Nutritional status influences socially regulated foraging ontogeny in honey bees
1 Program in Ecology and Evolutionary Biology, University of Illinois at
Urbana-Champaign, IL 61801, USA
2 Department of Entomology, University of Illinois at Urbana-Champaign, IL
61801, USA
3 Hughes Undergraduate Research Fellowship Program University of Illinois at
Urbana-Champaign, IL 61801, USA
4 Neuroscience Program, University of Illinois at Urbana-Champaign, IL
61801, USA
* Author for correspondence (e-mail: amytoth{at}uiuc.edu)
Accepted 27 October 2005
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Summary |
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Key words: Apis mellifera, division of labor, foraging, honey bee, lipid, nutrition, social inhibition
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Introduction |
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In insect societies, the behavior of individual colony members has been
selected to promote colony growth and reproduction
(Wilson, 1971). Most worker
behaviors, including foraging, benefit the colony and can be considered
altruistic. Not only is foraging an activity that carries a high risk of
individual mortality (Jeanne,
1986
), but food collected by foragers is mostly given to the
colony. For example, honey bee pollen foragers deposit pollen loads directly
into the comb for storage, and nectar foragers regurgitate their loads to
receiver bees that pass the nectar to other bees or place it in the comb for
storage (Winston, 1987
). By
and large, an individual social insect forager does not seek food in the
environment for individual sustenance, but instead contributes the food it
collects to colony energy reserves. It is thus not surprising that there are
strong social influences on the initiation of foraging in social insects
(Robinson, 2002
). Nonetheless,
it is also possible that social insect workers are induced to forage in
response to signals of their own nutritional physiology, as in solitary
animals. If so, this would suggest that mechanisms that activate foraging in
solitary ancestors of social insect species were employed during social
evolution to sculpt a more altruistic form of foraging.
In colonies of most social insect species, young workers engage in nest
work and old workers perform foraging. For example, honey bees typically
perform tasks inside the nest such as brood care (`nursing') during the first
23 weeks of adult life and then become foragers. Despite this
well-established pattern, the age at which specific tasks are performed is
extremely flexible, as bees are able to accelerate, delay or reverse their
pattern of behavioral development
(Robinson, 1992). The
transition to foraging in honey bees is accompanied by changes in diet
(Crailsheim et al., 1992
),
reduced lipid stores (Toth and Robinson,
2005
), and reduced blood proteins
(Crailsheim, 1986
) including
the lipoprotein vitellogenin (Fluri et
al., 1982
). The correlation between reduced internal nutrient
stores and foraging has been observed in numerous species of ants, bees and
wasps (Blanchard et al., 2000
;
Toth and Robinson, 2005
).
Recent work suggests the association between nutrition and foraging may go
beyond correlation. Schulz et al.
(1998) found that starvation
of honey bee colonies causes precocious foraging, although effects on
individual nutritional physiology were not examined. Schulz et al.
(1998
) ruled out the
possibility that foraging behavior was activated by the presence of empty food
comb, and instead implied that individual nutritional state may be a more
important factor. Toth and Robinson
(2005
) found that abdominal
lipid stores in honey bees decline prior to the onset of foraging, suggesting
this change in nutritional status itself could activate foraging. These
results suggest that despite the fact that foraging is altruistic and socially
regulated in honey bees, individual nutritional physiology may also play a
role. The first goal of our study was to test the hypothesis that lipid
depletion in honey bees leads to early initiation of foraging behavior.
A better understanding of how social and nutritional factors interact is
essential to developing a more complete picture of how the regulation of
altruistic foraging behavior occurs in animal societies. In a honey bee
colony, young bees are inhibited from becoming foragers by direct contact with
older bees (Huang and Robinson,
1992,
1996
,
1999
; Leoncini et al.,
2004a
,b
).
Recently, a pheromone mediating this process was chemically identified
(Leoncini et al., 2004b
), but
this does not rule out the possibility that social inhibition could also
involve a nutritional component. As suggested by Blanchard et al.
(2000
), it is possible that
food transferred from older bees via trophallaxis (exchange of
regurgitated liquid food) could lead to enhanced nutrient reserves in young
bees, delaying the onset of foraging. Therefore, the second goal of our study
was to explore how social interactions might interact with nutritional factors
to influence foraging ontogeny in honey bees.
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Materials and methods |
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Measurements of abdominal lipid stores
Methods to analyze lipid stores were as in Toth and Robinson
(2005). Bee abdomens were
detached and all internal organs removed, leaving the cuticle with adhered fat
body tissue. Each sample was then individually homogenized in a glass tissue
grinder in 2:1 chloroform:methanol using the Folch extraction method
(Perkins, 1975
), and allowed
to extract overnight. The samples were filtered through glass wool and
adjusted to a constant volume of 2 ml.
Lipid quantification in sample extracts was accomplished using colorimetric
assays. Samples from Experiment 3 were examined using a 0.25% potassium
dichromate in 85% sulfuric acid as described previously
(Toth and Robinson, 2005). An
improvement on this technique using 0.6% vanillin in 85% phosphoric acid
(Van Handel, 1985
) helped
reduce variance between the samples, and this method was used for samples from
Experiments 1 and 2. A 100 µl sub-sample of each lipid extract was dried
completely, 0.2 ml concentrated sulfuric acid was added, and samples were
heated in boiling water for 10 min. Then 2.0 ml vanillin reagent was added to
each sample, which was vortexed and dark-incubated for 15 min to allow pink
color formation. Absorbance at 525 nm was measured for each sample using a
Molecular Devices Spectra Max 190 multi-well spectrophotometer (Sunnyville,
CA, USA). A standard curve using known amounts of pure cholesterol was used to
calculate lipid amounts. Each lipid sample was analyzed twice in independent
assays and average values were used for subsequent analysis.
Effect of TOFA on fatty acid synthesis
To experimentally reduce lipid stores, 1-day-old honey bees were fed a diet
containing TOFA (5-tetradecyloxy-2-furanocarboxylic acid, kindly provided by
Merck, Inc., Whitehouse Station, NJ, USA). TOFA interferes with acetyl coA
carboxylase, the enzyme catalyzing the rate-limiting step in fatty acid
synthesis (Halvorson and McCune,
1984; McCune and Harris,
1979
). TOFA has previously been shown to interfere with lipid
deposition in another insect species
(Popham and Chippendale,
1996
), but specific effects on fatty acid biosynthesis have been
shown only for vertebrates (Parker et al.,
1977
). 1% TOFA in sucrose solution was determined to be a lethal
dose for honey bees (data not shown), so we tested a dose of 0.1% TOFA. One
hundred 1-day-old bees were collected, placed in plastic cages, and fed either
50% sucrose, or 50% sucrose with 0.1% TOFA. Food was replaced daily and the
amount of sucrose eaten recorded to determine whether TOFA affected food
consumption. Cages were kept in a 34°C incubator. Four separate trials
were performed, and results was pooled from all trials. When bees were 5 days
old, a subset (N=5) of both groups (with and without TOFA treatment)
was removed from cages, anaesthetized on ice, and injected with 20 µl 13.5%
[14C]acetate (1.4 GBq mmol1) in bee saline, which
amounted to an estimated activity of 6x105 d.p.m. per bee.
Bees were replaced in the 34°C incubator in cages with sucrose and pollen
for 5 h to allow incorporation of 14C via fatty acid
synthesis. They were then freeze-killed on dry ice and lipid stores extracted
in 2:1 chloroform:methanol as described above. The solvent was allowed to
evaporate overnight, 5 ml of Fisher ScintiVerse (Fair Lawn, NJ, USA)
scintillation fluid was added to each sample, and the direct c.p.m. of each
sample measured using a Packard Tri-carb 2100TR Liquid Scintillation Analyzer
(Ramsey, MN, USA).
Experiment 1: Effects of dietary manipulations on lipid stores and behavioral maturation
To test whether experimental lipid depletion can accelerate foraging
ontogeny in honey bees, we performed an experiment in which we manipulated
lipid stores with treatments combining a lipid-free diet and TOFA. Three
trials were performed. A dose of 0.1% TOFA suspended in a diluted honey
solution (5:1 honey:water) was used for all field experiments, because this
dose was shown to effectively reduce the rate of fatty acid synthesis in the
laboratory (see Results). Treatments were administered to separate
experimental `single-cohort colonies'. Each single-cohort colony contained a
mated, caged queen, 1200 paint-marked 1-day-old bees, one empty frame of
honeycomb, and one honeycomb frame in which dietary treatments were added (and
replenished daily). Because the queen was caged no brood was produced, which
eliminated any potential differences in brood production and brood pheromone
between treatments. Some bees initiate foraging in single-cohort colonies when
they are about 1 week old, about 2 weeks earlier than usual, due to the lack
of an existing foraging force (Leoncini et
al., 2004a). Single-cohort colonies thus provide an efficient
method for measuring the effect of various colony manipulations on age at
onset of foraging and are used extensively for this purpose
(Ben-Shahar et al., 2002
;
Schulz and Robinson, 2001
;
Sullivan et al., 2000
). The
same mix of genotypic backgrounds was used for all single-cohort colonies
within each trial.
The following four treatments were used: (a) honey solution without TOFA and an excess of pollen (typical diet), (b) honey solution without TOFA and no pollen (pollen-deprived), (c) honey solution containing TOFA and no pollen (TOFA), (d) honey solution containing TOFA and an excess of pollen (TOFA+pollen). Because pollen is the only external source of dietary lipid, bees in pollen-deprived colonies had a lipid-free diet and could only accumulate lipids by de novo synthesis from dietary carbohydrates. Bees in TOFA-treated colonies were predicted to have lower rates of de novo lipid synthesis, and therefore reduced lipid stores. Bees in the colonies fed TOFA+pollen, however, could accumulate lipid stores directly from dietary lipids, and were therefore predicted to have partially reduced or normal lipid stores. The TOFA+pollen group was included only in Trial 3. In each trial, a subset of bees from each colony was collected on day 45 (prior to the onset of foraging) for lipid analysis. Lipid measurements thus reflect the young bees' lipid stores after dietary treatments, but before foraging began.
Observations were conducted to determine the proportion of bees from each
colony that foraged precociously. All colonies within each trial were
monitored simultaneously by two observers for 34 days (when bees were
59 days of age), for 1 h in the morning and 1 h in the afternoon or
early evening. Foragers were identified as bees returning to the hive entrance
with pollen loads in their corbiculae or with abdomens distended, most likely
with nectar (Huang et al.,
1994). Foragers were paint-marked on the abdomen (Testor's enamel
paint) so that individuals were only counted once. After foraging observations
were completed, we calculated the proportion foraging from each treatment
group based on the cumulative number observed foraging and the number present
at the end of the experiment (Schulz and
Robinson,
2001
).
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Experiment 2: Effects of nutrition and social inhibition on behavioral maturation
We determined whether the previously established process of social
inhibition of foraging depends on nutritional factors. Each trial (of four
trials in total) involved four single-cohort colonies consisting of
10001200 1-day-old bees. Each colony was given a combination of two
treatments (Table 1), both used individually in earlier studies, but never
before combined. The nutritional treatment colony starvation
has been shown to cause precocious foraging
(Schulz et al., 1998). The
social inhibition treatment (SI) consisted of transplanting a group of
foragers into a hive of young bees; this has been shown to inhibit precocious
foraging (Huang and Robinson,
1992
). The four combined treatments were (1) starved SI+, (2)
starved SI, (3) fed SI+ and (4) fed SI. Since trophallaxis is
already implicated in the process of social inhibition in connection with
exchange of an inhibitor pheromone
(Leoncini et al., 2004b
), this
experiment focused specifically on whether nutritional changes that occur as a
result of food exchange are necessary for social inhibition. We hypothesized
that if foragers inhibit behavioral development via a nutritional
mechanism involving passage of food during trophallaxis, we would observe no
effect of social inhibition under starved conditions. Conversely, if social
inhibition can inhibit precocious foraging in starved young bees, this would
suggest that this form of social inhibition does not involve nutritional
influences.
For the nutritional manipulation, each colony was either fed (given full access to an excess of pollen and honey) or starved (given 50 ml honey in a honeycomb frame for 3 days, after which any remaining food was removed and replaced with an empty honeycomb frame). The social inhibition manipulation involved adding either foragers (forager transplant) or 1-day-old bees (control transplant) on day 23 of the experiment. Returning pollen and nectar foragers were collected from another field colony, chilled so they could be tagged (see below), and then added to each SI+ colony. Because of the high mortality of transplanted foragers, dead foragers were removed at night and replaced the following day to maintain a high and constant level of social inhibition (a minimum of 200 live foragers). Fewer control transplant bees were added (approximately 200 total, no replacement) due to the substantially lower mortality of this group of bees.
Transplanted bees were confined to their hive to prevent them from
foraging, bringing food back to the hive, and negating the starvation
treatment. This was accomplished using the `big-back' technique
(Withers et al., 1995). A
plastic tag was glued to the dorsal surface of the thorax of each transplanted
bee (for both forager and control), and a screen with openings just big enough
for untagged workers to fit through was placed over the hive entrance. Each
colony was provided with a Bee BoostTM queen pheromone strip (Phero Tech,
Delta, BC, Canada) instead of a real queen. A strip was used to prevent queen
mortality, sometimes seen in starved colonies (A.L.T., personal observation),
and to prevent brood production in the colonies. This ensured that our results
would not be affected by brood cannibalism
(Weiss, 1984
) or influences of
brood on food consumption (Hrassnigg and
Crailsheim, 1998
).
Foraging observations were made when focal bees were 58 days old, and the proportion of bees foraging from each group was determined as described above (Experiment 1). In Trial 1, a subset of bees from each colony was collected on day 5 (prior to the onset of foraging) for lipid analysis. These measurements were made to ensure the social inhibition treatment had no unforeseen effect on lipid stores.
Upon introduction, transplanted bees may have carried small amounts of food
in their crops that could have been shared with starved colony members. This
was unlikely to have affected the starvation treatment, for two reasons.
First, they were added on day 23 of the experiment, at which point
starved bees still had access to the honey added at the beginning of the
experiment. Second, the amount of sugar carried in the crops of transplanted
foragers was unlikely to have been large enough to affect the starvation
treatment. Returning nectar foragers have an average of 4 mg sugar per load
(Fewell and Winston, 1996).
Thus, 200 foragers would have supplied a maximum of 1 g sugar, which is only
enough to sustain 1000 bees for a few hours (A.L.T., personal
observation).
For logistical reasons, control transplanted bees were added on day
23 of the experiment and were 1 day younger than focal bees. Adding
1-day-old bees to a group of slightly older bees (differing in age by only a
few days) is known to lead to a slight increase in foraging by the `older'
cohort (Jassim et al., 2000).
However, this effect has been observed only when the younger cohort makes up a
substantial proportion of the colony (5097%) and differs in age by
several days (Jassim et al.,
2000
; Page et al.,
1992
). In our control transplant colonies, we added a much smaller
cohort of younger bees (1020% of the colony) and they were only 1 day
younger than focal bees.
Experiment 3: Effects of social isolation on lipid stores and behavioral maturation
To further explore the relationship between social interactions and
nutrition, we investigated whether social contact with other bees is necessary
for the accumulation of normal fat stores in young adult bees. Bees reared in
social isolation (caged to prevent all physical contact, including antennation
and food exchange) are known to exhibit precocious foraging
(Huang and Robinson, 1992). If
social contact is important for the accumulation of lipid stores, it is
possible that the early onset of foraging previously observed in isolated bees
is partially attributable to nutritional depletion resulting from the
isolation.
We tested whether bees reared in social isolation have reduced lipid stores
relative to control bees reared in typical colonies. We collected 1-day-old
bees and paint-marked each on the thorax, according to treatment group
(isolated or colony-reared). We then placed each isolated bee
(N250) in an individual wooden cage (with one side screened) with
bee candy (powdered sugar and honey mixture) only (Trial 1), or bee candy and
pollen (Trial 2). Bees were given bee candy only in Trial 1 to mimic the
experimental protocol of earlier studies
(Huang and Robinson, 1992
).
Obtaining the same result as Huang and Robinson
(1992
) in Trial 1 (see
Fig. 5), pollen was added in
Trial 2 in order to rule out additive effects of pollen depletion during
isolation on lipid and foraging measures. We placed the cages containing
individual workers in a wooden frame modified to hold them, placed the frame
in a screened frame box, and then placed the frame box in a typical colony
(Huang et al., 1998
). The
screened frame box prevented bees in the host colony from having direct
interactions with isolated bees, but did expose isolated bees to typical
colony odors and hive temperature conditions. Isolated bees were given fresh
water daily and checked for mortality; survival was 67.1% (167/249 in Trial 1)
and 95.2% (240/252 in Trial 2). Control bees were 1-day-old bees collected on
the same day and from the same mix of source colonies used for the isolated
bees. One thousand paint-marked control bees were introduced to the same
typical field colony used to house the isolated bees, and allowed to move
about freely.
|
Statistical analyses
All statistical analyses were performed using the SAS program (SAS
Institute 2000). Results of the effects of isolation on lipid stores were
analyzed using two-tailed, unpaired t-tests assuming equal variance.
Results of the fatty acid synthesis assay were pooled for all trials and
analyzed using a mixed model analysis of variance (ANOVA) to account for the
effect of trial (SAS PROC MIXED). Analyses of lipid levels for each trial of
Experiments 1, 2, and 3 were conducted using ANOVA (SAS PROC GLM). All lipid
measurements were log-transformed to normalize the data, and extreme outliers
were removed on the basis of Studentized residual values. Analyses of age at
onset of foraging for each trial were conducted using 2 tests
(SAS PROC FREQ). For experiment-wide analyses of all trials, a mixed model
ANOVA was used with trial as the random term (SAS PROC MIXED).
Post-hoc comparisons were adjusted for multiple comparisons using a
Tukey's adjustment.
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Results |
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Experiment 1: Effects of dietary manipulations on lipid stores and behavioral maturation
In all three trials, there was a significant effect of dietary treatment on
abdominal lipid amounts (ANOVA, Trial 1: F2,37=6.92,
P=0.003; Trial 2: F2,42=5.63, P=0.007;
Trial 3: F3,56=4.72, P=0.005;
Fig. 1A). A pooled analysis of
all three trials showed the same result (ANOVA,
F3,140=12.06, P<0.0001;
Fig. 1B). Post-hoc
tests showed that lipid levels differed significantly between all treatments:
bees fed a typical diet had the highest lipid levels, bees deprived of pollen
were intermediate, and bees fed TOFA (without pollen) had the lowest. Lipid
levels for bees fed a typical diet were similar to those typically found in
nurses, and those of TOFA-treated bees were similar to those typically found
in foragers (Toth and Robinson,
2005).
|
In the one trial in which there was also a TOFA+pollen group (Trial 3), these bees had lipid levels that were not significantly different from bees fed a typical diet (0.834±0.104 mg, Tukey-adjusted post-hoc test, P=0.86). Although the TOFA+pollen treatment was tested in just one trial, these results are consistent with the prediction that TOFA depletes lipid stores only when bees have no access to dietary sources of fat.
In all three trials, the proportion of bees foraging differed significantly
between the treatment groups (2 test; Trial 1:
22=94.23, P<0.0001; Trial 2:
22=90.34, P<0.0001; Trial 3:
23=80.46, P<0.0001;
Fig. 2A). In a pooled analysis,
there was also a significant effect of dietary treatment on the proportion of
bees foraging (ANOVA, F2,4=34.66, P=0.003;
Fig. 2B). Post-hoc
contrasts showed that the colonies fed TOFA had a significantly higher
proportion of foragers than bees fed typical or pollen-deprived diets, (these
latter two groups did not differ). In Trial 3, approximately 4.5% (33 out of
731) of bees in the TOFA+pollen group foraged (data not shown), a value which
is similar to the mean percent foraging for bees fed a typical diet (mean
across three trials=4.8%). The results of Trial 3 suggest that the TOFA+pollen
treatment had no effect on foraging behavior, consistent with the lipid
results. It is therefore unlikely that the behavioral effects of TOFA were due
to non-target side effects.
|
Experiment 2: Effects of nutrition and social inhibition on behavioral maturation
In all four trials, the proportion of bees foraging differed significantly
among the four treatment groups shown in Table 1 (2 tests,
Trial 1:
23=255.58, P<0.0001; Trial 2:
23=125.62, P<0.0001; Trial 3:
23=134.23, P<0.0001; Trial 4:
23=57.14, P<0.0001;
Fig. 3A). A pooled analysis
also showed significant effects of starvation (ANOVA:
F1,9=154.9, P<0.0001) and social inhibition
(F1,9=33.76, P= 0.0003), but no significant
starvationxsocial inhibition interaction (F1,9=0.64,
P=0.4439; Fig. 3B).
Post-hoc analyses showed that bees in the starved/SI group
showed the highest amount of foraging, followed by starved/SI+ bees, then
fed/SI bees and then fed/SI+ bees.
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Experiment 3: Effects of social isolation on lipid stores and behavioral maturation
Lipid stores were significantly lower in isolated bees as compared to
colony-reared bees in both trials (unpaired two-tailed t-tests: Trial
1: t18=4.59, P=0.0002; Trial 2:
t36=5.63, P=0.023;
Fig. 4). Similar results were
obtained with isolated bees given either bee candy only (Trial 1) or bee candy
and pollen (Trial 2), suggesting that isolation results in reduced lipid
stores even if bees have a full complement of food during isolation. Lipid
results from this experiment, although from 7-day-old bees (compared to
5-day-old bees in Experiments 1 and 2), are comparable to those of the other
experiments; e.g. lipid levels for both the typical group of Experiment 1 and
the colony-reared group of Experiment 3 ranged between approximately 0.9 and
1.2 mg. Therefore, lipid levels of typical 5- to 7-day-old young bees are
likely to be in this range.
|
Chi-squared tests revealed that a significantly higher proportion of
isolated bees foraged precociously as compared to colony-reared bees
(2 tests: Trial 1:
21=36.34,
P<0.0001, Trial 2:
21=11.73,
P=0.0006; Fig. 5), as
expected from a previous study (Huang and
Robinson, 1992
). Although the data suggest a slightly higher
proportion of isolated bees foraging from Trial 2 (fed bee candy with pollen)
compared to Trial 1 (bee candy only), when the data are viewed relative to
colony-reared bees in each trial, this trend does not hold. Because the
baseline number of bees foraging within a trial can vary widely depending on
nectar flow and weather conditions, the most important comparisons are made
within trials. Viewed in this way, Trial 1 shows approximately 3x
elevated foraging in isolated compared to colony-reared bees, and
approximately 9x in Trial 2; this suggests that foraging was most
elevated under isolation treatment in the absence of pollen. This
interpretation lends further support to the hypothesis that nutritional
deprivation activates foraging.
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Discussion |
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TOFA caused a 4050% reduction in lipid stores and this resulted in a
detectable behavioral change. In contrast, a lower level of lipid depletion,
resulting from pollen deprivation, did not affect behavior. This suggests that
the relationship between nutrition and foraging ontogeny may be
`well-buffered', such that bees may forage precociously only in response to
severe colony food shortage. Nutritional status may be unaffected in a
relatively short period of pollen dearth because bees can utilize excess food
reserves, as found in the European races of Apis mellifera
(Winston, 1987). In contrast,
nutritionally mediated effects on behavior may be more pronounced in African
races of A. mellifera living in tropical regions where less honey
reserves are stored (Winston,
1987
) and colony starvation is more frequent
(Schneider and McNally, 1992
).
Racial or intraspecies differences in physiology can be important life history
adaptations for species that are able to occupy widely different environments
(Martin et al., 2004
), such as
the honey bee.
TOFA treatment caused a decrease in fatty acid synthesis, but it is not
known whether decreased fatty acid synthesis occurs naturally in bees to cause
their striking loss of abominal lipids prior to the onset of foraging
(Toth and Robinson, 2005).
Pollen consumption decreases after a few weeks of adult life
(Crailsheim et al., 1992
), but
bees continue to receive worker jelly as noted above
(Crailsheim, 1991
). Other
possibilities include an age-related increase in metabolism
(Harrison, 1986
) and an
age-related increase in octopamine levels
(Harris and Woodring, 1991
;
Schulz and Robinson, 1999
;
Wagener-Hulme et al., 1999
), a
biogenic amine that plays a role in insect lipid mobilization
(Fields and Woodring, 1991
).
The proximate mechanisms underlying the lipid loss in honey bee fat bodies
associated with behavioral development deserve further attention.
We observed an increase of approximately twofold in the proportion of bees
foraging in response to TOFA treatment, which is a large change in
colony-level task allocation. However, this still amounts to only 20% of the
treated bees showing a behavioral effect. Several factors might account for
this result. First, perhaps there was unequal distribution of TOFA-containing
food or pre-existing differences in lipid stores due to differences in
genotype or larval environment; there was considerable variability in lipid
levels among TOFA-treated bees (data not shown). Second, it is likely that no
single treatment can stimulate all bees in a colony to forage because the
effects of any physiological manipulation might be attenuated by social
mechanisms that aid in the maintenance of colony division of labor
(Beshers and Fewell, 2001;
Huang and Robinson, 1999
).
Separate pathways appear to be involved in nutritional and social mediation
of foraging ontogeny in honey bees. This interpretation is consistent with the
recent finding of a pheromone found in foragers that inhibits behavioral
development, which appears to be transferred to young bees during food
exchange (Leoncini et al.,
2004b). The fact that we saw a similar effect of social inhibition
in starved and fed colonies suggests that this pheromone acts similarly under
both conditions. This agrees with experimental evidence documenting no
differences in rate of trophallactic contacts resulting in food exchange
between starved and fed colonies (Schulz
et al., 2002
). Although we detected separate nutritional and
social influences on foraging ontogeny, our results also indicate that social
interactions do affect lipid levels in young bees. This is consistent with
previous findings showing that nurse bees distribute nutritious `worker jelly'
widely to other adults, including young bees
(Crailsheim, 1991
).
The storage protein vitellogenin is also synthesized in the fat bodies, and
Amdam and Omholt (2003)
proposed in a theoretical model that high levels of vitellogenin inhibit the
ontogeny of honey bee foraging behavior. The model emphasizes interactions
between vitellogenin and juvenile hormone, a hormone that is known to
influence the age at onset of foraging
(Robinson et al., 1989
;
Sullivan et al., 2000
). Recent
empirical work supports this model, showing that injection of vitellogenin
dsRNA (which interferes with vitellogenin synthesis) caused precocious
foraging (M. Nelson, G. V. Amdam, M. K. Fondrk, and R. E. Page, personal
communication). Vitellogenin is a lipoprotein, so the regulation of
vitellogenin synthesis might be linked with lipid availability. Our results
suggest that future models on the physiological regulation of honey bee
behavioral maturation should incorporate other nutritional factors such as
stored lipid, in addition to vitellogenin.
Signaling pathways related to individual nutritional status
(Garofalo, 2002) may be
involved in the regulation of social foraging in other taxa as well. For
example, homologs of mammalian neuropeptide Y (NPY) and its receptor have been
implicated in gregarious feeding behavior in C. elegans and
Drosophila (de Bono and Bargmann,
1998
; Wu et al.,
2003
). Signaling between adipose tissue and the brain is a
burgeoning topic in vertebrates, especially as it relates to obesity in humans
(Konturek et al., 2004
).
Insect homologs to several vertebrate neuropeptides have been reported in
Drosophila and other insects
(Nassel, 2002
), and some
appear to share similar biological functions
(Garofalo, 2002
). However,
relatively little is known about mechanisms that communicate information about
internal nutrient status from the fat body to the brain in insects. Our
results suggest that studying nutrient signaling pathways could be important
for understanding the evolution of altruistic foraging and worker division of
labor in social insects.
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Acknowledgments |
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References |
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