The tremble dance of honey bees can be caused by hive-external foraging experience
Department for Behavioral Physiology and Sociobiology, Würzburg University, Biozentrum, Am Hubland, 97074 Würzburg, Germany
Accepted 24 March 2003
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Summary |
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Key words: Apis mellifera, tremble dance, nectar foragers, nectar receivers, search time, unloading delay, waggle dance, foraging efficiency, honey bee
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Introduction |
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Kirchner and Lindauer (1994)
set out to test whether other factors than a long unloading delay can cause
tremble dancing, as was suggested by earlier studies
(Lindauer, 1948
;
Schneider, 1949
;
Schick, 1953
;
von Frisch, 1967
). Unlike
Seeley (1992
), who kept
conditions at the feeder constant during his experiment, these earlier studies
stimulated tremble dancing by manipulating the food source, e.g. by forcing
foragers to crowd at the feeder (von
Frisch, 1967
). However, unloading delays were not measured. This
would have been important, as a manipulation of the food source may affect the
duration of unloading delays (Kirchner,
1993
). Therefore, Kirchner and Lindauer
(1994
) tested whether crowding
at the food source caused nectar foragers to tremble dance because it delayed
the first unloading contact. They found that crowding stimulated tremble
dancing, and that it increased the time to the first unloading contact
(initial unloading delay) as well as the entire time before unloading contacts
that was not devoted to dancing or unloading (total unloading delay). From
this, Kirchner and Lindauer
(1994
) concluded that crowding
caused longer initial, and especially total, unloading delays, which then
caused nectar foragers to tremble dance. However, the study did not provide
information about how long after their return into the hive nectar foragers
started to dance. This information is important, because dancing can occur
before unloading, as Kirchner and Lindauer
(1994
) themselves note. Thus, a
forager that starts to tremble dance shortly after her return into the hive
can still experience a long delay until her first unloading contact, but this
long delay could not have caused the tremble dance. This means that not only
the delay until the start of unloading has to be measured, but also the delay
until the start of dancing.
I performed experiments to determine whether crowding at the food source caused tremble dancing because it delayed the time to the first unloading contact or the first dance. To do so, I manipulated the density of nectar foragers at the food source by reducing the size of an artificial feeder, and recorded a nectar forager's dance and the time interval between her entrance into the hive and her first unloading contact, or, if she started to dance before she unloaded, to her first dance.
To additionally examine whether tremble dancers from a non-manipulated colony usually experience long unloading delays, I recorded the unloading delays of nectar foragers that returned from natural food sources.
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Materials and methods |
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Food source
The food source used for the experiment was a grooved-plate feeder (e.g.
Seeley, 1995) that was located
25 m from the hive. The diameter of the feeder varied during the experiments
(see `Experiment' below). The feeder provided a concentrated sugar solution
[Apiinvert® (Südzucker), 2.4 mol l-1; sugar composition
61% glucose, 39% fructose] and supplied most, or all, of the food collected by
the colonies, as natural nectar sources were scarce during this time. Empty
feeders were refilled immediately by an assistant.
Experiment
During experiments in July and August 2001, I recorded the time interval
between a nectar forager's entrance into the hive and the start of her first
unloading contact or first dance, and the type of her dance (waggle dance,
tremble dance or no dance) before and during the manipulation of an artificial
food source. I recorded data during four experiments with each C1
and C2 for a total of eight experiments. Experiments started
between 09:00 and 13:00 h and consisted of a control phase that was followed
by a manipulation phase. Each control and manipulation phase lasted
approximately 50 min. During the control, the feeder had a circumference of 79
cm (diameter 25 cm) and was big enough to allow simultaneous access to all
visiting nectar foragers. During the manipulation, the feeder had a
circumference of 16 cm (diameter 5 cm), and was too small to allow
simultaneous access. To control the demand for nectar receiver bees in the
hive, the number of foragers that visited the feeder was kept constant
throughout the experiment (see below).
Measuring dances and unloading delay
To determine the number of nectar foragers that performed waggle dances,
tremble dances or no dances during each control and manipulation phase of the
experiment, I recorded the first dance that each observed forager performed.
Nectar foragers that did not dance were observed during their entire stay in
the hive. I recorded unloading delay as the time interval between a forager's
appearance in the entrance tunnel of the hive and the start of her first
unloading contact (tu), or, if she started to dance before
she unloaded, the start of her first dance (td). Only
trophallactic contacts of 3 s or longer were considered to be unloading
contacts. td is also referred to as `unloading delay',
because it is the best estimate for the time interval that informs a forager
about the availability of nectar receiver bees, usually the forager's
unloading delay, that an observer can have for a forager that starts to dance
before her first unloading contact.
Controlling the number of nectar foragers
I trained 200 nectar foragers of the observation colony to the feeder
before the experiments started. To recognize nectar foragers of the
observation colony, I marked bees entering the hive with one color, and added
at the feeder another color (for training and marking technique, see
von Frisch, 1967). At all
times, an assistant captured with forceps any unmarked bees from the feeder
and kept them in a wood cage until the training or experiment was finished. To
compensate for loss of foragers between experiments, 1030 additional
foragers from the observation colony were allowed to access the feeder after
each experiment. Although the total number of marked foragers might have
changed between experiments (e.g. decreased due to death, or
increased due to additional marking of foragers), it is unlikely that the
number of foragers changed significantly during an experiment. To
check whether approximately the same number of foragers visited the feeder per
unit time during each control and manipulation phase of the experiment, the
feeder assistant recorded every 5th min the number of nectar foragers at the
feeder during 3 control and 2 manipulation phases in experiments with
C1, and during 4 control and 3 manipulation phases in experiments
with C2. The assistant did not record the number of nectar foragers
when the tending of the feeder needed undivided attention.
Nectar foragers visiting natural food sources
To determine the dances and unloading delays of foragers that visited
natural food sources in May and June, 2001, I observed 63 nectar foragers from
C1 on 3 days, and 27 nectar foragers from C2 on 2 days
without providing a food source. Observations started at 08:00 h and lasted
until 15:0019:00 h. To reduce the probability of observing bees other
than nectar foragers, observations were interrupted when hive bees performed
their conspicuous orientation flights. Of the non-dancing bees, only those
that had at least one trophallactic contact before they exited the hive again
were considered to be nectar foragers. Although I could not distinguish
between foragers for water and for nectar, the probability of a forager
gathering water instead of nectar is much smaller (e.g.
Seeley, 1986). Hence, it is not
likely that water foragers introduced a large bias in the study. As foragers
were not marked, I was not in all cases (approx. 29%) able to observe
non-dancing nectar foragers throughout their entire stay in the hive. As
foragers were most likely to waggle dance, the sample size for non-dancing
nectar foragers might be biased upward. Bees that were lost out of sight had
on average been observed for approx. 75% of the time that full observations
lasted. Thus, the results for tremble dancers and, especially, waggle dancers
might be biased downward.
Statistical analysis
To analyze whether tremble dancing was caused by a long unloading delay, I
compared the unloading delays of waggle dancers and tremble dancers in each
control and manipulation phase of the experiment. I did not compare the
unloading delays of a group of dancers between phases, because even
if unloading delay increases in the manipulation phase, this increase could
only be the cause of tremble dancing if waggle dancers did not experience a
similar increase in unloading delay.
Measurements are given as means ± one standard deviation
(S.D.). Statistical tests used are given in the text.
All data were analyzed using the ME edition of Microsoft Excel and the 2002
edition of Statistica. Bonferroni corrections for multiple comparisons were
performed according to Sokal and Rohlf
(1995). The adjusted
-level is noted in the text.
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Results |
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Number of nectar foragers did not change during experiment
To estimate the number of nectar foragers that simultaneously visited the
feeder, an assistant recorded the number of nectar foragers at the feeder
every 5th min during 7 control phases and 5 manipulation phases. In
C1, the average number of nectar foragers at the feeder was
72±10 foragers min-1 during the control phase
(N=3), and 76±11 foragers min-1 during the
manipulation phase (N=2). In C2, the average number of
nectar foragers was 47±11 foragers min-1 during the control
phase (N=4), and 57±6 foragers min-1 during the
manipulation phase (N=3). The number of nectar foragers at the feeder
was lower during the control phase than during the manipulation phase, but
this difference was not significant for either colony (MannWhitney
U-test; P>0.275 for each comparison). For the following
analysis, data from C1 and C2 were pooled.
Manipulation increased tremble dancing rate
During the control phase, 36 nectar foragers performed a tremble dance, 115
performed a waggle dance, and 59 did not dance. During the manipulation phase,
161 nectar foragers performed a tremble dance, 23 performed a waggle dance,
and 45 did not dance. The probability for a nectar forager to tremble dance
was significantly higher during the manipulation phase than during the control
phase of the experiment (Fig.
1, MannWhitney U-test; P=0.005,
N=8). The probability to waggle dance was significantly lower during
the manipulation phase than during the control phase (P<0.001),
and the probability to not dance did not change (P=0.431).
|
Most nectar foragers danced before they unloaded
Fig. 2 shows the percentage
of nectar foragers that started to dance before they unloaded. During the
control phase of the experiment, 57% of the waggle dancers (N=115)
and 92% of the tremble dancers (N=36) started to dance before they
had their first unloading contact. During the manipulation phase of the
experiment, 48% of the waggle dancers (N=23) and 90% of the tremble
dancers (N=161) started to dance before they had their first
unloading contact.
|
Tremble dancers and waggle dancers did not differ in
tu or td
Fig. 3 shows dancing (waggle
dancing, tremble dancing or no dancing) as a function of the time interval
between a forager's entrance into the hive and her first unloading contact
(tu) or first dance (td). Mean values
and sample sizes are given in Table
1. Tremble dancers and waggle dancers did not differ in
tu during either the control phase (MannWhitney
U-test; P=0.666) or the manipulation phase of the experiment
(MannWhitney U-test; P=0.352). Tremble dancers and
waggle dancers did not differ in td during the control
phase (MannWhitney U-test; P=0.784), but during the
manipulation phase, tremble dancers had a significantly shorter
td than waggle dancers (MannWhitney
U-test; P<0.001). Non-dancing nectar foragers did not
differ in tu from waggle dancers or tremble dancers
(MannWhitney U-test, P>0.07 for all
comparisons).
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Nectar foragers visiting natural food sources
To record unloading delays of unmanipulated nectar foragers, I observed 38
waggle dancers, 23 tremble dancers, and 29 non-dancing nectar foragers that
had visited natural food sources. 68% of the waggle dancers and 78% of the
tremble dancers danced before they had their first unloading contact. Tremble
dancers and waggle dancers did not differ in either tu
(MannWhitney U-test; P=0.527) or
td (MannWhitney U-test; P=0.830).
Non-dancing nectar foragers had a significantly longer tu
than either tremble dancers or waggle dancers (MannWhitney
U-test; adjusted -level 0.017, P>0.020). Values
are given in Table 1.
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Discussion |
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Most tremble dancers (approximately 91%) started to dance before they had
their first unloading contact, and usually started to dance as early as, or
earlier than, waggle dancers. Because tremble dancers may dance for up to 1.5
h, and rarely stop dancing to unload
(Seeley, 1992;
Thom et al., 2003
), these
tremble dancers could have had their first unloading contact late during their
stay in the hive. Therefore, Kirchner and Lindauer
(1994
), who measured the time
to the first unloading contact, but not to the first dance, are likely to have
reported longer unloading delays than tremble dancers actually
experienced.
In comparison to the study by Seeley
(1992), I observed (1) a higher
level of tremble dancing during both control and manipulation phases of the
experiment, and (2) possibly more tremble dancers that danced before they had
the first unloading contact. Both observations suggest that nectar foragers
had a higher motivation to tremble dance in this study than in Seeley's 1992
study. During the manipulation phase of the experiment, a higher motivation
for tremble dancing could have been the different tremble dance stimulus
(crowding instead of long unloading delays). During the control phase, nectar
foragers may have had a higher motivation to tremble dance, e.g. because
unwanted foragers may have released alarm pheromone when they were captured,
or the many nectar foragers that visited the feeder simultaneously
(4776 bees) interfered at a low level with each other. Kirchner and
Lindauer (1994
), who also
trained 200 foragers to a well-sized feeder, found even higher levels of
tremble dancing (32% of all foragers) than this study (17% of all foragers).
In general, crowding may have affected several parameters at the food source,
including access to the feeder, efficiency of food loading, or concentration
of alarm pheromone, which could have motivated nectar foragers to tremble
dance.
Although the exact parameters that crowding changes at a food source are
not yet identified, the short unloading delays of tremble dancers are not
likely to be artefacts. Many tremble dancers that had visited natural food
sources had equal, or shorter, unloading delays than waggle dancers. This
suggests that tremble dancing is an adaptive reaction to stimuli external to
the hive. These stimuli, like crowding, are likely to be related to a decrease
in foraging efficiency. One example is given by von Frisch
(1967), who reports that
tremble dancing can be elicited by sticky food sources such as
Asclepias (Asclepiadaceae) flowers. Therefore, the results of this
study suggest that the tremble dance may have an additional function to the
recruitment of nectar receiver bees. Tremble dancing in this study was not
caused by a situation usually associated with a shortage of nectar receiver
bees, and hence may not serve to adjust the number of nectar receiver bees.
Instead, when tremble dancing is a reaction to a decrease in foraging
efficiency at the food source, it may be supposed to direct foragers away from
this, and possibly toward other, food sources.
It may be important to notice that not only tremble dancers, but also
waggle dancers often (4857%) started to dance before they had their
first unloading contact. Hence, these waggle dancers did not seem to have
information about the availability of nectar receiver bees but, like tremble
dancers, may have been stimulated to dance mostly by the quality of the food
source. As neither the waggle dance nor the tremble dance seem to always
regulate the number of nectar receiver bees, it can be supposed that nectar
receiver bees regulate their activity themselves. For example, nectar receiver
bees may often adjust their activity by assessing and reacting to the
conditions on the dance floor. Unlike waiting, and thus inactive, foragers who
miss valuable opportunities to gather nectar, inactive nectar receiver bees
may impose a relatively small, or no, net cost on the colony. This could be
because nectar receiver bees are usually middle-aged workers
(Seeley et al., 1996), which
have been suggested to be often unemployed
(Seeley, 1995
;
Kühnholz and Seeley,
1997
). Furthermore, nectar receiver bees might enhance colony
foraging efficiency not only by unloading nectar foragers, but also by
sampling the quality and availability of nectar, which may later enable them
to chose more profitable food sources. Hence, it can be speculated that the
net cost to the colony that these unemployed workers impose by waiting for
nectar foragers may be low, and often negligible. Therefore, nectar receiver
bees may often regulate their activity based on information they acquired by
sampling nectar foragers, and only be recruited by the tremble dance when a
sudden nectar influx requires an exceptionally fast increase in the number of
nectar receiver bees.
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Acknowledgments |
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Footnotes |
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References |
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