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First published online November 14, 2008
Journal of Experimental Biology 211, 3691-3697 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.021071
Sensory coding of nest-site value in honeybee swarms
1 Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853,
USA
2 Department of Entomology, University of California, Riverside, CA 92521,
USA
* Author for correspondence (e-mail: tds5{at}cornell.edu)
Accepted 29 September 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: sensory coding, group decision making, nest-site selection, Apis mellifera
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Glimcher, 2003;
Sugrue et al., 2005) and in
animal groups (Pratt et al.,
2002; Passino et al.,
2008). Decision making is an important topic for neuroscience and
sociobiology alike because of its pivotal role in translating sensory inputs
into the adaptive actions of individuals and groups. The translation process
involves building a sensory representation of the external world, then
transforming this sensory representation into a decision, and finally
implementing the chosen course of action
(Fig. 1). The most striking
progress toward understanding the neurobiology of individual decision making
has been made in studies of eye-movement choice in monkeys
(Schall, 2003;
Smith and Ratcliff, 2004). The
strongest progress toward understanding the sociobiology of group decision
making has been made in studies of nest-site choice in colonies of ants and
bees (Franks et al., 2002;
Seeley et al., 2006;
Visscher, 2007).
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;
Glimcher, 2003). Similarly, in
honeybee swarms, the build-up of information underlying the choice of a nest
site to the north, for example, takes the form of increased numbers of scout
bees visiting the northern site (Seeley
and Visscher, 2004). Furthermore, both in monkey brains and bee
swarms, the decision-making system includes mutually inhibitory linkages
between the different sites of evidence accumulation, a feature that boosts
the likelihood that only a single alternative is chosen, the one with the
highest evidence total (Shadlen et al.,
1996; Passino et al.,
2008).
Another feature of the decision-making process that monkey brains and bee
swarms have in common is sequential sampling of sensory information. That is,
they do not base their decisions on a single, instantaneous sampling of
sensory information, as is typically assumed in signal-detection theory
(Green and Swets, 1966), but
instead they gather sensory information over periods lasting up to several
seconds (monkey brains) or several hours (bee swarms). If the sensory
information is noisy, then acquiring it over time in multiple samples will
minimize the effects of noise in the sensory system and thereby improve the
reliability of the decision making. Prior studies of the
sensory-transformation component (Fig.
1) of decision making by honeybee swarms have shown how a swarm's
sensory units (scout bees) produce signals (waggle dances) on the surface of
the swarm that form a sensory representation of the alternative sites, and how
this sensory representation stabilizes over the course of a decision-making
event (Lindauer, 1955;
Seeley and Buhrman, 1999;
Passino et al., 2008). Previous
studies have also shown how the signals produced by a swarm's sensory units
show a pattern of rapid response decay, i.e. decreased response over time to a
constant stimulus (potential nest site)
(Seeley, 2003;
Visscher, 2003).
One important aspect of the sensory-transformation component of a swarm's
decision-making process that remains poorly studied, however, is exactly how
the bees code the value of a potential nest site in the waggle dances produced
to represent this site. The sensory coding of nest-site value is critical to
the decision-making process, for it is what gives better sites an advantage
over poorer sites in the competition among sites to accumulate the threshold
number of affiliated scout bees. Lindauer
(Lindauer, 1955) stated that
scouts reporting better sites perform longer and livelier dances, but his
evidence was limited. To give us solid information on this topic, we presented
honeybee swarms (one at a time) with a two-alternative choice between a
high-value nest box and a medium-value nest box, and we recorded the behaviors
of the scout bees as they reported on these two alternatives. Specifically, we
recorded the strength of each waggle-dance signal produced by individually
identified scout bees as they provided the swarm with sensory information on
the two nest boxes. These recordings reveal not only how the signals for the
high- and medium-value alternatives differed in average signal strength, but
also how much signal noise there can be in a swarm's sensory information about
alternative nest sites.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The swarms we used were artificial swarms of honeybees (Apis
mellifera L.) prepared one at a time from four colonies that we brought
to the island. Each colony was headed by a `New World Carniolan' queen
purchased from Strachan Apiaries in Yuba City, CA, USA. We prepared a swarm by
shaking 1.0 kg of bees, about 8000 individuals, from the combs of a hive into
a screen cage with their queen in a smaller cage among them, feeding this cage
of bees with sucrose solution (1:1 sucrose:water by volume) for 3 days. The
production of abundant wax scales signified that these bees had shifted into a
condition like that of a natural swarm, and we then set them up on a stand for
observation. The swarm stand was that described by Seeley and Buhrman
(Seeley and Buhrman, 1999).
This stand spread the swarm out over one surface of a board, so that
activities on the swarm's surface could be more easily monitored.
We set up each swarm, one at a time, on a porch of the old Coast Guard
building, and positioned two nest boxes 40–50 m apart, either 240 m to
the north of the swarm, near Broad Cove, or 250 m to the east of the swarm,
near Devil's Glen [roughly, sites 1 and 5 shown in
figure 2 in Seeley and Buhrman
(Seeley and Buhrman, 2001)].
The distance of each nest box from the swarm site was determined via
GPS using a Garmin GPSMAP 76 receiver (Garmin International, Olathe, Kansas,
USA). Table 1 shows for each
trial when it was performed, where the nest boxes were located, and how many
scout bees were monitored. For most of the swarms, we conducted two trials on
two consecutive days, with the two nest boxes moved from the Broad Cove
location to the Devil's Glen location (or vice versa) at the end of
the first trial, so that in the second trial the swarm had to start over in
its search for a home site. At the end of each trial, we collected the scout
bees that we had monitored during that trial, so different bees were studied
in each trial. The two nest boxes used in this study were the same as those
used in a previous study on the island
(Seeley and Buhrman, 2001).
The cavity volume of these nest boxes is adjustable, and in the present study
we set one nest box to 40 l to provide a high-value nest site, and one to 15 l
to provide a medium-value nest site. (Colonies in 40 l hives have a higher
probability of winter survival than those in 15 l hives: P=0.74 and
0.28, respectively; Seeley, unpublished data. This is because the former have
larger stores of honey, which is the `heating fuel' of an overwintering
honeybee colony.) Each box was housed in a separate, open-fronted shelter [see
figure 1 in Seeley and Buhrman
(Seeley and Buhrman 2001)] so
that the two nest boxes had the same exposure to the wind, sun and rain.
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Scout bee marking
After the swarm was set up, an observer was stationed at each nest box,
where he/she waited for scout bees to arrive. When a scout arrived, she was
caught in a 15 cm diameter, 40 cm deep insect net, either by placing it over
the nest box entrance while the bee was inside or by catching her in flight.
The bee was then marked with one or two spots of shellac-based paint, while
trapped in the net, and then released into the nest box, through its entrance.
The paint marks were applied in such a way that the bees were individually
identifiable (von Frisch,
1967). This procedure was repeated for the first four to seven
scout bees that appeared at each nest box (see
Table 1); up to several dozen
other scout bees also visited each nest box. When not engaged in marking scout
bees, the observer at each nest box watched the entrance of the nest box and
recorded on a data logger (Tandy Model 102 computer, running a program that
maps keystrokes to individual bee identities and creates a text record of the
times of such keystrokes) each time he/she observed a particular scout bee at
the nest box. These logged data on marked scout sightings gave us precise
information on the time that each marked scout spent at the nest box each time
she visited it (a scout bee typically makes multiple visits to a potential
nest site). Also, every 10 min, the observer counted the number of scouts
(marked and unmarked) that were visible outside the nest box.
Swarm observations
Meanwhile, at the swarm cluster, a third observer waited for the marked
scout bees to return and perform waggle dances on the cluster's surface. All
their dances were recorded on videotape. To build a record of when each marked
scout bee was at the swarm cluster, the observer scanned the swarm's surface
every 5 min and noted which marked scouts were present; this yielded a record
of bee presence/absence for each marked bee for each 5 min block of time. The
observer was also able to notice 60% of the marked bees' arrivals at and
departures from the swarm, and these records gave us a more detailed picture
of when each marked scout was at the swarm cluster.
Data transcription and analysis
We played back the videotapes of each swarm and noted when each marked
scout performed a waggle dance and how many circuits of the waggle dance she
performed. Each scout bee visited and reported on just one of the two nest
boxes during the course of a trial. Because scout bees tend to make repeated
visits to potential nesting sites, and can perform a waggle dance after each
visit, we determined for each marked scout, (1) her record of signaling
(dancing) during each return to the swarm from the nest box, and (2) her total
amount of signaling (total number of dance circuits produced to advertise a
nest box) summed over all returns to the swarm. All the dances performed by
each scout bee were for just one of the two nest boxes.
Descriptive statistics are reported as the mean ± 1 s.d. To test for
a difference in total signal strength between marked scouts from the 40 l and
15 l nest boxes, we used a mixed-model, repeated-measures ANOVA, which enabled
us to check for nest box effects (fixed), swarm effects (random) and
interactions. A repeated measures ANOVA was appropriate because for each swarm
and each nest box there were multiple bees producing data. To test for
differences in the proportions of bees dancing, etc., between the marked
scouts from the 40 l and 15 l nest boxes, we used 
2 tests.
Finally, to test for differences between the mean values of various measures
for the marked scouts from the 40 l or the 15 l nest box (e.g. time spent
inspecting the nest box, number of waggle runs produced after the first
inspection of the nest box, etc.), we used t-tests when the data were
normally distributed and Mann–Whitney U-tests when they were
not.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Comparison of dance responses for high- and medium-value sites
Fig. 3 provides a synoptic
picture of the results obtained in all seven trials of the experiment. We see
that there were notable differences between the scout bees from the high-value
(40 l) and the medium-value (15 l) nest boxes in the total number of dance
circuits produced per bee. Although there was great variation among the bees
of each group, on average the dance circuit total per bee was higher for
scouts from the 40 l nest box compared with those from the 15 l nest box:
89±93 dance circuits vs 29±49 dance circuits
[repeated-measures ANOVA: F1,66=10.52, P<0.003
(nest box); F3,66=0.79, P>0.50 (swarm);
F3,66=0.23, P>0.75 (interaction)]. Also, fully
80% (33 of 41) of the scouts from the 40 l nest box produced dance circuits,
whereas only 49% (18 of 37) of those from the 15 l nest box did so
(2=8.71, P<0.004).
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These differences in the strength and likelihood of dancing between the two
groups of scout bees do not reflect a difference in initial attention paid to
the high-value and medium-value nest boxes. The two groups do not differ in
the average time a bee spent at a nest box during her first visit there:
scouts visited the 40 l box for 17.5±8.3 min (range 5–37 min)
vs 14.2±10.0 min (range 2–40 min) for scouts visiting
the 15 l box [repeated-measures ANOVA: F1,66=1.66,
P>0.25 (nest box); F3,66=0.24,
P>0.75 (swarm); F3,66=0.79, P>0.50
(interaction)]. Nevertheless, the scout bees evidently judged the values of
the two nest boxes differently during their first visits to these boxes, for
upon their first returns to the swarm cluster, fully 76% (31 of 41) of the
scouts from the 40 l nest box danced, whereas only 43% (16 of 37) of the
scouts from the 15 l nest box did so (2=8.51,
P<0.004).
Rapid decay in dance response and visits to a site
We can see in Fig. 2 that
the scout bees in the 17 July 2007 trial did not perform waggle dances each
time they returned to the swarm cluster, but instead tended to do so only
during their first few returns. This rapid decay in the dance response was
typical. When we considered all 51 scout bees that performed dances within the
seven trials of the experiment, we found that the average period during which
a bee performed dances (i.e. the time interval from when she started her first
dance to when she finished her last dance) was surprisingly short: scouts
visiting the 40 l box, 28±28 min (range 1–106 min); scouts
visiting the 15 l box, 19±20 min (range 1–60 min;
t49=1.27, P>0.20).
Fig. 2 also shows that shortly
after a bee's dance response decayed to zero, she ceased visiting the nest
box. Considering again all 51 scouts that performed dances, we found that once
a bee had made a return to the swarm without dancing, she made only
0.84±0.87 additional visits to her nest box (range 0–3 visits).
Evidently, as a bee's motivation to perform dances for a site decays away, so
does her motivation to make visits to the site.
Fig. 4 shows that the decline in the dance responses of the scout bees followed a pattern of linear decay. Overall, we found that the slope of the decay line was –17.2 dance circuits per return to the swarm (Fig. 4B). We also found, however, that the rate of this decay was not uniform among bees, with some bees letting their dancing decay rapidly over just one or two returns to the swarm, and others letting it decay more slowly over several returns to the swarm (Fig. 4A).
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2=4.62, P<0.02). Furthermore, the first reports
made by the initial scouts tended to be longer than those made by the
subsequent scouts. Among the 41 scouts that visited the 40 l nest box, the
seven initial scouts produced 97.3±66.9 dance circuits on their first
returns to the swarm cluster, whereas the 34 subsequent scouts produced only
39.2±43.6 dance circuits (U[34,7]=176,
P<0.06). Similarly, among the 37 scouts that visited the 15 l nest
box, the seven initial scouts produced 43.0±52.7 dance circuits on
their first returns to the swarm cluster, whereas the 30 subsequent scouts
produced only 14.3±30.7 dance circuits
(U[30,7]=128, P<0.40).
Spatial precision of recruitment
The spatial precision that is possible in the recruitment of scout bees to
a nest site was demonstrated by the set of events depicted in
Fig. 2. On the morning of 17
July, the two nest boxes were 40 m apart at a distance of 240 m from the swarm
cluster, so their angular separation from the swarm was only 10°. The nest
boxes were mounted in identical lean-to shelters. Both shelters were
positioned along the north side of a grassy road and both had their open sides
facing south, i.e. toward the road. Consequently, the two nest boxes were
matched in visibility. Shrubby vegetation lined the 40 m of roadside between
the two nest boxes, so they could not be seen simultaneously, except from
above. The two nest boxes were discovered nearly synchronously: 40 l nest box
at 09:33, 15 l nest box at 09:39. Furthermore, the two scout bees that
discovered these two nest boxes returned to the swarm cluster at about the
same time: Red from the 40 l nest box at 09:44, and Red–White from the
15 l nest box at 09:41. However, only one bee performed a dance; Red produced
162 dance circuits in the time period 09:44–09:50. By 9:50, when Red's
dance was finished, there was a clear difference in recruitment to the two
nest boxes: 23 bees were counted outside the 40 l nest box, whereas 0 bees
were counted outside the 15 l nest box.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The population-level coding of information about option value neatly solves
the problem of noisy individual-level coding of this information when there
are multiple bees reporting on each option more or less simultaneously.
However, at the start of the decision-making process, when the scouts are just
starting to discover, inspect, and report on potential nest sites, there will
be only a few bees reporting on each one and they will not be reporting
simultaneously, so there will be much stochasticity in the sensory input to a
swarm. Fig. 2 shows, for
example, how for the first few hours of decision-making process of one typical
swarm the scout bees' reports on the two experimental nest boxes varied
greatly from one 5 min block to the next, with signaling for the 40 l nest box
only in some blocks, signaling for the 15 l nest box only in other blocks, and
no signaling for either nest box in many blocks. Given this high-level of
sensory noise initially, even at the population level, it is not surprising
that at first there is also much unpredictability in the evidence accumulation
(build up of scouts) at the alternative nest sites [see for example,
figure 2 in Visscher and
Camazine (Visscher and Camazine,
1999) and figure 5
in Seeley and Buhrman (Seeley and Buhrman
2001)]. Swarms cope with this high noise initially in the evidence
accumulation by having a high quorum threshold for choosing a site:
10–20 bees at the entrance to the site, or some correlate thereof
(Seeley and Visscher, 2004;
Passino and Seeley, 2006). This
threshold is generally not reached until several hours have passed, by which
time sizable populations of bees will be reporting on the various sites under
consideration, hence there will be relatively low noise in the
population-level coding of the values of the sites and thus low noise in the
differential accumulation of evidence as a function of site value.
The potential for decision-making errors arising from the individual-level
noise in the sensory coding is especially great when each site is first
discovered by a scout bee, for if she fails to report it with a waggle dance,
the site will be lost from the swarm's attention. A solution to this problem
would be to have each scout bee that makes the initial discovery of a site
likely to report on the site, thereby bringing it to the swarm's attention.
Remarkably, the bees appear to do exactly this. We found that those scout bees
that first visited the nest boxes in each trial almost always
(P=0.86) performed dances upon return to the swarm, whereas the
scouts that visited the same nest boxes subsequently (probably having been
recruited to the boxes) were much less apt to dance (P=0.55). We do
not know what gave these initial scouts an especially strong stimulus to
dance. Perhaps it was each initial scout's experience of finding the site by
herself (not having followed dances to find it) or of inspecting the site by
herself (no encounters with other bees, no pheromones left by other bees,
etc.). This `discoverer-should-dance' solution is not foolproof, however. In a
study of the decision-making ability of swarms
(Seeley and Burhman, 2001), in
which swarms were presented with a five-alternative choice (one 40 l nest box
and four 15 l nest boxes), one swarm failed to choose the 40 l option because
the two scout bees that discovered it both failed to perform dances.
Consequently, the swarm `overlooked' the best alternative and chose one of the
inferior ones.
We have shown that a scout bee codes the value of a potential nest site by
adjusting the number of dance circuits that she produces to report the site
(Fig. 3), but this may not be
the full story. In his pioneering study of swarm decision making, Lindauer
(Lindauer, 1955) stated that
scouts reporting better sites appear to perform dances that are both
longer and livelier than do scouts reporting poorer sites.
Seeley and Buhrman (Seeley and Buhrman,
2001) checked Lindauer's observation by presenting a swarm with
both an excellent (40 l) and a mediocre (15 l) nest box and video recording
the dances of the scout bees for the two nest boxes, as they were performed
side-by-side on the swarm cluster. (Note: they did not follow individually
marked bees, so they could not measure the total number of dance circuits that
each bee produced over multiple bouts of dancing, as was done in the present
study.) They found that, on average, the scout bees from the better nest box
produced more dance circuits per return to the swarm. They also found that the
bees increased the number of dance circuits per return to the swarm
(C) by boosting both the duration (D, in seconds) and the
rate (R, in circuits per second) of dance-circuit production (note
that C=DxR). Close analysis of the video
recordings revealed that the scout bees adjusted R by changing the
duration of the return-phase portion of each dance circuit, decreasing it to
increase R. Evidently, it is this reduction in the return-phase time
in the circuits of dances for better sites that gave Lindauer
(Lindauer, 1955) the impression
that dances for better sites are livelier. We strongly doubt, however, that
adjusting R (dance liveliness) provides sensory coding in addition to
what is accomplished by adjusting C (dance length). In a study of how
bees report on food sources, it has been shown that nectar foragers adjust
C as a function of food-source profitability, and that they do so by
adjusting both D and R
(Seeley et al., 2000), but
that the difference in recruitment effectiveness between dances for a richer
and a poorer food source is explained fully by the difference in number of
circuits (C) in these dances
(Seeley and Towne, 1992). We
suspect that the same situation holds in reporting on nest sites: differences
in recruitment to sites that differ in value are explained fully by
differences in C between the dances representing the sites.
We have also confirmed previous reports
(Lindauer, 1955;
Seeley, 2003;
Visscher, 2003) that nest-site
scouts show decay in their dance response to a nest site, decreasing the
number of dance circuits produced per return to the swarm cluster
(Fig. 4). Seeley
(Seeley, 2003) reported an
average rate of dance decay of –15.7 dance circuits/return, and we found
a very similar value: –17.2 dance circuits/return. Sensory receptor
neurons often exhibit decay (adaptation) as a means of improving their ability
to report stimulus changes (Shepherd,
1988; Young,
1989), but this is probably not the functional significance of the
decay in dance response of nest-site scouts, since they are providing
information about stimuli (potential nest sites) that are changing little, if
at all. Their decay evidently serves instead to improve a swarm's
decision-making ability, by limiting the amount of positive feedback that each
bee generates in the build up of bees at her site and by limiting the number
of visits that each bee makes to a site. A modeling study of the bees'
decision-making process has shown that if there were no decay in the dance
response, then a swarm's decision-making speed would increase but its accuracy
would decrease; the swarm would be prone to making fast errors
(Passino and Seeley, 2006). The
decay of each scout bee's enthusiasm for her site also means that the
competitive process of accumulating bees committed to different sites is
`leaky'; shortly after a bee ceases dancing for a site she also ceases
visiting the site. Leakage in the accumulation of evidence is a key feature of
several models developed in mathematical psychology to model the neurobiology
of decision making [e.g. the leaky competing accumulator model of Usher and
McClelland (Usher and McClelland,
2001)]. In these models, leakage seems to improve decision making
by increasing the time over which noisy evidence accumulates until sufficient
information for a decision is obtained, i.e. leakage in the accumulation
process helps prevent fast errors.
In closing, it should be noted that a swarm's ability to build a useful
sensory representation of the alternative nest sites depends critically on
each scout bee tightly coupling her information about the value of a site and
with her information about the location when she produces her waggle dances.
Unless each scout bee makes location-specific signals of value, a swarm will
be unable to generate adaptively differential accumulations of decision
evidence (scout bees) at the different sites, and so achieve the decision
transformation (Fig. 1). It has
long been known how nest-site scouts code site location in their dances
(Lindauer, 1955), and this
report now makes it clear how they code site value. And because we know that
each nest-site scout visits and performs dances for just one site at a time
(Seeley and Buhrman, 1999)
(see also the records of individual bees in
Fig. 2), we can be confident
that there is a tight coupling of value information and location information
in their dances. Although unintended, the bees gave us an impressive
demonstration of just how effective this value-location coupling is when, on
the morning of July 17, the scout bee Red performed a dance indicating the
location of a high value site (the 40 l nest box), and this stimulated a rapid
buildup of scout bees at the 40 l nest box, but not at the 15 l nest box just
40 m (10°) away!
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Acknowledgments |
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