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Starvation Reveals no Effect of Body Size on Pupal Hibernation in the Flesh
Fly, Sarcophaga crassipalpis
Melanie C. Buskirk and Daniel A. Hahn
Many insects respond to harmful environmental conditions, such as the cold associated with winter, by entering
a hibernation-like state termed diapause. Diapause is a physiologically distinct state of programmed
developmental arrest initiated in response to stimuli signaling upcoming bad conditions. The flesh fly,
Sarcophaga crassipalpis, will diapause in the pupal stage when exposed to short photoperiods, such as those
found during fall and winter, as a larva. During larval development, diapause-destined individuals of S.
crassipalpis accumulate greater nutrient reserves in the form of lipid and blood proteins than their non-
diapausing counterparts. These additional reserves are thought to be critical for providing metabolic fuel for
survival through the long non-feeding pupal diapause and as anabolic precursors for resuming development after
the arrest period. The goal of our research was to determine how body size, which correlates with metabolic
fuel loads, affected the probability of an individual entering diapause and the duration of the diapause period.
We effectively used dietary restriction during larval life to produce pupae with a range of body sizes. We
expected that small individuals with low reserves would abort the diapause program and develop directly, even
when exposed to diapause-inducing conditions, allowing us to estimate the minimum larval weight threshold for
entry into diapause. Furthermore, of the individuals that entered diapause, smaller pupae were expected to
undergo a shorter diapause due to inadequate nutrient reserves. We found no evidence of an effect of body size
on diapause, and, contrary to predictions, smaller individuals spent slightly longer within the pupal diapause program.
Almost all organisms experience times when environmental conditions are unfavorable for growth or
reproduction. Seasonal change, for example the onset of a cold winter, is among the most ubiquitous
environmental challenges. Therefore, organisms have evolved a variety of strategies to deal with this
adversity including dormancy, hibernation, and torpor. In insects, unfavorable environmental conditions
typically induce a dormant state called diapause. Diapause is not just a simple arrest of growth and development,
but it is a hormonally distinct alternate life history tactic wherein an insect will become dormant and live off
of internal nutrient reserves without feeding for months (Tauber et al. 1986). In many insects, diapause is induced
by short photoperiods and cool temperatures, such as those experienced during the fall and winter months, and it
is thought that diapause evolved as a mechanism to survive adverse winter conditions (Denlinger 1972).
Although diapausing insects benefit from avoiding potentially lethal environmental conditions, diapause is an
energy-intensive process in which no feeding occurs and insects are forced to live off of stored reserves for
long periods of time. This leads to significant costs of diapause in many insect species. For example, the
parasitoid wasp Asobara tabida experienced a significant reduction in fat reserves, dry weight, and fecundity as
the length of the diapause period increased (Ellers and vanAlphen 2002). Likewise, a 60% loss of fitness in
the mosquito, Wyeomyia smithii, occurred in the form of reduced survivorship to adulthood, fecundity, egg load,
and adult life span as a result of completing the diapause program (Bradshaw et al. 1998). Therefore, insects
that enter hibernal diapause trade an improved probability of surviving overwintering with significant costs to
overall fitness (Ishihara and Shimada 1995).
The stress of diapause, coupled with the need to meet the energetic demands of post-diapause development,
induces many insect species to increase their metabolic reserves. For example, prior to diapause, larvae of the
flesh fly Sarcophaga crassipalpis accumulated nearly twice the lipid and hemolymph protein reserves as their
non-diapausing counterparts (Adedokun and Denlinger 1984; Rivers 1994). Similar fat sequestering by
diapause-destined larvae has been documented in the pink bollworm Pectinophora gossypiella and European
corn borer Ostrinia nubilalis, and in diapause-destined adults such as with the ironclad beetle Anatolica eremit,
and the alfalfa weevil Hypera postica (Adkisson 1961; Beck and Hanec 1960; Edelman 1951; Bennett and
Thomas 1964). In the extreme case, a five-fold increase in pre-diapause fat reserves has been documented in
the common mosquito Culex pipiens (Buxton 1935).
Due to the significant energy demands of diapause, larger individuals with greater nutrient stores are typically
more likely to survive the overwintering period. Similarly, small larvae that contain low nutrient reserves may
abort the diapause program in favor of direct development. For instance, even in the presence of diapause-
inducing conditions, undersized larvae of the blow fly Calliphora vicina failed to undergo diapause and instead
became sexually mature adults (Saunders 1997). The cost of diapause is so great that there is strong evidence of
a minimum weight threshold for diapause-destined individuals in the longicorn beetle, Psacothea hilaris. Within
this species, light larvae abort diapause if they do not reach a weight threshold that is a 330% increase over
that which is required for metamorphosis (Munyiri et al. 2004; Munyiri et al. 2003). This preference for
direct development in undersized individuals likely evolved as a survival program in nature, when the costs
of overwintering were too great compared to completing development prior to winter.
Diapause can occur in various stages of development, including eggs, larvae, pupae, and adult. While the existence
of a minimum viable weight has been substantially supported in two insect species that diapause as larvae,
no studies report the effect of size on other life stages, such as pupae or adults. The pupal diapause of the flesh fly
S. crassipalpis provides an excellent opportunity for studying the effect of body size on pupal diapause propensity
and survival. Diapause in the flesh fly occurs when larvae are exposed to cooler temperatures and
shorter photoperiods both as an embryo in the female uterus and early in the larval stage. While a directly
developing individual will proceed from larval feeding to reproductively viable adult in 3-4 weeks, a fly that
has entered the diapause program will arrest in the pupal stage for several months before adult development
occurs (Denlinger 1972).
The intention of this study was to determine how size affects entering and completing diapause in pupae of
S. crassipalpis. The pupal and adult body sizes of both diapausing and non-diapausing individuals are dictated
by larval food intake (Nijhout 1981). Therefore, we used starvation of larvae as a tool to manipulate pupal and
adult body size. Larvae were removed from food at regular intervals during development to induce a range of sizes
at the completion of feeding. Specifically, our goals were to determine the minimum viable weight for pupariation,
the minimum viable weight for diapause, and the effect of weight on diapause length. We expected that viable
adult eclosion was to rely heavily on early life conditions such as larval weight at extirpation; therefore we
predicted strong relationships between starvation and subsequent body size influencing key life stages. Due to
the significant energy demands of diapause, the minimum viable weight for development through diapause
was projected to be higher than that for direct developers, as demonstrated in previous studies of the species
C. vicina and P. hilaris (Saunders 1997; Munyiri et al. 2004; Munyiri et al. 2003). Finally, similar reasoning leads
us to expect that the energy reserves accumulated by larger individuals would promote a longer diapause in
those pupae that weighed more at extirpation.
METHODS AND MATERIALS
Larvae used in the following experiments were derived from a laboratory colony of S. crassipalpis Macquart.
Adults were reared in 30 x 30 x 30 cm screened cages and provided water, sugar, dried milk, and liver ad
libitum. The first group of adults was maintained with a long-day photoperiod of 15L : 9D (light : dark) at 250C
to promote direct development in their progeny (Denlinger 1972). Direct-developing larvae were then maintained
at 200C under the same light cycle. The second group of adults was held in a short-day length of 9L : 15D and 250
C, conditions known to promote diapause in their progeny. Larvae from short-day adults were subjected to 200C
and a short-day photoperiod from deposition until the conclusion of the experiment. All larvae were reared
in aluminum foil packets placed inside a 500 mL plastic container with two mesh-covered windows for gas
exchange. Approximately 1.5 cm of sawdust lined the bottom of the containers to provide a substrate for
pupariation. Each packet contained 100 larvae and 50 + 0.9 g of homogenized beef liver as food.
To generate a continuous distribution of body sizes, two individuals were removed from each packet at 48, 57,
72, 81, 96, 105, 120, and 129 hours after larviposition. Individuals were washed in Ringer's physiological
saline, dried gently using a Kim Wipeï¿½, and weighed to the nearest 0.1 mg. Larvae were placed individually into
Petri dishes lined with filter paper to absorb excess moisture and returned to their original treatment
temperature and light cycle until pupariation.
Individuals were weighed five days after pupariation, the time at which they had become fully formed pupae.
Pupae were observed daily for adult eclosion. Eclosion state was categorized as "no eclosion" from the
puparium, "partial eclosion" in which the individual broke through the operculum but died before becoming
fully liberated, and "full" or eclosion which produced an adult with a normal appearance. Pupae failing to eclose
after 160 days were evaluated to determine the life cycle point at which death occurred.
Data analysis was performed using the JMP Statistical Software and figures were made in SigmaPlot. ANCOVA
was used to analyze short day and long day weight relationships throughout all sampling periods, with a
Bonferroni correction for eight post-hoc comparisons, with significance evaluated at p < 0.009. We defined
a minimum viable weight for pupariation and for adult eclosion by inferring 50% survival thresholds derived
from logistic regression.
Extirpation weight and time spent feeding
Removing larvae from their food at specific intervals allowed us to produce a wide range of body sizes in pupae
and subsequently in adults (Fig. 1). Larval weight increased in a sigmoidal pattern with time spent feeding in
both long day and short day treatments. There was an interaction between treatment and time of extirpation on
body mass. Short day individuals were consistently lighter at all extirpation times up to 105 hours, after which
weight did not differ between the two treatments (Fig. 2, Table 1).
Figure 1. Selective starvation of larvae yielded a broad range of pupal and adult body sizes.
* * Z
0.175 , I
48 57 72 81 96 105 120
Hours Spent Feeding
Figure 2. Non-diapause individuals were heavier than diapause-destined individuals for most of the
larval period, but diapause individuals caught up in mass by the end of larval development.
Asterisks denote comparisons that were different in weight after a Bonferroni correction for
multiple comparisons. Note that both groups overlay each other at the 120 h time point.
Effects of treatment and extirpation time on weight. While there was no clear effect of
treatment on weight, a significant interaction was found between extirpation time and
Source df F P
Whole Model 16 707.2141 <0.0001*
Extirpation time 7 1552.081 <0.0001 *
Treatment 1 0.3359 0.5624
time*trmt 644 7.3835 <0.0001*
Error Total 660
Extirpation weight and probability of pupariation
Larger larvae at extirpation were more likely to pupariate in both long day and short day treatments (Logistic
fitLD, Xzz2=160.64, P<0.0001; Logistic fitsD, X2=232.77, P<0.001). The minimum viable weight, defined as
the weight at which individuals have a 50% likelihood of pupariation, for larva in the long day treatment was
45.19 mg (33.20-56.29, 95% CI), and 44.73 mg (36.5-53.5, 95% CI) in the short day treatment. There was
no difference in the minimum viable weight for pupariation between the two treatments, and these weights
were 23.7% and 23.6% of the mean weight of the maximum weight sample. As an additional measure of
minimum weight for pupariation we calculated the mean of the lightest 5% of individuals to successfully pupariate
in each treatment. There was no difference in the lightest 5% weight in either treatment. The lightest 5%
to pupariate in the long day treatment had a mean weight of 38.03mg (31.00-45.06, 95% CI) and the lightest
5% within the short day treatment had a weight of 44.25mg (40.80-48.74, 95% CI), which was 19.9% and 23.2%
of maximum sample respectively.
Extirpation weight and diapause
Notably, the mean of the lowest 5% larval weight of those short day individuals that entered diapause was 59.86
mg (55.39-64.34, 95% CI), which was 31.6% of the maximum sample and significantly different from the mean
of the lowest 5% for pupariation in the short day treatment. However, no effect of extirpation weight on
the probability of entering diapause was found when analyzed with logistic regression, a more conservative
statistical tool (X2=1.564, P=0.2111). Therefore, we conclude that smaller individuals were equally as likely to
enter diapause as their larger counterparts.
Extirpation weight and pupal weight
There was a strong linear relationship between larval weight at extirpation and pupal weight. The slopes and
y-intercepts of the relationship did not differ between long day and short day treatments, suggesting that
the association between larval size and pupal size is the same for diapause and direct developing individuals
(Linear regressionLD F1,242=11585.81, P<0.0001, R2=0.979, pupal wt = 1.0609272(larval wt)-0.468192;
Linear regressionsDp F=14046.98, P<0.0001, R2=0.982, pupal wt=1.0528666(larval wt)-0.491556).
Extirpation weight and probability of survival to adulthood
Although the MVW for pupariation was 45.19mg and 44.73mg for the long day and short-day
treatments, respectively, smaller individuals that were able to pupariate were less likely to eclose than
larger individuals in both treatments (Logistic fitLD, X2=201.38, P<0.0001, R2=0.5138; Logistic fitsD,
X2=202.92, P<0.001, R2=0.4497). Within the long day treatment, the minimum viable weight for eclosion was
68.39 mg (56.96-79.28, 95% CI) and 79.46 mg (68.09-90.30, 95% CI) in the short day treatment, which is
35.9% and 41.9% of maximum weight sample respectively. Though the 95% confidence intervals overlapped for
the minimum viable weight for eclosion, indicating no treatment effect, the short day larval mass is notably
greater than the long day larval mass. The mean larval mass of the lightest 5% to fully eclose was 60.45 mg
(53.73-67.17, 95% CI) in the long day treatment and 58.35 mg (53.83-62.87, 95% CI) in the short day
treatment, which was 31.7% and 30.8% of maximum sample weight, respectively.
Effects of extirpation weight on time spent in diapause
Within the short day treatment, a significant negative relationship was found between size and diapause
duration, surprisingly indicating that smaller individuals spent longer in diapause than larger individuals (Fig. 3).
0.00 0.05 0.10 0,15 0,20 0.25
Larval Weight (g)
Figure 3. Smaller individuals spent less time in diapause than larger individuals.
y = -104.34 x + 97.50, R2 = 0.11, F1,203= 24.87, p<0.0001.
Diapause, the non-feeding developmental hibernation in insects, is energetically demanding and has been
associated with fitness costs in numerous species of insects (Ishihara and Shimada 1995; Ellers and vanAlphen
2002; Saunders 1997; Munyiri et al. 2003; Munyiri et al. 2004). Therefore, we predicted a greater
weight requirement among larvae destined for entry into the diapause developmental program than for
direct development in S. crassipalpis, and we predicted that larger individuals would stay in diapause longer
than smaller ones. We found no evidence for a minimum weight threshold for entering diapause, and, contrary to
our predictions, we found that small individuals spent slightly longer in diapause than larger individuals.
Previous literature documents that diapause-destined individuals of S. crassipalpis accumulate almost double the
fat and protein stores as non-diapausing larvae (Adedokun and Denlinger 1984; Rivers 1994). These reports
appear to be in conflict with our findings that diapause-destined larvae were consistently lighter than their
non-diapausing counterparts throughout the most significant growth period. One consideration may be that
diapause-destined individuals did indeed accumulate greater nutrient reserves, but were smaller in somatic body
size than direct-developing larvae of equal masses. Smaller size may be attributed to excess fat and
protein accumulation at the cost of lean body tissue, such as flight muscles and reproductive tissue (Numata
and Hidaka 1980; Loeb and Birnbaum 1981; Wolda and Denlinger 1984). Biochemical analysis of individuals from
a companion study will allow us to determine if fat and protein content are elevated in diapause-destined individuals.
Although many studies have shown that diapause-destined individuals are heavier than their counterparts, this is
not always the case. For example, lighter short-day larvae have been documented in a few species, such as the
black swallowtail Papilio polyxenes and the field cricket Teleogryllus commodus (Blau 1981; Tanaka and
Tsubaki 1984). Within Papilio spp., diapause-destined larvae are smaller because short photoperiods induced
reduced feeding time and because no additional nutrient uptake occurs between the end of larval feeding
and pupariation, larval weight corresponds very strongly with pupal weight (Tanaka and Tsubaki 1984).
Metamorphosis is an energy intensive process that occurs within the puparium (Munyiri et al.2003; Nelliot et
al. 2006). Lighter individuals that have pupariated because they surpassed the minimum weight threshold can
still have inadequate nutrient reserves to eclose as an adult. In our study, smaller larvae at extirpation were
less likely to eclose as full adults. The minimum viable weight was approximately 42% of the average weight of
fully fed individuals.
We predicted that a greater weight threshold would function to ensure that diapausing individuals had
adequate reserves to survive the long and costly over-wintering period. Larvae with inadequate reserves to
survive hibernal diapause were expected to abort the diapause program and resume direct development, with
the idea that they may reproduce before the onset of adverse winter weather and that their progeny would
diapause. Recent research shows a distinct weight threshold for entrance into this developmental strategy.
Saunders (1997) reported that small larvae of the blow fly C. vicina subjected to diapause-inducing conditions
will abort the diapause program and favor direct development. Similarly, smaller larvae of the longicorn beetle
were more likely to abort the diapause program than large individuals (Munyiri et al.2003; Munyiri et al.2004).
Our findings stand in contrast to previous literature, which supports the existence of a significantly greater
weight requirement for over-wintering insects. We found no evidence of a weight threshold for pupal diapause in
S. crassipalpis, and we suggest that more studies of body size thresholds for diapause be performed across
species that diapause in different life stages.
We also predicted that smaller individuals would experience a shorter pupal diapause period. Typically,
smaller individuals contain less metabolic reserves, which indicates a decreased ability to sustain a long non-
feeding pupal stage. Contrary to expectations, lighter diapausing individuals spent slightly longer in the
puparium. According to the regression analysis, the 176.6mg difference between the lightest and heaviest
larvae indicates an increase of nearly three weeks in diapause for the smallest individuals. Perhaps lower
metabolic rates in smaller individuals during diapause could have contributed to this difference, and this will
be examined in future studies.
In the field, the diapause program in S. crassipalpis begins with pupal diapause, a programmed arrest
of development starting early in the fall when temperatures remain favorable for development. Diapause is
followed by a post-diapause quiescence within the puparium, which is maintained by temperatures being below
the threshold for development. The post-diapause phase is broken in the spring by warmer temperatures, at
which point adult differentiation occurs. This mechanism allows the synchronized emergence of adults, even
when diapause is initiated at different points in the fall (Denlinger 2001).
While most individuals complete diapause, a previous study has shown that survival drops considerably during
post-diapause quiescence (Hayward et al. 2005). Reduced survivorship during this period may be attributed
to declining metabolic resources in the time period between the end of diapause and adult differentiation.
Previous work in S. crassipalpis has shown that two-thirds of fat reserves are consumed during the early
diapause period, leaving little for the post-diapause quiescence period and adult development (Adedokun
and Denlinger 1985). Our study focused on the effects of body size on only the diapause period. Future work
will focus on post-diapause quiescence and evaluate how size might affect survival through post-
diapause quiescence. We predict that smaller individuals will show a decreased survival when forced to
undergo diapause followed by the energetically-costly post-diapause quiescence period as in natural populations.
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