Proc. Natl. Acad. Sci. USAVol. 91, pp. 4471-4474, May 1994Neurobiology

Development of sun compensation by honeybees: How partiallyexperienced bees estimate the sun's course

(learnlng/nemory/spatial cogiton/navigation/orientatlon)

FRED C. DYER* AND JEFFREY A. DICKINSONDepartment of Zoology, Michigan State University, East Lansing, MI 48824

Communicated by Charles D. Michener, January 28, 1994 (receivedfor review September 18, 1993)

ABSTRACT Honeybees and some other insects, in learn-ing the sun's course, behave as if they can estimate the sun'sposition at times of day when they have never seen it, but thereare competing ideas about the computational mechanismsunderlying this ability. In an approach to this problem, weprovided incubator-reared bees with opportunities to fly andsee the sun only during the late afternoon. Then, on a cloudyday, we allowed bees to fly for the first time during the morningand early afternoon, and we observed how they oriented theirwaggle dances to indicate their direction offlight relative to thesun's position. The clouds denied the bees a direct view ofcelestial orientation cues and thus forced them to estimate thesun's position on the basis of their experience on previousevenings. During the test days, experience-restricted beesbehaved during the entire morning as if they expected the sunto be in an approximately stationary position about 180° fromthe average solar azimuth that they had experienced on pre-vious evenings; then from about local noon onward they usedthe evening azimuth. This pattern suggests that honeybees areinnately informed of the general pattern of solar movement,such that they can generate an internal representation thatincorporates spatial and temporal features of the sun's coursethat they have never directly seen.

A wide variety of animals can use the sun's azimuth as a truecompass, compensating for its daily movement relative toterrestrial features (1-3). Complicating this task is that theazimuth changes at a variable rate over the day, shiftingrelatively slowly as the sun rises in the morning or sets in theevening and rapidly as the sun crosses the local meridian atmidday. Furthermore, the daily pattern of change, theephemeris function, varies with season and with latitude.Animals are generally thought to learn the current localephemeris function, rather than using the average rate of shiftof the azimuth. What little is known about this learningprocess suggests that animals do not merely memorize aseries of time-linked solar positions. Instead, in a wide rangeof invertebrate (4-12) and vertebrate (13-15) taxa, animalshave been shown to estimate solar positions that they havenever seen. For example, in a classic series of experiments,Lindauer (4, 5) showed that incubator-reared honeybees(Apis mellifera) that were allowed to see only the western halfofthe sun's course (from noon onward each day) could, whenthey flew for the first time in the morning, use the sun tosearch for food in a direction in which they had been trained.Thus, somehow they had correctly learned to expect the sunin the eastern half of the sky in the morning. In this paper weask what integrative mechanism might underlie this apparentability ofbees to compute solar positions that till gaps in theirexperience of the sun's course.

Four distinct computational strategies have been proposedto account for the ability of insects to estimate unknownpositions of the sun. Three of these assume the existence ofneural computations that operate on time-linked measure-ments of the sun's position relative to the landscape, tocalculate a compensation rate specific to each gap in theanimal's experience that needs to be filled. First, the animalmight "interpolate" at a linear rate to estimate the sun'sposition between temporally adjacent known positions. Sec-ond, she might extrapolate" the sun's course forward at alinear rate based upon the azimuth and rate ofmovement thatshe has observed most recently. Third, she might extrapolate"backward" at a linear rate based upon the azimuth and rateofmovement that she has observed at a later hour on previousdays. Each of these hypothesized mechanisms could be usedto assemble, through repeated measurements of the sun'sposition over the day, a representation of the current localephemeris function. Although studies of honeybees (Apisspp.) (6, 16) and desert ants (Cataglyphis spp.) (8, 17) havetended to favor the linear interpolation hypothesis, other dataseem best accounted for by the forward (9, 18) and backward(9) extrapolation hypotheses. Some data, including Lindau-er's (4, 5) observations, are consistent with all of theseproposed mechanisms.A more recent study of Cataglyphisfortis (19) suggested an

entirely new hypothesis: that the ants might rely upon aninnate knowledge of the general pattern of solar movement,which allows individuals with limited experience to developan approximate representation ofthe sun's entire course. Theapproximate representation is assumed to be adjusted byexperience to match the sun's actual course more closely.Experimental data decisively excluded the linear interpola-tion and extrapolation hypotheses for this ant; the evidencefor the new hypothesis, however, was open to other inter-pretations (see ref. 19).We developed an approach to this problem that is inspired

by Lindauer's studies of experience-restricted bees but thatrelies upon observations of dance orientation rather thanflight orientation. The bees' communicative waggle dancesencode in their orientation the direction offood relative to thesun and thus reflect the bees' determination of the currentsolar azimuth (20). By testing bees on cloudy days, we forcedthem to rely upon an internal estimate of the solar azimuthinstead of a direct measurement. Fully experienced beesorient their dances on cloudy days by drawing upon anaccurate memory of the sun's entire course relative tofamiliar features of the terrain (16, 21). We hoped that dancesby experience-restricted bees would reveal how they esti-mated the sun's position when they flew under cloudy skiesat a new time of day.

METHODSWe performed experiments with two small colonies formedentirely of bees that had emerged from brood comb in an

*To whom reprint requests should be addressed.

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4472 Neurobiology: Dyer and Dickinson

incubator. The experimental bees were allowed out of thehive only during the last =4 hr of daylight each afternoon, sothat they could see the sun over only 45-50° (z2MO) of itsdiurnal course. During the daily flight period bees weretrained to visit a feeder offering sugar syrup 350 m south ofthe hive (along a line of tall trees to provide a reliablereference for flight orientation and for learning the sun'scourse; refs. 16 and 21) and were given identifying labels.During times other than the flight period, colony 1 was movedindoors, where diffuse light was provided through a windowto expose bees to the natural photoperiod. Colony 2 remainedin place at all times and was set up to provide differingexperience to two groups of bees. One group, which servedas experience-restricted bees, was labeled on the thorax withlarge plastic tags, while a second group, which was allowedto fly throughout the day, was labeled with dots of paint.Modifying a method developed by G. S. Withers, S. E.Fahrbach, and G. E. Robinson (personal communication),we placed a metal grating over the hive entrance to preventthe departure of tagged bees, but not paint-dotted or un-treated bees, until the beginning of the daily flight period. Inboth colonies, the experience-restricted foragers flew duringthe afternoon training period for at least 7 days prior to thetest; Lindauer (5) found that bees with afternoon experiencecan estimate the morning position of the sun after 3-5 daysof experience. On the day of a test, we allowed all bees outof the hive in the morning under a cloudy sky and through awindow in the hive observed their dances after they returnedfrom the training feeder. The orientations of waggling runsrelative to gravity were measured with a protractor.The cloud cover during both experiments was thick and

homogeneous and produced almost continuous light rain.Clouds depolarize sky light and block the sun from view, thusdepriving bees of celestial orientation cues. Bees were oncethought to determine their orientation relative to the sun oncloudy days primarily by detecting the sun directly in theultraviolet (22). More recent studies, however, suggest thatbees should rarely, if ever, be able to see the sun when it isinvisible to human observers. Physical measurements ofradiance patterns across an overcast sky (23) failed to detectthe sun in any wavelength, unless it became visible to thehuman eye. Also, observations of bees dancing on overcastdays showed that the sun or blue sky is virtually alwaysvisible to human observers when bees base their dances ondirect measurements of celestial cues during the flight ratherthan on memory (16); we could detect no such inhomogene-ities in the cloud cover during our experiments.

RESULTSThe dance orientations of the experience-restricted bees,which had never before flown or danced during the morningor early afternoon, fell into a striking pattern that crudelyapproximated the actual course of the sun (Figs. 1 and 2).With considerable consistency among bees, and among dif-ferent dances by the same bees, dances performed in themorning suggested that bees expected the sun to be almostexactly 1800 from its position in the late afternoon. The beesmaintained this orientation until a short interval at middaywhen, as a group, they changed their dance angles by 1800.(The shift occurred about an hour earlier in colony 1 than incolony 2, perhaps because bees in the two colonies experi-enced slightly different photoperiod cues.) After the shift thebees maintained the new orientation with little change. Thissame pattern was exhibited by bees that performed manydances throughout the day and thus does not represent twopopulations of differently oriented bees. Strikingly, the onlyexceptions to the pattern were two bees in colony 1 thatadopted the evening angle in the morning and the morningangle in the afternoon (Fig. 1).

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FIG. 1. Solar azimuths (in degrees clockwise of north = 0°)inferred from dances performed by experience-restricted bees incolony 1 after flights under a thick, uniform cloud cover to a familiarfeeding station in the south. The solid curve shows the actual path ofthe solar azimuth and the dashed lines (1-3) show the paths generatedby three mechanisms by which insects have been hypothesized to fillgaps in their experience of the sun's course. Data (+, o, A) are from554 dances performed by 46 different experience-restricted beesduring a continuous period of overcast weather from 10:00 23 July1992 to 10:30 24 July. For bees dancing to food in the south (1800clockwise of north), the solar position being used by a bee can beinferred from her dance angle 8 (measured to nearest 5° clockwisefrom vertically upward) as 1800 - 8 when 00 < 8 < 1800, and 180 +(360° -8) when 360 > 8> 180. The open symbols (o, A) are the datafrom two bees that differed qualitatively from the pattern exhibitedby the remainder. All bees had at least 7 days of experience flying tothe food before they were tested. Prior to the test day, bees could flyonly between 15:00 and sunset (=19:20) (shaded area); thus theycould see only about 19%o of the sun's entire diurnal course at thistime of the year. Control observations showed, as expected (16, 21),that bees oriented their dances to take the sun's position into accountwhen they saw it during the training period and when they saw it forthe first time on a flight outside the training period. The sun azimuthcurve is from 21 July 1992, the last time the bees could have seen thesun (22 July was also cloudy). Predicted angles and rates of com-pensation from given (time, azimuth) coordinates were obtained asfollows. 1. Linear interpolation (6, 8): bees are assumed to compen-sate at a constant rate (16.1 deghr-1) from the azimuth at the end ofone training period (19:20, 298°) to the azimuth at the beginning ofthenext training period (15:00, 2540). 2. Forward extrapolation (9, 18):bees are assumed to measure the rate of azimuthal shift over the last

hour of the training period (9.8 deg-hr-1), then to estimate the sun'sposition in the morning by compensating clockwise at this ratethrough the night from the end of the previous day's training period(19:20, 2980). 3. Backward extrapolation (9): bees are assumed tomeasure the net rate of shift over the first hour of the training period(9.7 deg-hr-1) and to compensate counterclockwise at this rate todetermine the azimuth at times prior to the start ofthe training period(15:00, 2540) on subsequent days.

The linear interpolation, forward extrapolation, and back-ward extrapolation hypotheses failed to predict the particularorientations adopted by dancers at most times of day, andnone of these hypotheses predicted the abrupt shift in ori-entation at midday. Conceivably some combination of thesehypotheses explains the bees' behavior, but we believe itmore parsimonious to reject all three, at least for the condi-tions of this experiment.Another possible interpretation of the data, given that the

solar positions estimated by dancers usually did not deviateenormously from the actual azimuth, is that bees obtainedduring the flight a skewed, but nevertheless direct, measureof the sun's position. As discussed, the completeness of thecloud cover during our experiment should have precluded

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Neurobiology: Dyer and Dickinson

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FIG. 2. Solar azimuths inferred for dances performed by bees incolony 2 after flights under a cloudy sky on 28 August 1992. The beeshad 9 days of experience flying to the food before they were tested.(A) Data (+) from 180 dances by 29 different experience-restrictedbees, which had previously flown only during a daily flight periodfrom 14:30 to sunset (=18:40) and thus had seen only about 23% ofthe sun's diurnal course. Sun azimuth curve is from 27 August 1992.Predictions 1-3 were derived using the methods described in thelegend to Fig. 1. (B) Data (e) from 60 dances by at least 11 differentbees that previously had flown to the food throughout the day. (Tenof the dances were by paint-dotted bees whose identity could not bedistinguished; the number of different dancers therefore could havebeen as high as 20.) The cloud cover was thick and uniform andproduced almost continuous light rain; heavy rain prevented the beesfrom flying between 12:00 and 13:00.

this possibility. Also, it seems most unlikely that bees ex-tracting a weak visual signal from the noise of the overcastsky should have been so consistent in their measurement ofthe sun's position. Finally, a control is provided by ourexperiment with colony 2 (Fig. 2), in which experience-restricted bees conformed to the basic pattern already de-scribed, while bees that had previously foraged throughoutthe day tracked the course of the sun more accurately, as

expected from previous work (16). Had celestial cues beenvisible through the cloud cover to bees on their flightspreceding the dances, the behavior of the two groups, whichflew together under the same sky, might have been similar.Thus, we conclude that both groups internally generated anestimate of the sun's position relative to local landmarks, butdiffered because of the extent of their past experience.The bees' behavior over the day is well described by a

simple step function in which a single morning angle isreplaced by a single afternoon angle at midday (10:50 for

FIG. 3. Illustration of 1800 step function (heavy lines) used tomodel the bee's estimation of the sun's course at times of day otherthan when they have previously seen it. Plotted for comparison arethe ephemeris functions on the June solstice for three differentlatitudes: a, 42.750 N (the latitude at which the present study wascarried out); b, 250 N; c, 100 N. The step function is constructed byassuming that afternoon-experienced bees measure the sun's averageposition relative to local landmarks during the daily training period.They subsequently expect the sun to be at this same position duringtimes of day after local noon and at the azimuth 1800 from thisposition during times of day prior to local noon. Only the stepfunction for 42.750 N is drawn on the graph.

colony 1, 12:00 for colony 2), such that the morning angle isexactly 1800 from the azimuth experienced at the middle ofthe afternoon flight period (2700 for colony 1, 2560 for colony2) (Fig. 3). For the experience-restricted bees (excluding thetwo exceptional bees in colony 1, which seemed to use a 1800step function that was out ofphase by 12 hr or 1800), the stepfunction accounts for the variance in the data significantlybetter than does the actual ephemeris function (colony 1: Fs= 2.011, df = 536, 536, P < 0.001; colony 2: Fs = 2.764, df= 179, 179; P < 0.001). For the fully experienced bees incolony 2, by contrast, the actual ephemeris function providesa significantly better fit (Fs = 2.637, df = 59, 59, P < 0.001).

DISCUSSIONOur results decisively eliminate three previously proposedcomputational hypotheses to explain how honeybees esti-mate unknown portions of the sun's azimuthal course. Wesuggest instead that bees are innately informed of certaingeneral spatial and temporal features ofsolar movement. Thisallows partially experienced bees to construct an internalrepresentation that not only reflects the portions of the sun'scourse previously seen but also approximates the dynamicsof solar movement at other times of day. In the bees'approximation, as in the actual ephemeris function, (i) thesun's position at dawn is about 1800 from its position nearsunset (as measured relative to local landmark features), (ii)the rate ofchange ofthe azimuth is similar in the morning andin the afternoon, and (iii) the sun moves from the eastern tothe western half of the sky at midday. With experiencerestricted to the late afternoon, the bees' representationresembles a 1800 step function. With further experience itconforms more closely to the actual ephemeris function.

Strikingly similar behavior has recently been reported fordesert ants (Cataglyphisfortis), observed while using the sunfor homing (19). Ants that had previously left the nest only inthe morning behaved when tested in the afternoon as if theyexpected the sun to be about 1800 from its morning position.However, the testing was mainly restricted to the late after-

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4474 Neurobiology: Dyer and Dickinson

noon and so did not reveal how ants represented the sun'scourse throughout the day. Also, the data could not deci-sively exclude the faint possibility that the experience-restricted ants had previously observed the sun's afternoonazimuth from the nest entrance (19). Our experiments notonly strongly indicate that honeybees with restricted priorexperience can derive an approximate representation of thesun's overall pattern of movement but also provide a clearpicture of the accuracy and dynamics of this representation.

This mechanism of sun-azimuth learning suggested by thebehavior of experience-restricted bees and ants would offercertain advantages for a short-lived, small-brained animal.Most important, in comparison with the interpolation andextrapolation models outlined earlier, it would allow individ-uals to acquire a relatively accurate representation of thesolar ephemeris function, without needing to sample morethan a small portion of the sun's course. In some circum-stances the accuracy could be scarcely improved by addi-tional experience. For example, during some seasons at lowlatitudes, the solar ephemeris function closely resembles thestep function used by afternoon-experienced bees and (pre-sumably) by morning-experienced ants: the azimuth changeslittle during the morning, then switches abruptly by about1800 as the sun crosses the meridian, then changes littleduring the afternoon (Fig. 3).A step function gives a good description ofour data, but the

actual operations that underlie the development of a bee'sinternal ephemeris remain to be determined. In fact, evidenceagainst the notion that bees represented the sun's courseliterally as a step function was provided by the behavior ofthefew bees in colony 1 (n = 4) that danced repeatedly during therapid transition at midday. All changed their orientationsprogressively rather than instantaneously, as if they hadrepresented the sun's course as a continuous function. Twobees behaved as if the sun shifted clockwise across thesouthern horizon and two behaved as if it shifted counter-clockwise across the northern horizon, implying that theyhad obtained conflicting or incomplete information during thetraining period about which direction the sun was "sup-posed" to move. These observations reinforce the conclu-sion that bees can estimate global properties of solar move-ment that they have never seen, as if they have an innate'template" (24) guiding the learning process. They alsounderscore the importance of experience in fine-tuning thespatial and temporal correspondence between the bees' rep-resentation of the sun's course and the actual ephemerisfunction.The hypothesis that bees (and ants; ref. 19) are innately

informed of the general pattern of solar movement mayaccount for other results that have heretofore been inter-preted in other ways (6, 8, 9, 16, 17). Most strikingly, it mayexplain observations of bees dancing in the tropics on dayswhen the sun's arc passed within 50 ofthe zenith at local noon

(6). Apparently unable to resolve an azimuth during the =0.5hr spanning local noon, bees behaved as if they estimated thesun's midday course. They rotated successive dances pro-gressively but rapidly to compensate for the =1800 change ofthe azimuth; some bees turned steadily clockwise, somecounterclockwise. This finding had suggested that bees com-pensated by linear interpolation between the solar positionsin the morning (east) and afternoon (west) and that theirdirection ofcompensation was ambiguous because the gap tobe filled was 1800. That our bees exhibited similar behaviorwithout having seen the morning or midday sun suggests thatlinear interpolation need not be invoked for the middaybehavior of bees in the tropics. It remains to be determinedwhether the interpolation and extrapolation mechanismsoutlined earlier play any role in learning the current ephem-eris function. Whatever computational processes are in-volved, the method we have outlined offers a promising routeto exploring them in more detail.

We thank R. Jander and T. S. Collett for invaluable suggestions.This research was supported by a grant from the U.S. NationalScience Foundation (BNS 8820010).

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