Research article

Physiological costs of growing fast: does accelerated

growth reduce pay-off in adult fitness?

KLAUS FISCHER1,*, ILJA ZEILSTRA1, STEFAN K HETZ2

and KONRAD FIEDLER1

1Department of Animal Ecology I, University of Bayreuth, D-95440 Bayreuth, Germany;2Department of Animal Physiology, Humboldt University, D-10115 Berlin, Germany

(*author for correspondence, tel.: +49-921-553079; fax: +49-921-552784;

e-mail: klaus.fischer@uni-bayreuth.de)

Received 24 March 2004; accepted 9 August 2004

Co-ordinating editor: Leimer

Abstract. Accumulating evidence suggests that, in contrast to earlier assumptions, juvenile growth

rates are optimised by means of natural and sexual selection rather than maximised to be as fast as

possible. Owing to the generally accepted advantage of growing fast to adulthood, such adaptive

variation strongly implies the existence of costs attached to rapid growth. By using four popula-

tions of protandrous copper butterflies with known differences in intrinsic growth rates within and

across populations, we investigate a potential trade-off between rapid growth and the propor-

tionate weight loss at metamorphosis. While controlling for effects of pupal time and mass, we

demonstrate that (1) protandrous males, exhibiting higher growth rates, suffer a higher weight loss

than females throughout, that (2) population differences in weight loss generally follow known

differences in growth rates, and that (3) males have by 6% higher metabolic rates than females

during pupal development. These results support the notion that a higher weight loss during the

development to adulthood may comprise a physiological cost of rapid development, with the pay-

off of accelerated growth being reduced by a disproportionally smaller adult size.

Key words: growth rate, Lepidoptera, life-history trait, metabolic rate, trade-off

Introduction

An increasingly large body of evidence indicates that growth rate is a life-

history trait in its own right that may vary adaptively (Abrams et al., 1996;

Arendt, 1997, 2003; Nylin and Gotthard, 1998; Gotthard, 2000). Empirical

evidence for adaptive variation in growth rates was gained from studies on

insects, spiders, fish, molluscs, amphibians, reptiles, and mammals (see refer-

ences in Gotthard et al., 1994; Arendt, 1997). Traditionally, life-history theory

has explicitly or implicitly assumed that juvenile growth rates generally operate

near their physiological maximum, and that variation is attributable to

environmental variables such as temperature and food availability only

(e.g. Stearns and Koella, 1986; Roff, 1992; Stearns, 1992). However, growth

Evolutionary Ecology 18: 343–353, 2004.� 2004 Kluwer Academic Publishers. Printed in the Netherlands.

rates were frequently found to be optimised by natural selection rather than

maximised (e.g. Gotthard et al., 1994; Nylin et al., 1994, 1996; Abrams et al.,

1996; Lankford et al., 2001; Arendt, 2003). As the benefits of growing fast,

providing a higher chance of surviving to reproduction, is generally accepted

(Roff, 1992; Stearns, 1992), these findings strongly imply the existence of costs

attached to high growth rates.

There are basically two categories of such costs, ecological and physiological

ones. Potential ecological costs include a higher risk of predation due to a

higher foraging activity of fast growing individuals. This interrelation is well

supported by theoretical and empirical evidence (e.g. Lima and Dill, 1990;

Werner and Anholt, 1993; Gotthard, 2000; Lankford et al., 2001). In contrast,

the issue of potential physiological costs related to high growth rates has been

rarely addressed (Gotthard et al., 1994), a prominent exception being the

inverse relationship between growth rate and locomotor ability (e.g. Billerbeck

et al., 2001; Arendt, 2003). Some studies tested the hypothesis that high growth

rates should, based on overall higher metabolic rates, confer lower starvation

endurance, two of which revealed support for the prediction (Stockhoff, 1991;

Gotthard et al., 1994; but not Gotthard, 1998).

In many temperate-zone insects males typically exhibit shorter development

times and concomitantly increased growth rates than females due to selection

for protandry (e.g. Fagerstrom and Wiklund, 1982; Wiklund et al., 1991;

Zonneveld and Metz, 1991; Fischer and Fiedler, 2000a). Therefore, protan-

drous insects should provide useful modells to investigate potential costs

related to accelerated growth. Here, we address this issue by using four prot-

androus copper butterfly populations, one of Lycaena tityrus from Southern

Germany and three geographically isolated populations of Lycaena hippothoe

from Western Germany, the Central Alps, and Western Hungary. The latter

three show, in addition to sex-specific growth rates, variation across popula-

tions (Fischer and Fiedler 2001, 2002a, 2002b). When reared in a common

environment, the Hungarian population, being the only bivoltine one within

this principally monovoltine species (Tolman and Lewington, 1998), exhibits

considerably higher growth rates than the other two (by 8.7–59.1%, depending

on temperature; Fischer and Fiedler, 2002a). During post-diapause develop-

ment, the monovoltine alpine animals show about 7% higher growth rates than

their (also monovoltine) Western German con-specifics, presumably as an

adaptation to the short growing season in high altitude habitats (Fischer and

Fiedler, 2002b).

Those differences within and across populations enable us to investigate

potential physiological costs associated with increased growth rates. Propor-

tionate weight loss during metamorphosis may represent such a cost (Gotthard

et al., 1994; Fischer and Fiedler, 2000a), as animals need to spend time and

energy in achieving a high pupal mass. If, for fast growing individuals, this

344

investment is not proportionally reflected in adult size (generally believed to be

closely related to fitness; e.g. Peters, 1983; Honek, 1993), this is equivalent to a

relative reduction in the pay-off of accelerated growth.

Assuming that a faster development is less efficient than a slower one

(Gotthard et al., 1994; Arendt, 1997; Fischer and Fiedler, 2000a), we predict

differences in weight loss following the known differences in growth rates: (1)

As all populations exhibit protandry (Fischer and Fiedler, 2000a, 2001, 2002b),

males should suffer a higher proportionate weight loss than females through-

out. (2) Across the three L. hippothoe populations, the Hungarian one should

suffer the highest weight loss, followed by the alpine and finally the Western

German population. Finally, we explore a potential mechanistic source for

differences in proportionate weight loss. Based on the assumption of generally

elevated metabolic rates in fast growing individuals, we predict (3) a higher

mass-specific CO2 production in the pupal phase in fast growing males as

compared to females, potentially accounting for differences in weight loss.

Material and methods

Study organisms

L. tityrus (Poda, 1761) is a temperate-zone butterfly, ranging from Western

Europe to Central Asia. The species is bivoltine with two discrete generations

per year in most parts of its range (Tolman and Lewington, 1998). Larvae of

the last brood enter diapause, overwintering half-grown in the third instar. Ten

freshly emerged females were caught in July 2003 near Bayreuth (Northern

Bavaria, Germany; 400 m a.s.l.).

Lycaena hippothoe (Linnaeus, 1761) is also a temperate-zone butterfly, with a

range from Northern Spain in the west throughout much of the Northern

Palaearctic region to the easternmost parts of Siberia and China (Tuzov, 2000).

Adults fly in one generation throughout its vast range, except for the bivoltine

Western Hungarian population (Tolman and Lewington, 1998; Tuzov, 2000).

Larvae (of the last brood) enter diapause, overwintering half-grown (usually)

in the third instar (Fischer and Fiedler, 2002a). The three populations con-

sidered here include the nominate form L. hippothoe hippothoe from Western

Germany (Westerwald, 580 m a.s.l.), the alpine subspecies L. hippothoe eury-

dame (Hoffmannsegg, 1806) from the central Alps (Senales valley, 1800 m

a.s.l.), and the bivoltine subspecies L. hippothoe sumadiensis Szabo, 1956 from

Western Hungary (orseg, 200 m a.s.l.). Freshly emerged females (8, 10, and 9 of

L. h. hippothoe, eurydame, and sumadiensis, respectively) were caught in 1998

and 1999 in each of these populations.

345

Experimental arrangement

For oviposition captured females were transferred to Bayreuth University and

maintained in an environmental cabinet at a constant temperature (25–27 �C)and under long-day conditions (L18:D6). Females were placed individually in

glass jars (1 l) covered with gauze. Each jar contained leaves of the larval food-

plant Rumex acetosa as oviposition substrate as well as highly concentrated

sucrose solution for adult feeding. Eggs were removed daily, pooled (within

populations), and maintained in lots of about 100 in glass vials at a temper-

ature of 20 �C (L18:D6 throughout). After hatching, young L. hippothoe larvae

were randomly divided among four groups and exposed to constant temper-

atures of 15, 20, 25, and 30 �C, whereas all L. tityrus larvae were reared at

20 �C. Hatchlings were reared singly in transparent plastic boxes (125 ml)

containing moistened filter paper and fresh cuttings of R. acetosa in ample

supply. The boxes were checked daily and supplied with new food when

needed. In order to even out minor temperature differences within cabinets, the

boxes were shifted around daily.

Following the onset of diapause, dormant (L. h. hippothoe and eurydame)

larvae were transferred to another cabinet (T 4 �C, photoperiod L8:D16) for

hibernation. Note that under the given experimental arrangement, L. tityrus

and L. h. sumadiensis larvae generally developed directly into adults without

diapause, whereas the vast majority of L. h. hippothoe and eurydame larvae

entered diapause development (Fischer and Fiedler, 2002a). After a diapause of

about 5–6 months, these larvae were again assigned to the four different

rearing temperatures, and reared in the way outlined above until adult eclo-

sion. For all individuals, we measured development time, pupal and adult

mass. Pupae were weighed on the day following pupation, adults on the day of

eclosion after having excreted meconium. From these data, growth rates (mean

weight gain per day; Fischer and Fiedler, 2002a; 2002b) and proportionate

weight loss during metamorphosis ([1 ) (adult weight/pupal weight)] · 100;

Gotthard et al., 1994) were calculated.

Respirometry

L. tityrus pupae were used to test for sex-specific differences in CO2 release rate

(as a proxy for metabolic rate) at the Humboldt University, Berlin. CO2 release

was measured for single pupae using a two channel DIRGA (URAS 4, 0 . . .

100 ppm, Hartmann and Braun, Germany) with two flow-through respirom-

eters optimised for fast response. Data were logged to a computer via the serial

interface of the URAS 4 at an accuracy of ± 0.1 nmol g)1 min)1 and a

sampling rate of 1 s)1. A flow rate of 50 ml min)1 of CO2-free air was main-

tained by two independent mass flow controllers (MKS 1259, range

346

100 ml min)1; MKS instruments, Methuen, Massachusetts, USA). Calibration

was checked by the internal calibration function of the URAS 4. Air temper-

ature during experiments was kept at 20 ± 0.1 �C by a computer controlled

peltier cooling device, relative humidity at 80 ± 2%. Each experimental run

lasted for at least 150 min. Animals were allowed to habituate to the experi-

mental conditions for 30 min. After that time, mean mass-specific CO2 output

rate M.CO2 (nmol g)1 min)1) was calculated by averaging the CO2 output rate

over at least 90 min. This relatively short period was considered sufficient as

animals showed continuous CO2 release over longer periods (>12 h) in pilot

experiments. For more details on the experimental set up see Mbata et al.

(2000). Pupae were weighed before and after testing to calculate the water loss

during the experiments. To account for potential changes in metabolic rate

across the pupal stage, all pupae were tested at a similar age (i.e. on days 9–11

following pupation).

Statistical methods

For L. hippothoe, effects of population, temperature and sex on propor-

tionate weight loss were analysed by a three-way analysis of co-variance

(ANCOVA). As pupal mass and pupal time may passively affect weight loss

(due to differences in volume-surface ratios and the exposure times of pupae

to their environment, potentially affecting evaporation rates), both traits

were controlled for as covariates. Analogously, effects of sex on weight loss

were tested with a one-way ANCOVA in L. tityrus. The first three axes

extracted by principal component analyses (results not shown) consistently

depicted a growth, a mass, and a weight loss variable, respectively. Thus,

there should be no autocorrelation problems with adding pupal mass as

covariate in the ANCOVAs. All statistical analyses were performed using

StatSoft (1999). Throughout n gives the number of individuals and means

are given ± 1 sd.

Results

Weight loss at metamorphosis across sexes and populations of L: hippothoe

AnANCOVA revealed highly significant effects of population, temperature, and

sex on the proportionate weight loss during metamorphosis (Table 1). Overall,

sex had the strongest effectwithmales loosing about 62%of the initial pupalmass

as compared to about 58% in females (Table 2; Fig. 1). The sex difference was

highly consistent across populations and temperatures. Differences across

populations were less pronounced though highly significant. Hungarian

347

L. h. sumadiensis showed the highest values throughout except formales at 15 �C,where L. h. eurydame experienced a marginally higher weight loss (Table 2).

Moreover, alpine L. h. eurydame exhibited a higher weight loss than western

German L. h. hippothoe except for females at 20 �C and males at 25 �C. Weight

loss averaged at about 61% for L. h. sumadiensis, 59% for L. h. eurydame, and

58% for L. h. hippothoe across sexes and rearing temperatures. Further, weight

loss generally increased with increasing temperature, which was slightly more

pronounced in males than in females, causing a significant temperature by sex

interaction (Table 1, Fig. 1). Additionally, the significant temperature by pop-

ulation interaction suggests some slight differences among populations in the

response to temperature. While pupal development time did have an impact on

proportionate weight loss, pupal mass did not as could be expected from the

results of a principal component analysis (Table 1; see Methods).

We failed, however, to find a direct link between growth rate and weight loss

within (population by sex by temperature) groups. Correlation coefficients ran-

ged between )0.34 and 0.41 and were (after Bonferroni correction)

Table 2. Proportionate weight loss during metamorphosis (mean ± sd) for males and females in

three populations of Lycaena hippothoe at different experimental temperatures

T

(�C)L. h. hippothoe L. h. eurydame L. h. sumadiensis

Males Females Males Females Males Females

(%) n (%) n (%) n (%) n (%) n (%) n

15 55.4 ± 6.7 35 54.3 ± 4.7 25 59.1 ± 4.5 31 55.2 ± 3.3 32 58.8 ± 4.9 46 57.6 ± 4.7 52

20 59.7 ± 3.2 32 56.7 ± 3.2 34 61.9 ± 4.0 28 56.2 ± 3.9 43 62.8 ± 4.3 50 58.7 ± 3.8 56

25 61.1 ± 3.8 30 56.6 ± 2.1 48 60.7 ± 3.5 26 56.9 ± 2.9 40 63.5 ± 3.2 62 58.9 ± 2.9 50

30 61.5 ± 4.5 38 57.5 ± 3.6 29 62.4 ± 5.5 32 58.2 ± 2.8 44 66.9 ± 3.9 53 60.6 ± 3.7 64

Table 1. Three-way analysis of co-variance (ANCOVA) for the effects of population, temperature

and sex on the proportionate weight loss during metamorphosis in Lycaena hippothoe (total

n = 971). Effects of pupal mass and pupal time were controlled for as covariates. Significant

p-values are given in bold

Source df F p

Population 2945 52.2 <0.0001

Temperature 3945 17.1 <0.0001

Sex 1945 217.2 <0.0001

Pupal time 1945 13.9 0.0002

Pupal mass 1945 0.5 0.4801

Population · temp. 6945 3.3 0.0030

Population · sex 2945 1.2 0.3027

Temperature · sex 3945 5.5 0.0010

Pop. · temp. · sex 6945 1.8 0.0987

348

non-significant throughout (p-values ranged between 0.02 and 0.80, group

sample sizes between 25 and 64).

Weight loss at metamorphosis and metabolic rates across sexes in L: tityrus

As expected, males had higher growth rates than females (18.9 ± 0.7 vs.

17.5 ± 1.0 %/day; t183 ¼ 10.9, p<0.0001) conferring shorter larval times

(25.2 ± 0.9, n ¼ 107 vs. 27.3 ± 1.2 days, n ¼ 78; t183 ¼ )13.8, p<0.0001). An

ANCOVA confirmed a highly significant sex difference in weight loss (males:

60.6 ± 3.5%, n ¼ 107; females 56.6 ± 5.4%, n ¼ 71; sex: F1174 ¼ 36.6,

p<0.0001; pupal time: F1174 ¼ 1.1, p ¼ 0.30; pupal mass: F1174 ¼ 0.7,

p ¼ 0.40). This difference caused a highly significant sexual size dimorphism in

adult mass (males: 45.8 ± 5.1 mg; females: 51.6 ± 8.7 mg; t176 ¼ )5.7,p<0.0001), while variation among sexes in pupal mass was marginal and non-

significant (males: 116.2 ± 8.9 mg; females: 119.3 ± 13.9 mg; t183 ¼ )1.9,p ¼ 0.066). After removing outliers (defined as >1.5 times the range of the

25th–75th percentiles), mass-specific CO2 production of pupae differed

significantly across sexes (males: 212.0 ± 14.1 nmol g)1 min)1, n ¼ 39;

females; 200.1 ± 14.3 nmol g)1 min)1, n ¼ 37; t74 ¼ 3.7, p ¼ 0.0005). This

difference persisted when using the whole data set and the non-parametric

Kolmogorov-Smirnov test (males: 211.7 ± 20.8 nmol g)1 min)1, n ¼ 43;

females 204.6 ± 21.3 nmol g)1 min)1, n ¼ 40; p<0.025). Water loss during

experiments did not differ among males and females (t77 ¼ )0.1, p ¼ 0.94).

Again, there were no significant correlations between growth rate and weight

loss within both sexes (males: r ¼ 0.01, p ¼ 0.90, n ¼ 107; females: r ¼ 0.13,

p ¼ 0.28, n ¼ 71).

50

55

60

65

70

15 20 25 30

temperature [˚C]

wei

gh

t lo

ss [

%]

Figure 1. Proportionate weight loss at metamorphosis for Lycaena hippothoe males and females

from three populations at different experimental temperatures. Filled symbols: males, open sym-

bols: females. Diamonds: L. h. sumadiensis, triangles: L. h. eurydame, squares: L. h. hippothoe. For

sample sizes and standard deviations see Table 2.

349

Discussion

Accumulating evidence suggests that growth rate is a life-history trait in its

own right and in that a target of natural selection (e.g. Arendt, 1997; Nylin and

Gotthard, 1998). These findings are of wide-ranging importance for funda-

mental issues addressed by life-history theory, such as the relationship between

age and size at maturity (e.g. Abrams et al., 1996; Arendt, 1997; Nylin and

Gotthard, 1998; Gotthard, 2000). As in a number of other species (cf. Gotthard

et al., 1994; Arendt, 1997), growth rates were found to vary across sexes and

populations of copper butterflies. Those differences presumably represent

adaptations driven by sexual selection and the opportunities and constraints

imposed by the given environment (Fischer and Fiedler, 2000a, 2001, 2002a,

2002b). If thus growth rates are at least sometimes not maximised, this can only

be understood if a fast development carries some kind of cost (Arendt, 1997).

Based on the variation found, we predicted differences in proportionate weight

loss at metamorphosis, assuming that higher growth rates confer higher weight

losses.

By analysing weight loss in four populations of copper butterflies we could

show that (1) protandrous, faster developing males suffered a higher weight

loss than females throughout, that (2) population differences in weight loss

generally followed known differences in growth rates, and that (3) males and

females differ in metabolic rates during pupal development. Thus, our results

correspond closely to our a priori predictions, giving support for the notion

that a higher weight loss during the development to adulthood may comprise a

physiological cost of rapid development. To further illustrate the relevance of

such presumed costs the sexual size dimorphism among males and females

comprises a valuable example. The difference between males and females (with

males being generally smaller in spite of their accelerated growth) is much more

pronounced in the adult than in the pupal stage, where it is in some cases even

absent (see above for L. tityrus; see further Fischer and Fiedler, 2000a, 2001,

2002b).

The sex difference in weight loss was highly consistent across species and

populations, regardless of rearing temperature, food quality, and develop-

mental pathway (Fischer and Fiedler, 2000a, 2000b; present results). It was

also found in another butterfly, Pararge aegeria (Gotthard et al., 1994). But

why should weight loss differ across sexes and populations? Because of con-

trolling for pupal mass and time as covariates, which was not the case in earlier

studies (Gotthard et al., 1994; Fischer and Fiedler, 2000a), we can largely rule

out that passive effects such as evaporation rates cause those differences. In

L. h. eurydame sexes differed in weight loss, although pupal mass and devel-

opment time are equal (Fischer and Fiedler, 2002b). Likewise, L. h. eurydame

exhibited a higher weight loss than L. h. hippothoe in spite of equal pupal

350

masses and a generally shorter pupal development time in the alpine popula-

tion (Fischer and Fiedler, 2002b). Thus, different mass to surface ratios or

pupal times cannot explain those differences in weight loss.

Based on our results we suggest that there might be a causal link between

growth rate and weight loss. This is, however, not supported by correlation

analyses. The failure to confirm a direct link within groups is not entirely

surprising, as there is substantial variation in both traits, which may make it

hard to corroborate a consistent pattern within treatment groups (Gotthard

et al., 1994). Apart from genetic and environmental sources of variation,

methodological constraints further hamper analyses. Measuring butterfly fresh

weight is always a balance between being too early (meconium not entirely

excreted) and too late (weight loss due to desiccation). Moreover, allocation

patterns might be largely or entirely fixed due to a lack of genetic variation

today, thus representing a historical trade-off (e.g. Stearns, 1992). This may

also explain conflicting results found in Pararge aegeria, where sex-differences

in weight loss persisted also in the Madeira population not showing higher

male growth rates (Gotthard et al., 1994). One should note here that protan-

dry, being related to seasonal environments, is expected to occur in almost the

entire range of Pararge aegeria (Nylin et al., 1993).

As proximate reason for the differences in weight loss we suggest generally

elevated metabolic rates in fast growing individuals and populations, persisting

in the pupal stage (cf. Stockhoff, 1991; Gotthard et al., 1994; Gotthard, 1998).

Although pupal development times, a possible correlate of higher metabolic

rates, do only marginally differ between sexes (though there is a consistent

trend for males being faster; Fischer and Fiedler, 2000a, 2002a, 2002b), met-

abolic rates during pupal development were indeed found to be significantly

higher in L. tityrus males than in females. Interestingly, the sex difference in

metabolic rate is very similar to the one in weight loss, with males showing by 6

and 7% higher values. The males’ increased metabolism is considered to result

from selection for early male emergence and thus rapid development (Fag-

erstrom and Wiklund, 1982; Wiklund et al., 1991; Zonneveld and Metz, 1991;

Fischer and Fiedler, 2000a).

In conclusion, our results suggest that a higher proportionate weight loss

during pupal development may comprise a physiological cost of a faster

development, which reduces the pay-off of high growth rates, as achieving a

high pupal mass is not proportionally reflected in adult size. However, we do

acknowledge that our study is correlative in nature, and that experimental

approaches using more direct manipulations of growth rates (e.g. artificial

selection) are required to settle the issue. This is especially true as we could not

show a direct link between growth rate and weight loss. Identifying the costs

associated with rapid growth is an important issue in life-history theory, and

will remain a challenge to evolutionary ecologists for some time to come.

351

Acknowledgements

We thank K. Reinhold and K. Gotthard for valuable comments on earlier

drafts of this manuscript. S. Bauerfeind, K. Kaminsky, C. Ruf, and A. Servant

helped with butterfly rearing, and D. P€uschel assisted with CO2 measurements.

We acknowledge financial support from the Friedrich-Ebert-Foundation and

the German Research Council (DFG grant no. Fi 846/1-2) to K. Fischer.

References

Abrams, P.A., Leimar, O., Nylin, S. and Wiklund, C. (1996) The effect of flexible growth rates on

optimal sizes and development times in a seasonal environment. Am. Nat. 147, 381–395.

Arendt, J.D. (1997) Adaptive intrinsic growth rates: an integration across taxa. Q. Rev. Biol. 72,

149–177.

Arendt, J.D. (2003) Reduced burst speed is a cost of rapid growth in anuran tadpoles: problems of

autocorrelation and inferences about growth rates. Funct. Ecol. 17, 328–334.

Billerbeck, J.M., Lankford, T.E. and Conover, D.O. (2001) Evolution of intrinsic growth and

energy acquisition rates: I. Trade-offs with swimming performance in Menidia menidia. Evolution

55, 1863–1872.

Fagerstrom, T. and Wiklund, C. (1982) Why do males emerge before females? Protandry as a

mating strategy in male and female butterflies. Oecologia 52, 164–166.

Fischer, K. and Fiedler, K. (2000a) Sex-related differences in reaction norms in the butterfly

Lycaena tityrus (Lepidoptera: Lycaenidae). Oikos 90, 372–380.

Fischer, K. and Fiedler, K. (2000b) Response of the copper butterfly Lycaena tityrus to increased

leaf nitrogen in natural food-plants: evidence against the nitrogen limitation hypothesis. Oeco-

logia 124, 235–241.

Fischer, K. and Fiedler, K. (2001) Dimorphic growth patterns and sex-specific reaction norms in

the butterfly Lycaena hippothoe sumadiensis. J. Evol. Biol. 14, 210–218.

Fischer, K. and Fiedler, K. (2002a) Life history plasticity in the butterfly Lycaena hippothoe: local

adaptations and trade-offs. Biol. J. Linn. Soc. 75, 173–185.

Fischer, K. and Fiedler, K. (2002b) Reaction norms for age and size at maturity in response to

temperature: a test of the compound interest hypothesis. Evol. Ecol. 16, 333–349.

Gotthard, K. (1998) Life history plasticity in the satyrine butterfly Lasiommata petropolitana:

investigating an adaptive reaction norm. J. Evol. Biol. 11, 21–39.

Gotthard, K. (2000) Increased risk of predation as a cost of high growth rate: an experimental test

in a butterfly. J. Anim. Ecol. 69, 896–902.

Gotthard, K., Nylin, S. and Wiklund, C. (1994) Adaptive variation in growth rate: life history costs

and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99, 281–289.

Honek, A. (1993) Intraspecific variation in body size and fecundity in insects: a general relation-

ship. Oikos 66, 483–492.

Lankford, T.E., Billerbeck, J.M. and Conover, D.O. (2001) Evolution of intrinsic growth rates and

energy acquisition rates. II. Trade-offs with vulnerability to predation in Menidia menidia.

Evolution 55, 1873–1881.

Lima, S. and Dill, L.M. (1990) Behavioral decisions made under the risk of predation: a review and

prospectus. Can. J. Zool. 68, 619–640.

Mbata, G.N., Hetz, S.K., Reichmuth, C. and Adler, C. (2000) Tolerance of pupae and pharate

adults of Callosobruchus subinnotatus Pic (Coleoptera: Bruchidae) to modified atmospheres: a

function of metabolic rate. J. Insect Physiol. 46, 145–151.

Nylin, S. and Gotthard, K. (1998) Plasticity in life-history traits. Annu. Rev. Entomol. 43, 63–83.

Nylin, S., Gotthard, K. and Wiklund, C. (1996) Reaction norms for age and size at maturity in

Lasiommata butterflies: predictions and tests. Evolution 50, 1351–1358.

352

Nylin, S., Wiklund, C., Wickman, P.-O. and Garcia-Barros, E. (1993) Absence of trade-offs

between sexual size dimorphism and early male emergence in a butterfly. Ecology 74, 1414–1427.

Nylin, S., Wickman, P.-O. and Wiklund, C. (1994) Genetics of development time in a butterfly:

predictions from optimality and a test by subspecies crossing. Proc. R. Soc. Lond. B 257,

215–219.

Peters, R.H. (1983) The ecological implications of body size. Cambridge University Press, Cam-

bridge, UK.

Roff, D.A. (1992) The evolution of life histories: theory and analysis. Chapman and Hall, New York,

USA.

StatSoft (1999) Statistica 5.5 for Windows. StatSoft, Tulsa, USA.

Stearns, S.C. (1992) The evolution of life histories. Oxford University Press, Oxford, UK.

Stearns, S.C. and Koella, J.C. (1986) The evolution of phenotypic plasticity in life-history traits:

predictions of reaction norms for age and size at maturity. Evolution 40, 893–914.

Stockhoff, B.A. (1991) Starvation resistance of gypsy moth, Lymantria dispar (L.) (Lepidoptera:

Lymantriidae): trade-offs among growth, body size, and survival. Oecologia 88, 422–429.

Tolman, T. and Lewington, R. (1998) Die Tagfalter Europas und Nordwestafrikas. Franckh-Kos-

mos, Stuttgart, Germany.

Tuzov, V.K. (2000) Guide to the butterflies of Russia and adjacent territories. Vol. 2. PenSoft

Publishers, Sofia and Moscow, Bulgaria and Russia.

Werner, E.E. and Anholt, B.R. (1993) Ecological consequences of the trade-off between growth

and mortality rates mediated by foraging activity. Am. Nat. 142, 242–272.

Wiklund, C., Nylin, S. and Forsberg, J. (1991) Sex-related variation in growth rate as a result of

selection for large size and protandry in a bivoltine butterfly (Pieris napi L.). Oikos 60, 241–250.

Zonneveld, C. and Metz, J.A.J. (1991) Models on butterfly protandry: virgin females are at risk to

die. Theor. Popul. Biol. 40, 308–321.

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