By Geoff Tribe, Karin Sternberg and Jenny Cullinan
Patrolling his patch!
Ever wonder about the antics of the yellow-haired carpenter bee hovering around a flowering shrub (Fig. 1), then darting off, only to return seconds later to hover briefly again? This is the male Xylocopa caffra which is distributed throughout South Africa. The females are unlike the males in that they are black and hairy with two bands of yellow hair (Fig. 2).
What the males are doing is to patrol a patch of flowers to which females are attracted out of necessity whilst foraging in order to mate with them. A patrolling male will aggressively chase away intruding males and will even attempt to discourage you from coming too close by mock diving at you. Stretch out your arm and point your finger at the carpenter bee and it will often approach the finger directly and will follow the finger as it is moved slowly up and down – as if it is an intruder.
Xylocopa caffra males make quick circuits of an area of several square meters and females that are receptive allow themselves to be seized in flight (Watmough, 1974). The receptive female will vibrate her wings and help the male carry her in flight, a successful mating flight ending 50 meters or so up in the air about a kilometre away.
Exposing interstitial membranes
What is most fascinating is that the normally completely yellow male, when hovering around its patch of flowers, lowers its abdomen and exposes two of its interstitial membranes which appear as two black bands on the abdomen (Fig. 3). The most likely explanation for this behaviour is that the male is releasing a sex pheromone, both as a species specific chemical signal and female sexual attraction. When the male momentarily darts away, the membranes are less exposed when compared to when it hovers.
For semi-social carpenter bees which nest in tunnels they construct within dead branches of trees or dried Aloe inflorescences, this method of patrolling patches of flowers that females must visit for the collection of pollen and nectar, is obviously suffice for the sexes to meet. The success of these encounters is enhanced by the permeation of a sex pheromone released by the male while patrolling his patch of flowers. Males of the carpenter bee Xylocopa hirsutissima have a different strategy and fly to the top of the mountain where they spread mandibular gland secretion over the ventral surface of their abdomen while hovering in the air awaiting the female (Velthuis and Camargo, 1975).
Drone Congregation Areas
For highly specialized social insects like honeybees, a more intricate and highly efficient behaviour has evolved to bring virgin queens and drones together. Mating in honeybees takes place in the air at considerable distance from the hive. These are called drone congregation areas (DCA) where thousands of drones congregate in certain locations in the air where they await the arrival of a virgin queen. Drones from as many as 240 colonies have been recorded in a DCA at one time. The phenomenon of DCAs is still little understood but certain characteristics pertaining to them are known. Both drones and queens independently find these locations, some of whose locations have been known for hundreds of years and are therefore persistent from year to year (Zmarlicki and Morse 1963). Drones and queens from hives brought in from outside the region are immediately able to find these DCAs.
Thousands of drones milling about in a DCA greatly reduce the chance of a queen being eaten by alpine swifts (Fig. 4a), bee-eaters, redwinged starlings (Fig. 4b) or other avian predators.
Swallows in Perth, Western Australia were found to have up to 19 drones in their stomachs (Tribe 1989). Even spider’s webs may prove a hazard, even within a DCA (Fig. 5). A virgin queen always leaves on her mating flight during a worker orientation flight which persists until the queen returns – thus further reducing the chance of predation.
Advantages of a Drone Congregation Area
Obviously the DCA must serve an important function, especially if one considers the resources entailed in rearing hundreds of drones in each honeybee colony each year. The amount of drone comb and the number of adult drones present is positively correlated with the number of workers in the hive and represent a maximum of 14% of the total brood at any time. The number of drones kept in an active colony is restricted to about 1000. Because it takes 24 days from egg to emergence (compared with 19 days for an African worker) the larger drones consume abundant pollen. The cessation of the rearing of drone brood is in response to pollen shortage, while the killing or expulsion of drones by workers is mostly the result of a shortage of nectar and may occur at periods throughout the year (Currie 1987). Because the mating flights of drones and virgin queens are not random but concentrated into distinct areas, mating takes place in the shortest possible time. In times of very low drone population density, queens have a reasonable chance of being mated in a DCA. The lifespan of a drone is between 13-59 days.
The main advantage of a DCA appears to be to lessen the chance of a virgin queen mating with a related drone which is detrimental to the colony. With the sometimes thousands of drones drawn from diverse colonies in the area, the possibility of mating with a related drone is much reduced. In addition, queens of European races mate with an average of 8 drones and up to 17 (Woyke, 1962) which further reduces the level of inbreeding if she inadvertently mates with a related drone. By using DNA fingerprinting techniques, Moritz et al. (1996) determined that Apis mellifera capensis queens of the same population will have mated between 24 and 44 times.
Although the spermatozoa from one drone (12.7million) is suffice to fill the spermatheca of the queen, as the spermatozoa move from the oviduct past the spermatheca, fractions of the sperm of each drone is absorbed into it. Only about 370 000 spermatozoa (3%) are retained in the spermatheca. On the eversion of the aedeagus of the drone (like a glove blown inside out) (Fig. 6), the clump of sperm is followed by mucus and following the dissection of a recently mated queen the number of drones with which a queen has mated can thus be calculated.
The mated queen determines whether she must lay a fertilized or un-fertilized egg by measuring the cell width with her forelegs before commencing oviposition. At the height of summer a huge number of drones are present in a DCA, the majority of which will never mate – an estimate that only 4% of drones mate naturally. This huge investment in the transfer of genes indicates the importance of DCAs.
Characteristics of Drone Congregation Areas
DCAs vary greatly but most appear to have some form of relief in the form of trees or mountains near which they are established. Usually they occur high above the ground and are discerned from the noise the drones make whilst flying which sounds like a huge swarm of bees about to settle. Years back in Pretoria an irate grounds manager of a rugby club phoned to ask if we could remove a huge swarm of bees that interfered with their rugby matches on Saturday afternoons. It was quickly ascertained that no one had ever been stung, nor had any bees been observed but that the swarm ‘hovered high above the ground’. The rugby field was below a DCA and was flanked by high Eucalyptus trees. A DCA may expand or contract in size throughout the year but there is always a ‘core’ area which persists from year to year.
DCAs in Europe are recorded located at heights of 15-25m above ground (range of 8-40+m) over open ground or on summits, often in areas demarcated by buildings or rows of trees. They were 50m to 5km from the apiary and their individual sizes fluctuated from 30 to 200m in diameter but there was always a ‘steady centre’. Researchers found that drones of European races did not follow queens out of DCAs but always remained within its limits and could not be attracted to ground level with queen pheromone lures. Certain DCAs were more attractive than others and the number of drones visiting a DCA varied between sites and on different days. The sun was not used to orientate to DCAs. And of course there were no dances among the drones to indicate the location of a DCA! Successful matings from 10 to 16km distant have been recorded but the usual distance is from 5-7km. By placing drone-less colonies on islands or in desert areas, it was shown that to prevent mating an isolation of at least 15km from the nearest hive was required.
Drone flight in Pretoria during the summer months began at about 12h00 and ended after 17h00 with peak flight times between 14h30-15h45. The average number of flights undertaken by flight mature A. m. scutellata drones in Pretoria was 3.7 flights/day (n=23) with a range of 3-5 flights. Individual marked drones made multiple flights in an afternoon with a mean duration of 21min 30sec (range 12min 15sec to 33min 53sec). Using 8m/s as the flight speed, an A. m. scutellata drone is able to travel a distance of 10.3km in 21.5min with a maximum of 16.4km. When visiting a DCA no further than 1 to 1.5km distant (in ±3min), a drone could be cruising within the DCA for 45min on each flight. Between flights, drones would spend an average of 4 minutes feeding on uncapped honey. With three flights in an afternoon, including feeding intervals between flights, drones on average would spend 72min/day on mating.
From limited data it appeared that the older the drone, the longer the duration of the mating flight. The African bee produces and maintains larger numbers of drones even in resource-scarce conditions than do European races, which accounts for the huge numbers found in DCAs.
The first orientation flight of an Apis mellifera scutellata queen would take place on the third day after emergence. Usually there were orientation flights on two successive days before the virgin queen departed on a mating flight. The queen would only leave the hive during a worker orientation flight and such orientation flights would persist until the queen returned to the hive. The queen would fly once or several times in the same afternoon or on successive days until she was fully mated.
Gary (1971) recorded queen flight at 340m/min (5.6m/s), enabling a queen to take 2min 56sec to fly 1 000m. On Sylt Island (Germany) where the wind hardly ever stops blowing, matings took place at windspeeds of up to 5m/s (Tiesler 1972). The mean duration of a queen flight in Pretoria was 13 minutes 17 seconds (range 6min 11s – 21min 58s) (Fletcher and Tribe, 1977). Thus the A.m. scutellata queen could fly 4 515m in 13.28min or a return journey of 2 257m. Two further queen flights in November 1979 gave a duration of 19min 49sec and 26min 34sec which gives a maximum range of 9km. Drones evert within 1-6 seconds on mounting the queen. Upon eversion, the drone falls backwards and the resulting pressure within the aedeagus causes the non-chitinized section to rupture, the drone falling to the ground while the queen flies off with the ‘mating sign’.
Flight experienced workers appear to determine if and when the queen departs on her mating flight. They orientate in front of the hive in ever widening circles, possibly gauging if weather conditions are suitable for flight. In an observation hive, a virgin queen primed for a flight can be seen preening herself on the comb. Ever more workers vacate the hive on their orientation flight, and the cue for the queen to leave happens after several of the orientating workers return to the hive and run ‘randomly’ around on the comb. The queen, while trying to find the exit (because the cover is off the observation hive), invariably ‘jumps’ onto the glass window and then quickly follows the bees out of the entrance.
Behaviour within the Drone Congregation Area
Drones form comets within the DCA of several hundred individuals which can dissipate as fast as they may be formed (Fig.7). Comets may be formed even in the absence of a queen when they orientate to any object that may enter the space such as butterflies, or even to another drone. Despite the literature recording that drones of European races of honeybees never descend near the ground (Gary 1962), in October 1986 in Floreat Park, Perth, Western Australia drone comets were observed flying at head height in an open park surrounded by trees (Tribe 1989b). Within the DCA of about 100m x 50m, individual drones were flying at knee height.
The queen is approached from below where she is silhouetted – hence the function of the abnormally large eyes of the drones. Because of its small visual acuity, a drone must fly within 1m of an object the size of a queen in order to see it (Butler and Fairey 1964). Queens may return fully mated on their first flight or may undertake subsequent mating flights on the same day or subsequent days.
Types of DCAs
How do drones and queens independently locate DCAs? Olfaction, especially pheromones, plays a crucial role in the life of the honeybee and no doubt this extends also to the formation and function of DCAs. Pioneering research into DCAs in Pretoria showed what appeared to be three types of DCAs which were used interchangeably in response to varying weather conditions: ‘barrier’, ‘sheltered’ and ‘convectional’. The most regularly visited DCA was situated downwind from a ridge which formed a barrier (e.g. A in figure 9, the most consistent DCA). After consulting weather bureau personnel, it was determined that a breeze passing over the ridge on an otherwise relatively still day would cause an eddy downwind. The height of the ridge and the velocity of the wind would determine the strength of the eddy and its distance from the ridge. Drones fly in the afternoons on hot days and ground that bakes in the sun during the day results in late afternoon breezes as cooler air is drawn in as the hotter air rises which often results in showers of rain.
Eight DCAs were located around the apiary situated on the University of Pretoria Experimental Farm in 1975 with an average distance from the apiary of one kilometre (Fig. 8). By monitoring the wind speed at the entrance to the hive, it was determined that queens would not fly if the wind speed ≥5m/s, and drones at ≥7m/s. On extremely windy and usually overcast days, a DCA which normally attracted a smaller number of drones would supplant the barrier DCA in numbers. It occurred in the sheltered lee of a kopje where the air within was relatively calm compared to the gusts of wind all around it (D in figure 9). On Lion’s Rump in Cape Town there is such a DCA which can be looked down upon where the drones can be observed flying. Here again there is relatively calm air while all about the easterly rages.
At the height of summer in Pretoria with its oppressive heat with nary a breeze, the air is filled with the sound of drones. Huge convection currents were initiated by the air above the hot soil attracting in cooler air with the DCAs expanding considerably in size in response to this.
When comparing DCAs in Europe with those in Africa, it must be remembered that in Europe most honeybee colonies are hived and relatively few are feral, whereas in Africa the opposite is true and drones within a DCA are mostly from wild swarms in natural nesting sites. The late Beowulf Cooper when visiting the Pretoria DCAs related that DCAs in the United Kingdom were perceptibly warmer within them than without and regarded this as a distinctive feature for their formation in Britain. Cooper (1977) proposed a thermal vortex of warmer air within the DCA contributing to its formation.
This is what appears to be happening. The drones exiting their hives on mating flights appear to fly mostly upwind or alternately downwind until they reach an area of mild turbulence where they congregate. Here they fly around randomly within the limits of the eddy. Drones from comets caught in nets in DCAs (Fig. 9) were transferred to plastic bottles where they were marked by dabbing them with ‘tippex’ of different colours according to their DCA location. As they emerged between the fingers of the hand placed over the mouth of the bottle, a distinct musty smell could be detected (which incidentally attracted the occasional worker bee which would not leave). This odour could be a pheromone which not only assists the queen in finding the DCA but helps create the comets. Guard bees have been recorded in prolonged lapping over much of the dead body of a drone, especially near its thorax, apparently to salvage some highly desirable substance (Australian Beekeeper 1979, 80(8): 174). Crushed drones are highly attractive to worker bees and may produce a substance which is attractive to workers in summer, enabling a drone to drift to other colonies with immunity (Holmes and Henniker 1972). Another indication of a substance produced by drones is when drones and workers were returned to their queenless colony they were accepted, but the workers when confined to a cage with their queen and drones and returned to their colony are killed – but not the queen or drones (Orὅssi-Pál 1959). Drones could be attracted in DCAs with drone extracts as efficiently as with queen extracts – head extracts being the most successful (Ruttner H. 1972). In the presence of queen pheromone the drones will form comets as one drone follows the other. They will attempt to mate with any object silhouetted above them, a butterfly or stone thrown into the air.
A queen flying into a DCA releases queen pheromone (9-oxodecenoic acid) which results in the immediate formation of comets which zigzag after her, following her pheromone plume from at least 420m downwind of her. Drones are attracted by 9-oxodecenoic acid from distances of 50m and more while the queen tergite gland’s pheromone is effective only within short distances (less than 30cm) and increases copulation activity (Renner & Vierling 1977). A pheromone is also produced from the abdominal tergites in virgin queens 8 days or older and in mated queens, probably in the glands described by Renner and Baumann (1964) which are most active at the time of mating (Butler 1971). Production of a chemical from the abdominal sternites shows that it is restricted to nubile virgin queens because ‘wipes’ of newly emerged and very young laying queens had none of the perfume (Boch, Shearer and Young 1975). Several comets may be seen simultaneously within the DCA, dissipating as they lose the scent and reforming at will. They approach from below the queen and mate in the air, each drone in turn removing the previous ‘mating sign’ before inturn mating with her. Thus the reason why DCAs form in certain areas appears to be to facilitate through pheromones, the fast and efficient mating of the queen by following the pheromone plume.
Of interest is the question of why the multitudes of drones within a hive do not attempt to mate with their own mated or virgin queen who is continually secreting queen pheromone? Presumably the pheromone ‘bouquet’ released by a virgin as opposed to that of a mated queen is perceptibly different. Yet if mating within the hive were to occur, it would negate the major function of a DCA to prevent in-breeding. The difference between an inactive drone within the hive and that of a drone in a DCA is one of flight. Thus presumably flight changes the physiology of a drone and makes it responsive to queen pheromone. This could be a result of the accumulation of carbon dioxide in their tissues caused by exercise.
Could sound play an integral part in the formation of a DCA? Quietly sitting in a meadow, one of the most harmonious sounds is that of honeybees going about their business. Yet we are all familiar with the raised, high-pitched sound of an angry bee. Sound plays almost as important a role within the hive as that of pheromones. The piping of queens, the moaning of bees besieged by banded bee pirates (Palarus latifrons), the distress calls of worker bees in a queenless A. m. capensis colony, and many more sounds are familiar to the beekeeper. In addition, the male semi-social carpenter bee Xylocopa hirsutissima is known to raise its flight tone when it perceives the female approaching the top of the mountain that it is patrolling (Velthuis and Camargo, 1975).
Sounds have frequencies which are distinct, and in some instances the frequency or vibration may be more important than the sound that we hear. For example, following the departure of the old queen in a reproductive swarm, several virgin queens cut their way out of their queen cells. They soon detect the presence of the other queens and are further agitated by the workers which goad them on by harassing them. To shake off the harassing workers, the queen pipes with her wings. This high pitched sound causes the workers around her to freeze, and she scoots away temporarily before they again catch up with her. In an observation hive it is possible to follow the path of the queen as she pipes on the opposite side of the comb by observing the bees ‘freezing’ in the absence of the queen on this side. The sounds/ vibrations are carried through the comb.
The sound of drones returning to their hive after a mating flight is distinctive and cannot be confused with that of a worker bee. The screeching sound of a Stuka fighter aircraft in a bombing dive was deliberately built into the plane to terrify the enemy on the ground. Surely then, the loud and distinctive sound of a drone in flight also has an important purpose? The sound (and vibrations in the air?) of several thousand drones in a DCA could serve to make the locating of the DCA easier for both drones and virgin queens. Sound could also assist, besides sight and pheromones, in the creation of a DCA and the formation of drone comets and also to help distinguish a drone from a queen within the DCA. While marking drones in a DCA several would accidentally have ‘tippex’ splattered on their wings. This would result in a different sound being produced as it flew off which immediately attracted other drones to it. A major function of a DCA is to facilitate the complete mating of a virgin queen in the shortest possible time and a combination of sound, sight and pheromones may serve to accomplish this.
Evolution of male bee pheromone glands for mating?
While monitoring the number of times marked drones flew each afternoon and the duration of their flights, it was observed on many occasions that returning drones had the two interstitial abdominal membranes exposed – in exactly the same position as that of Xylocopa caffra males. Although dissections of drones were made to discover any underlying pheromone glands, they were so small that the equipment used could not detect them. If this is the source of a mating pheromone, it appears that it may be present in many bee species from solitary, sub-social and social species. Besides different flight times, the comparison of the composition of this pheromone could possibly help explain the sexual isolation of the different species of Apis and their phylogenetic linkages.
The authors at work:
Boch, R., Shearer, D.A. and Young, J.C. 1975. Honey bee pheromones: field tests of natural and artificial queen substance. Journal of Chemical Ecology 1(1): 133-148.
Brὔckner, D. 1979. Effects of inbreeding on worker honeybees. Bee World 60(3): 137-140.
Butler, C.G. 1971. The mating behaviour of the honeybee. Journal of Entomology 46: 1-11.
Butler, C.G. and Fairey, E.M. 1964. Pheromones of the honeybee: biological studies of the mandibular gland secretion of the queen. Journal of Apicultural Research 3: 65-76.
Cooper, B.A. 1977. Have you heard a drone assembly? British Isles Bee Breeders’ Association, 9pp.
Currie, R.W. 1987. The biology and behaviour of drones. Bee World 68(3): 129-143.
Fletcher, D.J.C. and Tribe, G.D. 1977. Natural emergency queen rearing by the African bee, A. m. adansonii, and its relevance for successful queen production by beekeepers. In African Bees: Taxonomy, Biology and Economic Use, ed. D.J.C. Fletcher. Pretoria: Apimondia. Part I, pp. 132-140; II pp. 161-168.
Gary, N.E. 1962. Chemical mating attractants in the queen honey bee. Science NY, 136: 773-774.
Gary, N.E. 1971. Observations on flight-experienced queen honeybees following extra-apiary release Journal of Apicultural Research 10(1): 3-9.
Holmes, F.O. and Henniker, N.H. 1972. Attractiveness of drones to worker honeybees. Gleanings in Bee Culture 100(10): 297.
Johannsmeier, M.F. (Ed.) 2001. Beekeeping in South Africa. Third Edition, Revised. Plant Protection Research Institute Handbook No 14, Agricultural Research Council, Pretoria. 288pp.
Moritz R.F.A., Kryger P. and Allsopp, M.H. 1996. Competition for royalty in bees. Nature 384: 31.
Orὅssi-Pál, Z. 1959. The behaviour and nutrition of drones. Bee World 40(6): 141-146.
Renner, M. and Baumann, M. 1964. Ueber Komplexe von subepidermalen Drὔsenzellen (Duftdrὔsen) der Bienenkὅnigen. Naturwissenschaften 51: 68-69.
Renner, M. and Vierling, G. 1977. Die Rolle des Taschendrὔsenpheromons beim Hochzeitsflug der Bienenkὅnigin. Behavioral Ecology and Sociobiology 2: 329-338.
Ruttner, F. 1968. The life and flight activity of drones. Australia Beekeeping 69(4): 279-284.
Ruttner, H. 1972. Neue Versuche ὔber die Flugbahnen der Drohnen ὔber den Alpen. Apimondia Science Bulletin, Bucharest, pp 79-81.
Tiesler, F.K. 1972. Mating stations in the islands north of Germany. Apimondia Science Bulletin, Bucharest, pp. 91-95.
Tribe, G. 1982. Drone mating assemblies. South African Bee Journal 54(5): 99-100, 103-112.
Tribe, G.D. 1989a. Drones caught in a spider’s web within a drone congregation area. South African Bee Journal 61(5): 110-111.
Tribe, G.D. 1989b. A drone congregation area in Perth, Western Australia. South African Bee Journal 61(4): 83-86.
Velthuis, H.H.W. and Camargo, J.M.F. de 1975. Further observations on the function of male territories in the carpenter bee Xylocopa (Neoxylocopa) hirsutissima Maidl (Anthophoridae, Hymenoptera. Netherlands Journal of Zoology 25(4): 516-528.
Watmough, R.H. 1974. Biology and behaviour of carpenter bees in southern Africa. The Journal of the Entomological Society of Southern Africa. 37(2): 261-281.
Woyke, J. 1962. The hatchability of ‘lethal’ eggs in a two sex-allele fraternity of honeybees. Journal of Apicultural Research 1: 6-13.
Zmarlicki, C and Morse, R.A. 1963. Drone congregation areas. Journal of Apicultural Research 2(1): 64-66.
Geoff Heathcote-Marks, Dominique Marchand and Geoff Tribe
American Foulbrood (Paenibacillus larvae) is an exotic bacterial disease which appeared in South Africa some 20 years ago and to which our indigenous honeybees had not before been exposed. After its initial discovery in the Cape Peninsula where it wreaked havoc amongst several commercial beekeepers, the disease spread throughout the Western Cape where sporadic outbreaks were reported over the intermediate years. Then in 2015 there was again an upsurge in the disease in which major losses were inflicted on mainly commercial beekeepers which raised major concerns.
The economy of the Western Cape is underpinned by the export fruit industry which in turn is reliant on pollination by honeybees. With the expansion of the industry in recent years, there is already a shortage of pollination units. This is now exacerbated by the presence of American Foulbrood (AFB) which is only contained either by incinerating infected hives or by radiation treatment which adds to the cost. Why commercial beekeepers are more adversely affected by American Foulbrood as compared with that of hobbyist beekeepers appears to be the greater mobility of hives of the former and the higher infection rate experienced at the depot where honey is extracted due to intermingling of hive parts and the drifting of bees.
Hobbyist beekeepers in Pinelands
The recent discovery of American Foulbrood in the Cape Town suburb of Pinelands has raised some interesting questions. Several hobbyists keep hives within the suburb and there are many wild swarms to be found both within trees and in air vents etc. in houses. Swarms are trapped or removed within and in the surroundings of the suburb but there is no commercial activity where hives are taken to orchards for pollination purposes. The suburb provides many flowering plants for the bees to utilize including ornamental eucalypt species such as the red flowering gum, Corymbia ficifolia (Fig.1), the sugar gum Eucalyptus cladocalyx and many other tree species such as the Brazilian pepper tree. Garden flowers and indigenous plants in many open spaces provide both nectar and pollen especially in spring, but there is always something flowering throughout the year.
Several incidences of AFB infected hives have been recorded in Pinelands both in hives and in wild swarms. The current case has been well documented. The bees took up residence in an owl-box at a height of 6 metres from the ground in late November 2014. Here they flourished for about a year. However, they were observed to abscond on 30 December 2015, settling in a tree for a brief time before disappearing in a swirl of bees. They left behind about 8 sturdy combs about 22 cm deep and wide, of which 4-5 had been brood combs. All the honey had been consumed by the departing bees. Some diseased brood which had the typical sunken appearance and perforations in the cappings together with the characteristic scattered brood pattern (Fig.2) remained to show the extent of the disease. The ‘matchstick’ test confirmed the presence of AFB (Fig. 3).
What raised many questions were the following observations. Although there were two hives on the property, no robbing of the vacated owl box was observed – which raises the question whether the smell or sliminess (Fig. 4) of the infected combs act as a deterrent to potential robbers? If this were so, it would serve to help contain the spread of the disease to a great extent. This foul odour which is symptomatic of the disease is foreign to African bees, and if it acts as a deterrent, then it must contain some interesting compounds. African bees are not adverse to collecting water from urine, from animal dung, or from making their nest in a tree frequented as a sleeping place for baboons which foul the whole area, yet show no adverse reaction to such powerful odours when foraging.
Another interesting observation was that despite the nest having been vacated about a month ago, the indigenous small hive beetle, Aethina tumida, had not consumed the combs which, although devoid of honey, had plenty of pollen stores and dead brood on which to feed. Several small hive beetles were observed when the owl box was dismantled, but only a single larva was seen (Fig. 5). The small hive beetle belongs to a family of scavengers who nearly always are present in a colony but flourish if the colony should begin to falter through starvation or disease. The small hive beetle is highly adapted to living within a honeybee colony as it is one third the size of a worker bee, has a round, smooth dome and when confronted it merely pulls in its appendages and holds tightly to the substrate. Hence it is able to enter worker cells where it feeds on eggs, pollen and honey. In a strong hive the small hive beetle hides away in crevices where the bees cannot access them. The bees’ response is to confine them in a propolis jail where they are prevented from mating or laying eggs. However, the small hive beetle confined as such is able to solicit food from its captors. This normal reaction where one worker bee may solicit food from another by antennal contact is mimicked by the confined beetle, which is then fed by the misled bee. Should the swarm abscond, the small hive beetle breeds rapidly and their larvae within a short while are able to consume the entire nest and then exit to pupate in the soil in front of the nest. In this way, much like hyenas, they act to control the spread of disease.
The small hive beetle recently found its way to North America and Australia where it has overwhelmed hives because the European races of honeybees on those continents were unfamiliar with it and were unable to contain or expel it. The prolific use of propolis by the African bee may in part be a consequence of containing the small hive beetle where wild nests in cavities may be enveloped in a propolis sheath which denies the beetle places in which to hide (Tribe 2000).
Similarly, wax moth larvae were present only in a small section of the honey-crown (possibly where the lowest titre of diseased spores would be found) (Fig.6) but had not also consumed the brood combs. Were they perhaps also deterred by the presence of the disease?
The above observations are limited to the colonies inspected and it is not known if the above applies to most colonies infected with AFB.
How is AFB spread to wild swarms?
How did this owl-box swarm become infected with AFB? Had they brought the disease with them as a trace of spores when they took up residence and which then took a year to overwhelm the colony? The two hives on the property showed no signs of AFB but will continue to be monitored. Absconding was most definitely as a result of the disease, a behaviour which is consistent with African bee races when faced with adverse conditions (Hepburn & Radloff 1998). The honey containing AFB spores that the absconding bees ingested before departure would be consumed within a few days and in theory they would then have rid themselves of the disease and be free to begin elsewhere again. This is one method that beekeepers use to rid their hives of the disease by shaking the bees into a new hive, burning the infected hive, and starving the bees for about a week to rid them of the spores. Could the owl-box swarm have absconded once before due to the disease but not entirely rid themselves of the disease which slowly built up to overwhelm them?
Natural health of African bees
Beekeepers in southern Africa have adapted their methods to tie in with the ecology of the African bee. The underlying basis of beekeeping in South Africa relies on the trapping of migrating, absconding or reproductive swarms to replenish their ‘stock’. Absconding is ubiquitous in the African races and is induced by dearth, predation or deterioration in nest quality (Hepburn 1993). To those in Europe, Australia or the Americas (the latter two continents having been devoid of honeybees before European colonists arrived) who work with European races of honeybees, this would seem fairly primitive. What is so different in southern Africa is that because they are indigenous, more than 80% of honeybee colonies are still to be found in the wild. Even those that are hived are never really domesticated – they as easily abscond and may again at some stage be re-captured by a beekeeper in a trap-box. However, the great advantage here is that the African bee is still being subjected to natural evolutionary pressures and can be regarded as being extremely healthy genetically. The Varroa destructor mite from Asia which wrought havoc in those countries farming with European honeybees, despite great apprehension initially, was brought under control by the African bee because of two main traits – that of having a shorter life cycle, thus the mite not being in full synchrony with that of its host, and of being more aggressive and physically biting and removing them from the hive. Could we hope that the African bee has the means in its ‘repertoire’ of behavioural traits to neutralise AFB?
Absconding as a defence mechanism?
American Foulbrood appears not necessarily to cause the death of a honeybee colony, which if strong enough after detecting the disease, will abscond before being overwhelmed. If the honey engorged before they absconded is used within a few days and the newly constructed combs are not contaminated with AFB spores, then the colony has a good chance of surviving and ultimately thriving.
Fletcher, D.J.C. 1975-1976. New perspectives in the causes of absconding in the African bee (Apis mellifera adansonii L.) South African Bee Journal I & II. 47(6): 11-14; 48(1): 6-9.
Hepburn, H.R. 1993 Swarming, absconding and migration in southern African bees. South African Bee Journal 65(3): 61-66.
Hepburn, H.R and Radloff, S.E. 1998. Honeybees of Africa: 5. Swarming, migration and absconding. Springer –Verlag, Berlin Heidelberg.
Tribe, G.D. 2000. A migrating swarm of small hive beetles (Aethina tumida Murray). South African Bee Journal 72(3): 121-122.
By Karin Sternberg, Jenny Cullinan and Geoff Tribe
Like all living creatures, the honeybee faces many dangers in trying to survive – from environmental hazards such as fires and drought, to the many organisms which wish to feed off their honey and nutritious brood. Those colonies which survive and prosper will be the ones which send out many drones and reproductive swarms which will disperse their genes to the advantage of the species. Because at least 80% of honeybee colonies in Africa are wild (Fig. 1) and relatively few have been hived, the evolutionary pressures acting on the species is being maintained. Even those hived are never domesticated – they have a strong tendency to abscond, for reasons such as starvation or an excess of parasites, or to migrate to seasonal honey flows in adjacent regions. These swarms will in turn be hived again because beekeeping in southern Africa is based on the annual trapping of wild swarms, whether migrating or reproductive, for ‘making increase’ – bringing the number of hives up to optimum again.
Another of the dangers not often pondered are the ambush predators, the robber flies and wasps, many of them generalist predators of soft-bodied insects such as flies, but the diet of several species consists largely of honeybees. The banded bee pirate Palarus latifrons (Fig.2) can be a major problem for beekeepers in the dry, hot and sandy regions of southern Africa. Foraging bees are captured as they leave the hive and are paralyzed by the female wasp which makes a cavity in the soil in which the bee is placed. On this bee the wasp lays an egg which hatches into a larva and consumes the bee.
As many as 80 bee pirates have been seen in front of a hive at the Heuningberg near the town of Porterville on the West Coast. The bees become so intimidated that they cease foraging – only pouring out as the sun sets and the wasps have departed as it cools and they become inactive. The bees fill the entrance with their bodies and create a ‘moaning’ sound which is quite distinctive. The wasps alight on the entrance board and try to entice a bee away from the massively defended entrance. Often the only solution is for the bees to abscond because they are starving.
Robber flies (Fig.3) regularly capture honeybees in flight usually away from the nest where they sit on the sand or perch on rocks or twigs from which they make forays at foraging bees or any passing soft-bodied insect. Around Vachellia (Acacia) karroo trees in flower in the Tanqua Karoo, they tend to perch on nearby rocks and capture the many flies which visit the flowers. There is no information on the numbers of robber flies in any area or any quantifiable data on their detrimental effect on honeybee populations.
The wasps of the genus Philanthus are well known predators of honeybees but will also prey on a wide range of bee and wasp species. The yellow bee pirate Philanthus triangulum which preys regularly on honeybees has another strategy: it ambushes the bees on the flowers on which they are foraging (Fig.4).
It is widely distributed and is common in Europe where it is known as the ‘Bee Wolf’. The wasp stings the bee in the throat which it then malaxates, feeding on the honey which is forced from its crop. The paralysed bee is taken to a burrow excavated in the sand where it is stored in a cell with others to provision the larvae with food in the same way as the banded bee pirate. While observing a bee wolf out foraging on a flower, its behaviour changed when a honeybee came into range. It later dug a nest in a sandy bank and then flew off only to return 12 minutes later with a honeybee it had captured (Fig.5).
Recently vast numbers of wasps of the Bembix genus were observed in the vicinity of honeybees drinking water in seepage beside a stream in the Cape Point section of the Table Mountain National Park. With temperatures as high as 36°C a number of bees were collecting water (Fig. 6).
Tracking Bembix in the late afternoon light, we found an aggregation of about 50 nests located in soft soil on the bank above the stream and many Bembix furiously and almost chaotically digging at the surface at intense speed creating new nesting sites (Fig.7). Bembix wasps do not have it all their own way. Adult wasps are preyed on in turn by some birds, lizards and antlions, Neuroptera and probably also crab spiders, robber flies and mantids; while bombyliid flies are known parasitoids of their larvae, and chrysidids, cuckoo wasps, mutillids (velvet ants) and true ants are known to rob Bembix nests. One of the Bembix observed was carrying a winterschmitiid mite (Fig. 8), attached to the thorax with its suctorial plates. Many of the mites are phoretic, travelling on the body of adult insects without being a parasite. (S. Gess, pers. comm).
The alien European wasp, Vespula germanica (Fig. 9), is now firmly established in the south-western Cape and with time will migrate up the eastern coast into other provinces. It nests in the ground, as opposed to the other invasive wasp, Polistes dominulus, also from Europe which makes grey ‘mache’ nests the size of a football under the eaves of houses. Vespula germanica feeds on soft bodied insects including honeybees at flowers and is able to raid hives, collecting both adults and brood to feed to their larvae. The mild climate in southern Africa allows them to build massive nests in the ground, to persist throughout the year, and to invade the fynbos.
There is a great variety of organisms which feed on honeybees, of which those which have a close association are recorded and their biology mostly unraveled. But there appear to be yet many more opportunistic species of predators of honeybees which are only rarely recorded when they are chanced upon. They occur in diverse environments from fynbos to semi-desert biomes and their slow attrition on the numbers of foragers must ultimately have an effect on the well-being of the honeybee colony.
Pulawski, W.J. and Prentice, M.A. 2008. A revision of the wasp tribe Palarini Schrottky, 1909 (Hymenoptera: Apoidea: Crabronidae). Proceedings of the California Academy of Sciences, Series 4, 59(8): 307-479
We are grateful to Dr Sarah Gess of the Department of Entomology and Arachnology, Albany Museum for the information supplied concerning these wasps.
The authors at work:
Review of the book: “Termites of the Gods” by Siyakha Mguni, Wits University Press, South Africa (2015) with emphasis on the connection with honeybees.
By Geoff Tribe
Scenes of honeybee nests and honey hunting are depicted in rock art (Fig. 1) at various locations in southern Africa. There is a particular painting from the shelter at the Toghwana Dam site in southern Zimbabwe which has been reproduced many times (Pager 1971, Guy 1972, Crane 1982) in beekeeping literature (Fig. 2) depicting what has been interpreted as a man with a lit torch besides a bees’ nest with a stream of bees emerging from one side of the nest. This would intimate that smoke was used by the Bushmen (San) in calming the bees, even though the ‘flames’ of the torch are directed backwards as if blown thus by a strong wind.
Siyakha Mguni demonstrates convincingly in his book “Termites of the Gods” that this painting actually depicts termite alates leaving the nest but still has a spiritual connection with honeybees.
This Toghwana Dam painting falls into the category of ‘formlings’, of oblong or ovoid blobs enclosed by a line surrounding them, whose semblance has puzzled archaeologists over the last 200 years with many varied and unsatisfactory explanations been given. These formlings are concentrated in shelters mostly in southern Zimbabwe but occur also in the northern most regions of South Africa. The largest formling depiction is found in the Waterberg District of Limpopo Province and covers 12m² in area on the rock face.
This book is a study of these ‘formlings’ and the elucidation of their meaning, where we are taken into the spiritual beliefs of the San and their cosmic world view. Siyakha Mguni has presented an interesting hypothesis as to their meaning, although he does not claim to be able to understand everything associated with the concept of formlings.
Importance of fat
For the San, fat is a substance that possesses strong ‘potency’ – a supernatural force which like electricity, is an invisible but powerful force which manifests itself in the form of light, heat and kinetic energy. This potency is believed to be particularly saturated in large antelope (eland, kudu, hartebeest and gemsbok) and giraffes, buffalo, elephant and rhino which contain relatively large amounts of fat. Certain insects, principally honeybees and termites, are also regarded to possess strong potency, as does their honey and fat respectively. It is recorded elsewhere that early European hunters in Africa were fully aware of this demand for fat by indigenous peoples, where the killing of a hippo or elephant was regarded with much joy because of the copious amounts of fat which was normally a rare resource. Small antelope are largely devoid of fat.
For example, William Burchell the naturalist and explorer, while traversing Bushmanland from Klaarwater (Philippolis) to Graaff Reinet in 1811 was visited by four female San whom he hospitably received. He records “A wooden bowl, in which was left a quantity of liquid Hippopotamus grease, was eagerly seized upon, and its contents drunk off, with an avidity most nauseous to behold; while that which still adhered to the bowl, they carefully scraped out with their hands, and smeared on their bodies” (Buchanan,2015). For people who had been subsiding on lizards, snakes, tortoises, ant’s eggs and roots, this was a substantial meal. As indicated by Burchell, the fat, usually mixed with herbs such as Buchu where available, was also used as a sunscreen, to keep the skin moist, and as a deterrent to biting insects.
The early part of the book entails the analysis of the explanations given by earlier researchers and then delves into the spirit world of the San. The conclusion that he draws is that these formlings represent the inner, underground cavern within the centre of a termite nest where the relatively enormous queen termite is found surrounded by her eggs and pupae. Known as ‘Bushman rice’, these eggs and pupae were excavated by the Bushmen and eaten. However, the reproductive flying ‘white-ants’ or alates, (Fig.3) were far more prized because they were filled with fat, a substance much in demand by hunter-gatherers.
Biology of Flying termites or alates
On exiting the termitaria in their thousands usually after rain, assisted by workers and guards (Fig. 4a+b), the alates would disperse over a wide distance and on landing would find a mate, shed their wings and begin a new colony, their fat reserves seeing them through until the first workers begin to take over certain chores in a division of labour. To attract a male, the female would release a pheromone. This pheromone has a musty smell as witnessed in the camping ground of Moremi Game Reserve in Botswana where the staff switched on all the lights in the ablution block, opened the doors and windows wide and placed the plugs in the bath. The next morning the baths were filled with thousands of alates which were collected, gently fried and either eaten directly or placed into containers for later consumption. Nobody had a bath for several days due to the musty pheromone smell! Because the alates are eaten by almost every predatory creature from birds to lizards and baboons to mongooses, the release of alates from termitaria is usually synchronized, the cue being rainfall, and the area is saturated with them, allowing many to escape predation.
Alates emerging from underground chambers
Siyakha Mguni interprets the Toghwana Dam painting as a termite nest from which termite alates are emerging and the ’lit torch’ in the hands of the man as a stick with a grass bundle at the end to be used as a plug to block the exit hole as a common harvest strategy to ensure that large quantities of alates are collected in one haul. They could then control the emergence rate as the termites would have to remove the straw before again issuing forth the following evening (or during the day if overcast or damp). He supports his argument by linking the projections on the outer enclosure of many formlings as that of mushrooms which frequently appear on the surface of termitaria. In wet seasons, from the fungus gardens of the symbiotic genus Termitomyces grow their fruiting bodies which appear as mushrooms on the outside of the termite mounds. An example of such mushrooms can be seen on this termitarium in Mokala National Park near Kimberley (Fig. 5).
Association with honeybees
Paintings of formlings are found in the hotter lowveld areas where fungus growing termite species proliferate but are absent in the colder high-altitude regions such as the Drakensberg and Maloti mountains. Here the eland takes on a greater spiritual significance, as do honeybees in the Drakensberg. Honeybee nests according to MGuni are also associated with termites and the fat that they represent, combs full of honey being referred to as being ‘fat’ by the San and ready to be exploited.
Honeybees are associated in other ways with termitaria where they often nest in the hollow centre of deserted termite mounds (Johannsmeier, 1979) or in the hollow chamber leading into subterranean nests where they build narrow but long combs. The termite mounds of the snouted harvester termite, Trinervitermes trinervoides occur almost throughout southern Africa and honeybees gain access to the mounds through holes constructed by rodents and other small mammals. Often the centres of the mounds are hollowed out by the action of rhinoceros and other beetle larvae which feed on the accumulated grass fragments on which the fungus grows and on which the termites feed their larvae.
The San cosmos
The San cosmos is an inseparable amalgamation of the natural and spirit realms. Trees are often associated with formlings because in nature termitaria often have trees growing out of them or the termitaria envelope them. Mguni’s interpretation of the San cosmos is of the termite nest in the earth as ‘God’s house’, with a tree growing out of it and into the sky which is also regarded as part of ‘God’s house’. Between the spirit domains of the subterranean and the sky is where the humans and other creatures live, and where shamanic mediation can connect the San with the cosmic realms. Bees and termites being social insects share symbolic associations in San thought and cosmology, there being a strong equivalence between fat (termites) and honey (bees) in terms of their physical character and manifestation in nature. When bees (as potent insects) swarm, they are believed to saturate the atmosphere with potency, and this is depicted for example in Botha’s Shelter (Fig. 6). The San believe that they are able to harness this potency from depictions of potent animals in their rock paintings and in their trance dances which help them to connect with the spirit world.
[P.S. The photographs and drawings in this book are superb]
Buchanan, S. 2015. Burchell’s Travels: the life, art and journeys of William John Burchell 1781-1863. Penguin Books, 240pp.
Crane, E. 1982. The Archaeology of Beekeeping. London: Duckworth. 360pp.
Guy, R.D. 1972. The honey hunters of southern Africa. Bee World 53(4); 159-166.
Johannsmeier, M.F. 1979. Termite mounds as nesting sites for colonies of the African honeybee. South African Bee journal 51(1): 9, 11-13.
Pager, H. 1971. Ndedema: a documentation of the rock paintings of Ndedema Gorge. Graz: Akademische Druck- und Verlagsanstalt.
Pager, H. 1973. Rock paintings in southern Africa showing bees and honey gathering. Bee World 54: 61-68.
By Geoff Tribe
In 1778 a curious incident was recorded by a renegade deserter from the Dutch East India Company in the vicinity of the Augrabies Falls which is believed to be the first record of poisonous honey in southern Africa. Since then other accounts of such poisonous honey have been recorded in certain regions within South Africa which are equally intriguing. Beekeepers in South Africa are fully aware of this poisonous honey and there is no danger of anyone dying because such honey is never placed on the shelves but is used by the beekeepers to feed their bees in the dearth season where the bees readily utilize it and are never poisoned themselves. Fortunately, poison honeys are often so bitter that consumption is limited.
Henrik Jacob Wikar
Henrik Jacob Wikar was a Swedish-Finn born in Gamlakarleby, Finland, in 1752 and arrived in the Cape of Good Hope in 1773 as a soldier of the Dutch East India Company. His gambling caused him to become indebted and apparently overcome by shame (or the threat of the debtor’s prison!) he deserted from the Company’s service in April 1775. Wikar kept a diary and was probably the first European to see the Augrabies Falls (Fig. 1a+b) and map the Orange River (!Garib or ‘Great River’), living amongst the indigenous people in the area until he was granted a full pardon by Governor Van Plettenberg and returned to Cape Town in July 1779. The area he covered was between Goodhouse (a corruption of the Hottentot word ‘Gudaos’ meaning ‘sheep ford’) and Koegas (‘stabbing hippopotamuses/Seekoeisteek’) between Upington and Prieska (Winquist, 1978; Nienaber and Raper, 1983).
Wikar recounted in his Journal that there were two types of trees which the Bushmen (San) used as poisons on their arrows which grew in the mountains along the Great River. The caterpillars that feed on the leaves of the one tree are collected, dried, crushed and rubbed onto the arrows with spit. The second tree he described had a strong-smelling sap that exuded once a branch is broken off and which made you blind should it get into your eyes. As he records “One day my brother companion Ouga brought me some honey which he said we might make beer of, but which he forbade me to eat. I did not quite understand why, and I did not take much heed, but I had hardly eaten a spoonful when my throat began to burn like fire, and not two minutes later my whole body became affected, and, by your leave, with apologies, I began to purge and got rid of worms looking like tape quite three fathom long [one fathom is 1.8 metres], and even longer, whereupon I fainted and the Hottentots poured water on me until I recovered consciousness; then I began vomiting so much that I had to lie down all that afternoon from weakness and fainting. I had been troubled with worms from childhood, so that sometimes I did not know which way to turn for the pain in my body, but since this occurrence, the Lord God be thanked, I have felt no pain. When it was all over, the Hottentots told me that the bees had sucked the flowers of the tree I had mentioned, and that was why the honey was so poisonous” (Maclennan, 2003). In 1818 Robert Moffat the missionary, recorded that at the Augrabies Falls his companions complained that their throats became hot after eating honey, drinking water only increasing the pain, and a local warned them not to eat the honey in that vale as it came from poisonous Euphorbia bushes (Juritz, 1925; Smith 1985).
Euphorbia or milk-wood species
The poisonous honey that Wikar ate presumably originated from the flowers of Euphorbia avasmontana which occur in pockets of concentration in the mountains along the Orange River and is known to beekeepers in that region. They flower in winter when few other plants are in flower and their yellow flowers (Fig.2) are attractive to many insects, but it is only the social honey bee which can maintain a brood temperature high enough to enable them to readily exploit this nectar source. Thus combs of honey at this time may consist entirely of nectar from this source. What is of interest is that the bees are able to utilize this honey in the normal way and it is not poisonous to them or their brood. That the Hottentots were to make mead from the poisonous honey perhaps indicates that in this form it is not toxic to humans. Obviously the Hottentots were fully aware of the properties of the honey and how to neutralize it and still use the honey. In Bushman mythology, their deity Gao!na turns himself into honey in order to poison a man who had displeased him – indicating such knowledge was prevalent amongst them (Woodhouse, 1985).
Great Fish River valley
The vegetative parts of Euphorbia species are known to be poisonous to both mammals and fish. Branches of Euphorbia shrubs thrown into pools of water have long been used by indigenous tribes to poison fish which are collected on the surface of the water and eaten. Euphorbia juice is also used as one of the ingredients used on poison arrows of the Bushmen and Hottentots in years past. The Euphorbia latex acts both as a cohesive and to produce irritation at the site of the arrow wound so as to favour absorption of the poison (Watt and Breyer-Brandwijk 1962). Baboons are known to feed on the stems of Euphorbia and then pass out – a phenomenon suggesting that they get a ‘high’ from doing so (Hood, 2005). This is especially true in the Great Fish River valley which abounds in a multitude of diverse Euphorbia species which produce white, sticky, latex if a stem is broken. Copious amounts of this latex is eaten by a number of mammals including kudu, eland, impala and baboons, but especially the black rhinoceros (Fig.3) which feeds regularly on the sweet noors, Euphorbia bothae (Hood, 2005).
All the succulent Euphorbia species are poisonous to a greater or lesser degree but 22 species are recorded as being eaten by stock or wild animals (Watt and Breyer-Brandwijk, 1962). Baboons were observed on a farm north of Windhoek in Namibia feeding on branches of Euphorbia virosa (Fig.4a+b) where they munched on them, despite the thorns, as if on corn-on-the-cob.
To have the skin torn by the thorn of, for example Euphorbia virosa, which occur throughout southern Namibia and into Namaqualand, results in a suppurating sore which takes weeks to heal. Having once collected seed capsules of E. virosa in which by so doing, some latex oozed onto my fingers, washing my hands in a running stream a bit later and then drinking water with cupped hand resulted in a strident and bitter taste in my mouth despite the miniscule amount ingested.
Incidentally, not only are several mammal species able to utilize Euphorbia plants, but insects such as the ‘koringkriek’ (Hetrodes pupus) have been observed feeding on the spineless Euphorbia dregeana in Namaqualand without ill effect.
Baboon and rhinoceros consumption of Euphorbia bushes
The story of Henrik Wikar may be linked both to that of the baboons above passing out after eating stems of E. bothae and that of the rhinoceros bot fly Gyrostigma rhinocerontis which deposit their eggs into soft indentations in the hide mainly in front of and below the anterior horn and between the anterior and posterior horns (Barraclough, 2005). Upon hatching the maggots enter the host through the nostrils or mouth and eventually attach themselves to the lining of the stomach wall where they presumably feed on blood and tissue exudates. The fly is spectacular in appearance, black with an orange-red head, being 4 centimetres long with a wingspan of 7 centimetres. Several hundred of these large spiny maggots may occur within a rhinoceros. It was suggested that all three narratives indicate that the latex of the Euphorbia species is used medicinally in order to rid the body of parasites (Tribe, 2005). In most cases the animals feeding on the latex are older with presumably a higher incidence of internal parasites. In the Western Cape of South Africa baboons can be a problem in that they strip the bark of Pinus spp, causing the upper third of the tree to die. The youngsters emulate the dominant male which results in fairly large patches of trees stripped within each plantation. The strong resinous α-pinene odour of these exotic trees presumably induce the older, dominant males to use it medicinally because they chew it but don’t in fact use it as a food source.
Regions of spiny Euphorbia concentration.
Euphorbia species are characteristic of the Valley Thicket vegetation of the south eastern region of South Africa (Fig.5).
Beekeepers in the Sundays River Valley in the Eastern Cape in earlier days had great difficulty marketing their honey due to the harsh burning sensation caused by the honey produced from dense stands of euphorbias (Juritz, 1925). Euphorbia ingens, E. triangularis and E. ledienii in particular produce masses of yellow flowers in dense concentrations, but within this region are many other species that are scattered more widely. Eventually a solution to the problem was found by removing the supers of noors honey after the euphorbias had ceased flowering and placing them in storage to be replaced on the hives during seasonal dearth periods. Honeybees utilize noors honey without any ill effects. Where ‘noorsdoorn’ shrubs are more widely scattered in the general vegetation, the amount of noors in the honey is greatly diluted and mostly edible.
Symptoms of noors honey ingestion
Usually the strong burning sensation in the throat which is immediate and persists for some hours accompanied by nausea is enough to stop ingesting the honey. No fatal cases of ingesting noors honey could be found in the literature. However, not all noors honeys are equally potent because some may be diluted with nectar from other non-poisonous plants, or it appears that the potency of the poison also varies between Euphorbia species. Having ingested a teaspoon of noors honey, I can confirm the burning sensation which followed an immediate sugar taste but suffered no further effects. Juritz (1925) records that honey from another plant in the Euphorbia family – Spiroslachys johnstonii – which occurs in Swaziland causes a person to become temporarily mentally affected.
Active principles of poisonous honeys
The active principle in noors honey was found to be soluble in ether and can be removed from the honey in this way (Juritz, 1925). Plants containing pyrrolizidine alkaloids such as rhododendrons, oleander and azaleas (Ericaceae family) are sources of poisonous honey, the pyrrolizidine alkaloids on their own are not highly poisonous, but our livers metabolize them into substances that are toxic (Winston, 2002). Other sources of nectar that contain pyrrolizidine alkaloids include common borage, Echium, tansy ragwort, lavender and comfrey.
Early record of poisonous honeys
Poisonous honey is not confined to southern Africa and has been recorded from the earliest historical times. Woodhouse (1985) recounts that in The Golden Fleece by Robert Graves, that although Butes the Athenian was a connoisseur of honey he sampled the Colchis honey which local Thessalians had warned him was poisonous as it originated in the ‘high azalea forest’ but had a bitter but refreshing taste, reduced him to insensibility and nearly spelt disaster for the Argonauts. The fleeces of sheep were placed in streams leading into the Black Sea and the gold flecks adhering to the oils in the wool were recovered once the skin was removed and dried out. Xenophon’s troops were poisoned with honey in 401 B.C. in Georgia where the Greek soldiers robbed wild nests along the route and after eating the honey, lost their senses, vomited and couldn’t stand up (Krochmal, 1994). Those who consumed small amounts were intoxicated while those who ate more acted like mad men. Most effects wore off within 24 hours, but it took several days for them to recover completely. A similar scenario occurred with Pompey and his army in the Trebizand region of the Black Sea but they were unfortunate to be ambushed by the enemy before they had a chance to recover (Krochmal, 1994). The defenders had deliberately placed toxic honeycomb along the route of Pompey’s troops where three of his squadrons were annihilated while intoxicated. In both these cases Rhododendron ponticum was said to be the source of the poisonous honey and is to this day harvested from Apis dorsata nests in the Himalayas where it induces intoxication and hallucinations when consumed in small amounts. The Trabzon region of Turkey near the Black Sea is notorious for poisonings due to the toxin in the rhododendron family which has been identified as acetylandromedol, a type of grayanotoxin, while in others it is said to be mellitoxin (Krochmal, 1994). Acetylandromedol inhibits breathing and induces hypnosis.
Colchis honey found around the Black Sea region of Turkey was known to the ancient Greeks as meli chloron (‘golden honey’) and tavern keepers up north mixed it with ale to provide an extra kick.
Pollen is often ingested by humans as a protein source and health food. If originating from the same source as poisonous honey, this pollen can be just as poisonous, giving the same intoxication and hallucination effects. This was recounted by Jack Burton (2015) who was given a jar of pollen collected from pollen traps on hives from the rhododendron-, azalea- and mountain-laurel-covered hills near the coastal mountain town of Vernonia, Oregon, USA. He went through all the symptoms of honey poisoning, from exhilaration to absolutely miserable as the effects of the sub-lethal dose wore off. The poisonous pollen has no effect on the honeybee larvae.
Poisonous honeys from honeydew
Poisonous honey need not only originate from plants. In the Whangamata district on the Coromandel Peninsula in New Zealand toxic honey is produced when bees gather honeydew excreted by vine-hopper insects (Scolypopa spp.) that have fed on the native tutu bush (Coriaria arborea). Although the neurotoxin tutin has no ill effects on bees or vine hoppers, it is highly toxic to humans – as little as one teaspoon of toxic honey can affect the nervous system.
In ancient Greece cult priests fed meli chloron to a select group of young women, the mysterious Melissai, the Bee Oracles of Mt. Panassos who – divinely maddened – were inspired to speak truthfully of the future (Burton,2015). Bees were associated with Dionysus, God of Madness, and his Maenads to whom honey was sacred, that some honeys – properly handled and administered – may contain a key to the door between worlds (Burton, 2015). In A.D. 946, Russian foes of Olga of Kiev accepted several tons of fermented honey (mead) from her followers, and while they lay in a stupor, 5 000 of them were massacred. When the Hottentots told Henrik Wikar that they were to make mead from the poisonous honey, it was possibly not to neutralize the effects of the poison but perhaps to use it in one of their sacred trance dances? The effects of poisonous honey whatever its origin was always the same as it acts on the central nervous system causing tingling sensations and numbness, dizziness, psychedelic optical effects such as whirling lights and tunnel vision, giddiness and swooning and impaired speech in which words and syllables are uttered out of sequence (Burton, 1995). Symptoms may progress to vertigo, delirium, nausea, respiratory difficulty, very low pulse rate, muscle paralysis, unconsciousness and even death. It is highly conceivable that this poisonous noors honey was used in a similar fashion where the poisonous compounds were perhaps somewhat diluted and made less virulent when transformed into mead.
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Krochmal, C. 1994. Poison Honeys. American Bee Journal 134(8): 549-510.
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Watt, J.M. and Breyer-Brandwijk, M.G. 1962. Medicinal and Poisonous Plants of Southern and Eastern Africa (Second Edition). E & S Livingstone Ltd, Edinburgh and London, 1457pp.
Winquist, A.H. 1978. Scandinavians & South Africa: Their impact on cultural, social and economic development before 1900. A.A. Balkema, 268pp.
Winston, M. 2002. Poison Honey. Bee Culture 130(9): 15-16.
Woodhouse, B. 1985. Toxic Honey. The Digging Stick 2(3):6.
By Geoff Tribe, Karin Sternberg and Jenny Cullinan
An interesting pattern discerned in the natural nests of wild honeybees in pristine Coastal Fynbos and Succulent Karoo has been the lavish use of propolis to form an enclosing wall at the entrance to the nest.
The vast majority of nests in the coastal fynbos are located under boulders and half of those in the succulent Karoo within deserted aardvark burrows. These nests have been completely sealed off except for the few exit holes within the propolis sheath (Fig. 1a+b).
The nest within a cliff in the coastal fynbos was partially propolised with part of the combs still exposed. The value of such propolis barriers could be gauged from the behaviour of the bees which started rebuilding these protective shields soon after a wild fire had passed through and destroyed them (Fig.2). The choice of nesting sites in the two biomes differs considerably as a result of the climate and topography and yet this phenomenon occurs in over 95% of the nests under rocks or in burrows. The propolis forms an immediate mechanical barrier but due to its chemical properties, imparts social immunity to honeybees through both contact and volatile emissions. Propolis is used by honeybees for a variety of purposes and certain races of the Western Honeybee (Apis mellifera) are known to use propolis more abundantly than others, particularly colonies of wild bees. Why should this be so, and what are the main cues for using propolis? A look at African races of honeybees that do or don’t use propolis when related to their environment, and where and when propolis is used may give some insight into this behaviour.
Use of propolis
A colony of honeybees collects 150-700g of propolis per hive/annum (Ghisalberti 1979, Prost-Jean 1985). Various reasons have been suggested for the ‘excessive’ use of propolis by certain races of honeybees and the Greeks very early named the substance for what they regarded as its major function – pro = before or in defence of, polis = the city.
Several environmental cues have been suggested that initiate the collection and use of propolis. The one most often touted is the enclosure of the nest with the onset of winter which is initiated by shortening day length and dropping temperatures. However, a direct correlation has never been established between the two although there is an increasing use of propolis with the onset of winter, possibly due to a reduction in nectar flow and the availability of excess foragers. This has also been observed in the African bee. If the distribution of propolis within a hive were to be quantified, the amount used in building a wall to enclose the colony, thus enhancing increased control of temperature and humidity within the hive, would account for at least half of all the propolis used in the hive. But this is not always so in the case of a wild colony in a cavity in which much propolis is used to line the cavity walls, the possible reason for this will be explained below.
Dead mice, decaying death’s head moths and other intruders are often coated with propolis which could be regarded as disease control because they are too large to remove. The large hive beetle (Hoplostomus fuligineus) of which up to 750 have been recorded in a hive, are impervious to stings (Fig.3) and cannot be removed by the bees. They burrow through comb eating bee larvae and are most destructive. The only recourse the bees have is to coat them with propolis and this has the effect of preventing them from exiting through the narrow hive entrance where they then die. The beetles lay their eggs in dung and those which do escape can often not fly as their elytra are fused together with propolis (Tribe 2009).
Constituents of propolis
Propolis is the generic name for the resinous substance collected by honeybees from various plant sources whose composition varies depending on its origin. The chemical composition of resins is complex and variable within and among plant families, traits that make resin production a good defence against rapidly evolving pests and pathogens (Wilson et al. 2013). Exudate from trees, plant wounds, and waxes from buds, such as from Protea repens and Leucadendron, are major sources of propolis, the waxes protecting the delicate new buds against harmful ultraviolet radiation. These plant exudates are present on all continents and honeybees introduced to continents where they were never present (such as Australia, New Zealand and the Americas) find no difficulty in obtaining propolis. The genus Populus is widely regarded as a preferential source of resin for honey bees in temperate regions (Wilson et al. 2013). Apis mellifera scutellata has in addition been recorded collecting pieces of leaves of Baccharis dracunculifolia (Compositae) with which to press the propolis into the corbiculae of the hind legs (Yoneda et al. 2001). Tree resins and developing leaves and buds have a high concentration of a wide variety of polyphenols which may differ radically from each other from different parts of the world.
Propolis may vary tremendously depending upon what is available in the immediate vicinity of the honeybee colony but consists of waxes, resins, balsams, aromatic and ethereal oils, pollen and other organic material in a ratio of say, 30% waxes, 55% resins and balsam, 10% ethereal oils and 5% pollen (Bee World 1973). Propolis may vary in colour from mustard-yellow to dark brown and the colour from the same source may vary depending on the season and the state of development of the buds. What bees are collecting are the chemical defences of plants used against fungi, bacteria and various predators. Resins of trees for example function to expel or encapsulate bark beetles while at the same time protecting the wound from fungal pathogens. The medicinal uses of garlic for humans are well known where, following the wounding of the corm, the volatiles mix with oxygen to form a potent compound which acts as an enhanced deterrent. Propolis is hard and brittle when cold, but becomes sticky when warm. At temperatures of 25-45°C propolis is soft and pliable and most varieties will melt between 60-70°C and some only at 100°C. Beeswax melts at about 63°C. Honeybees maintain a hive temperature of 34°C within the brood area. The yellow colour imparted to beeswax is known to be due to the presence of some constituents of propolis (Ghisalberti 1979).
Propolis has antibacterial, antimicrobial and antifungal activity; the largest group of compounds isolated are flavonoid pigments which are ubiquitous in the plant kingdom. Myrrh and frankincense of ancient times were aromatic resins obtained from trees either through bark incision or extraction from beekeeper’s propolis derived from balsam (Iannuzzi 1983a). Propolis may have been used by ancient Egyptians for embalming purposes. The Biblical ‘balm of Gilead’ was a bee-collected resinous material i.e. propolis used to heal wounds.
During the Anglo-Boer War a preparation of propolis and Vaseline, ‘propolisin vasogen’, was used as a medication due to its antibacterial properties in aiding the healing of wounds and tissue regeneration (Ghisalberti 1979). Propolis is effective against 38 skin fungi and on second degree burns. Propolis also has a surface anaesthetic action with negligible penetrating power in which the active principle is suggested to come from its essential oil. An alcohol extract was reported to be 3.5 times as strong as cocaine and was used in dental practice in the USSR in 1953.
Control of American Foulbrood
Lindenfelser (1969) discovered that an alcohol extract of propolis inhibited the growth of American Foul Brood (Paenibacillus larvae) disease in honeybees. The extract was fed directly, or mixed in dilute honey, or sprayed as an aqueous or saline solution on to the combs. At 500μg/ml the disease was controlled only during treatment, but higher concentrations destroyed healthy larvae and caused deformities. Resin from different species of plants varied in their ability to inhibit P. larvae with North American poplars differentially inhibiting the growth of P. larvae (Wilson et al. 2013). Thus, a bee’s choice of resin could have profound consequences for their ability to reduce the overall microbe load within the nest cavity. Stingless bees increase resin foraging in response to ant attacks, while honey bees increase resin foraging when intentionally exposed to the larval fungal pathogen Ascosphaera apis, the cause of chalkbrood (Simone-Finstrom & Spivak 2012).
Collection of propolis
Honeybees scrape the waxes and resins from various plants and pack it into their corbiculae or pollen baskets and return to the hive where they wait in a remote part of the hive until bees needing propolis come and pull pieces off her loads (Bee World 1973). The individual bees that both use it and collect it are specialists of foraging age. Bees that normally forage propolis also use it in the hive and are middle-aged, the latter known as ‘cementing’ bees. Resin collection usually takes place in the warmer part of the day between 10h00 and 15h30 on sunny days when it is more pliable. Honey bees have a high fidelity to a single botanical source of resin during a single foraging trip and it appears that availability, proximity, and perhaps toxicity may play roles in the selection of resins by bees (Wilson et al. 2013). Propolis may contain as many as 300 different chemicals which make it difficult for an organism to develop resistance.
The small hive beetle
The small hive beetle, Aethina tumida (Fig.4.), is native to sub-Saharan Africa and is found to a lesser or greater degree in most colonies of honeybees. If the colony is strong and healthy, these beetles are kept in check and harassed by the bees and thrown out of the hive if the bees are able to get a grip on them. But the beetle is highly adapted to its life within the hive where it is able to fit into a cell and feeds on honey and the eggs of bees. The hemispherical beetles are hairless, half the size of a worker bee, and they tuck their legs under their bodies and tightly adhere to the substrate so that a bee may not dislodge it (Tribe 2009). As the bee attempts to bring its sting into operation, it must release the beetle it has cornered which then takes the opportunity to scoot away. If a colony is diseased or begins to fail, then the beetles immediately become active, mate, and lay copious numbers of eggs. The resultant larvae devour the entire contents of the hive, causing a characteristic stink and then bail out and pupate within the soil in front of the hive. They function as the scavengers of the honeybee world where, for example, diseased colonies are neutralized and destroyed. Propolis however, is rarely eaten by the small or large hive beetles or by wax moths.
The presence of the small hive beetle appears also to result in excessive use of propolis within the hive (Tribe 2000). Researchers at Rhodes University have shown that honeybees keep the beetles at bay by encasing them in propolis ‘igloos’ or prisons if they cannot extract them from narrow crevices. But the beetles are able to survive in the hive by mimicking the begging of food by another bee, in which certain bees are deceived into feeding them (Neumann et al. 2001). In wild nests, especially in decaying holes in trees, the inside of the cavity may be totally lined with propolis which denies hiding places for these beetles.
Several wild swarms built under branches of trees have been recorded being totally encased within a propolis sheath (Tribe & Fletcher 1977). First a propolis layer is laid down under the branch or intertwining branches to which the combs are then attached. Here the main advantage appears to be the enhanced control of temperature and humidity, although the control of pests is also facilitated by this. These nests are usually so successful that the weight of their combs, which are weakened by high summer temperatures, eventually causes the entire colony to crash to the ground (Tribe 1979). Other pests with which the bees have to contend are the large hive beetles, wax moths, bee pirates and death’s head moths where narrow entrances in propolis sheaths are easily defended.
Propolis and races of Apis mellifera
Different races of Apis mellifera are recorded to use propolis to a greater or lesser degree (Ruttner 1986). The ‘Punic’ or ‘Tellian’ bee, Apis mellifera intermissa, is a uniform black race inhabiting the region of North Africa from the Atlas Mountain to the Mediterranean Sea and Atlantic Ocean (Tunisia, Morocco, and Algeria). This race is recorded to use excessive amounts of propolis. The coastal Mediterranean vegetation gives way to inland areas in which intense climatic extremes are experienced – a reason why European races of bees imported on a large scale (mostly from Italy and France) have failed to become established. Not only is there a huge daily variation in temperature which would warrant the lavish use of propolis as a means to control temperature and humidity within the nest, but the Tellian bees are known to be susceptible to brood diseases; a further reason for an abundant use of propolis.
Excessive use of propolis is also recorded for Apis mellifera iberica which is closely related to the Punic bee and A.m. mellifera which survives winter temperatures as low as -45°C and is adapted to a continental climate with its severe extremes of temperature.
Holistic defence mechanisms
Randy Oliver (2010) gives a good account of the honeybee immune system. As a complex super-organism, the honeybee colony is imbued with defences at various levels that are physical, chemical and behavioural at colony level but they are also endowed with an effective immune system at the level of the individual bee. The large honey stores of the Western honeybee which is necessary to see it through the dearth period, be it drought or winter, as well as their nutritious brood, represents a considerable food resource to predators. Firstly, the siting of nests in inaccessible clefts in rocks or high up in trees has immediate survival value. Mass attack following the marking with alarm pheromone of mammalian predators serves as a major deterrent at colony level. Smaller predators such as wax moth larvae, small hive beetles and Varroa mites are either stung or physically removed by biting with the mandibles.
Behavioural defence involves the use of undertaker bees which carry dead or dying bees beyond the boundaries of the colony; hygienic bees with their ‘washer-woman’ action remove fungi; while sick brood is detected before it becomes infective and is removed from the hive. Diseased bees voluntary leave the colony, never to return. At the individual level, eggs are laid in clean cells isolated from others and the larvae spin cocoons within the capped cells to further protect the pupae. Antimicrobial enzymes are added to the nectar to produce honey and pollen is inoculated with beneficial moulds and bacteria to preserve it within designated cells. Should parasites reach levels that are too high with which to cope, the swarm may simply abscond.
The stomach of the honeybee is possibly the most vulnerable to diseases such as AFB and nosema despite an arsenal of immune cells (haemocytes) and antimicrobial peptides to engulf and neutralise them. An additional weapon in the arsenal of the bees is self-medication using the defensive chemicals of plants.
Propolis vapours and contact as prophylactic medication?
One cost of social living is an increased rate of disease transmission among individuals, and honey bees are highly prone to a diverse set of pathogens and parasites (Wilson et al. 2013). Propolis deposited in the hive has important immunological benefits which exhibit phytoinhibitory and phytotoxic properties induced within the hive presumably from vapours because potato tubers kept in a hive did not sprout and after an extended period they suffered permanent inhibition (Ghisalberti 1979). An aqueous extract of propolis was also shown to inhibit germination. When comparing propolis treated colonies with controls, they were shown to have a significant reduction in the overall bacterial loads (Simone-Finstrom & Spivak 2010). Thus the presence of propolis in a honeybee colony may reduce the investment in the innate immune response by acting as an external immune defence mechanism i.e. the honeybee immune system is quieted in the presence of a layer of propolis enveloping the inside of a bee nest (McNeil 2010). This is the first direct evidence that the bees’ nest environment affects immune-gene expression (Simone-Finstrom & Spivak 2010). A degree of self-medication is evident where bees have been observed to embed strands of propolis in cleaned cells as a disease resistance mechanism and place propolis on the rims of cells. Cells are coated with a thin layer of propolis to sterilize them and bees entering or leaving the hive are additionally cleansed of microbes as they pass through various structures made of propolis.
Observations at natural nests have shown how bees utilize the innate antibacterial properties of propolis. In preparation for foraging trips and when the propolis is warm and sticky, bees have been seen licking at the propolis and ‘washing’ themselves with it. Bees walk across the propolis surfaces before leaving and after returning from foraging flights. It is thought that the propolis acts as a disinfecting zone. Because bees can “taste” through their feet this might be a form of protection through absorbing the antimicrobial properties of propolis prior to and after foraging (Sternberg, Cullinan, Tribe 2015).
Propolis appears to be a multi-purpose substance which is used in a wide variety of situations according to its need, this largely being determined by its environmental circumstances especially where extreme fluctuations in temperature are experienced. An aspect of the value of propolis within a colony is its value as natural prophylactic medicine acting directly on the bee itself (McNeil 2010). On warm days the aromatic odour of the propolis which permeates the nest and the volatiles that fill the cavity could have a profound effect on reducing the overall microbe load within the nest. Is it perhaps possible that besides contact, the inhalation by the bees of these anti-biotic elements contributes to the general health of the bees within the colony? Thus the growing of plants with known antimicrobial resins around apiaries could possibly further promote bee health.
The honeybees of Africa have never been entirely domesticated, there being vastly more colonies in the wild than in hives. Thus the African bee still retains much of its natural health that made it so adaptable and vigorous in the wilds of Africa.
…to be continued.
The following video clip has been slowed down to 60% of the original speed and shows bees at one of the wild nests wiping themselves with propolis before flying off on their foraging trips. The entire wall over which the bees are walking is made of propolis:
The authors at work:
Bee World. 1973. Bee products: Propolis. Bee World 54(2): 71-73.
Ellis, J.D. 2002. Life behind bars: why honey bees feed small hive beetles. American Bee Journal 142(4): 267-269.
Ellis, J.D., Delaplane, K.S., Hepburn, H.R., and Elzen, P.J. 2002. Controlling small hive beetles (Aethina tumida Murray) in honey bee (Apis mellifera) colonies using a modified hive entrance. American bee Journal 142(4): 288-290.
Ellis, J.D. and Hepburn, H.R. 2003. A note on mapping propolis deposits in Cape honey bee (Apis mellifera capensis) colonies. African Entomology 11(1): 122-124.
Ghisalberti, E.L. 1979. Propolis: A review. Bee World 60(2): 59-84.
Iannuzzi, J. 1983a. Propolis: The most mysterious hive element. American Bee journal 123(8): 573-575.
Iannuzzi, J. 1983b. Propolis: The most mysterious hive element. American Bee Journal 123(9): 631-633.
Lindenfelser, L.A. 1969. In vivo activity of propolis against Bacillus in larvae. Invertebrate Pathology 12: 129-131.
McNeil, M.E.A. 2010. Marla Spivak: getting bees back on their own six feet. American Bee Journal, Part 1: September: 857-860, Part 2: October: 949-953.
Neumann P., Pirk C.W.W., Hepburn H.R., Solbrig A.J., Ratnieks F.L.W., Elzen P.J. and Baxter J.R. 2001. Social encapsulation of beetle parasites by Cape honeybee colonies (Apis mellifera capensis Esch.). Naturwissenschaften 88: 214-216.
Nicodemo, D., Couto, R., Malheiros, E., De Jong, D. 2012. Propolis production and its relation to wax production rate in Apis mellifera beehives. In: Científica , Jaboticabal, v.40, n.1, p.90 – 96, 2012.
Oliver,R. 2010. Sick Bees – Part 3. The Bee Immune System@ Scientific Beekeeping.
Ruttner, F. 1986. Geographical variability and classification. In: Bee Genetics and Breeding, Academic Press Inc. pp. 23-56.
Simone-Finstrom, M. and Spivak, M. 2010. Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41: 295-311.
Simone-Finstrom, M. and Spivak, M. 2012. Increased resin collection after parasite challenge: A case of self-medication in honey bees? PLoS One 7(3) e34601, doi:10.1371/journal.pone.0034601.
Tribe, G.D. 1979. The fate of the propolized nest. South African Bee Journal 51(6): 12-15.
Tribe, G.D. 2009. Creatures within the hive. Village Life 34: 38-43.
Tribe, G.D. 2000. A migrating swarm of small hive beetles (Aethina tumida Murray). South African Bee Journal 72(3): 121-122.
Tribe, G.D. and Fletcher, D.J.C. 1977. A propolized nest in the open. South African Bee Journal 49(4): 5-8.
Wilson, M.B., Spivak, M., Hegeman, A.D., Rendahl, A. and Cohen, J.D. 2013. Metabolomics reveals the origins of antimicrobial plant resins collected by honey bees. PLoS One 8(10):1-13.
Yoneda, M., Shibata, I. and Takahashi, S. 2001. Leaf collecting behaviour of Africanized honeybee. Poster: Apimondia, Durban, 28 Oct.-1 Nov., 2001.
By Geoff Tribe & A. David Marais
Of the three aardvark burrows found on the farm Zoethoek in the Succulent Karoo north-east of Touwsrivier, two were inhabited by honeybees and the third was still in use by an aardvark. In contrast, none of the 17 aardvark holes inspected recently in mountain fynbos vegetation on Aurora Mountain above the town of the same name (32° 41’ 04’’S 18° 32’ 10’’E) contained honeybee nests. This is because the topography, vegetation and climatic conditions of the two sites differ greatly.
Autumn foraging by the aardvark colony
The honeybee nest in the aardvark hole on the plateau was first discovered in May 2013 (Fig. 1a). Exposed combs could easily be seen near the bottom of the burrow (Fig.1b). On a subsequent visit in January 2015, the combs were completely covered with bees and the swarm was actively foraging (Fig.2). The nest was inspected again on the 26th of April 2015. In the interim a propolis wall had been built in front of the combs (Fig. 3). As a result of 20mm of rain having fallen four weeks previously, the bees were actively foraging and white pollen was being brought to the nest – the origin of which was never discovered.
The driest period of the year in the Succulent Karoo is from January through February into March when the number of plants in flower is minimal and accessible water is hard to find. Although Hessea stellaris (Fig. 4), Ornithoglossum undulatum (Fig. 5), and an Oxalis species were in flower, no honeybees were seen to visit them.
Honeybees were soon attracted to water from a tap which was allowed to drip continuously near the shearing shed about a kilometre away (Fig. 6a). Presumably the odours released from the patch of soil dampened by the water indicated its presence to the bees. The fighting amongst the bees indicated that they were from at least two colonies (Fig. 6b); the attacked bees being vastly in the minority.
Carrion flowers and their deceptions
Honeybees however, were not involved in the pollination of five plant species of the carrion flower group which were in flower. Belonging to the Stapelieae, their flowers release foetid odours which mimic their oviposition substrates and thus attract flies for pollination. The most important pollinators of stapeliads belong mainly in the Calliphoridae (blowflies), Sarcophagidae (flesh flies) or Muscidae (houseflies). It is interesting to note that these succulent plants that extend from this semi-arid region into very arid regions, evolved to attract the ubiquitous flies that may be more prevalent than bees in such barren areas. Unlike bees which sense light better in the ultraviolet region, these flowers are a deep red that may be mistaken for meat by flies. The presence of fur-like projections on some flowers such as Stapelia hirsuta (Fig. 7a) may further imitate the appearance of a wounded or dead animal. Some of these flowers may even have yellow or white markings that further improves the resemblance by suggesting fat. In this way, Huernia zebrina (Fig. 7b) attracts blowflies. Flies which breed in dung invariably lay their eggs in clumps in crevices in the dung from which white larvae hatch. Stapelia glanduliflora (Fig. 7c) for instance, has its flowers fringed by vibratile white cilia which move in the slightest breeze and are thought to resemble that of fly maggots. Flies are believed to be attracted to this movement as they are gregarious when depositing eggs. In especially Stapelia species the flies are so deceived that they lay their eggs on the flower, only to have them predated by ants. The flies are attracted by both the appropriate colouration of the plant and the odour which act in concert, the odour profiles being species specific and independent of generic affiliation (Jὔrgens et al. 2006).
Intricate pollination mechanism
All these features may be attractive to flies but the final conviction comes with the odour the plants emit. The chemicals in these odours are not unique to the Stapelieae: they have been identified in some malodorous arums and orchids. Chemical analyses have even shown that there are different blends that conform to odours from cadavers, carnivorous faeces, herbivorous dung and urine. Bees would not be attracted to these flowers but flies are. There may be some selection according to their detection of the chemicals and the structural features of the plant. Only the right size of insect will successfully collect and transfer the pollen because a certain amount of force is needed to remove the pollinarium (Meve & Liede 1994). Probably the results of a low insect count, these plants, in a similar fashion to orchids, place their 200-300 pollen grains in a sac (pollinium). Two such sacs are connected to a central node to form the pollinarium with the two thin rods forming an inverted V-shape. The fly, exploring the flower towards the ‘nectar’ opening, is deployed as the vector for pollination when its proboscis or other part of its anatomy dislodges the sticky pollinarium. The fly may even have been fooled in laying eggs on the flower with the maggots having no hope of maturing. The pollinarium is carried to the next flower where it is detached in specialized grooves as the fly once again probes for liquid at the nectar opening.
Stapeliads in flower on Zoethoek
The five species in flower (i.e. Quaqua acutiloba, Quaqua mammillaris, Huernia barbata, Piaranthus parvulus, and Stapelia surrecta identified by Dr Peter Bruyns) have relatively inconspicuous flowers and only mild odours within this family of large and colourful flowers (Figs 8.a-e).
One species on the farm, but not in flower at the time of this visit, does have a strong carrion odour: Hoodia gordonii (Fig. 9) whose attractant consists of 94 compounds (Jὔrgens et al. 2006) which presumably have the potential of attracting a variety of fly species.
Though quite spiny, it had been partly consumed by porcupines (Fig.10); presumably because there was little else on which to forage. The Quaqua mammillaris had been partly consumed by baboons which rejected many portions as they too are spiny. Baboons and porcupines appear to have a special liking for the roots of Euphorbia rhombifolia (Fig. 11) which is dug out and consumed over the entire farm.
Ecology of stapeliads
The ecology of the stapeliads is also interesting. After the pollinarium is lodged on the complex central structure of the flower, two seed pods are produced. These eventually dry and split open to reveal small brown to black seeds that are attached to a very fine parachute. The seeds are released and dispersed by wind. The heat generated on the soil surface during the day (where temperatures of 41°C have been recorded) results in strong winds at night. These seeds are blown up against the bases of spiny Ruschia paucifolia bushes together with other debris. Here, in response to rain they germinate within the debris and grow within these spiny bushes which protect them from predators. When conditions, typically in late summer along with some rain, are favourable, these plants flower. Owing to their growth under bushes or in crevices, they need to attract their pollinators. The (mal)odour may not be sensed by flies from afar but the flower may be seen. The Quaqua mammillaris is a larger plant and bears its flowers directly on the fleshy and spiny stems on which the pollinator can see them. The Stapelia surrecta makes its flower visible by placing it on a long pedicle that projects beyond the canopy of the bush.
Migration of animals
Stapeliads are in synchrony with their environment. They respond to sufficient rainfall by flowering from 3 to 4 weeks later. When animals could still migrate in days of old, herds of antelope would follow the rain and the fresh grazing that it produced. No doubt this would support the growth of flies and the mimicry of the smell of dung would be useful for the pollination of the carrion flowers. The phenomenon of a migrating herd was described by George Mossop in 1877 in his book “Running the Gauntlet” on the Transvaal Highveld near the present day town of Davel. One day while out hunting with an elderly Boer by the name of ‘Ghert Visajie’, Mossop saw many thousands of game on the plain. They suddenly began to trot in opposite directions, leaving an open lane of two miles wide as far as the eye could see. He then heard the distant low rumblings of what appeared to be thunder although it was a perfectly clear day. ‘Visajie’ shouted a warning and spurred his horse up the side of a kopje (hillock) where they watched a huge cloud of dust, about two miles wide, rushing towards them. This great cloud of dust came rushing up with the thunder of hoofs making the earth tremble. Then a line of wildebeest came into view, followed by a mass of game of all kinds which took an hour and a half to pass. ‘Visajie’ explained that their grass had been grazed to the ground and now they were moving on to where it had rained in the distance. The game in possession of the grazing made the lane open for them to pass through to new grazing lands further on. This phenomenon would be repeated again and again, with those now in possession of grazing eventually becoming the migrating herd and being let through by the other herd until an annual circle had brought them back again.
Chemicals used in attraction
With such animals are the constant hoards of flies of various species which pester them. The antelope in turn are trailed by predators, especially lions, which follow in their wake. These flies may be biting flies which feed on the blood of their mammalian hosts; feeding on the liquids such as around their host’s eyes or sweat; on the carcasses of the prey brought down by predators; or those flies which breed in the dung of the various mammalian species. The chemical nature of the odours which attract flies consist of oligosulphides (which mimic carrion) and phenol, indole and p-cresol (which mimic faeces). The stapelia attractants can be divided into four groups – those that mimic herbivore faeces (high in p-cresol content but low amounts of polysulphides); carnivore/omnivore faeces or carcass (high polysulphides but low amounts of p-cresol); carnivore/omnivore (high amounts of heptanal + octanal); and urine (hexanoic acid) (Jὔrgens et al. 2006). At this time, several weeks after the rain has fallen, as the animals migrate through the now green region, the stapeliads are in flower and they virtually ‘borrow’ these flies for pollination. Only flies are attracted, for despite the huge diversity and abundance of dung beetle species in southern Africa whose primary attraction is to dung (Tribe and Burger 2011), they are not attracted to stapeliad flowers.
Two divergent pollination systems
Within this Succulent Karoo there are thus two entirely divergent systems at play involving specialized pollinators with completely different attractants – that of a scented flower with a reward of sweet nectar and the other of foul smelling carrion. In the former system there appears to be mutualism in that the flowering plants and the pollinator benefit from each other. Honeybees have a well-developed communication system which is able to immediately recruit large numbers of foragers to a transient nectar source unlike that of flies. In the case of the carrion flowers, the flies are exploited – there is no benefit to the flies and their survival clearly depends on other factors but is nevertheless essential for the carrion flowers. Stapeliad flowers are considered as deceptive flowers because they defraud the flies while imitating a substrate for oviposition (Meve & Liede 1994). The ecology of both categories of pollinators is intricately linked to their environment which determines their behaviour in all respects.
Dr A David Marais is a Professor in Chemical Pathology at the University of Cape Town Health Science Faculty. Both Dave and Geoff have a mutual interest in the Stapeliads – the carrion flowers which emit a stench and are pollinated by a variety of flies and not by bees!
Dr Geoff Tribe is a Specialist Researcher – Entomology, Plant Protection Research Institute (retired), has done research on dung beetles, honeybees, forest entomology, slugs & isopods.
Bayer, M.B. 1978. Pollination in Asclepiads. Veld & Flora 64(1): 21-23.
Bruyns, P.V. 2005. Stapeliads of Southern Africa and Madagascar Volumes I & II. Umdaus Press, Pretoria, South Africa. 606pp.
Jὔrgens, A., Dὅtterl, S. and Meve, U. 2006. The chemical nature of fetid floral odours in Stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae). New Phytologist 172: 452-468.
Meve, U. 1994. The genus Piaranthus R.Br. (Asclepiadaceae). Bradleya 12: 57-102.
Meve, U. and Liede, S. 1994. Floral biology and pollination in stapeliads – new results and a literature review. Plant Systematics and Evolution 192: 99-116.
Mossop, G. 1990. Running the Gauntlet. Publisher: Gordon Button. ISBN 0-620-14756-3
Tribe, G.D. and Burger, B.V. 2011. Olfactory ecology. In: Simmons, L.W. and Ridsdill-Smith, T.J. (Eds) Ecology and Evolution of Dung Beetles. Wiley-Blackwell. pp 87-106.
By Geoff Tribe, Karin Sternberg and Jenny Cullinan
Solitary and sub-social bees such as the allodapines, anthophorids, xylocopids and megachilids construct their nests in the branches and stems of dead plants. Such nesting sites include the inflorescences of Aloe species and stems of Kniphofia, Watsonia and various Iridaceae species that contain pith which is excavated to form a chamber. In the case of the allodapines, the pith is removed, the entrance is narrowed and the eggs are laid within this chamber so formed. The megachilids have a more elaborate system where pieces of leaves are removed from plants and used to line their cavities. The much larger carpenter bees or xylocopids excavate tunnels in dead branches which are protected from rain, and construct partitions between the individual cells, each of which is provisioned with a lump of a paste consisting of nectar and pollen on which a single egg is laid.
These nesting sites being composed of dead plant material are thus highly flammable in a vegetation type whose existence relies on regular fires at about 15 year intervals to maintain itself. This would indicate that a fire would be highly detrimental to the local existence of these solitary and sub-social bee species. The fates of the solitary bees after the recent fire in Cape Point Nature Reserve following a lightning strike were investigated.
Within the park allodapine bees were found to construct their nests most frequently in the dead branch tips of the pincushion Leucospermum conocarpodendron and the Mimetes fimbriifolius (Fig. 1a+b+c+d) by hollowing out the pith and then artificially constricting the entrance which they defended either with their heads or stings protruding (Fig. 2a+b).
Several such nests could be found on one bush, the number appearing to be determined by the number of tips that had been broken and the pith exposed. The bees were observed collecting nectar and pollen from a wide variety of indigenous plants whose flowers were mostly yellow and the pollen easily obtainable for species which do not possess baskets on their legs to pack the pollen, but instead remove the pollen coating their hairy bodies on their return to their nests (Fig.3a+b). Some of the plant species that they pollinated were very small with tiny flowers and thus play an important, if largely unnoticed, ecological role in the maintenance of the fynbos.
The fire was indeed disastrous for these bees nesting in dead plant material since nearly all the nests were incinerated. Only the distal ends of a few individual nests in thicker tips of the pincushions and Mimetes survived although the entrances had not been reconstructed four weeks later, and the nests were seemingly deserted. Plants which respond to a fire and owe their continued existence to regular fires such as the fire-asparagus Asparagus lignosus, Kniphofia uvaria and Haemanthus sanguineus were in flower within three weeks and were already visited by various solitary bees within this burnt area (Fig. 4 a, b, + c). Had they migrated into this area from the un-burnt fynbos and established new nests? No new nests were observed but singed and still living Leucospermum conocarpodendron and Mimetes fimbriifolius bushes now had dead tips which presumably could provide new nesting sites for immigrant bees.
The ecology of most of these solitary bees is unknown and yet they appear to play an important role within the fynbos. An example of this, not previously recorded is the interaction between the allodapine bees nesting in the tips of L. conocarpodendron and the neddicky (Cistocola fulvicapilla) (Fig.5) bird inhabiting the fynbos. The neddicky feeds on small insects and their larvae (Ginn et al. 1990). In the presence of ants attempting to enter the allodapines’ nests, the allodapines would respond with a high-pitched piping sound and the intruder would invariable leave. This sound was recorded and then replayed in front of individual nests not being harassed by ants. This would result in the resident allodapine appearing at the entrance and similarly piping. Unexpectedly, a neddicky bird was observed moving around these branch tips containing several nests and producing a similar sound to the detriment of the bees which stuck out their heads and were plucked out by the bird and eaten.
The fire occurring at the end of the season when most allodapines of the next generation would have dispersed to construct new nests would result in the local extinction of the bees within the burnt area. Yet the post-fire response of the fynbos plants which came into flower appears to have begun a re-colonization of the area by the solitary bees.
Acknowledgement: We thank SANParks Table Mountain National Park for permission to study these bees within the park.
Ginn, P.J., McIlleron, W.G. & Le S. Milstein, P. (Eds) 1990. The Complete Book of Southern African Birds. Struik Winchester, 760pp.
By Geoff Tribe, Karin Sternberg and Jenny Cullinan
One of the major influences on the formation and maintenance of the fynbos biome is the periodic occurrence of fires which are regarded as necessary at intervals of every 15 years or so. Fynbos fires can be extremely hot if there is accumulated fuel and a wind driving the fire. Fynbos plants are adapted to fire and respond in various ways including serotiny where fire releases the seeds of various Proteaceae from their fire-resistant seed-capsules after the fire has passed. In response to the smoke these seeds which are stimulated by cooler tempertaures and rain germinate. Other plants may survive as underground bulbs or tubers and take the opportunity of the post-fire period of reduced competition to proliferate, with different species appearing on the surface and flowering in sequential waves.
Cape bee nesting sites. The natural distribution of the Cape honeybee (Apis mellifera capensis Escholtz) is extremely limited and closely follows that of the fynbos vegetation of the winter rainfall region (originally covering only 90 000 km²). The Cape honeybee co-evolved with the fynbos and is well adapted to its environment. The wild fire following a lightning strike on 5 March 2015 which cut through a section of Cape Point Nature Reserve before it was extinguished (Fig.1) left a desolation of ash and sand in its wake (Fig. 2).The adaptation of various creatures to fire-prone fynbos gives some insight into the importance in the selection of nesting sites within the fynbos by honeybees. Within this swathe were three natural colonies which had been monitored for nine months prior to the fire. The colonies were between 1 and 2.5kms apart.
The colonies in the burnt area were visited on 15 May 2015. All three colonies escaped initial destruction by the fire and this was primarily due to where they had established their nests – under boulders at ground level. But none of the colonies escaped totally unscathed and all had declined in vigour and in the number of active foragers. The highest yearly annual wind speed in southern Africa is recorded at Cape Point and, in addition, the now loose sand is being blown into the fully exposed nests which is exacerbating their efforts to survive. The winter rains are delayed and severe downpours could result when they do arrive which could flood the nests with sludge.
The nest of Colony 1 which was constructed deep under a boulder (Fig. 3a) appeared to have escaped relatively unscathed due to the propolis wall which protected the nest but had melted due to the heat from the fire (Fig. 3b). Fourteen combs were visible but the population had dwindled considerably although there was foraging activity with pollen from Serruria sp. growing outside the burnt area being brought back to the nest. Prior to the fire, Colony 1 was fairly protected from the elements by the growth of vegetation around it (Fig. 3c).
Colony 2 (Fig. 4a) appeared to have been severely affected by the fire, which judging from the numerous rocks about the entrance that were cracked (Fig. 4b), the heat was intense. The propolis wall had melted and the combs had melted except for the comb mid-rib (Fig. 4c). During the examination of the colony in cold windy weather, two bees emerged but were unable to depart normally on flights as if both were too cold and starved to do so. However, on the following sunny day foraging activity was witnessed (Fig. 4d).
From inspection, Colony 3 (Fig. 5a) had a propolis wall which enclosed the entire nest but which was melted by the fire – as had some of the combs which consisted only of the comb mid-rib (Fig. 5b). On a subsequent visit, of the seven combs that were visible, the bees were clustered on the end three combs but were still actively foraging (Fig. 5c).
Propolis and beeswax: It has been recorded that during the heat from a fire, bees keep the colony ventilated by vigorously fanning their wings to prevent the combs from melting (Root 1950). At temperatures of 25-45°C propolis is soft and pliable and most varieties will melt between 60-70°C and some only at 100°C. Beeswax melts at about 63°C. Honeybees maintain a hive temperature of 34°C within the brood area. Propolis is a mixture of different plant resins and gums collected from unopened flower buds, especially of Leucospermum and Protea species within Cape Point. Because it consists of the defensive chemical exudates of plants, it has many anti-bacterial and anti-fungal properties and is aromatic. The major components of propolis are resins (45-55%); waxes and fatty acids from both beeswax and plants (25-35%); essential oils (10%); protein – mainly pollen (5%); and trace elements – mainly iron and zinc (5%). Propolis used within the hive may have beeswax added to it to be more pliable but can also consist of pure plant exudates in outer structures. Its thickness depends on the purpose of the structure under construction. In the case of the colony which survived the fire, the propolis wall (pro = before; polis = the city) built at right angles to the combs, did indeed protect the nest. It appears that the main function of the propolis barrier was the exclusion of rain and cold. Propolis has many uses in that it can be used to control ventilation, waterproof the interior of a nest, to control temperature and humidity within the nest, and to exclude various pests from entering and hiding within the nest. The prolific use of propolis by the African honeybee may also be as a result of attempts to deny hiding places within the hive to the small hive beetle (Aethina tumida) by sealing crevices. Natural nests are often located in cavities which afford many hiding places to the small hive beetle, thus lining the cavity with propolis effectively seals the nest off from its immediate surroundings (Tribe 2000). The extent to which propolis may be used to insulate a nest was illustrated in the complete enclosure of combs hanging from under a branch of a tree in Pretoria, allowing bees to forage from just a few small openings in the propolis sheath (Tribe & Fletcher 1977).
Cape Point Nature Reserve: Unlike the summer rainfall honeybee race (Apis mellifera scutellata) of southern Africa, the Cape bee nests are more often located within shrubbery at ground level. This does not preclude them from constructing nests in elevated places like those for A. m. scutellata. In fact, in suburbs of Cape Town, Cape bee nests have been located several meters high in exotic palm and pine trees. Data on Cape bee nesting sites recorded in Cape Point thus far indicate that about 90% of selected sites are located under or within rock crevices (Fig. 6).
Because honeybees will reoccupy any site previously inhabited by other honeybees, it is likely that many of these sites have been in use for centuries. What was amazing was that bees often issued in a steady stream from a relatively small hole in the soil at the base of a rock at some of these nests. How were these bees able to locate such hidden nesting sites which must occupy a substantial cavity size below the rock of say, about 42 litres – which is the capacity of a Langstroth hive? It is probable that such nesting sites were located by scouts in the past when they were more exposed, possibly as a result of a fire followed by winds and then heavy rainfall which revealed the cavity under the rock. With an average fire frequency of 15 years, the debris and plant growth during this time around the site could have closed off most of the cavity, the bees maintaining only the narrowed entrance.
Are nesting sites a limiting factor? Is the availability of nesting sites a limiting factor on the number of colonies able to reside in Cape Point? This is difficult to answer without knowing how many reproductive swarms are issued each year from the established swarms.
An individual colony may issue none or several reproductive swarms a year (Fig. 7) – largely determined by the capacity to expand within the nesting space (i.e. over-crowding), the strength of the colony (nectar and pollen reserves) and the vigour of the queen. Usually the old queen departs with flight-experienced workers, leaving behind several queen cells from which virgin queens will shortly emerge. If the colony is still over crowded, one or more additional swarms may leave with virgin queens – but this is more common among A. m. scutellata. However, at least one swarm at Cape Point was unable to find a secure nest and built their combs from interlacing branches within a fynbos thicket. Any approach to this nest elicits an immediate hostile reaction, presumably because of the odour of crushed vegetation underfoot. In the event of a fire, this colony would be incinerated.
Abscond? What remains to be seen is whether the three colonies which escaped the fire will remain where they are or will abscond. The Cape Point fire was extinguished and foraging still exists outside the burnt swathe, although the foragers will have further to fly. In the past similar wild fires would burn over a vast area, leaving little or no forage for many weeks. For example, a wild fire in the Cedarberg burnt for six days and covered 13 500ha (Jarman 1982) turning the entire area into a wasteland for bees with no forage. However, the resilience of the fynbos was revealed at Cape Point in the appearance of fire-asparagus (Asparagus lignosus) shortly after the fire which began flowering within weeks – to the benefit of the numerous bees visiting it. Also emerged in response to the fire were Haemanthus sanguineus and a smattering of plants such as Oxalis which were also visited by foragers.
Honeybee predators: Cape Point Nature Reserve no longer has honey badgers (Mellivora capensis) which possibly occurred there in the past, thereby eliminating one of the honeybees’ most destructive enemies. Had they been present, there would be the annihilation of those colonies accessible to them, followed by the later re-establishment by reproductive swarms from other areas within the park – thus creating an on-going dynamic. Although baboons also readily raid honeybee nests and are prevalent in the reserve, none of the 31 colonies has thus far been raided by baboons.
The Authors at work:
Jarman, M. 1982. A look at the littlest floral kingdom. Scientiae 23(3): 9-19.
Johannsmeier, M.F. (Ed.). 2001. Beekeeping in South Africa. Plant Protection Research Institute Handbook No 14, Agricultural Research Council of South Africa. 228pp.
Root, A.I. 1950. The ABC and XYZ of Bee Culture. The A.I. Root Company, Medina, Ohio, U.S.A. 703pp.
Tribe, G.D. 2000. A migrating swarm of small hive beetles (Aethina tumida Murray). South African Bee Journal 72(3): 121-122.
Tribe, G.D. & Fletcher, D.J.C. 1977. A propolized nest in the open. South African Bee Journal 49(4): 5-7.
Acknowledgment: The permission granted by SANParks to locate and analyse the nesting sites of honeybees in the Table Mountain National Park is gratefully acknowledged.