the transmission of food between worker honeybees
TRANSCRIPT
THE TRANSMISSION OF FOOD BETWEEN WORKER HONEYBEES
BY J. B. F R E E Bee Department, Rothamsted Experimental Station
Introduction I n a honeybee community transmission of
food occurs between adult workers, and workers also feed the larvae, drones and the queen (see review by Ribbands, 1953).
Nixon & Ribbands (1952) showed that a small quantity of food collected by foragers can become widely distributed amongst the members of a colony within a few hours. In the present investigation, further information on the distribution of food throughout a colony has been obtained by recording the passage of food between marked workers of known ages.
A study has also been made of the behaviour patterns associated with the transmission of food, and an attempt made to discover some of the factors which determine whether at any given time a bee gives or receives food.
Observations on the Behaviour Patterns Associated with Food Transmission
Food transmission between two worker bees starts by one-* of them either begging for or offering food to the other. A bee who offers
food opens her mandibles, pushes forward the proximal part of her tongue and regurgitates a drop of fluid between her mouth-parts. When a bee begs for food she thrusts the tip of her tongue towards the mouth-parts of another bee. The stimuli which release these behaviour pat terns were investigated by Free (1956).
In order to study further the behaviour patterns associated with food transmission 5 well-fed bees, each about ten days old, which had been kept in a cage since emergence, were placed in a small glass-covered arena and not supplied with food. They were observed for fifteen minutes in each hour for ten consecutive hours and records made of begging, offering and food transmission. The combined results of 3 sets of observations are given in Table I.
During the first two hours bees mostly offered food to each other, and in many cases the bees that had food offered to them responded by offering food in return. Occasionally when a bee was offered food she extended her tongue as though to accept it and then withdrew her
Table I. Observations on the Behaviour Patterns of Bees which were Allowed to Starve
Bee offered food
1
2
3
4
5
6
7
8
9
10 . . . . . . i . . . . .
Number of occasions different patterns were observed
32
22
12
4
4
0
0
0
0
0
Hrs. in / arena
Offering bee offered to in turn
13
8
1
0
0
0
0
0
0
0
Food transferred
3
3
2
12
9
9
9
4
2
0
Bee begged for food
0
7
31
37
26
15
8
1
Begging Bee begged from in
turn
0
0
0
0
5
5
4
7
3
0
41
42 T H E B R I T I S H J O U R N A L O F A N I M A L B E H A V I O U R , V, 2
tongue and offered food herself. On two occa- sions when bees had been offering food to each other for several seconds one o f them ceased to offer food and instead accepted it f rom the other. It is apparent, therefore, that a bee who is offering food may stimulate other bees to accept it from her even when they are sufficiently well fed to offer food themselves.
The greatest amount of actual food trans- mission occurred during the fourth hour of observation and this was followed by a period during which begging behaviour was the most frequent. A bee can probably be stimulated to give food even though by so doing she leaves herself short of it, since on several occasions a bee that had just given food was seen to beg for some immediately afterwards.
During the last few hours of observation bees often extended their tongues towards other parts of bees' bodies than their heads, and bees from whom food was begged often begged for it in their turn. Sometimes when a bee begged from another who responded in this way she immediately ceased to beg, although at other times she appeared to beg even more vigorously. In such cases one bee occasionally gave way and, opening her mandibles, allowed the other to insert the tip of her tongue between them. It is possible, therefore, that a bee who begs for food may force another to feed her.
In other observations well-fed bees were placed, one at a time, in an arena containing starving bees. The well-fed bees always gave food to the starving ones and ultimately begged for food themselves. On 5 of 28 occasions the bees introduced were further stimulated to give more food after they themselves had begged for it.
Observations on the Transmission of Food within the Hive by Workers of Known Ages
From 14th July to 18th August groups each of 100 worker bees, twenty-four hours old or less, were added daily to a colony in an obser- vation hive, the bees of each group being given paint marks to distinguish them from bees of other groups. Observations were made on fifteen days between the 2nd and 18th August. When a marked bee was seen to feed another her identity and that of the worker she fed, (if marked) were recorded. At the beginning of observations the oldest marked bee present was 20 days of age, so that data collected for bees up to that age are numerically comparable,
The recorded number of feeds given and received by bees of different ages is shown in Fig. 1. Bees one day old hardly gave food at all [as also noted by ]stomina-Tzvetkova, (1953)], and bees two days old did not give food as frequently as more mature bees. Until they were twelve days old bees were generally fed more often than they gave food, but thereafter the opposite tended to be the case. No doubt some of these older bees had become foragers and were observed whilst passing nectar which they had collected in the field to house bees.
50 .
z20 I I I / • ~ NO. TIMES RECEIVED FOOD. I
tO �9 - - - , NO.TIME$ GAVE FOOD.
AGE OF BEE5 Cday~)
Fig. 1. The number of feeds given and received by bees of different ages.
The mean ages of marked bees who gave food to and received food from workers of different ages are given in Fig. 2. As the bees became older the mean age of the bees who fed them increased, as did the mean age of those bees they themselves fed. The mean age of the bees from whom workers received food was usually
" ~ ' r L X ~ MEAN AGE OFBEE5 WHO =E E,VEO FO00. l
~16/ , - - - - MEAN AGE OF BZEr~ WHO 2~ I ~s- GAVEFOOD. ..,' \ I
w i ~ / \ v / \ l ' ~
~ " " , \ , ~ J \ / V
7 - ~ , 4 ' ; ' ~ ' lb ' :z '. 1'4 ' ,'6 i'~ ' ~o AGE OF BEES.(dajs)
Fig. 2. The mean age o f bees who gave food to and who received food from workers of different ages.
FREE: THE TRANSMISSION OF FOOD BETWEEN WORKER HONEYBEES 43
171 htl Q ,,, ,o i n
t u D
. _ , fig t u i -
21-32
17-Z0
13 -1(~
9 - t 2
5 - 8
1-4 5 - 5 _ 9- t2 .
AGE (da,~s) OF' BEES j -
21
36 ] i9
11 - I V - I I
t 3 -16 17-Z0 THAT GAVE FOOD
Fig. 3. The distribution of feeds between bees of different ages.
23
z4
i2
21-3Z
greater than that of the bees to whom they gave food. There was thus a general tendency for food to pass from older bees, many of whom were foragers, to younger bees who were feeding the brood.
In Fig. 3 the distribution of feeds which were observed between bees of different age groups is given. Although there was a tendency for bees to feed and to receive food f rom bees of about their own age, bees of all ages were fed by, and fed, bees of a wide range of ages; thus two-day old bees were seen to feed bees thirty days old and vice versa.
The Amount of Food in the Honeystomachs of Bees who are Receiving and Giving Food in the
Hive
A colony housed in an observation hive was watched, and whenever a bee was seen to begin to give or to receive food she was immediately removed and the amount of food in her honey- stomach determined. In order that the results should not be affected by incoming tbod supplies the experiment was carried out on occasions when bees were not foraging. The results are given in Table II.
Although bees about to give food generally had more in their honeystomachs than those about to receive it there was a wide overlap in the weights of food in bees of the two groups. On the 7th September the honeystomach con- tents of bees who were offering and others who were begging for food were also weighed. Tile amount of food contained by bees who were begging for food and by those who were offering food varied f rom 0 to 38.0 mg. and 5.0 to 51.0 mg. respectively. It was, therefore, apparent that the behaviour of the bees was not governed entirely by the amount of food in their honey- stomachs, and it was thought possible that the results may have been influenced by other factors such as the passage of 'queen substance' through the colony (Butler, 1954) and the occupation at which a given bee was engaged.
Butler (1954) found that bees who had licked their queen, and thereby obtained queen sub- stance, offered food at least once within the next five minutes. On 13th, 14th and 15th October, 1954, bees who were observed to lick their queen were immediately removed f rom the colony and dissected and other bees who were collected at random from the colony at the same time were also dissected (Table III).
Table II. The Amount of Food in the Honeystomaeh of Bees about to Give or Receive Food
Date
7th & 8th Sept. 1954
17th, 25th, 26th, 27th, Feb. 1955
Bees about to give food
Mean wt. (mg.) of food in
honeystomach
29"8
17"8
Range
1.0--57-0
0'5--40.5
No. of bees
18
44
Bees about to receive food r r
Mean wt. (mg.) of food in Range
honeystomach
16"5
6"0
0.5--57.0
0--33'0
No. of bees
22
41
44 T H E B R I T I S H J O U R N A L OF A N I M A L B E H A V I O U R , V, 2
Table HI. A Comparison of the Honeystomaeh Contents of Bees observed to Lick their Queen and of Bees taken at Random from the Colony
Date
13th Oct.
14th Oct.
15th Oct.
Total
Bees observed to lick queen
Mean wt. (rag.) honeystomach
contents Range
13-5--73 "5
2.0---38.5
2.5--51 "0
2.0--73.5
No. of bees
6
6
6
18
Bees taken at random from the colony
Mean wt. (rag.) honeystomach
contents Range
23.5--73.0
2"0--28"0
1 "5--58.5
1-5--73"0
38 '5
15"7
20'0
24"7
58 -4
8-2
13"5
26.7
No. of bees
6
6
6
18
The amount of food contained by bees who had licked their queen was similar to that con- tained by bees taken at random from the hive, so it is apparent that the behaviour of bees who have recently obtained queen substance and offer food is not governed by the amount of food in their honeystomachs.
An attempt was next made to determine whether the environment influences the amount of food a bee retains in her honeystomach.
The results of Himmer (1926) and Lotmar (1939) indicate that little or no interchange of bees occurs between the outside and inside of a winter duster. On 5 occasions during the early part of 1955 samples of 20 bees each were taken from the fringe and centre of winter clusters and the honeystomach contents of the bees weighed. The results are given in Table IV.
Table IV. Mean Weight (mg.) of Honeystomaeh Contents of Bees taken from the Fringe and Centre of the Winter
Cluster
Date Samples from centre of cluster
8th Feb.
11 th Feb.
14th Feb.
17th Feb.
4th March
Samples from fringe of cluster
21.9
18"1
10.8
37 '4
19.3
5.5
3"3
5.2
5-2
1"8
In each case bees on the outside contained more food than those on the inside. When, however, bees from the fringe and centre of a cluster were placed in cages and supplied with food the bees of both groups filled their honey- stomachs to a similar extent. It is, therefore,
apparent, that the environment of a bee may determine to some extent the amount of food she contains.
Observations on Food Transmission between Bees Removed from Their Hive
In the next experiment the variation in the honeystomach contents of bees kept under the same conditions was investigated. Five hundred bees were taken from a hive and placed in a cage and well supplied with food. After twenty- four hours the feeder was removed from the cage, and 20 bees were examined every ninety minutes. The results are given in Table V.
Table V. The Weight of Honeystomaehs of Samples of Bees Removed at Intervals from a Cage in which no Food
was Provided
Hrs. after starvation
0 1.5 3.0 4.5 6.0
Mean wt. (mg.) of sample
34.5 27.3 18.7 7.1 2.5
Range (mg.)
17-64 10-54 344 142 1-12
Although the amount of food which the sample bees contained decreased steadily, there was at any one time a large variation between different bees. It was thought possible that little or no food exchange was taking place and that this accounted for the variation in the weight of honeystomach contents. In order to investi- gate this 22 distinctively marked bees were placed in a cage and supplied with food. The remaining food was removed after twenty-four hours and the bees individually weighed and returned to their cage once every ninety minutes. Only 9 of the bees decreased in weight steadily,
FREE: THE TRANSMISSION OF FOOD BETWEEN WORKER HONEYBEES 45
Table VL The Relationship Between the Behaviour of Bees and the Amount of Food in their Honeystomaebs
Behaviour of bees
Offered food . . . . . . . . . .
Offered in turn when food offered to them
Begged for food . . . . . . . .
Begged in turn when food begged from them
Mean wt. (mg.) of honeystomach
contents Range (rag.)
13.6
27"I
2.3
0"3
2--41
6--41
0--11
i 0--1
No. of bees
21
7
23
5
thus suggesting that considerable food trans- mission was taking place. Therefore, even bees kept under the same conditions (and when food transmission is occurring between them) retain very different amounts of food in their honey- stomachs.
Bees were taken from a hive and placed in a small arena. When a bee was seen to offer or beg for food she was dissected and her honey- stomachs content weighed. The results are given in Table VI.
Although there was again a general cor- relation between the weight of a bee's honey- stomach and her behaviour, individual bees showed considerable variation.
The following experiments were carried out to determine whether there is a closer correlation between the honeystomach contents and behaviour of recently emerged, uncon- ditioned bees than is the case with bees taken at random from their colonies. In the first series of experiments bees were taken from a colony, distinctively marked, and placed in a cage supplied with plenty of food. After twenty-four hours they were placed, 5 at a time, in a small arena and the number of times each bee offered food during the next ten minutes were recorded. They were then immediately dissected and their honeystomach contents weighed. This experi- ment was repeated 16 times. In 14 similar ex- periments bees four days old, who had been kept in a cage together since emergence, were used. A significant correlation (P<0.001) was obtained between the number of times these bees, who had been kept in a uniform environ- ment since emergence, offered food and the amount of food they contained, whereas no such correlation was obtained with bees who were taken at random from their colonies.
The Effect of Previous Experience on the Amount of Food Bees Retain in Their Honeystomachs In view of the results of the previous experi-
merits, it seemed possible that the past ex- perience of a bee might govern the amount of food she contains when she offers or begs for food. The following experiments were under- taken to investigate this.
The effect of previous starvation was first studied. Thirty bees were placed in each of 3 cages and the bees treated as follows. Cage (A): the bees were first starved for 24 hours, then fed for 24 hours and dissected. Cage (B): the bees were fully fed for 48 hours and then dissected. Cage (C): the bees were fed for 24 hours (the same period for which the previously starved bees of cage (A) were fed) and then dissected. The mean weights of the food contained by bees in cages (A), (B) and (C) were 32.3, 14.1 and 19.8 mg. respectively. Bees of cage (A) contained significantly more food than bees of cage (B) (P<0.001) and cage (C) (P<0.01). Previous starvation had, therefore, subsequently caused them to retain more food than the control bees.
The next experiment was made to determine whether a constant and plentiful supply of food influences the amount of food which bees retain in their honeystomachs. Two hundred bees were placed in a cage (a) and 300 in another cage (b). Every day 20 bees were removed from cage (a) and their honeystomachs content weighed. The number of bees in this cage was made up to 200 again by adding 20 bees from cage (b). The results ar e given below (Table VII).
The mean weights of the honeystomach contents of tile sample of bees decreased during the experiment. At the end of the experiment (21st July) the bees in the cage were starved for twenty-four hours and then fed again. The mean weight of the honeystomach contents of the bees of a sample removed on 23rd July had risen to 26.5 mg.
From the results of these experiments it may be concluded that the amount of food that bees
46 T H E B R I T I S H J O U R N A L OF A N I M A L B E H A V I O U R , V, 2
Table VII. Mean Weight of Honeystomaeh Contents of Samples of Twenty Bees Removed Daily from a Cage containing Plenty of Food
Date July 1955
13 14 15 16 18 19 20 21
Mean wt. (mg.) 24.5 22.6 22.0 13.9 13"8 15.1 11.2 12.2
retain in their honeystomachs is influenced by its previous availability.
In the following experiment the effect of the concentration of syrup on the quantity which bees imbibe was investigated. Bees were taken from a hive, given distinguishing paint marks, and placed together in a cage. They were starved for twenty-four hours and were then weighed individually and allowed to feed on sugar syrup of a predetermined concentration, and then weighed again immediately afterwards. The bees were separated at random into 3 groups of equal size, and the bees of each group were allowed to feed on a different concentration of syrup each day-- thus eliminating the effect of any day to day variation in conditions. The volumes of the 3 solutions imbibed were correlated with their concentration. (P < 0.05). (Table VIII).
Table VIII. Mean Volume (nun. 3) of Sugar Solution Ingested by Worker Honeybees
Sugar concentration 50 % 33 % 20 %
Volume ingested 20"5 16'9 13.8
Experiments were made to investigate the effect of a change in the concentration of the syrup on which bees were allowed to feed on the amount which their honeystomachs subse- quently contained.
On l l th September 30 bees were placed in each of 2 cages, (A) and (B). The bees in cage (A) were supplied with 10 per cent. sugar syrup and bees in cage (B) with 50 per cent. sugar syrup. On 15th September a sample of 10 bees from each cage was dissected. The honey- stomachs of bees of cages (A) and (B) contained the mean volumes of 8.3 mm. 3 and 19.9 mm. 3 of sugar syrup respectively (P<0.001). The bees of both cages were then fed on 30 per cent. sugar syrup and the remaining bees in each cage were dissected on 17th September. The mean volume of the honeystomachs contents of bees in cages (A) and (B) was 12.8 ram. 3 and 8.5 mm. 3 respectively. Bees of cage (A) (originally fed on 10 per cent. sugar syrup) had significantly more
(P<0.05) sugar syrup in their honeystomaehs than bees of cage (B) which had originally been fed on 50 per cent. sugar syrup.
In a similar experiment bees two days old or less were placed in 3 cages (A), (B), and (C) and supplied with 10, 30 and 50 per cent. sugar syrup respectively. Two days later the bees in all the cages were supplied with 30 per cent. syrup. After twenty-four hours 50 bees from each cage were dissected. The mean volume of the honeystomach contents of bees in cages (A), (B) and (C) were 11.1 mm.3, 9.2 ram.3 and 5.6 mm. 3 respectively. The bees of cage (A) contained significantly more food than bees of cage (C) (P < 0.001).
In a further series of experiments it was found that bees who had ceased to feed on syrup of a low concentration began drinking again directly they were offered syrup of a higher concentration.
The improvement or deterioration in the attractiveness, as well as the quantity, of syrup, therefore, had a marked effect on the amount bees retained in their honeystomachs, and it is highly probable that the quantity of food that different bees contain when they are willing to give, or receive, food depends to some extent on their past experience.
Discussion and Conclusions The work of R6sch (1925) and Perepelova
(1928) showed that during their lives bees generally undertake a series of occupational duties, although their observations and those of R6sch (1930), Ribbands (1952) and Lindauer (q952) showed that the length of time which individual bees spent on one particular duty was very variable and much affected by the needs of their colonies.
Ribbands (1953) supposed that the extensive transmission of food which occurs between the members of a colony might in some manner enable individual bees to become aware of their colony's requirements, and adjust their activities accordingly. To validate this hypo- thesis it is first necessary to show that food transmission between bees in different occupa-
FREE: THE TRANSMISSION OF FOOD BETWEEN WORKER HONEYBEES 47
tional categories takes place in both directions along the occupational series.
The present results indicate that although food is more often given by the older bees to the younger ones, there is also a considerable transfer of food in the opposite direction. It is most probable, therefore, that food and any substances it may contain* is passed freely between bees engaged in different duties, although because of the very large variation in the age of the bees undertaking given duties, it is not possible to demonstrate this con- clusively.
Bees who were about to give food had very varied amounts of food in their honeystomachs, as did bees who were about to receive food. It is possible that when undertaking certain duties bees retain more food than when occupied with other duties. From a study of the behaviour patterns associated with food transmission it appears probable that bees who require food (for wax and brood-food secretion) may be even able to stimulate bees with little food to feed them, and likewise bees with full honeystomachs (e.g. successful foragers) may be able to stimulate bees containing relatively large amounts of food to accept food from them.
Changes in the quantity and quality of food influence the amounts which bees retain in their honeystomachs, as well as influencing their foragingbehaviour (Frisch, 1934 and Ribbands, 1955). A bee's past experience, therefore, also plays a part in determining the amount of food contained in her honeystomach when she offers or begs for food.
Summary 1. A study has been made of the behaviour
patterns associated with food transmission be- tween worker honeybees.
2. There is a general tendency for food to pass from the older to the younger workers of a colony, although there is a considerable passage of food in the opposite direction. Younger bees generally receive food more frequently than they give it.
3. As worker bees grow older, the mean ages of the bees that feed them and to whom they give food also increase.
4. Although bees about to give food generally have more in their honeystomachs than those about to receive it the quantities of food con- tained in the honeystomaehs of bees in these two groups overlap considerably. The trans-
*Possibly "social" hormones.
mission of 'queen substance', the occupation on which a bee is engaged within the hive, and her environment, all influence the result.
5. The correlation between a bee's behaviour in connection with food transmission and the amount of food in her honeystomach is more marked in the case of recently emerged, un- conditioned bees, than in the case of bees taken at random from their colonies.
6. The amount of food that individual bees retain in their honeystomachs is influenced by their past experience.
Acknowledgements I am indebted to Dr. C. G. Butler and Dr. J.
Simpson for their criticism of this work and to Mr. H. Copleston for his help with some of the observations.
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recognition by a colony of honeybees (,4. melli- fera) of the presence of its queen. Trans. R. ent. Soe. Lond., 105, 11-29.
Free, J. B. (1956). A study of the stimuli which release the food begging and offering responses of worker honeybees. Brit. J. anim. Behav., 4, 94-101.
Frisch, K. v. (1934). Ueber den Geschmackssinn der Biene. EirLBeitrag zur vergleichenden, Physiologic des Geschmacks. Z, vergl. Physiol., 21, 1-156.
Himmer, A. (1926). Der soziale Wfirmehaushalt der Honigbiene I. Die Wgrme im niehtbrutenden Wintervolk. Erlanger Jb. Bienenk., 4, 1-51,
Istomina-Tzvetkova, K. P. (1953). Reciprocal feeding between bees. Pchelovodstvo, 1, 25-29.
Lindauer, M. (1952). Ein Beitrag zur Frage der Arbeit- steilung im Bienenstaat. Z. vergl. Physiol., 34, 299-345.
Lotmar, R. (t933). Der Eiweiss-Stoffwechsel im Bienen- yolk wiihrend der Ueber-winterung. Landw. Jb. Schweiz., 53, 34-70.
Nixon, I-L L. & Ribbands, C. R. (1952). Food trans- mission in the honeybee community. Proc. roy. Soc. B., 140, 43-50.
Perepelova, L. I. (1928). The nurse bees. Opuit. Pas., 551-7.
Ribbands, C. R. (1952). Division of labour in the honey- bee community. Proc. roy. Soc. B. 140, 32-43.
Ribbands, C. R. (1953). The behaviour and social life of honeybees. London: Bee Research Association.
Ribbands, C. R. (1955). Communication between honey- bees. II. The recruitment of trained bees, and their response to improvement of the crop. Pro& R. ent. Soc. Lond., A, 30, 26-32.
R6sch, G. A. (1925). Untersuchungen tiber die Arbeit- steilung im Bienenstaat I. Die T~tigkeiten im normalen Bienenstaate und ihre Beziehungen znm Alter der Arbeitsbienen. Z. vergl. Physiol., 2, 571-631.
Rtisch, G. A. (1930). Untersuchungen fiber die Arbeit- steilung im Bienenstaat. II. Die Tfitigkeiten der Arbeitsbienen unter experimentell ver~inderten Bedingungen. Z. vergl. Physiol., 12, 1-71. Accepted for publication 18th April, 1956.