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First published online July 14, 2008
Journal of Experimental Biology 211, 2408-2416 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016915
Differences in the sleep architecture of forager and young honeybees (Apis mellifera)
Department of Evolution, Systematics, and Ecology, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, 91904, Israel
* Author for correspondence (e-mail: bloch{at}vms.huji.ac.il)
Accepted 19 May 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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3 days
of age), which are typically active around-the-clock with no circadian
rhythms, also exhibit sleep behavior. We combined 24-hour video recordings,
detailed behavioral observations, and analyses of response thresholds to a
light pulse for individually housed bees in various arousal states. We
characterized three sleep stages in foragers on the basis of differences in
body posture, bout duration, antennae movements and response threshold. Young
bees exhibited sleep behavior consisting of the same three stages as observed
in foragers. Sleep was interrupted by brief awakenings, which were as frequent
in young bees as in foragers. Beyond these similarities, we found differences
in the sleep architecture of young bees and foragers. Young bees passed more
frequently between the three sleep stages, and stayed longer in the lightest
sleep stage than foragers. These differences in sleep architecture may
represent developmental and/or environmentally induced variations in the
neuronal network underlying sleep in honeybees. To the best of our knowledge,
this is the first evidence for plasticity in sleep behavior in insects.
Key words: Apis mellifera, sleep, response threshold, behavioral development, insect
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Tobler, 2005).
Accumulating evidence suggests that rest behavior in many invertebrates
meets the criteria for defining it as `sleep'
(Tobler, 1983;
Tobler and Stalder, 1988;
Hendricks et al., 2000a;
Shaw et al., 2000;
Ramón et al., 2004;
Stephenson et al., 2007). The
best studied invertebrate model is the fruit fly Drosophila
melanogaster, in which a combination of behavioral, neurophysiological
and genetic analyses have linked molecular and neuronal processes to sleep
behavior, demonstrating the usefulness of invertebrate models in the study of
sleep biology (Greenspan et al.,
2001; Hendricks and Sehgal,
2004; Shaw, 2003).
Sleep in flies is similar to mammals in the following ways: (1) consolidated
periods of immobility are homeostatically regulated, (2) the presence of an
elevated arousal threshold (Hendricks et
al., 2000b; Shaw et al.,
2000; Huber et al.,
2004), (3) characteristic brain electrical activity
(Nitz et al., 2002;
Andretic et al., 2005;
van Swinderen et al., 2004),
(4) a characteristic brain gene expression signature
(Cirelli and Tononi, 1999;
Cirelli et al., 2004;
Cirelli et al., 2005;
Zimmerman et al., 2006), and
(5) sleep is increased by antihistamines and reduced by caffeine and other
stimulants (Shaw et al., 2000;
Andretic et al., 2005). In both
mammals and flies, sleep persists in the absence of a functioning circadian
clock, demonstrating the importance of non-circadian mechanisms in the
homeostatic regulation of sleep
(Mistlberger et al., 1983;
Shaw et al., 2000).
Furthermore, as in mammals (Tobler,
2005), sleep rebound in insects is not affected by levels of
activity during sleep deprivation (Shaw et
al., 2000; Sauer et al.,
2004).
Honeybees (Apis mellifera) are among the first invertebrates for
which sleep behavior has been described
(Kaiser and Steiner-Kaiser,
1983). Honeybee foragers exhibit sleep, both in their natural hive
environment, and when isolated individually in the lab. Foragers sleep in a
posture characterized by a relaxation of the thorax, head and antennae. This
characteristic posture is associated with a decrease in muscle tonus and body
temperature, and an increase in response threshold, measured both
neurophysiologically and behaviorally
(Kaiser and Steiner-Kaiser,
1983; Kaiser,
1988). It was further suggested that deep sleep in foragers
(determined as periods lacking antennal movements) is correlated with rhythmic
electrophysiological activity in the brain, including the mushroom bodies
(Schuppe, 1995). Foragers
deprived of sleep for 12 h showed a rebound the next day; they increased the
duration of antennal immobility, one of the characteristics of sleep in bees
(Sauer et al., 2004). This
suggests that sleep in honeybee foragers is homeostatically regulated, similar
to sleep in mammals (Tobler,
2005), birds
(Martinez-Gonzalez et al.,
2008) and flies (Hendricks et
al., 2000a; Shaw et al.,
2000).
Foragers are relatively old workers, have strong circadian rhythms, and
sleep during the night. However, circadian rhythms are not typical to all
worker bees; young bees typically perform various in-hive activities
around-the-clock, with no circadian rhythms
(Crailsheim et al., 1996;
Moore et al., 1998). Young
bees that are isolated individually, or kept in small groups in constant
conditions, have no circadian rhythms in locomotor activity during their first
3–14 days (Moore, 2001;
Meshi and Bloch, 2007;
Bloch, 2008). Their
around-the-clock pattern of activity raises the question of whether young bees
sleep as foragers do. It is possible that young honey bees do not sleep at
all, which would make them an exception in the animal kingdom
(Lyamin et al., 2005;
Rattenborg et al., 2004). An
alternative hypothesis is that young bees do sleep like foragers, but
distribute their sleep throughout the day. A third hypothesis is that young
bees sleep, but their sleep is essentially different from that of
foragers.
In order to distinguish between these hypotheses, we characterized the sleep behavior of individually isolated young bees, and compared it to that of sister foragers. Our detailed behavioral observations and analyses of response thresholds lend weight to the third hypothesis. We show that young honeybees exhibit sleep behavior which is composed of the same stages observed in foragers, but that their sleep dynamics differ.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)]. Colonies H3 and H12 were headed by a naturally
mated queen (queens typically mate with 10–20 drones). We identified foragers by the presence of pollen loads in their corbiculate. We only collected foragers with undamaged wings. To obtain 1-day-old bees, we removed honeycomb frames containing pupae (sealed in cells) from source colonies in the field. We transferred the frames immediately to a light-proof container, which we placed inside a dark incubator [32±0.5°C; relative humidity (RH)=55±5%; monitored with an Onset HOBO (Contoocook, NH, USA) H01-001-01 data logger]. We collected the newly emerging bees the next day, when they were 0–24 h old.
Video recording
We video recorded bees from three different source colonies. In the
experiments with bees from colonies H3 and H12, we marked newly emerged bees
with a paint-dot on their thorax, and introduced them to a foster colony that
was housed in a two-frame observation hive (with transparent glass walls),
placed in a constantly dark environmental chamber (29±1°C; RH
50±5%). We connected the observation hive to the outside by a clear
plastic tube (length 60 cm, diameter 3 cm). After 48 h in the observation
hive, we collected two marked callow bees, as well as two foragers from the
same source colony (`genotype'). In the experiment with colony H3, we
collected the focal bees between 15:00 h and 17:00 h, whereas in the
experiment with colony H12, we collected them between 7:30 h and 8:00 h. These
time variations did not appear to influence the observed behavior, since the
results from the two colonies were essentially similar. Each of the four bees
was placed in an individual small cage (7.5x2.5x2.5 cm). The cages
were made of transparent glass, and were padded on one wall with a panel of
Palziv substrate. We provided each cage with a tube of sugar syrup (50%, w/w).
We placed the cages in a dark environmental chamber (28±1°C; RH
55±5%), which was illuminated by dim red light that bees cannot see
(von Frisch, 1967). Since some
of the callows from colonies H3 and H12 atypically appeared to have a
circadian rhythm, we monitored circadian rhythms in locomotor activity (see
below) before performing sleep observations, in the last experiment with
colony S25. Importantly, the callow bees from the three colonies were similar
in age (3 days old). After monitoring the bees for 48 h, we transferred two
foragers (with robust circadian rhythms), and two callows (that were active
around-the-clock with no circadian rhythms) to a dark environmental chamber
for video recording and sleep analysis. For the sleep analysis, we video
recorded the bees using an infrared-sensitive camera (Sony TRV 75E), over
successive 24 h periods. We started recording after the bees had acclimatized
to the lab for 2 h. We video recorded 64 bees, eight groups of four bees
(N=32 bees) from colony H12, and four groups of four bees
(N=16 bees) from colonies H3 and S25, each.
Analysis of video records
We used Pinnacle Studio (version 9.1; Pinnacle Systems Inc., Mountain View,
CA, USA) software to sample the video records to a computer. We omitted from
our analysis records of bees that died during the experiment (N=2),
were not visible throughout most of the experiment (N=4), were
continually active (N=2), or repeatedly slipped along the glass wall
during their rest period (N=8). We defined seven behavioral states
that we used for analyzing the remaining 48 records. Three characterized awake
bees, and the other four sleeping bees. We assigned a single prevailing
behavioral category (see Table
1 and Fig. 1 for
definitions of behavioral states) for every minute using the following
heuristic. If the bee showed `active' (A) behavior during any part of the
minute, we labeled the entire minute as `A'. Otherwise, if the bee showed
`immobile–active' (IA) and/or `grooming' (G) behavior, we labeled the
minute as `IA' or `G' respectively, according to the predominant behavior in
that minute (even if the bee also exhibited sleep behavior during this
minute). In minutes in which the bees did not show any of the awake
categories, we assigned the most prevailing sleep stage. In addition, we
counted the number of antenna movements for each minute for sleeping bees. We
defined a `bout' as a continuous episode in the same behavioral state.
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Analysis of response threshold
We determined the response threshold of bees to light. We placed each focal
bee in a small cage that was placed in a separate dark chamber
(23x6x20 cm), in an experimental room (28.5±0.5°C;
RH=50±5%). This enabled us to expose the focal bees to light without
disturbing bees in neighboring chambers. We started each experiment by
calibrating the light intensity. We placed the light source (an optic glass
fiber; Schott-Fostec, LLC, Elmsford, NY, USA) 2 cm away from a light meter
(LI-185A, Li-Cor, Lincoln, NE, USA), measured the light intensity of each
illumination level three times, and calculated the mean value. After this
calibration, we tested the response to light of the focal bees at various
arousal states. We illuminated the lateral part of the bee's head from a
distance of 2 cm (as in the calibration of the light intensities), for a
period of exactly 10 s. We increased the light intensity at intervals of 5 s
between light stimuli, and video recorded the bee throughout the entire
procedure. We used 20 discrete levels of light intensity. We defined a
response as the bee turned toward the light source, and/or moved her head more
than twice during, or immediately after (<1 s) the stimulus. The
response threshold for each bee was the lowest light intensity that triggered
a response.
We limited our analysis of response threshold to 3-day-old bees with no circadian rhythms, and foragers with robust circadian rhythms. In order to determine circadian rhythms, we monitored bee locomotor activity during the 2 days preceding the analysis (see below). In each experiment, we tested 20 foragers and 20 callows, out of 30 bees for which we monitored locomotor activity. We conducted seven trials with bees from colony S23 (N=58 bees tested), and 12 trials with bees from colony S25 (N=107 bees tested). Each trial started approximately 4 h after sunset, and lasted about 6 h. The response threshold analysis for foragers and callows at the different arousal states was carried out at approximately the same time of day. Thus, variation in circadian time cannot account for the observed variation in response threshold.
Locomotor activity
We placed each bee in a separate glass cage (as described above) in an
environmental chamber (28±1°C; RH= 45±5%), and monitored
locomotor activity with the ClockLab data acquisition system (Actimetrics Co.,
Wilmette, IL, USA). We used a high-quality monochrome image acquisition board
(IMAQ 1409, National Instruments Co., Austin, TX, USA), and a light-sensitive
black and white Panasonic WV-BP334, 0.08 lux CCD camera. The system collected
the data continuously, at a frequency of 1 Hz, as described by Yerushalmi et
al. (Yerushalmi et al., 2006).
Circadian rhythms in activity were assessed with the ClockLab software.
Statistical analyses
In order to test whether the sleep stages differed in bout duration and
amount of antenna movement, we carried out a separate statistical test on the
data set of each individual bee (we included only bees with N>10
samples for each sleep stage; foragers, N=17; callows,
N=24). We used non-parametric tests, since these variables were not
normally distributed [Kruskal–Wallis analysis with a correction for
ties, followed by multiple comparisons
(Siegel and Castellan, 1988)].
In addition to the individual analyses, we ran three-way ANOVAs to determine
the influence of colony, age (callow vs foragers) and sleep stage on
bout duration and antenna movement. For these analyses we used the average
values calculated for each individual bee, and used a data set that included
the values of all individuals. We carried out complementary t-tests
for each sleep stage to determine whether antenna movement and bout duration
differed between callows and foragers. We used non-parametric analyses to
determine whether the response thresholds differed between arousal states
(Kruskal–Wallis test), and between foragers and callows for each arousal
state (Mann–Whitney test).
We used a first-order Markov chain to model the likelihood of transitions
between behavioral states. A behavioral transition was defined as a change in
the behavioral state displayed between two consecutive minutes. We constructed
a separate transition matrix for each bee, in which each row represents
transitions originating from one behavioral state (X) to all other states.
Each cell represents the proportion of transitions to behavior Y, out of all
transitions originating from behavior X. In order to examine whether the
transition pattern of callows and foragers differed, we conducted a
`leave-one-out cross-validation' (LOOCV) analysis. We removed the data of one
bee, and computed two separate transition matrices (TX,Y)
for the remaining foragers and callows (denoted as the `foragers' transition
model', and the `callows' transition model', respectively). These models were
based on the average transition matrices of each group member. We calculated
the likelihood that the transition pattern of the removed bee originated from
each model using the following formula:
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Sauer et al., 2003;
Sauer et al., 2004). Our
experimental protocol, in which the bees could move freely inside their cages,
allowed us to identify and characterize three distinct sleep stages differing
in body posture and antennae position (Fig.
1; see Table 1 for
details). These three sleep stages were termed `first sleep stage' (FS),
`second sleep stage' (SS) and `third sleep stage' (TS). Bout duration differed
between the three sleep stages, and was typically shortest for the first sleep
stage, and longest for the third sleep stage (Kruskal–Wallis tests,
N=31–194 bouts/bee; P<0.05 in 16 out of 20 foragers
from three different colonies; Fig.
2A). The three sleep stages also differed in the number of antenna
movements per minute. The highest level of antenna activity was observed in
first sleep stage, and the lowest in third sleep stage (Kruskal–Wallis
tests, N=131–906 min/bee, P<0.05 in all 20
foragers; Fig. 2B). Callow bees exhibited the same three sleep stages as described above for foragers. Again as in foragers, the three sleep stages differed in their bout duration (N=36–237 bouts, P<0.05 in 19 out of 24 bees, the P-value was 0.052 for an additional bee; a similar trend was observed for the remaining four bees; Fig. 2C), and number of antenna movements per minute (Kruskal–Wallis tests, N=95–1094 min/bee, P<0.05 in all 24 callows; Fig. 2D).
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We found no consistent differences in the percentage of time that foragers and callows spent sleeping (supplementary material Fig. S2). In the experiment with bees from colony H3, callows slept more than foragers (t-test, P<0.05), whereas in colony S25 callows slept less (P<0.05). It is not clear whether this variation across trials reflects genetic differences between colonies, or stems from variability in experimental procedures (lab vs hive environment before monitoring sleep; see Materials and methods).
In an analysis of all motionless bees (including all behavioral states
besides active), we found that bees slept in 80% of all bouts in which they
did not move for 
5 min. This suggests that lack of movement for >5 min
can serve as an indirect measure of sleep in studies of locomotor
activity.
Response threshold
The response threshold varied with arousal states for both forager and
callow bees (Kruskal–Wallis tests, P<0.0001, followed by
one-tailed multiple comparisons, P
0.05 for both foragers and
callows; Fig. 3). Awake,
immobile–active bees responded to very low light intensities (<0.05
µmollphotons m–2 s–1), whereas bees in
the third sleep stage typically responded only to intense light
(>1000µmollphotons m–2 s–1). The
responses of bees in the first and second sleep stages were between these two
extremes (Fig. 3). There was no
significant difference in the response threshold of foragers and callows in
the same arousal state (Mann–Whitney tests, P>0.085 for all
behavioral states).
The dynamics of sleep behavior
Foragers were typically active throughout the subjective day, and limited
their sleep to the subjective night (Fig.
4A). The temporal pattern of activity was more variable in callow
bees. Callows from colony S25 were typically active around-the-clock, with
periods of sleep behavior distributed throughout the day (N=6). A
similar pattern of activity was also observed in 45% (N=9) of the
callows from the two other source colonies
(Fig. 4B). By contrast, in 55%
(N=11) of the callows from these two colonies, sleep behavior tended
to be more common during the subjective night, reminiscent of the pattern in
foragers (Fig. 4C). All sleep
bouts, in both foragers and callows, were interrupted by brief episodes of
awakening (transitions from sleep stages to immobile–active or grooming;
Fig. 4A–C). We could not
determine clear sleep cycles as those commonly reported for mammals. The
average sleep bout duration was shorter in foragers (two-way ANOVA, age
effect: P=0.04; colony effect: P<0.001; `age x
colony' effect: P=0.04; Fig.
4D). Consistent with this trend, the average number of bouts per
day was higher in foragers than in callows (two-way ANOVA, age effect:
P=0.016; colony effect: P=0.4; `age x colony' effect:
P=0.002; Fig. 4E).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Our detailed characterization of sleep behavior confirms and extends
earlier studies that focused on sleep in forager bees
(Kaiser and Steiner-Kaiser,
1983; Kaiser,
1988; Schmolz, 2002; Sauer et
al., 2003; Sauer et al.,
2004). An important aspect of the current work is that the bees
were free to move in their cages, and were not tethered, as in most previous
studies on sleep in bees. Our experimental procedure allowed bees to choose
their resting place, and change their body posture freely. Although the
experimental setup of the current study differs from previous ones, we also
found that sleep in honeybees is a dynamic process, and that deep sleep is
associated with an increased response threshold, relaxation of the antennae
and body, and reduced antennal movements.
The description of three sleep stages in bees is reminiscent of the
classification of sleep into distinct stages in mammals. For example, human
sleep is divided into five stages: NREM (non rapid eye movement) stages
1–4 and REM (rapid eye movement) sleep. These sleep stages are
categorized mainly by their electroencephalographic (EEG) pattern, but they
also differ in other behavioral and physiological parameters such as response
threshold, muscle tonus and activity level (e.g.
Grahnstedt and Ursin, 1980;
Thoman and Glazier, 1987;
Wilde-Frenz and Schulz, 1983;
Keenan et al., 1993). NREM1
and NREM2 are characterized by a relatively low arousal threshold and high
muscle tonus and body movements, and are therefore considered `light sleep';
NREM3 and NREM4 have higher arousal thresholds and reduced muscle tonus and
body movements, and are considered `deep sleep'. REM sleep is accompanied by a
near-to-complete loss of muscle tonus
(Keenan et al., 1993). As in
mammals, sleep depth in honeybees varies with stage. The first sleep stage
seems to be the lightest one, and appears as a transitory stage between
wakefulness and deep sleep. Bees in the first sleep stage exhibit the most
frequent antennae movements, are most sensitive to light stimuli, and have the
shortest bout duration. Nevertheless, the behavior and response threshold of
bees in the first sleep stage still differ significantly from those of bees
that are inactive but awake. The third sleep stage of honeybees appears to be
the deepest. Bees in the third sleep stage show the lowest number of antennae
movements, have the highest response threshold, the most reduced muscle tonus,
and the longest bout duration. Deep sleep in bees is also associated with an
increase in ventilatory cycle duration
(Sauer et al., 2003), and
reduced body temperature (Kaiser,
1988). In both bees and mammals, the transitions from arousal to
deep sleep and from deep sleep to awake states are typically gradual [for
mammals, see Feinberg and Ucbida (Feinberg
and Ucbida, 1993)]. However, although we did observe a general
tendency of movement toward and away from deep sleep, we did not recognize
clear sleep cycles as reported for humans. We noted that sleeping bees
occasionally showed bursts of rapid small-amplitude antenna movements, which
were associated with a specific body posture. This behavior, which was
observed for all bees and may correspond to the bursts of antennal activity
described in Kaiser (Kaiser,
1988) and Sauer et al. (Sauer
et al., 2004), was not analyzed systematically in the current
report. It should be noted that the classification into distinct sleep stages
was useful for sleep characterization and quantification, and enabled us to
rigorously compare young bees and foragers, but does not imply a step-like
transition between consecutive sleep stages or their underlying neuronal
mechanisms.
An additional similarity to mammalian sleep is the interruption of all
three sleep stages by brief awakenings, in both young bees and foragers. In
mammals similar sleep–wake transitions are observed across different
species, and the distribution of their episode durations follows a common
scale-invariant pattern, leading to the hypothesis that brief awakenings have
some yet unknown essential function in the process of sleep regulation
(Halasz et al., 2004;
Lo et al., 2004;
Diniz Behn et al., 2007).
Prior to our study, it was not clear whether young bees sleep at all, since
they are typically active around-the-clock with no circadian rhythms (reviewed
by Moore, 2001;
Bloch, 2008). Our findings show
that young bees, even those that are active around-the-clock, exhibit sleep
behavior. Moreover, body and antenna postures, antenna movements and response
thresholds are similar to those of foragers in the same sleep stage. Both
young bees and foragers progressed gradually from light sleep (FS) to deeper
sleep (TS), and passed from sleep to awake states a similar number of times.
However, their sleep architecture appears different. Overall, foragers had
more sleep bouts during the day that were on average shorter than in young
bees. They also tended to progress mainly from light to deep sleep, and from
there tended to pass directly to awake states, switching less often between
sleep stages. Young bees tended to pass more frequently between the three
sleep stages, and had longer bouts in the first sleep stage and shorter bouts
in the second and third stages.
The differences in sleep dynamics between young bees and foragers may
represent variability in the neuronal network underlying sleep behavior. In
mammals, the transitions between wake and sleep, and between sleep stages,
stem from complex interactions between sleep and wake-promoting centers
(reviewed by Merica and Fortune,
2004; Saper et al.,
2001; Fuller et al.,
2006; Lu et al.,
2006). The differences between callows and foragers could
represent developmental changes in the organization or function of the sleep
neuronal network, since callows are younger than foragers. In humans, there is
evidence for changes (`maturation') of sleep during early infant development
(Jenni et al., 2004;
Mirmiran et al., 2003). Young
bees and foragers also differ in the environment they experience, which may
contribute as well to the observed variation in sleep architecture
(Ribeiro et al., 1999;
Miyamoto et al., 2003;
Ganguly-Fitzgerald et al.,
2006). In this regard, it is interesting to note that
electrophysiological recordings suggest that sleep in honeybee foragers is
associated with distinct rhythmic activity in their mushroom bodies
(Schuppe, 1995). The mushroom
bodies, which differ in their neuroanatomy between young bees and foragers
(Withers et al., 1993;
Withers et al., 1995;
Farris et al., 2001), have
recently been implicated as the main brain region regulating sleep in
Drosophila (Joiner et al.,
2006; Pitman et al.,
2006).
To the best of our knowledge, this study is the first to show plasticity in
sleep behavior in insects. Even though both young bees and foragers have a
characteristic sleep state, there appear to be notable differences in their
sleep architecture. Since the behavior of bees is strongly influenced by the
social environment in the hive (Shemesh et
al., 2007), an important question for future research is whether
similar plasticity in sleep behavior also occurs in field colonies, in which
young bees typically care for the brood around-the-clock
(Moore et al., 1998).
LIST OF ABBREVIATIONS
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Acknowledgments |
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Footnotes |
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  K. Phillips DO YOUNG BEES SLEEP? J. Exp. Biol., August 1, 2008; 211(15): iii - iii. [Full Text] [PDF]
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Pr=the probability matrix of foragers
subtracted from that of callows. Blue colors represent transitions that are
more frequent in foragers; red colors represent transitions that are more
frequent in callows (see scale).