caused at the time of oviposition,
and behavioural interactions (Liu et al., 1984; Islam et al.,
1997; Pandey & Singh, 1999; Beckage & Gelman, 2004).
The lower parasitisation rate of newly born aphid nymphs
was associated with a relatively higher mortality (corrected)
of aphid nymphs, suggesting that young nymphs are more
susceptible to the injuries caused at oviposition, including
sting or venom injection or both. In contrast, parasitism
did not seem to induce mortality in older nymphs and adult
aphids as corrected mortality was close to zero. Rakhshani
et al. (2004) also observed a decrease in mortality rate with
an increase in age of aphid hosts. The lower parasitism rate
observed in older hosts may reflect the adult defensive
behavioural response. Aphids respond to parasitoid attacks
#

477

by releasing an alarm pheromone, shaking their body, kicking off, walking away, and clustering (Villagra et al., 2002)
and these defence behaviours have been shown to differ
among instars with an increase in the kicking behaviour
from L1 nymph to adult stage (Weisser, 1995). Moreover,
late aphid instars may show a greater physiological immune
response to parasitism as reported in the aphid Toxoptera
citricida when parasitised by Lipolexis oregmae (Walker &
Hoy, 2003). Thus, the longer handling time resulting from
aphid defence behaviour, and the aphid immune response,
could explain the decrease of parasitisation rate observed in
adult aphids.
Aphidius ervi was able to complete its development to
adulthood regardless of which host age was parasitised (no
difference in parasitoid emergence rate) and was capable of
overcoming the sub-optimal conditions that might be
expected in very small hosts. Parasitoid development time
was dependent on host age at oviposition, being longer in
young aphid nymphs and adults, and shorter for intermediate ages. The quadratic response of development time was
independent of parasitoid sex, even if males developed
faster than females. Different relationships between parasitoid developmental time and host age at oviposition have
been described: (1) positive relationships (Vinson, 1972;
Lawrence et al., 1976), (2) negative relationships (Fox
et al., 1967; Bertschy et al., 2000; Bell et al., 2003; Hu
et al., 2003), (3) constant relationship (Liu, 1985), (4)
shorter development time in first and fourth instars
(Sequeira & Mackauer, 1993), and (5) U-shaped relationships (Jones & Greenberg, 1998; Harvey et al., 2004).
The capacity of A. ervi to develop in hosts of all ages
suggests an ability to adjust to the constraints specific to
each instar. Young aphid nymphs have fewer resources
available for the parasitoid, which needs to slow down its
development until its host has reached a sufficient size. The
longer development time observed in young host instars
may be associated with the existence of a critical host size
required for parasitoid development as observed in
Encarsia formosa (Hu et al., 2002, 2003). In contrast,
adult aphids are large enough for parasitoid development,
but the parasitoid competes with the embryos of the host
for resources. Brough et al. (1990) showed that the allocation of nutritional resources to somatic and gonadal tissues
changes when aphids (Megoura viciae) approach reproductive age. The immune system of adult hosts is also stronger
(Walker & Hoy, 2003). As a consequence, even if adults
represent a larger resource, their physiology imposes constraints on the parasitoid’s development and this results in
an increase in their development time.
Host quality is known to influence sex allocation in many
parasitoid species where females are allocated to hosts of a
higher quality (Charnov & Skinner, 1985; King, 1987).
Koinobiont parasitoids are less likely to exhibit hostquality dependent sex allocation because they are less likely
to predict the future nutritional resources of growing hosts
(Waage, 1982). However, the sex ratio deposited by some
koinobiont parasitoids placed in a no-choice situation has
been affected by host size at oviposition (e.g. Pandey &

2005 The Royal Entomological Society, Ecological Entomology, 30, 473–479

478 H. Colinet et al.
Singh, 1999; Bertschy et al., 2000). In this study, although
the secondary sex ratio was always female biased, it was
dependent on host age at oviposition with a lower sex ratio
allocated to hosts of intermediate age. The occurrence of a
higher proportion of females in hosts of higher quality, the
aphid nymphs of intermediate ages, supports the host quality model of Charnov and Skinner (1985). The observed
shift of sex ratio could be due to either the control of sex
allocation by the females or differences in pre-emergence
mortality. From the few laboratory studies that deal with host
size/age related sex ratio in aphid parasitoids, it appears that
both phenomena have been established (Pandey & Singh,
1999; Wellings et al., 1986). The occurrence of more males in
the larger fourth instars and adults suggests that host size alone
does not determine the sex ratio. Srivastava and Singh (1995)
emphasised that other characteristics such as physiological
immunity and behavioural defence should also be considered.
For early instar nymphs and adults, successful parasitism
is associated with multiple trade-offs between different physiological and behavioural constraints. Factors such as the
susceptibility to oviposition injury, the amount of resources
to satisfy parasitoid nutritional needs, the behavioural
defence reactions, the immune system, the host’s metabolic
and nutritional status that change with reproduction can
influence the quality of the early instar nymphs and adults
and result in a lower parasitisation rate, a higher sex ratio,
and a longer developmental time. The higher quality of the
intermediate host ages results in more aphids being parasitised, a higher female-biased sex ratio, and shorter developmental time. Female parasitoids will probably use suboptimal hosts when their availability, either in terms of
accessibility or abundance, makes them profitable even
though individuals using these resources may suffer in
their individual fitness. This study clearly stresses the need
to incorporate the diversity of trade-offs existing between
different level parasitoid and host life-history traits (physiological and behavioural characteristics) in the prediction
of the host–parasitoid interactions.

Acknowledgements
This study was supported by Ministe`re de la Re´gion wallonne – DGTRE Division de la Recherche et de la
Coope´ration scientifique. The authors are grateful to
V. Cambier for providing the artificial diet.
References
Abbott, W.S. (1925) A method of computing the effectiveness of an
insecticide. Journal of Economic Entomology, 18, 265–267.
Beckage, N.E. & Gelman, D.B. (2004) Wasp parasitoid disruption
of host development: implications for new biologically based
strategies for insect control. Annual Review of Entomology, 49,
299–330.
Bell, H.A., Marris, G.C., Smethurst. F. & Edwards, J.P. (2003) The
effect of host stage and temperature on selected developmental
parameters of the solitary endoparasitoid Meteorus gyrator

#

(Thun.) (Hym., Braconidae). Journal of Applied Entomology,
127, 332–339.
Bertschy, C., Turlings, T.C.J., Bellotti, A. & Dorn. S. (2000) Host
stage preference and sex allocation in Aenasius vexans, an encyrtid parasitoid of the cassava mealybug. Entomologia experimentalis et applicata, 95, 283–291.
Brough, C.N., Dixon, A.F.G. & Kindlmann, P. (1990) Pattern of
growth and fat content of somatic and gonadal tissues of virginoparae of the vetch aphid, Megoura viciae Buckton.
Entomologia experimentalis et applicata, 56, 269–275.
Cambier, V., Hance, Th. & De Hoffmann, E. (2001) Effects of
1,4-Benzoxazin-3-one derivatives from maize on survival and
fecundity of Metopolophium dirhodum (Walker) on artificial
diet. Journal of Chemical Ecology, 27, 359–370.
Charnov, E.L., Los-den Hartogh, R.L., Jones, W.T. & Van Den
Assem, J. (1981) Sex ratio evolution in a variable environment.
Nature, 289, 28–33.
Charnov, E.L. & Skinner, S.W. (1985) Complementary approaches
to the understanding of parasitoid oviposition decisions.
Environmental Entomology, 14, 383–391.
Chau, A. & Mackauer, M. (2000) Host-instar selection in the aphid
parasitoid Monoctonus paulensis (Hymenoptera: Braconidae,
Aphidiinae): a preference for small pea aphids. European
Journal of Entomology, 97, 347–353.
Chau, A. & Mackauer, M. (2001) Host-instar selection in the aphid
parasitoid Monoctonus paulensis (Hymenoptera: Braconidae,
Aphidiinae): assessing costs and benefits. Canadian
Entomologist, 133, 549–564.
Fox, P.M., Thurston, R. & Pass, B.C. (1967) Notes on Myzus
persicae (Homoptera: Aphididae) as host for Aphidius smithi
(Hymenoptera: Braconidae). Annals of the Entomological
Society of America, 60, 708–709.
Gerling, D., Roitberg, B.D. & Mackauer, M. (1990) Instar-specific
defense of the pea aphid, Acyrthosiphon pisum: influence on
oviposition success of the hymenopterous parasite Aphelinus
asychis. Journal of Insect Behaviour, 3, 501–514.
Godfray, H.C.J. (1994) Parasitoids: Behavioural and Evolutionary
Ecology. Princeton University Press, Princeton, New Jersey.
Hardy, I.C.W. (2002) Sex Ratios: Concepts and Research Methods.
Cambridge University Press, Cambridge.
Harvey, J.A., Bezemer, T.M., Elzinga, J.A. & Strand, M.R. (2004)
Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size.
Ecological Entomology, 29, 35–43.
Harvey, J.A., Kadash, K. & Strand, M.R. (2000) Differences in
larval feeding behaviour correlate with altered developmental
strategies in two parasitic wasps: implications for the size–fitness
hypothesis. Oikos, 88, 621–629.
Harvey, J.A. & Strand, M.R. (2002) The developmental strategies
of endoparasitoid wasps vary with host feeding ecology.
Ecology, 83, 2439–2451.
Hu, J.S., Gelman, D.B. & Blackburn, M.B. (2002) Growth and
development of Encarsia formosa (Hymenoptera: Aphelinidae)
in greenhouse whitefly, Trialeurodes vaporariorum (Homoptera:
Aleyrodidae): effect of host age. Archives of Insect Biochemistry
and Physiology, 49, 125–136.
Hu, J.S., Gelman, D.B. & Blackburn, M.B. (2003) Age-specific
interaction between the parasitoid, Encarsia formosa and its
host, the silverleaf whitefly, Bemisia tabaci (strain B). Journal
of Insect Science, 3, 1–10.
Islam, K.S., Perera, H.A.S. & Copland, M.J.W. (1997) The effects
of parasitism by an encyrtid parasitoid, Anagyrus pseudococci on
the survival, reproduction and physiological changes of the

2005 The Royal Entomological Society, Ecological Entomology, 30, 473–479

Host age quality and parasitoid fitness
mealybug, Planococcus citri. Entomologia experimentalis et
applicata, 84, 77–83.
Jones, W.A. & Greenberg, S.M. (1998) Suitability of Bemisia
argentifolii (Homoptera: Aleyrodidae) instars for the parasitoid
Eretmocerus mundus (Hymenoptera: Aphelinidae). Biological
Control, 27, 1569–1573.
King, B.H. (1987) Offspring sex ratios in parasitoid wasps.
Quarterly Review of Biology, 62, 367–377.
Kouame, K.L. & Mackauer, M. (1991) Influence of aphid size, age
and behaviour on host choice by the parasitoid wasp Ephedrus
californicus – a test of host-size models. Oecologia, 88, 197–203.
Kouame´, K.L. & Mackauer, M. (1992) Influence of starvation on
development and reproduction in apterous virginoparae of the pea
aphid, Acyrthosiphon pisum. Canadian Entomologist, 124, 87–95.
Lawrence, P.O., Baranowski, R.M. & Greany, P.D. (1976) Effect
of host age on development of Biosteres (¼Opius) longicaudatus,
a parasitoid of the Caribbean fruit fly, Anastrepha suspensa.
Florida Entomologist, 59, 33–39.
Li, B. & Mills, N. (2004) The influence of temperature on size as an
indicator of host quality for the development of a solitary koinobiont parasitoid. Entomologia experimentalis et applicata, 110,
249–256.
Lin, L.A. & Ives, A.R. (2003) The effect of parasitoid host-size preference on host population growth rates: an example of Aphidius
colemani and Aphis glycines. Ecological Entomology, 28, 542–550.
Liu, S.S. (1985) Development, adult size and fecundity of Aphidius
sonchi reared in two instars of its aphid host, Hyperomyzus
lactucae. Entomologia experimentalis et applicata, 37, 41–48.
Liu, S.S., Morton, R. & Hughes, R.D. (1984) Oviposition preference of a hymenopterous parasite for certain instars of its aphid
host. Entomologia experimentalis et applicata, 35, 249–254.
Mackauer, M. (1986) Growth and developmental interactions in
some aphids and their hymenopterous parasites. Journal of
Insect Physiology, 32, 275–280.
Nicol, C.M.Y. & Mackauer, M. (1999) The scaling of body size and
mass in a host parasitoid association: influence of host species
and stage. Entomologia experimentalis et applicata, 90, 83–92.
Pandey, S. & Singh, R. (1999) Host size induced variation in sex
ratio of an aphid parasitoid Lysiphlebia mirizai. Entomologia
experimentalis et applicata, 90, 61–67.
Rakhshani, E., Talebi, A.A., Kavallieratos, N. & Fathipour, Y.
(2004) Host stage preference, juvenile mortality and functional
response of Trioxys pallidus. Biologia, 59, 197–203.
Roitberg, B.D., Boivin, G. & Vet, L.E.M. (2001) Fitness, parasitoids, and biological control: an opinion. Canadian
Entomologist, 133, 429–438.

#

479

SAS Institute Inc. (1990) SAS/STAT Users Guide, Release 6.12
Edition. SAS Institute Inc., Cary, North Carolina.
Sequeira, R. & Mackauer, M. (1993) The nutritional ecology of a
parasitoid wasp, Ephedrus californicus Baker (Hymenoptera:
Aphidiidae). Canadian Entomologist, 125, 423–430.
Srivastava, M. & Singh, R. (1995) Sex ratio adjustment by a
koinobiotic parasitoid Lysiphlebus delhiensis subba Rao &
Sharma (Hymenoptera: Aphidiidae) in response to host size.
Biological Agriculture and Horticulture, 12, 15–28.
Stadler, B. & Mackauer, M. (1996) Influence of plant quality
on interactions between the aphid parasitoid Ephedrus californicus (Hymenoptera: Aphidiidae) and its host, Acyrthosiphon
pisum (Homoptera: Aphididae). Canadian Entomologist, 128,
27–39.
Tripathi, R.N. & Singh, R. (1990) Fecundity, reproductive rate,
intrinsic rate of natural increase of an aphidiid parasitoid
Lysiphlebia mirzai. Entomophaga, 35, 601–610.
Villagra, C.A., Ramirez, C.C. & Niemeyer, H. (2002) Antipredator
responses of aphids to parasitoids change as a function of aphid
physiological state. Animal Behaviour, 64, 677–683.
Vinson, S.B. (1972) Effect of the parasitoid Campoletis sonorensis
on the growth of its host, Heliothis virescens. Journal of Insect
Physiology, 18, 1509–1514.
Vinson, S.B. (1990) Physiological interactions between the host
genus Heliothis and its guild of parasitoid. Archives of Insect
Biochemistry and Physiology, 13, 63–81.
Waage, J.K. (1982) Sex ratio and population dynamics of natural
enemies – some possible interactions. Annals of Applied Biology,
101, 154–164.
Walker, A.M. & Hoy, M.A. (2003) Responses of Lipolexis oregmae
(Hymenoptera: Aphidiidae) to different instars of Toxoptera
citricida (Homoptera: Aphididae). Journal of Economical
Entomology, 96, 1685–1692.
Weisser, W.W. (1994) Age-dependent foraging behaviour and host
instar preference of the aphid parasitoid Lysiphlebus cardui.
Entomologia experimentalis et applicata, 70, 1–10.
Weisser, W.W. (1995) Within patch foraging behaviour of the
aphid parasitoid Aphidius funebris: plant architecture, host behaviour, and individual variation. Entomologia experimentalis et
applicata, 76, 133–141.
Wellings, P.M., Morton, R., Hart, P.J. (1986) Primary sex-ratio
and differential progeny survivorship in solitary haplo-diploid
parasitoids. Ecological Entomology, 11, 341–348.

Accepted 18 March 2005

2005 The Royal Entomological Society, Ecological Entomology, 30, 473–479


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