|
PATRICK H. WELLS & ADRIAN
M. WENNER
Department of Biology,
Occidental College, Los Angeles, California 90041, and Department
of Biological Sciences, University of California, Santa Barbara,
California 93106
Von Frisch and later adherents of the theory that honey bees
communicate by means of an elaborate dance are challenged by
controlled experiments which show that their data can be explained
in terms of olfactory cues.
Whenever new data and interpretations are presented which
cannot be reconciled with established beliefs, it is proper and
desirable that supporters of the traditional view should examine
these data and interpretations with great care, and offer such
objections as can be generated. In 1969, on the basis of studies
of the recruitment of honey bee foragers to food sources, we
compared the predictive powers of the classical "language"
hypothesis of von Frisch(1) with those of a simple olfaction
model for forager recruitment and concluded that olfaction provides
the best interpretation of our data(2).
Investigators who believe that honey bees have a language have
since challenged our conclusion(3-5), and two other recent articles(6-7),
while not including a discussion of our results, cannot be reconciled
with our interpretations. Our purpose here is to examine the
principal objections to our interpretations and present additional
data.
Procedure and Results
From earlier experiments,
we knew that scent fed into a hive on one day influences forager
recruitment on the next. We established a hive and a line of
three experimental sites, each 200 m from it, in a dry field.
The sites were approximately 150 m apart and the prevailing light
breeze never blew towards or from the hive. Instead, the wind
moved from site 1 to site 3, with site 2 in the middle.
During experimental periods of three hours, we fed scented sucrose
to ten marked regular foragers at each of sites 1 and 3. Recruited
bees were captured and killed. On a following day we fed unscented
sucrose at sites 1 and 3 and planted scented sucrose at site
2, which had not been visited by bees from our hive. In this
situation, the language hypothesis predicts that recruited foragers
would be captured at sites 1 and 3, both visited by successful
foragers from the hive. If, however, recruited foragers locate
food sources by olfaction, they should arrive at site 2 which
was not visited by any bees from the hive.
In four repetitions of this experiment (on days 2, 7, 12 and
16) we captured a total of twenty-five new recruits at site 1,
224 at site 2, and eight at site 3. Thus, newly recruited foragers
had located a site in the field not previously visited by them
or their hivemates, and had failed to arrive at locations about
which they should have been well informed (according to the language
hypothesis).
When foragers are experienced at a food site, they are again
recruited to it by odour cues rather than by languag(8, 9) and,
when odour cues are rigorously excluded, recruitment of new foragers
fails (2, 10). For example, on control days of our experiments
reported in 1969 when no scented sucrose was made available (days
4, 9 and 14), arrival of recruits at our feeding stations was
drastically curtailed(2). As a further control, we allowed ten
bees to fly to each of four unscented feeders for 3 h (July 25,
1968) for a total of 1,374 round trips. During this period
only five recruits from a hive of 60,000 bees found the feeders(2).
Thus, both experienced and inexperienced foragers seem to require
olfactory cues to locate a food source in the field. In the absence
of compelling evidence to the contrary, it is conservative to
suggest that olfaction alone is sufficient to account for recruitment
of honey bees to a food source.
Objections to Our Model
In spite of his polemic,
Dawkins(3) does offer one substantive objection by arguing that
bees are easily distracted from their "intended" (linguistically
communicated) goals. In this view, the bees which arrive at site
2 have been distracted from sites 1 and 3, a possibility which
deserves serious consideration. But in our experiment, site 2
was downwind from 1 and upwind from 3. Is it likely that recruited
foragers could be simultaneously distracted upwind and downwind
from their intended goals, or that any animal can be attracted
to a downwind odour source? In any case, when all three sites
were provided with unscented sucrose (days 9 and 14), recruits
failed to arrive at sites about which they were supposedly linguistically
informed(2). We conclude that Dawkins's "distraction"
model is not supported by the data.
Esch and Bastian(6) reported interesting new data but did not
relate their findings to the literature on forager recruitment.
In each of their experiments, a group of bees was trained to
feed at a scent-marked site near the hive, and ten of the foragers
were marked and confined temporarily in a cage. The feeder was
next moved to a new location 200 m from the hive and the number
of regular foragers reduced to one marked bee. The ten marked
former foragers were then released and observed, to discover
whether they would be re-recruited to the scent-marked feeder
at the new location, as they should be on the hypothesis of linguistic
communication by dance attendance.
Fourteen of seventy experimental bees did attend dances and subsequently
found the new feeder location. Nineteen additional marked bees
attended dances and flew from the hive without arriving at the
feeder. The remaining thirty-seven marked experimental bees had
no contact with the dancer and did not fly to the new location
of the feeder.
Ten of the fourteen successfully re-recruited bees required between
one and nine exploratory flights with intermediate contacts with
the dancer. Only four succeeded on the first flight, two of them
within 1 min of flight time. Many of the nineteen unsuccessful
dance attenders also made several flights from the hive;
they attended between five and thirty-one dances (mean, 17.5)
and made between one and nine exploratory flights (mean, 3.4),
without finding the feeder.
For the fourteen successfully re-recruited bees the mean time
in flight between first attending the dancer and locating the
feeder was 8.5 min, compared with less than 0.5 min for experienced
foragers(11). Esch and Bastian did not report the durations of
flights by unsuccessful dance attenders.
In spite of these negative results, Esch and Bastian consider
that their data support the language hypothesis. Because four
bees found the feeder on their first flights, it is inferred
that, "since they could not have searched the entire experimental
area in such a short time . . .",
successful re-recruits must have had prior knowledge (obtained
from the dance) of the feeder location.
By focusing attention on the performance of successful bees Esch
and Bastian have failed to recognize that most of their data
actually contradict the predictions of the language hypothesis.
The population of experimental animals must be viewed as a whole.
In reality, there was a total of 100 exploratory flights by marked
bees after attending the dancer. If recruited bees simply flew
out equally in all directions from the hive, like spokes in a
wheel, 2% would be headed within 7 degrees of the feeder location,
a result which is consistent with the observations of Esch and
Bastian.
More generally, the data obtained by Esch and Bastian do not
bear out the claim by von Frisch(12): ". . . the tail-wagging
dance makes known the distance and the compass direction to the
goal. . . . This description of the location enables the newcomers
to fly rapidly and with certainty to the indicated flowers, even
when these are kilometres away . . . an accomplishment on the
part of the bees that is without parallel elsewhere in the entire
animal kingdom". Nor do they eliminate the alternative possibility,
that re-recruited foragers were flying about, using wind and
odour, while seeking the scent to which they had been trained.
The article by Gould, Henerey and MacLeod(7) contains many data
not available earlier, but some of their data do not fall in
line with what one might expect from the dance language hypothesis.
As in the study by Esch and Bastian, their experiments were ".
. . designed to examine the behaviour of individual recruits
as each attended a dance and subsequently arrived at a feeding
station". In their series 1 experiment, marked bees were
trained to two feeding stations 120 m distant from and in opposite
directions from the hive, and many workers in the hive were given
individual marks. During experiments, of 277 potential recruits
observed to attend dances, 240 failed to arrive at any station,
and only thirty-seven were subsequently captured at the feeding
stations. Of these, a third arrived at a station in a direction
opposite to and 240 m distant from that "indicated"
in the dance maneuver. This result contradicts the prediction
of the language hypothesis that all thirty-seven of the successful
recruits should have arrived at the "correct" station.
These investigators also found that successful recruits spend
a considerable amount of time in flight before reaching the food
source. The direct line flight time between hive and a feeding
station located at 120 m is less than 25 s(11), and recruited
bees generally fly from the hive within a minute and a half after
leaving a dancing bee (50% leave within 30 s)(13). The data in
Table 4 of Gould et al.(7) reveal that the twenty-five
bees which did arrive at the "correct" station flew
an average of more than thirty times longer than would be necessary
to "fly rapidly and with certainty" to the food source.
The twelve bees which ended up at the station in the opposite
direction averaged only thirty-six times as long as necessary
for a direct flight.
A greater number of marked bees arrived at the statjon regularly
visited by the foragers which recruited them than to the one
240 m from it, and some successful bees found the food source
quickly (two in less than a minute), so Gould et al. concluded
that quantitative information was communicated by the dance.
The authors thereby focus attention on successful performers
as did Esch and Bastian.
In another experiment, these authors fed sucrose of high molarity
at one station and very low molarity at the other. Most of the
dancing in the hive was by foragers regularly visiting the high
molarity food source and during the experiments most of the recruits
captured were at that location. This correlation is accepted
by the authors as evidence of linguistic communication.
As Gould et al. carefully pointed out, the validity of
their interpretations for both of the above experiments depends
upon the assumption that perfect odour symmetry existed between
the two stations. In experiments of this type even small asymmetries
of location odour do influence recruitment(13). Gould et al.
located their stations in aromatic vegetation. They got uniformly
high recruitment whether or not they added scent to the food,
yet there is considerable evidence that recruitment is minimal
to an unscented location(2, 10). The high recruitment they obtained
indicates that the feeding locations had odours detectable by
bees. The unanswerable question is: Did asymmetries of these
odours exist between two feeding locations 240 m apart?
Mautz(5) also was concerned with the behaviour of individually
marked workers which came in contact with a forager dancing in
the hive. In his experiments, 32% of marked workers that attended
dances found the feeder, and the amount of time the potential
recruits attended the dancer was positively correlated with success
at finding the food. In addition, the average flight time for
successful recruits was more than ten times that expected of
experienced foragers and the mean flight time of bees which flew
out but failed to find the feeder was twice that of the successful
recruits. Mautz noted that one bee found a goal at 400 m after
following only five waggle cycles of the dance.
As with Gould et al., and with Esch and Bastian, Mautz
assumed that his feeder locations were not recognizable by bees
as olfactorily distinctive and that only linguistic information
could be communicated more effectively by increased duration
of contact with the dancer. He does not discuss the possibility
that a recruit which spends more time attending a dancing bee
might, by so doing, gain a more accurate impression of the odour
characteristics of a specific location. Again we see a supporter
of the language hypothesis focusing attention on the successful
recruits.
Of the several papers we review, Lindauer's(4) was the most deliberate
and direct effort to obtain data contradictory to our findings.
The first type of experiment undertaken by Lindauer resembled
those of Gould et al.(7) in design, and yielded
similar data. Forager bees were trained from a hive to two feeding
sites, and were then fed high molarity sugar at one and low molarity
sugar at the other. Virtually all dancing was by bees visiting
the high molarity sugar site, and most successful recruits landed
there. Lindauer assumed, as did Gould et al. and Mautz,
a perfect symmetry (to bees) of environmental odours at his locations.
From this he inferred that, "if the recruits followed only
the odour signals given by the dancers . . . they should have
appeared in equal numbers at (both) sites". In accordance
with his assumption Lindauer attributed the asymmetry in recruit
arrivals to linguistic communication. Thus, the untested assumption
of station symmetry (to bees) is central to the reasoning of
Lindauer as well as to the above authors.
In his second experiment, Lindauer put out three stations in
a geometry similar to that used in our experiments(2) and trained
bees to stations 1 and 3 but not to 2. Then, with scented sucrose
at all three stations (a variation from our design), he collected
recruits. Although the stations were deliberately asymmetrical
(no foragers at station 2), approximately one-fourth of all captured
recruits arrived at station 2. The language hypothesis predicts
that the recruits should have travelled only to stations 1 and
3.
In order to reconcile these data with the language hypothesis
Lindauer generated ad hoc the auxiliary hypothesis that
potential recruits alternate their attentions between dancers
visiting sites 1 and 3, and subsequently "integrate the
directions communicated by both groups of foragers". Although
the "integration" model satisfies Lindauer as an explanation
of his data, it could not possibly predict the distribution of
recruits in our earlier experiments(14, 15) or, indeed, in the
recent experiments of Gould et al.(7).
Lindauer got good recruitment at his stations 1 and 3 when presenting
unscented food at those locations. Interpreted in the light of
our data(2, 10) these results suggest that Lindauer's feeding
sites were in some measure distinctive to bees. This may explain
the asymmetry of recruitment he observed when foragers to station
1 were killed and bees visited only a single station. Unfortunately,
the precise location and ecology of the sites for these experiments
are not given in his paper (except that it was near Frankfurt),
nor does he provide dates, wind speed and directions, number
and sequence of observations contributing to the total data and
other relevant information. These omissions make any interpretation
difficult and speculative. Another portion of Lindauer's paper
offers some philosophical and rhetorical objections to our paper,
but we will consider these later.
Thus all the authors we have discussed(4-7) explicitly or implicitly
assumed that the feeding stations they established in the field
were in no way distinctive to bees and that the environment can
be made symmetrical with respect to odours and other factors.
They also assumed that, in order to find the food, a recruit
must have prior quantitative information about its location.
These assumptions lead the authors to interpret arrival of new
workers at sites visited by dancing foragers as definitive evidence
of linguistic communication. As pointed out earlier they have
focused their attention on successful recruits. Experiments based
on these assumptions invariably lead to affirmation of the consequence
of the hypothesis (if bees have a language, recruits will reach
the food. Some recruits find the food. Therefore, bees have a
language). This reasoning is deductively invalid(19).
The experimental designs of these investigators suffer yet another
serious disadvantage. It is not logically possible experimentally
to establish the validity of the station symmetry assumption
(failure to display asymmetry does not prove that none exists).
It is quite practical, however, to seek positive evidence of
station asymmetry in experiments of this design. One way would
be to remove all directional information from dances performed
by foragers regularly visiting food sites. If, in spite of this,
recruits preferentially arrive at the feeder regularly visited
by the foragers which recruited them, it could be concluded that
they had done so without use of prior directional information,
and that honey bees can exploit subtle environment asymmetries
in the recruitment of new foragers to food sources.
We have incorporated the use of "directionless" dances
in the design of the experiments reported below.
Conditions and Observations
In the summer of 1970
we did experiments using a single frame observation hive and
two feeding stations located 150 m from it in approximately opposite
directions (west and east of the hive, but slightly north of
it). The hive and stations were located at the University of
California, Santa Barbara. Both stations were located in dry
fields, devoid of green vegetation. The West Station was nearer
the sea and upwind the East Station somewhat closer to the University
buildings. Otherwise, the sites appeared to be symmetrical.
Ten marked foragers were trained to feed at each station; all
successful recruits were either killed or marked as replacements
for regular foragers which were then killed. Observations were
made at the hive and stations during 3-h periods (0830-1130),
August 21 to September 4, 1970, and food was provided only during
those periods. A westerly breeze prevailed during this period
(up to 5 mile h-1 on most days) and the usual temperature was
65 - 75 degrees F.
A principal objective of the experiments was to examine relationships
among food molarity, forager behaviour, and recruitment. Therefore,
scent added to the food was held constant. All solutions used
were scented with lavender oil (32 l. l.-1). Sucrose solutions
of 0.8 M, 1.3 M, 1.8 M and 2.3 M were used. On any given day
a solution of lower molarity was offered at one station and one
of higher molarity at the other. Rotation of molarities between
the stations controlled for possible inherent differences in
location attractiveness, and on each day the stations acted as
controls against each other. The experiments were run blind:
the observers were not informed of molarities of sucrose provided
at the feeding stations on any given day.
The hive had glass sides and was equipped with a clear plastic
atrial chamber inside a diffusely lighted observation room. Hive
conditions (well populated, and with little natural forage) ensured
that our marked foragers danced in the atrial chamber, rather
than on the comb. These dances were on a horizontal surface,
and contained no discernible directional information. The straight
(waggle) portions of the dance were apparently randomly oriented
and highly variable within each dance episode.
Altogether, a total of 1,793 dances by our marked bees and 136
dances by unmarked bees foraging on natural sources were observed
during eleven days (33 h) of experimentation. Thus, during our
study periods, 93% of all dancing in the hives was by our marked
foragers.
Although we were largely successful in eliminating oriented dances
from our hive, occasionally a marked forager did enter and perform
a dance episode on the vertical surface of the comb. These occurrences
will be of great interest to proponents of the language hypothesis,
so we will present data on oriented dances before proceeding
to other aspects of the study.
There was a total of only 50 apparently oriented dances recorded
during 33 h of experimentation; 1.5 such dances h-1, on the average,
or approximately 2.8% of all dance episodes recorded for our
marked foragers. These occurred equally (24 to 26) for the two
stations and did not correlate with recruitment (Table 1).
These oriented dances were not distributed evenly throughout
the experimental period, but occurred sporadically. For example,
40% of them occurred on one day, August 30, 1970. Occurrence
of a block of oriented dances on a given day did not appear to
influence recruitment. A comparison of data for August 30, 1970
(which had the greatest number of on-comb dances during the eleven
days of experimentation) with the following (more typical) day
is illustrative, and is presented as Table 2.
| Table
1 |
Dances by Unmarked
Bees, Oriented Dances, Disoriented Dances, and Recruitment |
|
| |
First
hour |
Second
hour |
Third
hour |
Total |
| Dances by unmarked
bees |
77 |
38 |
21 |
136 |
| Oriented dances
by marked bees |
23 |
9 |
18 |
50 |
| Disoriented dances
by marked bees |
337 |
675 |
731 |
1,743 |
| Successful recruits |
64 |
115 |
143 |
322 |
| Data are partitioned
according to time of occurrence in our experiments. Total data
for 33 h of observation are presented. |
| Table
2 |
Comparison of
Visitation by Marked Foragers, Oriented and Disoriented Dances
by Marked Foragers, and Successful Recruitment of New Bees for
August 30, 1970 (with many Oriented Dances) and August 31, 1970
(with few) |
|
| |
Trips by marked foragers |
Oriented dances |
Disoriented dances |
Successful recruits |
|
1.3M |
1.8M |
1.3M |
1.8M |
1.3M |
1.8M |
1.3M |
1.8M |
| August 30, 1970 |
319 |
267 |
9 |
19 |
76 |
110 |
20 |
65 |
| August 31, 1970 |
304 |
312 |
1 |
2 |
59 |
143 |
19 |
67 |
| Total |
623 |
579 |
10 |
21 |
135 |
253 |
39 |
132 |
Table 1 also shows that dancing by unmarked bees foraging on
natural food sources declined as the experiment progressed. This
is consistent with our findings that insertion of a new food
source in the hive-environment system may change the behaviour
of bees regularly foraging on an established one(10). Presumably
this alteration is mediated through a change in the available
recruit pool.
From our data on oriented dances (Tables 1 and 2) it is not possible
to infer that these dances are responsible for the observed recruitment
of new foragers to those feeders we had established in the field.
There is, however, a positive correlation between the number
of disoriented dances (or total dances) and recruitment of new
foragers (Table 3).
| Table
3 |
Mean Number of
Trips by Marked Foragers; of Disoriented Dances by those Foragers;
and of Successful Recruits per 3 h Observation Period for 0.8
M, 1.3 M, 1.8 M and 2.3 M Lavender Scented Sucrose Solutions |
|
|
Molarity |
Forager trips |
Disoriented dances |
Successful recruits |
|
0.8 |
308 |
26 |
5 |
|
1.3 |
320 |
86 |
19 |
|
1.8 |
293 |
117 |
42 |
|
2.3 |
231 |
107 |
17 |
| Not less than
four or more than seven observation periods at each molarity. |
The experimental design is not rigorous enough to define the
asymmetry in environmental cues used by recruits while searching
for and locating a particular feeder in the field, but quantitative
directional information does not appear to be a part of that
system.
While doing this set of experiments, we also gathered information
on Nasanov gland exposures at the food source by bees foraging
on various molarities of sucrose. Our previous studies indicate
that Nasanov gland exposure by regular foragers fails to attract
undisturbed bees but apparently does provide a point of reference
for disoriented members of the colony. Gland exposure is apparently
a function of the interest potential recruits may have in a food
source, rather than food quality per se(2, 10). Nasanov
gland exposure by foragers visiting established food sources
in the field was depressed at the lowest molarity we used (Table
4), a fact which indicates that few recruits were in the field
searching for that source.
| Table
4 |
Relationships
Among Molarity of Sucrose Solutions Provided, Forager Visitations,
and Nasanov Gland Exposures by Marked Foragers |
|
|
Molarity |
Forager trips |
Nasanov gland exposures |
|
0.8 |
308 |
24 |
|
1.3 |
320 |
77 |
|
1.8 |
293 |
85 |
|
2.3 |
231 |
71 |
| Means for 3 h
observation periods are given (7> periods/molarity
> 4). |
Further Considerations
We have done several
experiments which were designed to determine whether honey bees
use linguistic communication under defined conditions(2, 8, 9,
14-16). Results indicated that the language hypothesis has little
heuristic value and fails as a predictive tool. The results further
suggest that if one wished bees to pollinate a particular crop,
it should be useful to regulate the odour carried into the hive
by foragers, rather than the angle of dance on the comb.
More generally, we feel that honey bee foraging ecology is regulated
by a complex system of hive, environmental and behavioural variables.
With sufficient knowledge, it should be possible to manipulate
the system and predict the consequences for the foraging ecology
of a honey bee colony. We then might say that we understand colony
function in terms which are neither teleological nor anthropomorphic;
and we would be in a position to attack pragmatically problems
of a comparative or practical nature. Accordingly, we have examined
interrelationships among Nasanov gland exposure, visits of marked
foragers to a food site, dancing in the hive, and recruitment
of new foragers, and correlated these with the amount of odour
in sucrose solutions provided in the field. In these experiments
we have had some success in manipulating the system(10), as have
Waller(17) and Friesen(18).
Waller showed that association of odours with food in the field,
but not odours alone, could increase bee populations in experimental
plots(17). Friesen examined interrelationships among wind speed
and direction, forager flight paths, odour levels and locations,
forager visitation and recruitment of new foragers to sites in
the field. He concluded that, after recruits leave the hive,
their success and distribution depend upon an interaction of
field variables affecting the distribution of odours(18). Thus,
evidence from several sources indicates that odour is of great
importance in the system of variables which regulate honey bee
foraging ecology.
Our comparison of the predictive values of the olfaction and
language hypotheses of honey bee forager recruitment was an attempt
to determine just how important odour is in this system(2). To
our surprise, our results and interpretations generated a controversy
which deeply polarizes interested biologists. Along this line
we must stress that the controversy does not emerge from a difference
of opinion about the acceptability of various parts of a body
of evidence.
The ingenious step and fan experiments of von Frisch have been
repeated many times, and our own published data clearly show
that when his procedures are closely followed, without insertion
of additional controls, distributions of successful recruits
may be expected to resemble those obtained by him(14, 15). Similarly,
when Lindauer used an experimental geometry modelled after ours,
he obtained data consistent with ours(4); and the data presented
in Table 3 of this paper resemble those obtained by Gould et
al. and by Lindauer when they used similar experimental
designs(4, 7). Neither the repeatability of experiments on honey
bee behaviour nor the care and accuracy with which workers in
this field gather and report data appears to be in question.
Proponents of the language hypothesis argue that the many repetitions
of the von Frisch experiments make it highly probable that his
interpretation is correct. One must realize, however, that the
amount of additional confirmation affected by each new favourable
repetition of an experiment becomes smaller as the number of
previous repetitions grows(19). Thus, even under the most favourable
conditions, sheer number of repetitions is never sufficient to
render a hypothesis immune to challenge. Furthermore, in the
case of the bee language hypothesis, the existence of a considerable
body of unfavourable evidence greatly diminishes the weight of
even a large body of confirming data(20).
Any hypothesis which is generated as an explanation of certain
observed events will, of course, imply their occurrence. The
events to be explained will then be taken as supporting evidence
for it. If the hypothesis is valid it also may lead to a priori
predictions of facts and events in conditions different from
those leading to its formulation.
It is exactly here that we have difficulty with the language
hypothesis of honey bee orientation. Each time we have inserted
previously omitted controls or altered the experimental design
to create new test implications, the distribution of successful
recruits to feeders located in the field is no longer that predicted
by the language hypothesis. Similarly, much of the evidence recently
obtained by Esch and Bastian, by Mautz, by Gould et al. and
by Lindauer is contrary to the
predictions of that hypothesis(4-7).
The difficultles we had in reconciling our data(14-16) with the
language hypothesis led us to propose the alternative olfaction
model(21, 22). The olfaction hypothesis allowed a satisfactory
explanation of the distribution of successful recruits in those
experiments which incorporated new controls(14-16) and could
encompass the large body of existing data on honey bee forager
recruitment. Furthermore, it had the advantage of simplicity.
Thus, in 1967 we had two hypotheses, olfaction and language,
each generated a posteriori to explain an existing body
of evidence. The language hypothesis had been well articulated
by von Frisch twenty years earlier(1), but it had been expanded
and modified through the years in an attempt to explain newer
results. Olfaction, while new in the sense that it challenged
the then currently accepted hypothesis and two decades of thought
habits, was essentially a return to the position held by von
Frisch and others in the earlier years of this century.
Lindauer not only presented new data but challenged our interpretation
on philosophical grounds when he invoked Aristotelian (Darwinian)
teleology as an argument in favour of language. He argued that
in nature "each morphological structure and behavioural
act is associated with a special function. On this basis alone,
it would seem unlikely that information contained in the waggle
dance of a honey bee is not transmitted to her nest mates"(4).
We have answered his challenge in part by discussing the relevant
data in terms of philosophy of science which we consider to be
more powerful(19, 20).
An inherent weakness of Lindauer's teleological argument can
be illustrated by giving one interesting example from another
field of biology. Methyl eugenol is extremely attractive to male
oriental fruit flies. In one test in Hawaii 1,300 male Dacus
dorsalis were attracted a half-mile upwind to a muslin screen
that had been treated with it. Methyl eugenol is not produced
by the female fruit flies nor does it attract them. It is not
a component of the natural food of this fly and probably has
no nutritional value. Yet male oriental fruit flies are irresistibly
attracted to it and "apparently cannot stop feeding when
they have free access to it, and they kill themselves with over
indulgence"(23). Their behaviour under these circumstances
certainly cannot be construed as adaptive.
Admittedly, this is an extreme example of non-adaptive behaviour,
but it does reveal a weakness in the teleology argument. The
mere presence of a characteristic behavioural pattern in an animal
cannot be construed as purposeful, adaptive or "associated
with a special function".
Lindauer(4) also challenged us on grounds that we have not individually
discussed three specific situations investigated earlier by von
Frisch and his colleagues. First, at distances quite close to
the hive, recruited foragers may be captured at scented dishes
other than the one visited by the foragers which recruit them,
while at distances of 100 m and beyond "the recruited workers
all fly in the direction of the feeding plate". That the
latter part of this quoted statement does not hold is well documented
by the data of Gould et al(7) as well as by ours(2, 14,
15), and even by Lindauers own data(4) unless one is willing
to accept his "integration" model. As for the first
part of the statement, when the feeding dishes are close to the
hive, we agree with von Frisch and Lindauer; the bees seem to
be using odour.
A second situation involves disoriented dances performed by foragers
on a horizontal surface. In an experiment using a tilted hive,
von Frisch got approximately equal recruitment in four directions
while regular foragers were fed in only one direction. Later
that day, with the hive put upright again, he got preferential
recruitment in the direction of the feeder visited by foragers(12).
We prefer a design in which two or more stations visited by bees
simultaneously serve as controls against each other, and we set
up our experiment accordingly. Our data on the effectiveness
of disoriented dances (Table 3) seem to be in disagreement with
those of von Frisch. During our 11 days of observation, new recruits
preferentially arrived at the sites visited by dancing foragers
even though there was no directional component in the dances.
The third situation involves the detour of foragers around an
obstacle to a feeder on the other side of it. In one experiment
performed by von Frisch, marked foragers were trained to fly
around a rocky ridge to a scented feeder. Scent plates were placed
on top of the ridge and 50 m laterally to the direct line between
hive and feeder. During a 90 min period, three new recruits were
captured at the lateral stations, eight on top of the ridge and
twenty-three at the feeder. Because the new recruits apparently
failed to follow the flight path used by the foragers which recruited
them, von Frisch feels that they were linguistically informed
of the feeder location(12).
We must argue that the flight paths and duration of searching
by the twenty-three successful recruits are not known, and that
a failure of bees to use the detour (if indeed they did not use
it) does not differentially support either language or olfaction.
Since neither hypothesis predicts that recruits will follow the
same path as the marked foragers, the experiment is not crucial
and the results do not support or refute either hypothesis.
We believe that experimentation does not "prove" or
"disprove" hypotheses, but rather affects their credibility.
If the credibility of a hypothesis at any given time is determined
by the total body of relevant information available, then the
language hypothesis of forager recruitment was very credible
in 1946 when von Frisch proposed it. It is less so now, for the
body of relevant information is quite different and includes
much unfavourable evidence. In fact, it is so much less credible
that we no longer can believe that honey bees communicate linguistically.
Do honey bees have a language? That is a question which may never
be answered with certainty. It may be more useful to examine
assumptions critically, state hypotheses and their consequences
with precision, review the evidence objectively, and ask: can
we now believe that honey bees have a language? Thus, it appears
that the honey bee forager recruitment controversy is not about
the nature of evidence but rather about the nature of hypotheses(25).
It is not what investigators observe (the data) but what they
believe (infer) that is at the heart of the controversy.
We thank Nelson Dee and Stephanie Niebuhr for technical assistance.
The research was supported by the US National Science Foundation.
An analysis of earlier events and attitudes leading up to the
bee language controversy is available elsewhere(24).
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4 |
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M., Amer. Nat., 105, 89 (1971). |
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(1971). |
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Wenner, A. M.,
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| 12 |
Von Frisch, K.,
Tansprache und Orientierung der Bienen (Springer-Verlag,
Berlin, 1965); translation, The Dance Language and Orientation
of Bees (Harvard University Press, Cambridge, 1967). |
| 13 |
Johnson, D. L.,
and Wenner, A. M., J. Apic. Res., 9, 13 (1970). |
| 14 |
Johnson, D. L,
Science, 155, 844 (1967). |
| 15 |
Wenner, A. M.,
Science, 155, 847 (1967). |
| 16 |
Wenner, A. M.,
Wells, P. H., and Rohlf, F. J., Physiol. Zool., 40,
317 (1967). |
| 17 |
Waller, G. D.,
J. Apic. Res., 9, 9 (1970). |
| 18 |
Friesen, L., Biol.
Bull. (in the press). |
| 19 |
Hempel, C. G.,
Philosophy of Natural Science (Prentice-Hall, Englewood
Cliffs. 1966). |
| 20 |
Popper, K., in
British Philosophy in Mid-Century (edit. by Mace, C. A.)
(Macmillan, New York, 1957). |
| 21 |
Wenner, A. M.,
and Johnson, D. L., Science, 158, 1076 (1967). |
| 22 |
Wenner, A., and
Wells, P., XXI Int. Apic. Congr. Summ., 88 (1967). |
| 23 |
Steiner, L. F.,
J. Econ. Ent., 45, 241 (1952). |
| 24 |
Wenner, A. M..
The Bee Language Controversy (Educational Programs Improvement
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| 25 |
Altmann, S. A.,
Nature, 240, 361 (1972). |
|
