Eur. J. Entomol. 98: 277-282, 2001
ISSN 1210-5759
Large larvae of a flush-feeding moth (Epirrita autumnata, Lepidoptera:
Geometridae) are not at a higher risk of parasitism: implications for the moth’s
life-history
Tiit TEDER12*and Toom as TAMMARU13
1Institute ofZoology and Hydrobiology, Vanemuise 46, Tartu University, 51014 Tartu, Estonia;
2Section ofEcology, Department ofBiology, University ofTurku, FIN-20014 Turku, Finland;
institute ofZoology and Botany, Riia 181,51014 Tartu, Estonia
Key words. Body size, parasitism risk, parasitoids, phenology, preference-performance linkage, life-history, Epirrita autumnata,
Geometridae.
Abstract. The effect of larval body size of Epirrita autumnata (Lepidoptera, Geometridae) on the risk of parasitism was studied in a
field experiment. The experiment involved three pairwise exposures of different larval instars to parasitoids. Three hymenopteran
species were responsible for most of the parasitism. Parasitism risk was found to be host-instar independent. This result was consis
tent across parasitoid species and experiments. The results suggest that host use by larval parasitoids cannot constrain selection for
larger body size in E. autumnata. However, high mortality due to parasitism may select for a short developmental period (the slowgrowth/high-mortality hypothesis), and smaller body sizes as a by-product. A strong selective effect of parasitism on the timing of
larval development in E. autumnata is also unlikely. The larger was the host, the larger was the adult size of the parasitoid and the
shorter its development time (for one species). We suggest that the lack of a preference-performance linkage in the system studied
may be related to the time stress associated with the short phenological window ofhost vulnerability.
INTRODUCTION
In insects, fecundity is often strongly correlated with
the body size of the female (Honek, 1993). Such a corre
lation implies a persistent selection for large adult size.
We are thus justified in asking what selective forces bal
ance this obvious fecundity advantage, and prevent a con
tinuous evolutionary increase in insect body size. The
answer is intuitively related to elevated mortality risks,
but it is not necessarily a trivial one (Leimar, 1996; Tammaru, 1998). In particular, for Epirrita autumnata (Bork
hausen) (Lepidoptera: Geometridae), an optimality
analysis (Tammaru, 1998) showed that realistic values of
constant, body-size independent larval mortality rates and
seasonal changes in host plant quality are insufficient to
explain why these insects do not grow larger by pro
longing their larval growth. However, if large larvae are
more likely to be killed, the resulting positively body-size
dependent mortality might be the ecological factor
capable of balancing the fecundity advantage of large
body size.
Parasitoids are often one of the main causes of mor
tality in herbivorous insects, and affect various ecological
traits of their hosts. The traits affected include food plant
preference (Ohsaki & Sato, 1990, 1994; Bjorkman et al.,
1997), and timing of life-history switches (McGregor,
1996). Numerous laboratory experiments, and some field
studies have shown that parasitism risk may depend on
host body size, and the dependence being often mediated
via behavioural responses of the parasitoids (e.g. van
Alphen & Drijver, 1982; Nealis, 1990; Sait et al., 1997).
Either small or large hosts may experience a higher risk
of parasitism in different host-parasitoid systems; adap
tive explanations for these patterns are largely based on
differences in parasitoid life-histories, especially koinobiosis and idiobiosis (Harvey, 1996, Harvey et al., 2000;
Strand, 2000). Host-size dependent parasitism is usually
discussed from a parasitoid’s perspective, while the
importance of this phenomenon in shaping the life-history
of the host has received markedly less attention (see,
however, Solbreck et al., 1989; Teder et al., 1999).
To assess the role of parasitism as a selective agent
acting on host body size, we conducted field experiments
and recorded the incidence of parasitism of different sized
larvae of E. autumnata. We asked if the risk of sizedependent parasitism could balance the high fecundity
advantage of large female size (Tammaru et al., 1996). In
addition, the design of the experiments enabled us to
assess whether parasitism affected the phenology of the
herbivore. Finally, we briefly discuss whether parasitoids
benefit from size-selective use of the host in the system
studied, and propose an explanation for the observed pat
terns of size selectivity.
MATERIAL AND METHODS
Study species
Epirrita autumnata, the autumnal moth, is a medium-sized
holarctic lepidopteran known for its tendency to achieve out
break levels of abundance in northern and mountainous Fennoscandia (Tenow, 1972; Haukioja et al., 1988; Ruohomaki et
* Corresponding author. Institute ofZoology and Botany, Riia 181, 51014 Tartu, Estonia; e-mail: tiit@zbi.ee
277
al., 2000). The populations are stable elsewhere. The species has
a univoltine life cycle. The eggs overwinter and hatch in spring.
The solitary, cryptic larvae feed on deciduous trees and shrubs.
E. autumnata is a typical flush-feeder (=spring feeder): its larval
performance is critically dependent on the phenological stage of
the foliage (Ayres & MacLean, 1987; Kaitaniemi et al., 1998;
Kause et al., 1999). Larval development lasts for about one
month and consists invariably of 5 larval instars (Tammaru,
1998) . A 5th instar larva may reach = 40 mm in length and 150
mg in weight, the size gain per instar being roughly two-fold for
length, and four-fold for weight. They develop relatively syn
chronously, but larvae of two or three different instars may still
occur at the same time. Pupation occurs in the ground in early
June, and the adults emerge in early autumn.
Larvae of E. autumnata are attacked by several hymenopteran
parasitoids (Ruohomaki, 1994; Kaitaniemi & Ruohomaki, 1999;
Teder et al., 2000). The most common encountered in the pre
sent study were the three solitary koinobiont species: Protapanteles immunis (Haliday) and Cotesia jucunda (Marsh.) (both
Braconidae), and an unidentified species of Campoletis (Ichneumonidae). The two former species (2.5-3.5 mm in length) are
bivoltine generalists parasitising various geometrids (Tobias,
1986). Their development from oviposition to pupation (i.e.
emergence from host larvae) takes about 3 weeks. The body
length of the Campoletis sp. is 6-8 mm, and irrespective of the
host instar parasitised, it always emerges from the prepupa of its
host.
Study areas and sites
The two-year (1998-1999) experimental field study was car
ried out in two forested areas outside the range where outbreaks
of E. autumnata occur: 1) about 20-30 km northeast of the town
of Turku (60°15’N, 22°25’E), southwestern Finland (1998), and
2) near the town of Tartu (58°22’N; 26°45’E), southeastern
Estonia (1999). The experiments were conducted at a total of
twelve sites, four sites in 1998 (within an area = 10 km2) and
eight in 1999 (within an area of = 2 km2). Most of the study sites
were mixed coniferous forests, dominated by Pinus sylvestris L.
or Picea abies (L.) Karsten with birches (Betula pubescens
(Ehrhart) and also B. pendula (Roth) in some sites) growing in
the understory.
Experiment design
To determine if parasitoids preferably attack certain larval
instars of E. autumnata, three separate host choice experiments
were conducted. At each of the 12 study sites, 16-20 birches
(mostly B. pubescens, occasionally B. pendula), 1-1.8 m in
height, separated by distances of 5 to 10 m, were chosen.
Laboratory-reared larvae of two different instars were released
onto the experimental trees. Three combinations of instars were
used; larvae moulting either into the 1) second and third instars
(conducted at four sites in 1998), 2) second and fourth instars
(four sites in 1999), or 3) third and fourth instars (four sites in
1999) . The numbers of larvae of each instar released were equal
on each tree (e.g. 5 second and 5 third instar larvae). The total
number of larvae used in the three experiments was 1452. In
each experiment, two densities were created, with ten (5+5) and
four larvae (2+2) on 40 % and 60 % of the trees, respectively.
These host densities correspond to those during minor and mod
erate outbreaks of E. autumnata, and greatly exceeded the
natural background densities in the study area. Using two dif
ferent densities was motivated by the original idea, which was
to study the effects of host density, as an additional factor, on
size-selectivity in host use. However, a subsequent data analysis
showed that larval density did not affect the patterns of parasit
278
ism. For the sake of clarity of presentation, we do not incorpo
rate this factor in the further analyses.
Larvae were exposed to parasitoids for a period corre
sponding to the duration of about one instar (7-8 days). The
experiments were performed at the time when laboratory-reared
larvae were approximately of the same age as those in the field.
After the exposure period, the released larvae were collected
and reared in the laboratory until they pupated or a parasitoid
emerged. For the parasitoids the dates of emergence and the
length of hind tibia, as measure of body size, were recorded.
Parasitoid size was used to assess the profitability of different
host instars for the parasitoids.
Data analysis
To determine if risk of parasitism differed for different larval
instars, the data were analysed using generalised linear models
(SAS PROC GENMOD, SAS Institute Inc., 1995). Parasitism
status of a host (parasitised/unparasitised) was treated as the
binary dependent variable, instar (second and third; second and
fourth; third and fourth instars in the respective analyses) and
study site as the categorical independent variables. Binomial
distribution was assumed and logit was used as the link
function. In additional analyses, parasitism caused by the most
common species of parasitoids was considered separately.
Finally, an analogous analysis of the total parasitism was per
formed with the data from the three experiments combined.
Larval instar was then coded on the relative binary scale
(younger instar/older instar) in each particular experiment, irre
spective of the instars involved.
Larvae that were not recovered from the field (44 % of the
larvae, pooled over study sites and experiments) and those that
died in the laboratory before pupation or emergence of a parasi
toid (about 10 % of the larvae) were not included in the statis
tical analyses. To analyse the effect of host instar on adult body
size of parasitoids, a two-way analysis of variance was applied,
with parasitoid sex as an additional factor. Student t-test was
applied to test the effect of host instar on parasitoid develop
ment time.
RESULTS
Distribution of parasitism among larval instars
Parasitism rate was highly variable between study sites,
varying from a few to about 75 percent. Species composi
tion of the parasitoids was also very differ (Table 1).
Parasitism risk was host-instar independent when parasi
toids were given a choice between second and third instar
larvae (Table 1a, 2a). Consistently, the levels of para
sitism by each of the two dominant parasitoids (C.
jucunda and P. immunis) did not differ between instars
(DF = 1, x2 = 0.03, p = 0.87, and DF = 1, X = 1-96,
p = 0.16, respectively). Other parasitoids were present in
numbers too low for a meaningful analysis.
The most numerous parasitoid in the Estonian experi
ments, Campoletis sp., showed no preference for a par
ticular host instar, neither when second and fourth instars,
nor when third and fourth instars were simultaneously
exposed (DF = 1, X = 0.16, p = 0.69, and DF = 1,
X = 1.27,p = 0.26, respectively). Other parasitoids were
too scarce to analyse separately. The levels of total para
sitism did not differ significantly between instars in the
experiment in which second and fourth instars were
exposed to parasitoids (Table 1b, 2b). However, there
was a slightly lower level of total parasitism of fourth
Table 1. Percentage parasitism of two simultaneously exposed larval instars of E. autumnata. Sample sizes refer to the numbers
oflarvae recovered (by instar) and used in the analyses.
Percentage parasitism Percentage parasitism by Percentage parasitism by
Total percentage para
Site
by Campoletis sp.
P. immunis
C.jucunda
sitism
(sample size)
a) 2nd and 3rd instars (Finland, 1998)
3rd
2nd
3rd
2nd
3rd
2nd
3rd
2nd
1 (41/41)
2.4
2.4
2.4
2.4
2 (34/48)
17.6
8.3
17.6
8.3
38.9
43.6
38.9
43.6
3 (36/39)
2.3
0
2.3
0
4.5
0
4 (44/49)
b) 2nd and 4th instars (Estonia, 1999)
2nd
4th
2nd
4th
2nd
4th
2nd
4th
5 (12/26)
8.3
0
8.3
3.8
3.8
16.7
22.2
18.5
11.1
0
11.1
0
44.4
18.5
6 (9/27)
7 (8/14)
12.5
50
12.5
0
25
50
8 (8/28)
60.7
12.5
3.6
87.5
64.3
75
c) 3rd and 4th instars (Estonia, 1999)
3rd
4th
3rd
4th
3rd
4th
3rd
4th
9 (39/43)
2.6
2.6
0
4.7
7.7
4.7
10 (37/41)
18.9
12.2
24.3
12.2
11 (23/34)
47.8
29.4
60.9
35.3
8.7
2.9
12 (14/30)
35.7
36.7
40
57.1
-
instar larvae when they were exposed with third instar
larvae (Table lc, 2c). This difference was due to parasitoids other than Campoletis sp. (a few C. jucunda among
these).
Consistently, an analysis of the data pooled over the
experiments did not support the notion that the larger
larvae are more likely to be parasitised, rather the reverse.
The corresponding tendency, however only approached
statistical significance (Table 2d). Calculated for the
entire data set, 23.6 % of the younger vs 20.0 % of the
older larvae were parasitised (N = 725). The 95 % confi
dence limits of the ratio of these values (lower 0.89,
upper l .56, SAS PROC FREQ CLI option) gives a simple
but illustrative power estimate of this analysis.
Effect ofhost instar on parasitoid development
Body size of the offspring of Campoletis sp. signifi
cantly increased with host instar (two-way ANOVA with
parasitoid sex as an additional factor: F2, 62 = 8.20, p <
0.001; all three pairwise contrasts between instars were
significant; sites pooled). The average lengths of the hind
tibia of parasitoids from second, third and fourth instars
were 1.87, 1.94 and 1.98 mm, respectively. Similarly,
body size of C. jucunda significantly increased with host
instar (one-way ANOVA: Fi, 16 = 7.10,p = 0.02; females
only, only one male emerged). The average lengths of the
hind tibia of C. jucunda that developed in the hosts’
second and third instars were 0.99 mm and 1.02 mm,
respectively. The number of C. jucunda emerging from
fourth instar hosts was too low for analysis. Most indi
viduals of P. immunis, the third most common parasitoid,
failed to emerge from their cocoons. The effect of host
instar on their body size could thus not be estimated.
Host instar strongly affected developmental period in
Campoletis sp. but not in C. jucunda or P. immunis. In
Campoletis, exact timing of parasitoid emergence could
not be recorded due to the below-ground pupation of the
host. However, irrespective of the host instar parasitised,
parasitoid larvae invariably emerged from host prepupae.
This allows us to conclude that parasitising a younger
instar larva would add an extra week to the parasitoid’s
development time. In contrast, there was no effect ofhost
instar on the parasitoid’s development time in the
remaining two species (C. jucunda: t = 0.44, DF = 29,
p = 0.67; P. immunis: t = 0.09, DF = 11,p = 0.93).
DISCUSSION
There was no evidence of a positively size-dependent
parasitism risk in E. autumnata. The only experiment
where a significant difference in parasitism rates was
detected, suggested the opposite: the smaller larvae suf
fered more parasitism (Table 1, 2c). A combined analysis
of the effects of host size on the incidence of parasitism
also indicated a greater risk for the smaller larvae rather
than vice versa (Table 2d). Risk of larval parasitism is
thus not likely to balance the strong fecundity advantage
(Tammaru et al., 1996) of large size in females of E.
autumnata.
However, even if mortality due to larval parasitism
cannot alone provide a sufficient adaptationist explana
tion for body size in E. autumnata, parasitoids may still
be a factor determining the cost of large adult size.
According to the slow-growth/high-mortality hypothesis,
longer developmental periods often imply higher vulner
ability to predation and/or parasitism (Loader &
Damman, 1991; Haggstrom & Larsson, 1995; Benrey &
279
Table 2. Results of analyses of the effect of host instar (rela
tive size in d) - see text) on the incidence of total parasitism.
Source
DF
P
X
al 2nd and 3rd instars
Site
3
62.96
<0.001
Instar
1
0.54
0.46
b) 2nd and 4th instars
3
36.38
<0.001
Site
1
0.16
Instar
1.99
c) 3rd and 4th instars
3
46.62
<0.001
Site
1
Instar
6.77
0.009
d) All experiments combined
2
Experiment
30.13
<0.001
1
Size
3.55
0.06
Denno, 1997). In terms of daily survival, the larval stage
is definitely the most vulnerable one in the life cycle of E.
autumnata (Tanhuanpaa et al., 1999, 2001). Mortality of
larvae attributable to parasitoids may reach levels (Ruohomaki, 1994; Teder et al., 2000, and this study) that
exceed mortalities in other stages of the life cycle com
bined. This should favour short developmental periods.
In contrast to parasitism, large larvae may be at a
greater risk of bird predation than small. In particular,
Tanhuanpaa et al. (2001) showed that mortality due to
bird predation was considerably higher during late instars
than early instars. However, the design of these experi
ments does not allow the separation of the effects of time
and size: larger larvae occurred later in the season when,
e.g., the foraging activity of birds could have been higher.
The effect of other principal predators, ants and spiders,
was shown to be spatially restricted and presumably of
less importance.
The present study also suggests that parasitism creates
no significant selective pressure on the phenology of the
larval stage in E. autumnata. In particular, our experi
ments may be alternatively interpreted as exposing larvae
of different ages. In this context the results suggest that
neither the larvae that are ahead nor behind the average in
development suffer from increased levels of parasitism.
These results complement those of Kaitaniemi and Ruohomaki (1999) who showed that the flight period of most
E. autumnata parasitoids exceeds the larval period of the
host: larvae reared outside the normal time schedule did
not escape parasitism. Combined with the results of the
present study, this observation allows us to exclude para
sitism as an important selective force acting on the timing
of larval development in E. autumnata. The need to syn
chronise larval development with suitable host plant phe
nology is apparently a much stronger determinant of the
optimal hatching date of the larvae (Ayres & MacLean,
1987; Kaitaniemi et al., 1998).
Parasitoids appeared to benefit from developing in late
instars of E. autumnata: body size of adult parasitoids
was positively correlated with host size. Additionally,
Campoletis sp. showed considerable host-instar
280
dependent variation in development time. Both these vari
ables have important fitness consequences: body size is
frequently a good indicator of fecundity (Harvey et al.,
1994; Sequeira & Mackauer, 1994; Ellers et al., 1998),
while a short development time may imply reduced risk
of mortality during preimaginal stages (Price, 1972; Slansky, 1986; Godfray, 1994). The latter is apparently true
for E. autumnata parasitoids as well: high predation rates
of moths during the larval stage (Tanhuanpaa et al., 2001)
imply a high mortality risk for juvenile parasitoids.
However, different profitabilities of parasitising
differently-aged larvae did not lead to a preference
performance linkage, a phenomenon demonstrated in
numerous laboratory studies on insect parasitoids (e.g.
van Alphen & Drijver, 1982; Liu et al., 1984, Liu, 1985;
Hopper, 1986).
Parasitoids may use suboptimally sized hosts for a
variety of reasons, e.g. because of their size-dependent
apparency (van Alphen & Drijver, 1982) or behavioural
defence (van Alphen & Drijver, 1982; Brodeur et al.,
1996; Harvey, 1996; Chau & Mackauer, 2000), or agedependent survival in hosts (especially koinobiont parasi
toids: Driessen et al., 1991; Sequeira & Mackauer, 1994;
Brodeur & Vet, 1995). Although this study did not
address the question of the causes of the non-selective
host use, we would like to highlight a potential explana
tion specific to the system studied. In particular, the
larvae of flush feeders like E. autumnata pass quickly and
synchronously through the larval stage. The parasitoids of
these moths are thus likely to be time-rather than egglimited and the resulting time-stress should favour lower
selectivity (cf. Jaenike, 1990; Mayhew, 1997, for exam
ples with herbivorous insects). Moreover, in E. autum
nata, high levels of larval parasitism (Teder et al., 2000,
and this study) suggest strong intra- and interspecific
exploitative competition among parasitoids that further
contributes to the ephemeral character of the resource for
parasitoids. This, in turn, should select for high oviposition rates, and reduced selectivity as a correlated
response.
ACKNOWLEDGEMENTS. We thank Grant Gentry, Jeffrey A.
Harvey, Antti Kause and an anonymous referee for their helpful
comments, and Tommi Andersson, Rein Karulaas, Pille Koiv,
Kai Ruohomaki, Siiri-Lii Sandre and Miia Tanhuanpaa for field
assistance. The study was partly supported by the Estonian Sci
ence Foundation (grant no. 4076) and the Kone Foundation.
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ReceivedNovember 16, 2000 ; revisedMay 18, 2001; accepted June 21, 2001