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Animal behaviour
Working against gravity:
horizontal honeybee
waggle runs have greater
angular scatter than
vertical waggle runs
Margaret J. Couvillon1,*, Hunter L. F. Phillipps1,
Roger Schu
¨rch2and Francis L. W. Ratnieks1
1
Laboratory of Apiculture and Social Insects, School of Life Sciences, and
2
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
*Author for correspondence (m.couvillon@sussex.ac.uk).
The presence of noise in a communication system
may be adaptive or may reflect unavoidable
constraints. One communication system where
these alternatives are debated is the honeybee
(Apis mellifera) waggle dance. Successful foragers
communicate resource locations to nest-mates by
a dance comprising repeated units (waggle runs),
which repetitively transmit the same distance and
direction vector from the nest. Intra-dance waggle
run variation occurs and has been hypothesized as
a colony-level adaptation to direct recruits over an
area rather than a single location. Alternatively,
variation may simply be due to constraints on
bees’ abilities to orient waggle runs. Here, we ask
whether the angle at which the bee dances on
vertical comb influences waggle run variation.
In particular, we determine whether horizontal
dances, where gravity is not aligned with the
wagglerunorientation,aremorevariableintheir
directional component. We analysed 198 dances
from foragers visiting natural resources and found
support for our prediction. More horizontal
dances have greater angular variation than dances
performed close to vertical. However, there is no
effectofwagglerunangleonvariationinthedur-
ation of waggle runs, which communicates
distance. Our results weaken the hypothesis that
variation is adaptive and provide novel support for
the constraint hypothesis.
Keywords: honeybee; Apis mellifera; waggle dance;
foraging; animal communication; signal noise
1. INTRODUCTION
Communication normally involves some imprecision in
the information transfer from the signal producer to the
signal receiver [1]. The reason for the presence of this
imprecision, which may occur at different stages (e.g.
signal production, transmission and reception), is a
matter of debate. Specifically, is the imprecision an
adaptive feature that has evolved to benefit the system
[2,3] or does it reflect constraints [4]?
One communication system central to this debate is
the honeybee (Apis mellifera) waggle dance, where a suc-
cessful forager, upon returning to the hive, performs a
stereotyped behaviour where she advances linearly in
one direction on the comb while waggling her body at
ca 15 Hz [5] from side to side (waggle run). She then
turns to the left or right and usually circles back to the
start (return phase) to repeat the waggle run. This circuit
of waggle run þreturn phase may be repeated 1 to 100þ
times, depending on resource quality [6,7]. The waggle
run conveys the direction and distance vector from the
nest to the resource location: distance is encoded in
the duration of the waggle run and direction by the
angle of the dancer’s body relative to the vertical [8].
The return phase is free of vector information [7,9].
For both angle and duration, there is a variation
among the repeated waggle runs [10 –12]. It has
been hypothesized that this scatter is adaptive because
it directs recruits to a general area, as opposed to a
specific point [6,13 –15], which is how scattered,
floral resources sometimes occur in nature. In contrast
to this tuned error hypothesis, under the physiological
constraint hypothesis, the bees simply cannot dance
more precisely [16,17] and the variation does not
serve an adaptive function.
In this study, we investigated whether variation
among waggle runs within a dance is affected by gravity.
We hypothesized that angular variation would be greater
when a bee is dancing horizontally (around 908or 2708)
on the vertical comb versus dancing vertically (around
08or 1808). The reason for this is that when a bee
makes a vertical waggle run, either up or down, the grav-
itational force is aligned to the waggle run (figure 1a).
In contrast, a bee making a non-vertical waggle run
will experience a gravitational force perpendicular to
the waggle run and proportional to the absolute value
of the sine of the angle from vertical (figure 1b,c). This
force is at its maximum when the bee is dancing
horizontally (figure 1d). In this way, we predict that
angular variation will increase from 08to 908or from
1808to 2708, and decrease from 908to 1808or
from 2708to 3608. Conversely, we predict no effect of
waggle run angle on variation in the duration of waggle
runs (figure 1,d
1
–d
3
) because gravity should not affect
the ability of a dancing bee to measure time.
2. MATERIAL AND METHODS
Using the methods of Couvillon et al. [10], we videotaped and decoded
waggle runs within natural dances performed by foragers returning to
three glass-walled vertical observation hives. Dances were decoded by
hand on iMac computers using FINAL CUT EXPRESS (v. 4.0.1). To
decode a waggle run, we extract two pieces of information: duration,
which we obtained by noting the start and stop times of waggle run,
and orientation clockwise from vertical, which we measured by
making two marks on the screen over the dancer’s thorax near the
start and end of a waggle run. We then measured the angle of
the line running throughthese two points relative to vertical plumbline
on the observation hive visible on the video (maximum measurement
error approx. 18). Previous work has shown that taking the mean
of any four, preferably consecutive, mid-dance waggle runs gives
a good estimate of the whole dance [10], so thus we did to obtain a
single angle and duration mean per dance. As a measure of variation,
we determined the standard deviation (s.d.) of angle and duration
for the four waggle run sample.
We decoded and analysed 198 dances with angles ranged from 08
to 3608. We converted angles over 1808to their mirror equivalent
angle between 08and 1808clockwise from vertical (e.g. 3008
become 608). Although angles are graphed in degrees, they were ana-
lysed in radians. Waggle run durations ranged from 0.31 to 4.83 s,
which correspond to resource distances of 200–5000 m [8]. These
are typical foraging ranges for honeybees [18,19].
We built two linear models using MINITAB (v. 14.2). In the first
model, we analysed the response variable of angle s.d. (radians and
square root-transformed) against the factors of angle average
(between 08and 1808, in radians), sine of this angle average and
duration average. In the second model, we analysed the response
Biol. Lett. (2012) 8, 540–543
doi:10.1098/rsbl.2012.0182
Published online 18 April 2012
Received 2 March 2012
Accepted 23 March 2012 540 This journal is q2012 The Royal Society
