Ethology 102, 360-370 (1996) 0 1 996 Blackwell Wissenschafts-Verlag, Be rh ISSN 0179-1613

htittd fir Zoologie, Karl-Franxens- Universitat Graz, Grax

Effect of Foraging Distance on the Thermal Behaviour of Honeybees during Dancing, Walking and Trophallaxis

A. STABENTHEINER

STABENTHEMER, A. 1996: Effect of foraging &stance on the thermal behaviour of honeybees during dancing, walkmg and trophallaxis. Ethology 102, 360-370.

Abstract By means of infrared thermography and without disturbing social interactions, the correlation between

thoracic temperature in honeybees, A p r s mc/&m cunicu, upon their return to the hive and their foragmg distance was investigated. Thoracic temperature while dancing and wallung and during trophdactic contact with hve bees decreased with increasing flight &stance. In bees foragmg 0.5, 1, 1.5 and 2 molar sucrose solutions from a distance of 120 m, dancing temperature amounted to 38.4, 40.1, 40.9 and 40.6 "C, respectively; while in bees foraging from a &stance of 2950 m it amounted to 36.6,38.4,38.6 and 39.1 "C, respectively. The rate of decrease in dancing temperature per 1000 m increase in flight distance was 0.64, 0.47,0.81 and 0.54 "C with a 0.5,1,1.5 and 2 molar sucrose solution, respectively. Both at short and at long flight distances, the relationshp between thoracic temperature and sucrose concentration of the food followed a non-linear curve, whch flattened at concenuations higher than 1 mol/l. The experiments showed that inside the hive the foragers' level of thermoregulation depends not only on the energy (sugar) content of the food; but rather, the level of thennoregulation corresponds to the general quality of the food source, whch includes both energy content and distance from the hive. Because the thermal behaviour of foragers correlates with several behaviod parameters inmcadng the bees' f o w g tendency and their eagerness to dance, thoracic temperature seems to be a correlate of the profitability of foraging.

Anton STABENTHEINER, Institut h r Zoologie, Karl-Franzens-Universitat Graz, Univcrsitatsplatz 2, A-8010 Graz, Austria.

Introduction

Honeybees, Apis melyera, foraging for sugar water from artificial feeding places increase their thoracic temperawe with increasing food quality (sucrose concentration) both at the feedmg site (STABENTHEINER & SCHMARANZER 1986; SCHMARANZER & STABENTHEINER 1988; WADDINGTON 1990) and inside the hive (STABENTHEINER 1991 ; STABENTHEINER & I-IAGM~~LLER 1991). In the Asian honeybees Aplj cwam and Aplj donatu, similar observations were made by DYER & SEELEY (1987) and UNDERWOOD (1991). At flight &stances of up to 500111, the relationship between the foragers' thoracic temperature during the stay inside the hive and sucrose concentration was

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Foraging Distance and Thermal Behaviour of Honeybees 361

shown to follow a non-hear curve which flattens at concentrations higher than 1 mol/l (STABENTHEINER 1994 a; STABENTHEINER et al. 1995). The present investigation provides evidence that thls relationship is non-hear also in bees foragmg from &stances greater than 500 m.

SCHMARANZER & STABENTHEINER (1 988) proposed that the thoracic temperature of foraging honeybees may be used as an inhect indcator of the bees’ foragmg motivation. Thls hypothesis is supported by the fact that several parameters of the foragers’ behaviour (crop load at takeoff and flight speed to the feedmg place, etc.; for literature see PFLUMM 1969) that indicate their food-source-specific foraging eagerness increase with sucrose concentration in a non-hear way similar to the increase of thoracic temperature during the stay inside the hve. However, the non-linear relationshp between thoracic temperature and sucrose concentration (STABENTHEINER et al. 1995) suggested that the thoracic temperature is not directly affected by the sucrose concentration as an equivalent of energy content. Therefore, it can be concluded that factors other than sugar concentration also influence the dancers’ thermal behaviour. Food sources farther from the hive have a lesser value to honeybees than sources within closer proximity (BEuTLER 1950; VON FRISCH 1965). If the thermal behaviour is vaned according to the general profitability of the food source, which includes the investments of time and energy to reach it (BELITLER 1950), then dancing temperature should decrease with increasing flight distance. This paper, therefore, investigates the correlation between thoracic temperature during different activities inside the hve and foraging lstance in bees collecting sucrose solutions of lffering concentrations. The use of real-time infrared thermography permitted both behavioural observations as well as measurements of body surface temperature without lsturbing social interactions.

Materials and Methods The experiments were performed in Aug. and early Sep. 1989 and 1990, and Aug. 1992 with three

different colonies at three farmland locations near Graz, Austria. The bees (A$ melh$m cumicu P o h ) were housed in two-comb observation hves (VON FIUSCH 1965) in 1989 and 1990 and in a four-comb hve (two parallel rows of combs) in 1992. In order to sheld the measurement site from solar rakation and to prevent dsturbance of the dancers by sunhght, the hve was placed inside a tent or a blockhouse. Because the glass- pane covering of the hive would have absorbed all infrared radiation, it had to be replaced by an infrared- transmissive plastic foil whch also minimized coohg of the hive (STABENTHEINER 1991). Calibrations applied to hs measurement condtion took into account the foil‘s attenuating effect on the radation emitted by the bees.

The air temperature within the hve was measured 1 cm above the dance floor witlun 5 cm of the dancers’ positions by several NiCr/Ni thermocouples (diameter of wires: 0.2 mm) whch were clamped beneath the infrared-transmissive foil. Temperatures were taken from Technoterm 9400 thermocouple thermometers.

The bees were marked indvidually by shellac colours and trained to gather sucrose solutions of 0.5,1, 1.5 or 2 molar concenaation from pneumatic feeding bowls at feeding stations, which were placed at distances of 120 to 2950 m from the hive. The bees repeatedly carried the solutions into the hive. At the feedmg stations, whch were protected by a sun shade, ambient air temperature and relative humidity were recorded. The weather ranged from sunny to partly cloudy. Measurements were resvicted to periods of little or no wind. In order to reduce variation in the hve and outside temperature, care was taken to conduct the experiments neither too early in the morning nor too late in the afternoon.

362 A. STABENTHEMER

Thoracic surface temperature was measured by means of an AGA 782 SW real-time thermovision system (AGEMA IR-Systems; SCHMARANZER 1983). The infrared ramation emitted by the bees was compared to the ramation of an AGA 1010 reference source, which was precision cahbrated to a black-body ramator of our own construction (STABENTHEINER & SCHMARANZER 1987). The thermographic scenes were stored on videotape and analysed later in the laboratory. Using an emissivity of 0.97 of the honeybee cuticle (STABENTHEINER & SCHMARANZER 1989, self-written PC-software allowed calculation of absolute body surface temperatures. Absolute measurement accuracy was 0.65 "C. Relative (comparative) measurements could be made to the nearest 0.25"C. For further details concerning thermographic measurement of honeybee body temperature see STABENTHEMER & SCHMARANZER (1987) or STDENTHEINER (1991).

Results

The evaluation of the infrared images was focused on the thorax, the main source of heat production. One thermogram was evaluated in the middle of each waggling run. During other activities (walking or trophallactic contact with luve bees) one thermogram was evaluated, in most cases, every 2-5 s (range: 1-8 s), dependmg on the visibility of the thorax in the infrared image. Fig. 1 shows typical curves of the thoracic surface temperature of two bees inside the hive. The bee that foraged a 1.5 molar sucrose solution from a distance of 170m (top curve) entered the luve and immedtately started dancing with a temperature of 41.1 "C. After a few waggling runs, during uophallactic contact with hive bees she first let her thorax cool down to 40.5 "C and afterwards heated it to 41.8 "C. When she left the hive her thoracic temperature was at 41.0 "C. The other bee, foraging a 1.5 molar sucrose solution from a distance of 1750 m (bottom curve), regulated thoracic temperature w i h a range of 38.9 to 40.5 "C, which was about 1.5 "C lower than that shown in the top curve. Dancing temperature ranged from 38.9 to 40.2 "C.

The duration of the stay in the hive between two foragmg flights tended to be longer the greater the flight distance (Fig. 1). However, because the exact time of

43

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I black: dancing gray: walking white: troDhatlaxis 170 m 9"\ -. ....an..

1750m Ti=32.4 OC I

0 1 2 3 4 5

Time (min)

F& I: Curves of thoracic surface temperature during the stay inside the hive of two honeybees foraging a 1.5 molar sucrose solution from different distances. Ti: air temperature near the bees; arrows: bees leave the

hve

Foraging Distance and Thermal Behaviour of Honeybees 363

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F&. 2: Relationslup between thoracic temperature during dancing, walking and trophdactic contact with hve bees, and fight &stance to the feedmg place in bees foraging sucrose solutions of different concentrations (average of mean temperatures per stay with SD). Lines: least-square regression hies (regressions different from zero at p < 0.001 for walking and trophaltaxis in (a) and (b) and at p < < 0.0001 for dancing in (a) and (b) and all curves in (c) and (d); t statistics). T,, average air temperature near the bees with SD; range of air temperature and relative humidty at the feedmg place: (a) 17.0-33.0 "C, 38-81 Yo; (b) 18.2-33.2 "C, 36-67 YO; (c) 17.2-31.4 "C, 47-74 YO; (d) 16.0-30.3 "C, 45-91 %. Numbers in parentheses represent number of values (stays in the hive and readings of TJ at a given &stance from lowest to highest

tempenture

364 A. STABENTHEINER

entering the hive could not be determined in all cases (bees were identified when they walked to the dance floor), this relationship was not investigated in detd.

From each of the temperature curves, mean thoracic temperatures were calculated for dancing, walking and trophallaxis. From these mean temperatures, average values were calculated. Statis tical comparisons of thoracic temperatures are based on mean temperatures. Fig. 2 summarizes the average temperatures of all experiments. Thoracic temperature increased with sucrose concentration during all types of activity (dancing, walking, trophallaxis) and at all flight &stances. The increase was steep between 0.5 and 1 mol/l and flattened towards higher concentrations (Fig. 3). This was consistent with earlier measurements in bees foragmg sucrose solutions from short distances of 30-500 m (STABENTHEINER & HACMULLER 1991; STABENTHEINER 1994a; STABEN-

At all concentrations, thoracic surface temperatures during dancing, walking and trophallaxis decreased significantly with increasing foragmg Qstance (Figs 2,3). In bees foraging 0.5, 1, 1.5 and 2 molar sucrose solutions from a distance of 120 m, dancing temperature calculated from the regression functions of Fig. 2 amounted to 38.4,40.1, 40.9 and 40.6 O C , respectively, and in bees foragmg from a distance of 2950 m it amounted to 36.6,38.4,38.6 and 39.1 O C , respectively. The rate of decrease in dancing temperature per 1000 m increase in flight &stance was 0.64,0.47,0.81 and 0.54 "C with a 0.5, 1, 1.5 and 2 molar sucrose solution, respectively. In bees collecting 0.5 molar

THEINER et d . 1995).

e- A

30 0:5 1:O 1:5 2:O

Sucrose concentration (molll)

F&. 3; Relationshp benveen dancrng temperature and sucrose concentration at dfferent foraging &stances measured dunng a period of constantly fine weather (average of mean temperatures per stay with SD). T,, average air temperature near the bees with SD. Small numbers, number of values (dances); 120 m, 8 bees; 2200 m, 10 bees; 2800 m, 5 bees. Sipficant differences between neighbouring concentrations (v-

test): **, p < 0.01; *, p < 0.05

Foraging Distance and Thermal Behaviour of Honeybees 365

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F&. 4: Relationshp between thoracic temperature during dancing (corrected for the effect of ambient temperature near the dancers, TJ, and flight distance to the feeding place in bees foragmg sucrose solutions of drfferent concenuations (average of mean temperatures per stay with SD). Bold Lines: regression lines with 95 YO confidence limits; for comparison, the regression Lines of other concentrations are also drawn in

(a). R: correlation coefficients; for number of values see Fig. 2

sucrose solutions from distances of up to 500m, temperature during trophallactic contact with hve bees was sipficantly lower than dancing temperature in three of five experiments (p < 0.05, U-test). At greater flight distances and higher concentrations, however, no pronounced trend was visible (Fig. 2). Comparison of those experiments where the number of measured dances was hgh enough (n > 8) showed that the variability of temperatures was rather high with a 0.5 molar sucrose solution and lower at hgher concentrations (Figs 2, 4; compare STABENTHEINER et al. 1995). Depicting measurements which were performed within a period of constantly fine weather shows

366 A. STABENTHEMER

that the distance effect is well pronounced even with a 0.5 molar sucrose solution (Fig.

As is shown in Figs 2 and 3, the air temperature near the dancers was not constant between dfferent measurements. Therefore, in order to get final evidence of the &stance effect, two groups of foragers from one colony gathering 2 molar sucrose solutions from &stances of 170 m and 965 m were thermographed simultaneously. All bees recruited by the dancers were captured at the feedtng stations. ms way the air temperatures inside and outside the hve, weather con&tions and other parameters possibly influencing the thermal behaviour were the same for the two groups. In the group foraging from a &stance of 170 m, average dancing temperature amounted to 40.9 "C (SD = 0.69, n = 20 dances, 11 bees), whereas in the group foragmg from a &stance of 965 m, the average dancing temperature of 39.8 "C (SD = 0.85, n = 18 dances, 8 bees) was significantly lower (p < 0.001, U-test). The mean air temperature near the dancers was 33.8 "C in both groups.

3).

Discussion

The experiments provide evidence that foragers of the honeybee, Apis mefffera, grade their thermal behaviour upon return to the hive in relation to two main variables of food source quality, i.e. flight &stance and sugar (or energy) content of the food. Thorax temperature during dancing, walking and trophallaxis is regulated to a higher level if the food source is near the hive. This effect could be observed with all concentrations tested (Figs 2 4 ) . Thermocouple measurements of dancing temperature by ESCH (1960) did not show a clear trend: in wagtad dancers, thoracic temperatures measured at ambient temperatures above 20 "C decreased with increasing distances of 150, 300 and 600 m, whereas the temperature of round dancers (50 m) was similar to that of the dancers foraging from a distance of 300 m.

STABENTHEINER et al. (1995) provided linear regression functions for the correlation between the bees' thoracic dancing temperature (Td) and the air temperature at the dance floor (TJ. The constants a and b of the function T d = a + b.T, amounted to: a = 26.92 and b = 0.3377 for a 0.5 molar sucrose solution, a = 32.94 and b = 0.2153 for a 1 molar solution, a = 36.86 and b = 0.1155 for a 1.5 molar solution and a = 36.57 and b = 0.1279 for a 2 molar solution. Correction for the influence of hive air temperature on dancing temperature by using constants b of these equations led to a reduction of the variability at a given distance and sucrose concentration (compare Fig. 2 with Fig. 4), but was not suited to explain the whole variability. Part of the variability may be due to seasonal effects (GERM & STABENTHEINER 1992) or might be attributable to dfferences in the colonies' general status.

Nevertheless, the reduction of the variablty of the present data by correcting them for the effect of hive air temperature on thoracic temperature allowed better comparison of the regression functions. With the corrected regression functions (Fig. 4) it is possible to create a plot of isotherms that shows which combination of sucrose concentration and flight distance stimulated the foragers to regulate thoracic temperature to a particular level (Fig. 5). For example, dancing temperature was approximately the same (about 39 "C) when a bee was foragmg 0.60.7 molar sucrose

Foraging Distance and Thermal Behaviour of Honeybees 367

Sucrose concentration (molll)

F&. 5: Plot of isotherms of dancing temperature that shows which combination of foraging distance and sucrose concentration stimulated the foragers to regulate thoracic temperature to a particular level. Points

were calculated from the regression functions of Fig. 4

from 100 m, 1 molar sucrose from 1900 m, 1.5 molar sucrose from 2700 m or 2 molar sucrose from 3300 m.

The relationship between dancing temperature and the sucrose concentration of the food follows a non-linear curve which flattens at concentrations higher than 1 mol/l not only in bees foraging near the hive (30-500 m, STABENTHEINER et al. 1995), but also in bees foragmg at greater &stances (Figs 2-4). In Fig. 3, dancing temperature was sigruficantly different between the 1 and 1.5 molar concentrations only in the experiment with 120 m flight distance. This is due to the non-linear increase of dancing temperature whch reaches a plateau at concentrations higher than 1 mol/l (STABENTHEINER et al. 1995). Dancing temperature is sigruficantly dfferent between these two concentrations if two groups (one gathering a 1 molar and the other one gathering a 1.5 molar sucrose solution) are thermographed simultaneously and thus ambient end experimental conditions are the same for both groups (STABENTHEINER et al. 1995).

This non-linear relation and the decrease of the dancing temperature with distance (Figs 2-4) shows that thoracic temperature is affected not only by the energy content of the food. Rather, thoracic temperature seems to be vaned according to the general quality of the food source, which includes the energy gain obtainable from the source, the investments of time and energy to bring the food to the hive, and probably other factors like water content and viscosity.

The present investigation, therefore, provides further support for the hypothesis that the thoracic temperature is a correlate of the bees’ tendency and motivation to forage from and their eagerness to dance for an artificial, constant-flow food source (SCHMARANZER & STABENTHEINER 1988; STABENTHEINER & H A G W E R 1991). This is

368 A. STABENTHEINER

supported by the fact that the following parameters of the foragers’ behaviour, whch reflect their excitement level and foraging motivation, increase with increasing sucrose concentration in a similar, nodnear way as thoracic temperature: the flight velocity to the feedmg place (relative to the surroundmg air; VON FRISCH & LINDAUER 19-55>, the percentage of dancing foragers (VON FRISCH 1965) and the duration of the dances (VON FRISCH 1965; WADDINGTON & KIRCHNER 1992), the time from the discontinuation of food supply to the retraction of the proboscis at a feeder (PKUMM 1969) and the percentage of foragers imbibing the solution without delay (VON FRISCH 1935), the crop loadmg at takeoff from the feeding site ( N ~ E Z 1966; PKUMM 1969, 1977, and the duration of ‘scent fanning’ (Sterzeln) and marking flights at a feeder (PFLUMM 1969). The relative recruitment rate between a poor and a rich food source decreases nodnearly with increasing difference in concentration (is. bees are recruited faster to more profitable food sources; SEELEY 1986).

T h e decrease in thoracic temperature with increasing &stance is accompanied by a decreasing tendency to forage (BEUTLER 1950; BOCH 1956; VON FRISCH 1965). BOCH (1956) reported that, given the same quhty of food, a distant feeding place releases less dancing than a nearby one, and that the threshold for dancing increases with flight &stance. The relative recruitment rate between a far and a near food source decreases linearly with increasing difference in distance (i.e. bees are recruited faster to nearby food sources; SEELEY 1986).

However, not only the &stance effect of the present study shows that, beside the energy content of the food, there are additional, ecological and behavioural parameters whch modulate the foragers’ level of thennoregulation. BALDERRAMA et al. (1992), for instance, reported that the metabolic rate at constant-flow food sources increases with reward (sugar flow per unit time). When the number of a colony’s foragers increases to a level that is suited to exhaust the colony’s food-storing capacity (SEELEY 1992), dancing temperature decreases (STABENTHEINER 1994 b; and unpublished observations). At a pond, water foragers gathering pure water needed for brood rearing @ve not in danger of being overheated) exhlbit thoracic temperatures s d a r to those of foragers collecting a 0.5 molar sucrose solution (SCHMARANZER 1990).

The modulation of thoracic temperature according to the bees’ foraging motivation, however, does not necessarily mean that the follower bees use temperature as a signal of profitability of foragmg, as dscussed as one of several workmg hypotheses in an earlier paper (STABENTHEINER & HAGMCJLLER 1991). Trials to test this hypothesis with a cold and a heated mechanical model of a dancing bee failed because the model experienced an increased rate of attacks when its temperature exceeded 34 “C (MICHEISEN 1993). Though this unexpected finding suggests that the attendants notice the dancers’ temperature, there is as yet no evidence that would support the idea of body temperature as a direct signal of foragmg profitability. SEELEY & TOWNE (1992) showed that the number of dances and dance circuits per dance increase with food quality (sucrose concentration of the food). Because the recruitment rate increased in parallel they concluded that it is the frequency and duration of dancing which represent food source profitability. Hence, no duect signal of the foragers’ rating of foraging profitability would be needed. In order to further confirm that t h l s is the predominant mechanism to match a colony’s foragmg activity to the profitability of food sources,

Foraging Distance and Thermal Behaviour of Honeybees 369

measurements of frequency and duration of dancing in relation to foragmg &stance would be needed.

While searching for the biological sipficance of distance and sucrose effect, physiological considerations have to be taken into account. Several of the honeybee’s leg muscles arise in the thorax (SNODGRASS 1956). A hgher thoracic temperature probably facilitates the energy turnover both in the flight muscles (GOLLER & ESCH 1991; LEONHARD & CWHEIM 1995) and in the walking muscles of the thorax. The foragers’ graded regulation of thoracic temperature inside the hive and out at food sources, therefore, may have the purpose of matching the general activity of the foragers to the profitability of foragmg (STABENTHEINER & HAGMULLER 1991). It may serve to gather food of high quality from nearby food sources as fast as possible and help to save energy if food of low quality has to be gathered far from the hive. In addtion, operating the flight muscles at a lower temperature and in &IS way reducing the strain for the flight muscles might help to optimize the long-term profitability of the whole colony’s foragmg activity (WADDINGTON 1990), whch is supported by the observation of NEUKIRCH (1982) that the life span of very ‘busy’ foragers is reduced compared with that of bees that made a smaller amount of foraging flights. In foragers doing extra work by carrying loads glued to their thorax, WOLF & SCHMID-HEMPEL (1989) also reported a reduction of the life span.

Acknowledgements

Supported by the Ausuian Fonds zur Forderung der Wissenschaftlichen Forschung (P8388) and the Ausuian Bundesministerium fiir Umwelt, Jugend und F d e . I am greatly indebted to Professor Karl HAGMILLER who enabled me to make th~s investigation and critically read the manuscript, and to Gabriel STABENTHEINER who provided electronics and software support. Thanks are also due to Paul GOSSL, Stefanie PACYNA and M o d a GERM for help with training of the bees, to Motuka GERM for doing part of the IR evaluation, to Sigurd SCHMARANZER for valuable &scussions and critically readmg the manuscript, to Mrs Glenda BROWN for language edting, and to two anonymous referees for helpful comments.

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