Oecologia (2005) 144: 353–361
DOI 10.1007/s00442-005-0076-6
E C O PH Y SI OL O G Y
Carol L. Boggs Æ Kimberly D. Freeman
Larval food limitation in butterflies: effects on adult resource
allocation and fitness
Received: 2 September 2004 / Accepted: 28 February 2005 / Published online: 11 May 2005

Springer-Verlag 2005
Abstract Allocation of larval food resources affects adult
morphology and fitness in holometabolous insects. Here
we explore the effects on adult morphology and female
fitness of larval semi-starvation in the butterfly Speyeria
mormonia. Using a split-brood design, food intake was
reduced by approximately half during the last half of the
last larval instar. Body mass and forewing length of
resulting adults were smaller than those of control ani-
mals. Feeding treatment significantly altered the allo-
metric relationship between mass and wing length for
females but not males, such that body mass increased
more steeply with wing length in stressed insects as
compared to control insects. This may result in changes
in female flight performance and cost. With regard to
adult life history traits, male feeding treatment or mating
number had no effect on female fecundity or survival, in
agreement with expectations for this species. Potential
fecundity decreased with decreasing body mass and
relative fat content, but there was no independent effect
of larval feeding treatment. Realized fecundity decreased
with decreasing adult survival, and was not affected by
body mass or larval feeding treatment. Adult survival
was lower in insects subjected to larval semi-starvation,
with no effect of body mass. In contrast, previous lab-
oratory studies on adult nectar restriction showed that
adult survival was not affected by such stress, whereas
fecundity was reduced in direct 11 proportion to the
reduction of adult food. We thus see a direct impact of
Communicated by Jay Rosenheim
C. L. Boggs (&) Æ K. D. Freeman
Center for Conservation Biology, Department of Biological
Sciences, Stanford University, Stanford, CA 94305-5020, USA
E-mail: cboggs@stanford.edu
Fax: +1-650-7235920
C. L. Boggs (&) Æ K. D. Freeman
Rocky Mountain Biological Laboratory, Crested Butte,
CO 81224, USA
Present address: K. D. Freeman
Department of Emergency Medicine, UCSF Fresno, Fresno,
CA 93702, USA
larval dietary restriction on survival, whereas fecundity
is affected by adult dietary restriction, a pattern remi-
niscent of a survival/reproduction trade-off, but across a
developmental boundary. The data, in combination with
previous work, thus provide a picture of the intra-spe-
cific response of a suite of traits to ecological stress.
Keywords Fecundity Æ Nymphalidae Æ Stress Æ
Survival Æ Trade-offs
Introduction
In holometabolous insects, adult morphology and fitness
are influenced by the availability and allocation of re-
sources from larval and adult feeding. Larval feeding
first supports growth of the larval insect. At some point,
growth stops, and accumulated larval nutrients are
allocated during metamorphosis into the adult body
plan. The resulting adult individual has a given body size
and given allometric relations among various body
parts, such as wings, flight muscles, ovaries, and so on.
Additionally, some nutrients may be allocated to
‘‘storage‘’, in the form of lipid or storage proteins for
example. The adult insect itself may feed (although not
all species do). The combination of incoming adult
nutrients (‘‘income’’) and stored larval nutrients (‘‘cap-
ital reserves’’) is then used in specific proportions to
support the adult functions of reproduction, survival,
and dispersal.
Variation in the quality or quantity of larval or adult
food can result in alterations to the normal pattern of
allocation. We can thus vary the larval or adult diets to
gain insight into the organization of allocation, by
examining the resulting changes in life history and/or
morphological traits. Some changes in quality or quan-
tity of food may have severe impacts on life history
traits, particularly if larval and adult diets provide dif-
ferent nutrients (e.g., Boggs and Ross 1993; O’Brien
et al. 2005). In contrast, other changes in quality or
354
quantity of food may have little or no effect. This would
occur, for example, if temporary decreases in adult food
availability are buffered by increased usage of larval
reserves (with later compensatory feeding by adults), or
if nutrients provided to the female by males at mating
can compensate for decreased availability of female
reproductive stores from larval feeding. Thus, under-
standing the effects of resource variation can aid in
predicting the extent to which a species’ life history traits
are buffered against environmental variation, with con-
sequent buffering of fitness and population dynamics
(Boggs 2003).
The allocation fate of larval resources during meta-
morphosis is particularly critical to the insect’s fitness,
since it both determines adult morphology and con-
tributes to adult life history traits, and thence fitness as
outlined above. Such allocation results in integrated
suites of specific adult morphological, life history, and
foraging traits. These have been documented among
species for Lepidoptera and Hymenoptera (Boggs 1981;
Boggs 1986; Karlsson and Wickman 1989; Rivero et al.
2001). Increased allocation of larval resources to body
(as opposed to reproduction) is associated with quali-
tatively and quantitatively richer adult diets, increased
survival, an increasing reliance on adult food for
reproduction and a more drawn out age-specific fecun-
dity pattern.
However, such adult trait suites reflecting trade-offs
associated with larval resource allocation have not been
studied intra-specifically to the same extent. Our
understanding is more or less limited to the observation
that a reduction in larval food quality or quantity gen-
erally results in reduced adult body size and fat content
with consequent negative effects on fecundity (e.g.,
Scriber and Slansky 1981; Fischer and Fiedler 2001;
Ernsting et al. 1992; Awmack and Leather 2002), or on
male reproductive success (e.g., Carroll 1994; Delisle and
Hardy 1997). While extremely useful, this information
does not yet provide insight into the organization of
allocation as a whole within any one holometabolous
organism, or the integrated suites of adult life history
and morphological traits that result.
Here we document the effects of larval food restric-
tion in a butterfly, Speyeria mormonia Edwards (Lepi-
doptera: Nymphalidae) on resulting adult morphology
and fitness parameters. As context, we already have
considerable information concerning the effects of adult
food restriction on reproduction and survival in this
species. Reproduction declines linearly with reductions
in adult nectar intake, with oocytes resorbed and their
nutrients re-allocated (Boggs and Ross 1993). Adult
survival is unaffected by adult nectar deprivation (down
to 33% of ad libitum feeding). The observed effect on
reproduction is reinforced by radiotracer and stable
isotope studies showing that 80% of egg carbon is de-
rived from adult nectar feeding (Boggs 1997; O’Brien
et al. 2004), even including synthesis of egg non-essential
amino acids from nectar carbon (O’Brien et al. 2005).
Most of the larval carbon in eggs is in the form of
essential amino acids (O’Brien et al. 2002; O’Brien et al.
2004, 2005).
Given the above information, we outline several
predictions and questions concerning the effects of larval
nutrient deprivation on adult morphology and fitness. In
keeping with results on other species, we first expect that
adults resulting from a larval nutrient stress treatment
would have smaller body mass than those fed an unre-
stricted diet. Second, we expect that those smaller adults
would have a lower reproductive success, based solely on
their smaller size. Third, we expect that the allometric
relationship between wing length and body mass may
change, reflecting either attempts to conserve repro-
ductive potential, or possible changes in wing loading
and ability to disperse out of a ‘‘bad’’ or deteriorating
environment (e.g., Fric and Konvicka 2002). Addition-
ally, we ask two new questions. First, is there an addi-
tional effect of larval nutrient stress treatment on
reproduction, beyond that accounted for by body mass?
This would occur if stress were accompanied by allo-
metric changes in allocation affecting the relationship
between mass and fat reserves or oocyte numbers, for
example. Second, is adult survival affected by larval
nutrient stress treatment, either due to changes in body
mass, or treatment effects independent of body mass?
This could occur for example if there were changes in the
relative proportion of nutrients allocated to body
building and somatic maintenance relative to other
functions. These data give us a more complete picture of
the within-species response of allocation to variation in
the larval and adult food environments, on which to
build a theory of allocation trade-offs.
Materials and methods
Speyeria mormonia is a univoltine butterfly found in
montane-zone meadows in North America. Adults feed
primarily on nectar from Compositae, and males and
older females feed at mud puddles, dung, and carrion
(Boggs and Jackson 1991; Sculley and Boggs 1996;
Boggs and Dau 2004). Larvae feed on Viola spp., after
diapausing over the winter as unfed first instars.
Larvae used in this study were the offspring of 25
females. Those females were caught in August 1995 from
a population near the Rocky Mountain Biological
Laboratory, Gothic, Gunnison County, CO, USA.
Larvae were transported to Stanford University, where
they were maintained in diapause for 4 months, until
December 1995. Larvae were then initially started in
groups of 36–50 individuals of the same family, placed in
net sleeves on potted V. soraria in a greenhouse at 27C
day: 21C night, with a 15:9 light:dark cycle. As larvae
became larger, they were split into smaller groups, down
to 5–10 larvae by mid-last larval instar.
Larvae were allowed ad libitum access to V. soraria
leaves until the middle of the last larval instar. As indi-
viduals reached that development point, larvae from
each family were arbitrarily split into two feeding

treatments, one of which continued with ad libitum ac-
cess (‘‘fed’’ treatment), and the other of which had two
medium sized leaves per five larvae per day (‘‘semi-
starved’’ treatment). In practice, larvae in the semi-
starved treatment received roughly half the amount of
food consumed by larvae in the fed treatment. Given
exponential larval growth, a large fraction of the nutri-
ents from larval feeding are obtained in the last instar
(Scriber and Slansky 1981).
Larvae spent 4–7 days in the semi-starved vs. fed
treatment. Since larvae were reared in groups, it was not
possible to track individual development times reliably.
Variation in treatment time was due in part to differ-
ences in the exact point within the last instar at which
larvae entered the treatment, which should be random
with respect to treatment. Additionally, it is possible
that larvae from the ‘‘semi-starved’’ treatment took
longer to pupation than those in the ‘‘fed’’ treatment
(e.g., Fischer and Fiedler 2001).
We measured the mass of each adult butterfly to the
nearest 0.1 mg in the afternoon of the day of adult
eclosion. We measured the length of each forewing to
the nearest 0.01 cm; winglength is recorded as the larger
of the two wings. Sample sizes for these measurements
for females were 67 individuals in the semi-starved
treatment (21 families, median family size 3, range 1–8)
and 91 individuals in the fed treatment (21 families,
median family size 4, range 1–11). Sample sizes for males
were 121 individuals in the semi-starved treatment (25
families, median family size 4, range 1–16) and 145
individuals in the fed treatment (24 families, median
family size 5, range 3–13).
Adults used in the study of life history parameters
were fed ad libitum on a 1:3 v:v honey:water solution
twice a day. Males were allowed to mature for several
days before being mated. Females were either frozen for
dissection or mated on the day of adult emergence. All
matings were outcrosses. Both ‘‘fed’’ and ‘‘semi-starved’’
females were mated to ‘‘fed’’ males, to assess the effect
on female fitness of female larval treatment. Addition-
ally, ‘‘fed’’ females were mated to both ‘‘fed’’ and ‘‘semi-
starved’’ males, to assess the effect of male larval
treatment. All females were mated only once, as is
generally the case in the field (Boggs 1986). Some males
Table 1 Adult morphological traits. See methods for details of ‘‘semi-starved’’ versus ‘‘fed’’ larval treatments
Treatment
Semi-starved
Males
Body mass (mg) 93.3±17.7 (121)
Forewing length (cm) 2.28±0.14 (121)
Females
Body mass (mg) 106.8±24.0 (66)
Forewing length (cm) 2.35±0.15 (67)
Values are untransformed means ± SD (n). ANOVA included family and larval treatment as category variables and mass was ln-
transformed for the ANOVA
355
were allowed to mate two times, with 2–5 days between
the first and second mating. For all individuals, family
number, mate’s family number, and dates of emergence
and mating were recorded. 19 semi-starved females from
14 families (median family size 1, range 1–3) were mated
and used in the analysis of treatment effects on lifespan
and fecundity, along with 34 fed females from 15 fami-
lies (median family size 2, range 1–4).
Mated females were kept in cages constructed from
glass Coleman lantern tops in the manner of Boggs and
Ross (1993). Eggs were counted and collected daily.
Adult female lifespan was recorded to the nearest day.
We dissected 66 newly emerged females (25 from 15
semi-starved families, median family size 1, range 1–5;
and 41 from 19 fed families, median family size 2, range
1–7) and 28 of the mated females upon death, and
counted the number of eggs in the ovaries. We calculated
the potential fecundity of each female as the sum of the
number of eggs laid (if any) and the number of oocytes.
Potential fecundity at death in mated females reflects
any egg resorption, which occurs under adult nutrient
stress (Boggs and Ross 1993). In addition, we qualita-
tively scored the fat stored in the abdominal cavity on a
scale of 0–2; 0=no fat reserves, 1=some fat reserves,
and 2=abundant fat reserves. Fat was thus measured
relative to body cavity size.
Analysis of variance or covariance using proc GLM
in Systat10 was used to evaluate effects of larval feeding
treatment on adult morphological and life history traits.
Female body mass was natural log transformed for these
analyses. While ‘‘family’’ was included in the statistical
tests as appropriate, we did not use it to explore heri-
tability or gene · environment interactions, since family
sizes were small and ‘‘family’’ includes both common
larval rearing environment and genetic components.
Rather, we used family to simultaneously control
genetics and pre-last instar feeding experience. Allo-
metric relationships are usually defined by a power
function (y=axb). In this case we determined the slope,
b, for body mass on wing length using the natural log
form of the equation (ln y=ln a + b ln x). After testing
for homogeneity of residual variances using an F test, we
tested for the significant differences between regression
slopes, again with an F test.
Fed F df P
118.4±19.8 (142) 130.6 1,236 <0.001
2.44±0.18 (145) 64.4 1,239 <0.001
150.5±21.2 (91 176.4 1,133 <0.001
2.58±0.21 (91) 52.6 1,134 <0.001
356
Results
Adult morphological traits
Body mass and forewing length were significantly smaller
in semi-starved individuals than in those fed ad libitum as
last instar larvae, for both males and females tested
separately using an ANOVA including treatment and
family as independent variables (Table 1). Family had a
significant effect independent of larval treatment on ln
body mass (males: F25,236=2.32, P<0.001; females:
F22,133=2.51, P<0.001), and on wing length in males
(F25,239=1.62, P=0.04) but not females (F22,133=1.05,
P=0.41).
Additionally, for both mass and wing length, sexual
dimorphism was smaller in semi-starved than in fed
individuals. There was a sex · treatment interaction ef-
fect when both sexes were considered together using an
ANOVA including sex, treatment, family and sex ·
Fig. 1 Allometric relationship between body mass and forewing
length for a male and b female Speyeria mormonia butterflies that
were semi-starved (open circle) or fed (open triangle). Regression
lines are body mass = a(winglength)b, with a and b derived from
the natural log form of the equation. Slopes and significance tests
are given in Table 2
treatment (ln body mass: F1,392=12.55, P<0.001; wing
length: F1,396=5.18, P=0.02).
Males and females of both treatments showed strong
allometric relationships between forewing length and
body mass (Fig. 1, Table 2). Given that wing length is a
linear metric and body mass estimates volume, an iso-
metric relationship would yield a slope of 3.0. All sexes
and treatments showed slopes less than 3.0, indicating
lighter bodies than expected for a given wing length
(Table 2).
Within a sex, residual variances were homogeneous
(females: F63,87=1.12, n.s.; males: F119,140=1.24, n.s.),
allowing tests for differences in slopes of the allometric
relationships. For females, individuals semi-starved as
last instar larvae had significantly higher slopes than
those fed ad libitum, indicating body mass decreased
more rapidly with wing length in semi-starved females
(Table 2, Fig. 1). Males showed a similar, but non-sig-
nificant trend (Table 2, Fig. 1).
Adult female life history traits
Neither male larval feeding treatment nor male mating
number had a significant effect on female lifespan,
realized fecundity, or potential fecundity (Table 3).
Likewise, family did not have a significant effect on fe-
male life history traits (lifespan: F20,32=1.62, P=0.11;
realized fecundity: F20,32=0.91, P=0.58; potential
fecundity of mated and virgin females combined:
F21,77=0.44, P=0.98, of mated females: F14,13= 1.26,
P=0.34, or of virgin females: F19,50=0.39, P=0.99).
These factors are therefore not included in the analysis
below.
Female lifespan was significantly greater for individ-
uals fed ad libitum as larvae vs. semi-starved in the last
instar, independent of adult body mass (Fig. 2). Body
mass itself had no significant effect on lifespan.
Female realized fecundity increased with lifespan
(Table 4, Fig. 3). Neither body mass nor female larval
treatment had a significant effect on realized fecundity,
independent of lifespan (Table 4).
Potential fecundity was measured as the sum of
realized fecundity and oocytes remaining in the ovaries
for mated females, and as oocytes in the ovaries for
newly emerged females. Mated females had a signifi-
cantly higher potential fecundity than did newly
emerged females (least squares means ± SE from an
ANCOVA with mating status, ln body mass and female
larval treatment: mated females: 347 ± 20 (n=28);
newly emerged females: 296 ± 14 (n=66); F1,90=4.56,
P=0.04). Since this species emerges with a full comple-
ment of oocytes (Boggs and Ross 1993), this difference
most likely represents detection/ counting error for the
smallest oocytes.
Potential fecundity increased with body mass
(F1,90=3.89, P=0.05; regression: fecundity= 787 +
217·ln body mass, r2=0.23), but female larval feeding
treatment had no effect (F1,90=2.28, P=0.13) when
 357

Table 2 Allometric relationship between body mass and forewing length by sex and treatment, calculated using ln (body mass)=ln a + b ·
ln(forewing length)

Slope 95% CI F df P

Males
Semi-starved 1.21 0.75–1.67 26.7 1,119 <<0.001
Fed 0.95 0.63–1.27 34.4 1,140 <<0.001
Females
Semi-starved 2.20 1.69–2.71 73.4 1,63 <<0.001
Fed 0.65 0.35–0.95 18.3 1,87 <<0.001

F, df, and P are values for the regression within sex and treatment. Slopes differed among treatments within females (F1,150=27.91,
P<0.001), but not males (F1,259=0.86, n.s.)

Table 3 Effect of male larval feeding treatment and male mating number on life history traits of their female mates, using an ANOVA
with male treatment and mating number

Male larval treatment Male mating number

F df P F df P

Female lifespan 0.04 1,48 0.83 0.05 1,48 0.83

Female realized fecundity 0.23 1,48 0.64 0.16 1,48 0.69
Female potential fecundity 0.54 1,24 0.47 0.17 1,24 0.68

newly emerged and mated females were considered
together. Considering only newly emerged females,
potential fecundity increased with each of body mass
and fat content of the abdomen, whereas female larval
feeding treatment did not have a significant effect on
potential fecundity (Table 5, Fig. 4). The interaction
term treatment x ln body mass was also insignificant
when included in the ANCOVA.
Thus, larval feeding treatment directly affects only
adult female lifespan and does not directly affect
fecundity. Larval semi-starvation only indirectly reduces
potential fecundity through a reduction in adult female
body mass (Fig. 5) and only indirectly reduces realized
fecundity through a reduction in adult lifespan. There is
no effect of treatment on potential fecundity indepen-
dent of body mass, or on realized fecundity independent
of lifespan.
For virgin females, fat score was greater in those in
the fed than in semi-starved treatment (least squares
means ± SE from an ANCOVA with treatment and
body mass: fed: 1.89 ± 0.06; semi-starved: 1.54 ± 0.09;
F1,63=6.94, P=0.01). Additionally, fat score increased
with body mass (F1,63=4.15, P=0.04). This indicates
that fat storage was greater in larger females indepen-
dent of larval treatment, even though the fat was scored
relative to body cavity size.

Discussion
Fig. 2 Effect of larval feeding treatment on female adult lifespan.
Bars represent SW. ANCOVA: larval feeding treatment: Adult morphological traits
F1,50=6.77, P=0.01; ln body mass: F1,50=0.94, P=0.34
As expected, body mass and wing length were smaller in
Table 4 Effect on realized fecundity of female traits, using an
ANCOVA semi-starved individuals of both sexes. However, female
somatic allocation shifted in response to a deteriorating
Source F df P last larval instar food environment, with body mass of
semi-starved individuals increasing more steeply with
ln body mass 0.16 1,49 0.70 wing length compared to well-fed individuals. This could
Larval treatment 0.001 1,49 0.97
Lifespan 36.74 1,49 <<0.001 result in changes in flight capability and metabolism,
depending on effects of larval nutrient stress on other
358

Fig. 3 Effect of female adult lifespan on realized fecundity.

Fecundity= 100.85 + 16.95 (lifespan); F1,51= 44.6, P<<0.001;
r2=0.47

aspects of wing morphology (e.g., Kingsolver 1999) and

on the relative allocation of mass between abdomen and
thorax (e.g., Dudley and Srygley 1994; Dudley 2000;
Berwaerts et al. 2002).
Allometric relationships between body mass and wing
length in field-caught insects will be influenced by vari-
ation in their larval diet, as well as by increased mea-
surement error for body mass due to variation in the
exact age at which mass is measured. Thus, we would
expect field regression slopes to be intermediate between
fed and semi-stressed greenhouse animals. For summer
1995 females in the field, the generation immediately
previous to the animals used in the greenhouse experi-
ment, the slope was 1.84 (95% confidence limits: 1.28–
2.41; F1,91=42.48, P<0.001) (CLB, unpublished data).
Changes in allometry between female body mass and
wing length are consistent with experimental results of
Nijhout and Emlen (1998), who showed that allometric
relations between various body parts could be altered
through resource competition during development.
Nonetheless, as for males here, changes in larval diet are
not always accompanied by changes in allometry be-
tween body mass and wing parameters in other species.
For example, Angelo and Slansky (1984) found signifi-
cant consistent allometric relationships between adult
wet body mass and wing area for each of four species of
Table 5 Effect of female traits on potential fecundity in newly
eclosed adult females, using an ANCOVA (a) with larval treatment
and (b) without larval treatment
Source F df
With larval treatment
ln body mass 2.68 1,62
Larval treatment 0.23 1,62
Fat score 8.39 1,62
Without larval treatment
ln body mass 6.73 1,63
Fat score 10.45 1,63
Fig. 4 Effect of fat score on potential fecundity of newly eclosed
adult females. Bars represent SE. Fat score 1=some fat in the
abdomen; Fat score 2=much fat in the abdomen
noctuid moths subjected to differing durations of larval
starvation. Likewise, Wissinger et al. (2004) found a
consistent allometric relationship among body parts
within a sex for individuals fed reduced, ambient, or
enhanced diets in a caddisfly, Asynarchus nigriculus
(Trichoptera: Limnephilidae), although overall body size
changed with diet. Unlike S. mormonia, A. nigriculus
occur in ephemeral habitats (temporary wetlands),
which may influence the consistency under larval food
stress of allometric relationships among body parts in-
volved in flight.
Adult life history traits
Female potential fecundity decreased with decreasing
body mass and fat content, but with no effect of larval
feeding treatment per se, independent of body mass. In
contrast, female adult survival decreased in the semi-
starved treatment, but with no effect of body mass.
These results stand in sharp contrast to the effect of
reducing adult food availability: in that case, dietary
treatment affected fecundity, but not survival (Fig. 5)
(Boggs and Ross 1993).
P Combining the results of larval dietary restriction (the
present study) with that of adult dietary restriction (Boggs
0.11 and Ross 1993), we can draw some conclusions regarding
0.63 allocation to reproduction and survival in a holometab-
0.005 olous insect with a nectivorous adult stage. With regard to
reproduction, these results suggest that the total amount
0.01
0.002 of larval reserves in combination with the amount of
nectar available in the adult stage determines reproductive

Fig. 5 Summary of effects of feeding regime on life history traits in
female S. mormonia based on the present study and Boggs and
Ross (1993)
potential. In general, a small adult has the reproductive
potential of any other similarly small adult, regardless of
why it became small. That is, there appear to be no
changes in allocation of larval resources that dispropor-
tionately affect reproduction as a result of larval semi-
starvation per se, given that we did not observe a larval
treatment effect independent of body mass. In contrast,
survival is influenced not by body size or adult food in-
take, but rather by whether the individual was semi-
starved during the larval stage. This suggests that there
may be something related to the timing of resource
acquisition that causes larval semi-starvation to play a
major role in adult survival. As one possibility, survival
effects could be connected to changes in allometry among
adult body parts noted above, and related to timing of
developmental pathways involved in production of the
adult body.
Taken as a whole, the effects of larval and adult food
restriction are reminiscent of a survival/ reproduction
trade-off, but one that is dependent on resource alloca-
tion patterns across a developmental life-stage bound-
ary. That is, larval food restriction results in the
maintenance of reproductive potential at the cost of
survival, while adult food restriction has the opposite
effect.
The experimental design used here simulates either
restriction of food availability or time available for
feeding in the larval stage. Other workers have explored
effects of larval food quality, usually testing the effects of
different larval host plants. For example, Leather et al.
(1998) showed in Panolis flammea (Noctuidae) that
females reared on a native host plant had higher adult
survival than those reared on either of two introduced
host plants from different provenances; male survival
was unaffected by larval host plant. Consistent with our
results, female realized fecundity was determined by
lifespan, rather than by larval host plant.
Our results showing decreased adult longevity in the
face of larval dietary restriction are, on the surface,
contrary to the widespread phenomenon within animals
that dietary restriction results in increased longevity
(c.f., Houthoofd et al. 2002). However, longevity is
generally measured in the life stage that is subject to
dietary restriction; our results are across life stages.
Additionally, selection experiments for food stress
resistance in Drosophila showed that developmental
times are increased, allowing accumulation of greater
mass from larval feeding and greater lipid stores, which
can buffer adult food stress in selected lines (Chippen-
359
dale et al. 1996; Harshman et al. 1999). Thus, at a
minimum, no increase in adult longevity would be ex-
pected if larval-derived stores are impacted by larval
dietary restriction.
Number of previous matings by a male or male larval
dietary treatment had no effect on female fecundity or
survival. Such an effect could occur, since females ab-
sorb compounds from the spermatophore passed by the
male to the female at mating (e.g., Boggs and Gilbert
1979; Boggs 1995). However, the extent to which male-
donated nutrients are used by the female should depend
on the opportunity for use of such nutrients, including
timing of egg maturation relative to the male donation,
the female’s adult diet, and the degree to which the
spermatophore is absorbed (Boggs 1990). S. mormonia
emerge with no eggs mature, and feed on nectar as an
adult, giving ample opportunity for use of male-donated
nutrients in egg manufacture. Thus, for S. mormonia,
compounds donated by males are either not sufficient or
not the right compounds to make up for effects of female
larval semi-starvation on fecundity and survival. Thus,
males do not help buffer females’ fitness against varia-
tion in the larval nutritional environment in this species.
Other species show mixed effects of the male larval
food environment or mating history on female repro-
duction, as would be expected if the role of male
donations varies among species. For example, in
Choristoneura rosaceana (Lepidoptera: Tortricidae), fe-
male fecundity was affected by the plant species fed on
by their male mate and by whether the mating was the
first or second by the male (Delisle and Bouchard 1995).
Likewise, female likelihood of re-mating was higher in
C. fumiferana for females mated to males with a poor
quality diet but fed the same plant species (Delisle and
Hardy 1997), although female fecundity and survival
were unaffected by male dietary treatment for those
females that did not re-mate. In contrast, male body size
(presumably affected by both genetics and environment)
and previous number of matings had no effect on female
fecundity or survival in Zeiraphera canadensis (Lepi-
doptera: Tortricidae) (Carroll 1994).
The inability of male S. mormonia to buffer the effects
on fecundity of female larval semi-starvation, combined
with the decrease in sexual dimorphism in body mass,
is not consistent with the hypothesis of Leimar et al.
(1994) that sexual dimorphism in body mass should
increase (with females maintaining mass to a greater
extent than males) in the face of low quality larval host
plants for monandrous species in which male nutrient
donations do not play a major role in female reproduc-
tion (see also Gwynne 2004). This hypothesis was sup-
ported by tests of changes in sexual dimorphism in body
or abdomen mass in both Pieris napi (Pieridae), (a poly-
androus species, with a large effect of male nutrient
donations on female fitness) (Leimar et al. 1994) and
Pararge aegeria (a monandrous species with small male
nutrient donations) (Karlsson et al. 1997). S. mormonia is
very similar to P. aegeria, both in having a low number of
matings by females ( 1.04 and 1.03 for P. aegeria and
360
S. mormonia, respectively) and a low coefficient of vari-
ation in wing length in wild-caught females (3.3% and
3.8% for P. aegeria and S. mormonia respectively) (Boggs
1986; Boggs 1987; Karlsson et al. 1997). Hence, differ-
ences in the extent of normally encountered larval host
variability should not explain the discrepancy between
species. As noted above, however, it is not clear whether
females are conserving abdomen mass relative to thorax
mass under larval nutrient stress, given the maintenance
of potential fecundity, but reduction in fat score. Either
such a change in allometry between thorax and abdo-
men, or the fact that the experiments of Leimar et al.
(1994) and Karlsson et al. (1997) stressed larvae for the
whole lifespan could account for the discrepancy in re-
sults. Nonetheless, the reasons for apparent differences
among these studies in conservation of reproductive
potential by females relative to males under dietary stress
remain to be explored.
Conclusions
We thus see a suite of life history and morphological
trait changes in response to nutrient stress in different
life stages of a holometabolous insect. Carbon is abun-
dantly available from the adult nectar diet, and deter-
mines fecundity through its immediate use in the
manufacture of eggs. At the same time, larval resources
are necessary for growth and development of a normal
sized and proportioned adult with adequate reserves of
compounds not available in the adult diet. Resultant
body mass impacts fecundity. However, survival is
determined by some other aspect of larval feeding
treatment, presently unknown, but likely due to alloca-
tion changes in response to stress. This type of under-
standing of the effect of stress at different life stages will
be critical to an integrated understanding of the ability
of organisms to buffer fitness, hence population size, in
increasingly variable environments.
Acknowledgements We thank Craig Fee and David Stiles for help
rearing and dissecting butterflies. Ilkka Hanski, Bengt Karlsson,
Craig Osenberg, Ward Watt, and the reviewers commented
helpfully on the manuscript.
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