First published online March 2, 2006
Journal of Experimental Biology 209, 1044-1051 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02125
Developmentally determined attenuation in circadian rhythms links chronobiology to social organization in bees
Shai Yerushalmi,
Shalev Bodenhaimer and
Guy Bloch*
Department of Evolution, Systematics, and Ecology, The Alexander
Silberman Institute of Life Sciences, The Hebrew University of Jerusalem,
Jerusalem, 91904, Israel
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Fig. 1. Size and division of labor in B. terrestris. (A) The relationship
between body size (forewing length) and the propensity to forage. Each filled
circle represents a single bee observed in Session A of Colony 2. The broken
line depicts the regression of foraging propensity on wing length
(y=0.16x–1.18, R2=0.46). Similar
results were obtained in Session B for this colony and in both sessions for
Colony 3 (size was not recorded in Colony 1). (B) Age-related plasticity in
worker task. Individually marked workers were observed for two sessions of 4
successive days each. The two sessions (A and B) were separated by a period of
3–4 days. The figure depicts the percentage of foragers (filled bars),
intermediate (hatched bars), and nurses (open bars) in session B as a function
of their task in session A. Data were pooled from the three colonies. Numbers
within bars indicate sample size. (C) Body size and age at first pollen
foraging. Foraging trips (a bee returning to the hive with pollen) of
individually marked bees were recorded using an automatic video system
equipped with motion detection technology. Large bees (marginal cell  2.75
mm; dotted line, N=59) began to forage at a younger age than small
bees (marginal cell <2.75 mm; continuous line, N=34;
Kaplan–Meier Survival Analysis with Breslow statistics,
P=0.007).
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Fig. 2. Division of labor and activity rhythms in free flying B.
terrestris colonies. (A) Representative actogram for a forager.
The numbers on the y-axis depict the day of observation. The height
of the bars within each day corresponds to the number of scans in which the
bee was active (see Materials and methods for details). Data for each day are
double plotted to facilitate visual detection of rhythmicity. This individual
has significant diurnal rhythms in activity. The bar at the bottom of the plot
depicts the illumination regime. Open bar=day (sunrise to sunset); filled
bar=night (sunset to sunrise). (B) Representative actogram for a nurse.
Details of plot as in A. Hatched part of the illumination regime bar depicts
the time of day for a bee that stays inside the constantly dark hive. This
individual has no diurnal rhythms in activity. (C) Representative summary of
the percentage of rhythmic nurses and foragers (Colony 2, session B). A higher
proportion of foragers have significant circadian rhythms (Fisher's Exact
Test, P<0.001; similar results were obtained for two additional
colonies in session B and for colony 2 in session A). (D) Development
of diurnal rhythms in young foragers and intermediates in free-flying colonies
(pooled data from all three colonies). The proportion of bees with circadian
rhythms was higher in session B (Fisher Exact Test, N=13,
P<0.05). There was no similar development of rhythm in nurses. (E)
Representative summary for the relationship between body size and the power of
circadian rhythms (Colony 2, session A, R2=0.34,
N=15, P<0.05). Similar results were obtained for an
additional colony. Note that in this experiment foragers experienced
day–night oscillations whereas nurses typically stayed inside the
relatively constant environment of the hive.
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Fig. 3. Body size and circadian rhythms in locomotor activity for B.
terrestris workers in a constant laboratory environment. Individual
workers were monitored from the day they emerged from the pupa. (A)
Representative actogram for an individual small bee. The height of the small
bars within each day corresponds to the locomotor activity in a 5 min bin.
Other details of the actogram are as in
Fig. 2A. This individual
emerged from the pupa at day 4, and had significant circadian rhythms at 6
days of age (power=273, determined after 6 days of age). There was an
alternation in FRP at 13 days of age. (B) Representative actogram for an
individual large bee. Details of actogram as in A. This individual is from the
same trial as the one in A, emerged from the pupa at day 3, and had
significant circadian rhythms for the first time at 3 days of age (power=505).
(C) The relationship between body size and the strength of circadian rhythms.
The broken line represents the regression for the power of circadian rhythms
on the length of the forewing marginal cell (an index for body size;
regression analysis; N=41, R2=0.2,
P<0.005; y=264x–447). (D) The power
of circadian rhythms in small and large bees. Numbers within bars indicate
sample size. The differences are statistically significant (unpaired
t-test, P=0.0015). (E) Age at onset of circadian
rhythms for large (broken line, N=17) and small (continuous line,
N=25) workers. The differences between small and large bees were
statistically significant (Kaplan–Meier Survival Analysis, Breslow
statistic, P<0.025).
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Fig. 4. Body size and circadian rhythms in locomotor activity for B.
terrestris workers in an oscillating (LD) laboratory environment.
(A) Actogram for a small bee. Details of the actogram as in
Fig. 3A. The background of the
plot delineates illumination regime: white background, light phase; gray
background, dark phase. This individual emerged from the pupa at day 1, had a
nocturnal activity pattern for the first 8 days, and then switched to a
diurnal activity pattern. Anticipation of light on is evident at 12 days of
age (black arrow). (B) Development of diurnal rhythms for large (top) and
small (bottom) workers. Filled bars, significant rhythms with peak activity
during the dark phase; open bars, peak activity during the light phase.
Asterisks and plus signs indicate days in which there were significant
differences in the proportion of small and large bees that were active during
the light or dark phase, respectively (Fisher's 2x2 Exact Test,
P<0.05). (C) Anticipation of light transition in small
(continuous line, N=14) and large (dotted line, N=33)
workers. Included are bees with nocturnal activity that anticipated light-off
and bees with diurnal activity that anticipated light-on (Survival Analysis,
P>0.05).
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© The Company of Biologists Ltd 2006
