Author Archives: ujubee

Honeybees in Southern African Rock Art and their Role in Bushman (San) Mythology

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

Fig. 1. San shelter

Fig 1. Example of a Bushman (San) shelter on the mountain above the village of Aurora where the wall is covered in faded paintings of a wide variety of animals and people seen from a distance as red blotches.

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.

Fig. 2

Fig 2. A drawing of a section of the paintings at the Toghwana Dam site interpreted earlier as bees emanating from a bees’ nest but now interpreted by Siyakha MGuni as termite alates leaving a termite nest (reproduced from a drawing by Harald Pager depicted on the cover of the South African Bee Journal 46 (6) of 1974).

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.

‘Formlings’

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.  

Fig. 3

Fig 3. Alates leaving an underground termite nest through a hole in the ground with soldier and worker castes in attendance on the Gifberg above Vanrhynsdorp, Western Cape.

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. 

Fig. 4a

Fig 4 a. Soldiers and workers around a hole in the ground on top of the mountain below which is the town of Aurora, Western Cape from which the alates were to emerge later.

Fig. 4b

Fig. 4b. Workers and guards around a hole in the ground on the farm Zoethoek, north-east of Touwsrivier in the dry Karoo from which alates later emerged.

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). 

Fig. 5

Fig 5. Fungal fruiting bodies (mushrooms) from the fungus which grows on the grass collected by the termites and on which the termites feed, appearing on the surface of the termitarium in Mokala National Park near Kimberley.

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.

Fig. 6a

A functioning termite mound in winter near Drakensville in the foothills of the KwaZulu-Natal Drakensberg.

Fig. 6b

That of an abandoned termite mound showing signs of weathering.

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.

Fig. 6

Fig 6. A swarm of bees depicted emerging from a crevice in the rock face in Botha’s Shelter, Ndedema (now Didima) Gorge, Drakensberg.

[P.S. The photographs and drawings in this book are superb]

References

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.

 

 

Poisonous Honey called ‘Noors’

By Geoff Tribe

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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

Fig. 2. The characteristic yellow flowers of Euphorbia species.

Fig. 2. The characteristic yellow flowers of Euphorbia species, Euphorbia coerulescens.

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).

Cape honeybee visiting Euphorbia caput-medusae in the Cape Point section of Table Mountain National Park.

Cape honeybee visiting Euphorbia caput-medusae in the Cape Point section of Table Mountain National Park.

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).

Fig. 3. Black rhinoceros in Mokala National Park south west of Kimberley.

Fig. 3. Black rhinoceros in Mokala National Park south west of Kimberley.

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.

Fig 4. Euphorbia virosa north of Windhoek on which baboons had been feeding.

Fig 4a. Euphorbia virosa north of Windhoek on which baboons had been feeding.

Fig 4b. Euphorbia virosa north of Windhoek: the baboons feeding on the stems (the white stems at the base had been stripped) were disturbed.

Fig 4b. Euphorbia virosa north of Windhoek: the baboons feeding on the stems (the white stems at the base had been stripped) were disturbed.

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).

Fig. 5. Euphorbia dominated Valley Thicket vegetation in Addo Elephant Park.

Fig. 5. Euphorbia dominated Valley Thicket vegetation in Addo Elephant Park.

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 bees 117

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.

Sacred honey

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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.

The Author…

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Dr Geoff Tribe

References

Barraclough, D. 2005. One big fly … Africa Geographic 13(5): 22.

Burton, J. 2015. Curious traits of the higher primates, flower power, and raving honey. www.sonomapicnic.com/06/ravhoney.htm.

Hood, D. 2005. Euphoric euphorbias. Africa Geographic 13(5): 25.

Juritz, C.F. 1925. The Problem of Noors Honey. Agricultural Journal of the Union of South Africa 10(4): 334-337.

Krochmal, C. 1994. Poison Honeys. American Bee Journal 134(8): 549-510.

Maclennan, B. 2003. The wind makes dust: four centuries of travel in southern Africa. Tafelberg, 377pp.

Nienaber, G.S. and Raper, P.E. 1983. Hottentot (Khoekhoen) Place Names. Butterworth Publishers, Durban/Pretoria, 243pp.

Smith, A.B. 1985. More about toxic honey. The Digging Stick 2(2): 8.

Tribe, G.D. 2005. Noors: an antidote to parasites? Africa Geographic 13(9): 8.

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.

 

The Reliance on Propolis by the Cape Honeybee

By Geoff Tribe, Karin Sternberg and Jenny Cullinan

propolis

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.
IMG_3997 IMG_3944 IMG_2269 IMG_3187The 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).

Fig. 2. An almost completely closed entrance to a nest in the wall of a cliff except for several exit holes allowing one bee to pass at a time.

Fig. 1a. An almost completely closed entrance to a nest in the wall of a cliff except for several exit holes allowing one bee to pass at a time.

Fig. 2b. Propolis walls covering the entrance to a wild honey bee nest in an aardvark burrow.

Fig. 1b. Propolis walls covering the entrance to a wild honey bee nest in an aardvark burrow.

The nest within a cliff in the coastal fynbos was partially propolised with part of the combs still exposed. Screen Shot 2015-02-15 at 09.08.39The 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.

Fig. 2. Rebuilding the propolis wall after a fire had moved through.

Fig. 2. Rebuilding the propolis wall after a fire had moved through.

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).

Fig. 3. The large hive beetle (Hoplostomus fuligineus)

Fig. 3. The large hive beetle (Hoplostomus fuligineus)

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. Screen Shot 2015-05-25 at 18.39.01  IMG_1502  IMG_5649These 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. IMG_9690 - Version 2 IMG_4014 - Version 2Resins 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).

Medicinal uses

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.Screen Shot 2015-08-27 at 11.51.10

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.

Fig. 4. Small hive beetle

Fig. 4. Small hive beetle

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; Screen Shot 2015-08-27 at 12.22.28hygienic 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?

IMG_3908

Bees use propolis to form an antibiotic envelope around nests and to coat the surfaces of comb, imbuing the colony with the antimicrobial properties of resins.

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.

propolis wall on wild nestObservations 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:

References

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.

Strenuous conditions in the Succulent Karoo: honeybees nest in aardvark holes and an alternative pollination system exists for some flowering plants.

By Geoff Tribe & A. David Marais

162 close-up without flies - Version 2

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

Fig 1a. Entrance to the aardvark burrow on the plateau at Zoethoek.

Fig 1a. Entrance to the aardvark burrow on the plateau at Zoethoek.

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).

S glanduliflora AS098

Fig. 7c. Stapelia glanduliflora has vibratile white cilia which perhaps resemble fly maggots.

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.

Fig. 9. Hoodia gordonii in flower in the Tanqua Karoo.

Fig. 9. Hoodia gordonii in flower in the Tanqua Karoo.

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.

Fig. 10. Damage caused by a porcupine predating a Hoodia gordonii plant on Zoethoek.

Fig. 10. Damage caused by a porcupine predating a Hoodia gordonii plant on Zoethoek.

Fig. 11. The poisonous Euphorbia rhombifolia in flower, September 2013.

Fig. 11. The poisonous Euphorbia rhombifolia in flower, September 2013.

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.

Stapelia leendertziae from the Nelspruit district with accompanying flies.

Stapelia leendertziae from the Nelspruit district with accompanying flies.

Orbea variegata from the south-western Cape with fly pollinator.

Orbea variegata from the south-western Cape with fly pollinator.

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.

The authors:

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!

Dave in action.

Dave in action.

Dr Geoff Tribe is a Specialist Researcher – Entomology, Plant Protection Research Institute (retired), has done research on dung beetles, honeybees, forest entomology, slugs & isopods.

Geoff saving tortoises

Geoff saving tortoises.

References

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.

 

The Fates of the Solitary and Sub-Social Bees following a Fire at Cape Point

By Geoff Tribe, Karin Sternberg and Jenny Cullinan

IMG_9793

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.

IMG_1763These 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).

IMG_4924Several 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). IMG_1472In 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.

Fig. 5. Neddicky, Cistocola fulvicapilla.

Fig. 5. Neddicky, Cistocola fulvicapilla.

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.

References

Ginn, P.J., McIlleron, W.G. & Le S. Milstein, P. (Eds) 1990. The Complete Book of Southern African Birds. Struik Winchester, 760pp.

 

Cape Honeybees, Fynbos, and Fires

By Geoff Tribe, Karin Sternberg and Jenny Cullinan

IMG_0007 - Version 2

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.

20150418-031

Figure 1. Aerial view of the swathe of destruction the fire caused in the Cape Point section of Table Mountain National Park in March 2015 (courtesy of Dr Jonathan Ball).

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.

Figure 2. The aftermath: ash, sand and blackened skeletons of shrubs.

Figure 2. The aftermath: ash, sand and blackened skeletons of shrubs.

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).

Fig. 3a. Colony 1 whose nest under the boulder (the dark area at ground level in the centre) was protected by a propolis wall escaped destruction.

Fig. 3a. Colony 1 whose nest under the boulder (the dark area at ground level in the centre) was protected by a propolis wall escaped destruction.

Colony 1 prior to the fire.

Fig. 3c. Colony 1 prior to the fire protected from the elements by the growth of vegetation around it.

Fig. 3b. The nest of Colony 1 whose 14 combs had been protected from the fire by a propolis wall that covered the cavity.

Fig. 3b. The nest of Colony 1 whose 14 combs had been protected from the fire by a propolis wall that covered the cavity.

Fig. 3c. Colony 1 prior to the fire.

The nest of colony 1 prior to the fire.

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).

IMG_0046

Fig. 4a. Colony 2 is located to the right side of the foremost boulder below where the orange lichens start.

Colony 2 prior to the fire.

Colony 2 prior to the fire.

4b. Rocks around the entrance to the nest cracked from the heat of the fire.

4b. Rocks around the entrance to the nest cracked from the heat of the fire.

Fig. 4c. The almost deserted combs of Colony 2.

Fig. 4c. The almost deserted combs of Colony 2.

Fig. 4d. Foraging activity at Colony 2.

Fig. 4d. Foraging activity at Colony 2.

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).

Figure 5a. The entrance to Colony 3 lies under the boulder with a seemingly horizontal crack in it and to the right of the reddish, lichen covered rocks (situated bottom left in the picture).

Figure 5a. The entrance to Colony 3 lies under the boulder with a seemingly horizontal crack in it and to the right of the reddish, lichen covered rocks (situated bottom left corner in the picture).

Colony 3 prior to the fire.

Colony 3 prior to the fire.

Fig. 5b. Bees of Colony 3 clustered on some melted combs. Note the remains of the melted propolis that once encased the nest entrance.

Fig. 5b. Bees of Colony 3 clustered on some melted combs. Note the remains of the melted propolis that once encased the nest entrance.

Fig. 5c. Bees of Colony 3 clustered on some combs while the others are deserted.

Fig. 5c. Bees of Colony 3 clustered on some combs while the others are deserted.

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).

Figure 6. Colony in the cliff face at Cape Point Nature Reserve.

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.

Fig. 7. Swarm of Cape bees during the canola flow at Caledon

Fig. 7. Swarm of Cape bees during the canola flow at Caledon

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:

References

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.

 

 

Restio Species as a Source of Pollen in Autumn in the Fynbos

By Geoff Tribe

IMG_4061 - Version 2

The cavity dwelling Western Honeybee inhabiting temperate regions relies on its honey stores to tide it over the seasonal dearth periods which is a feature of its natural environment. The fact that they live in cavities allows ample stores to be accumulated for this purpose. It is this behaviour of hoarding surplus honey that is exploited by commercial beekeepers to their advantage by migrating hives from one honey-flow of exotic crops to the next. In the summer rainfall highland areas a typical seasonal cycle may start with the Highveld gums (a variety of Eucalyptus species) in spring, then on to sunflowers, soya beans, Eucalyptus grandis plantations, and finally to the Aloe greatheadii var. davyana honey-flow in winter. The seasonal dearth period for the Cape bee (Apis mellifera capensis) which inhabits the winter rainfall region of South Africa occurs during the summer months from January to March when few indigenous plants are in flower under a hot cloudless sky. Yet the honeybees survive, albeit in some areas with the help of exotic plants, the most valuable being several Australian Eucalyptus species.

075 Fig. 1

Fig. 1. A view of DanielsHoogte Private Reserve nestled on the top of Aurora Mountain 800m above sea level.

An exploration of the mountain (Fig. 1) above the West Coast town of Aurora in the first week of May 2015 revealed an abundant but unexpected source of pollen for Cape honeybees in the form of a Cape reed species belonging to the Restionaceae family. Fynbos vegetation is distinguished by its constant association with these tufted reeds which have been used to provide thatching material from the time of early European settlement. In the summer rainfall regions the Restionaceae are replaced with grasses. Restio species are usually dioecious with male spikelets drooping and female spikelets erect and are wind pollinated.

The fynbos covered Aurora Mountain is surrounded below in the Sandveld by potato and wheat fields and is contiguous with the Piketberg Mountain. The mountain fynbos here comprises of at least five species of Restionaceae and five Protea species of which Protea laurifolia (fig. 2) and Protea nitida (Fig. 3) were in flower.

046 Fig. 3

Figure 3. Many insects including honeybees visited the flowers of Protea nitida.

One species of Bruniaceae (Fig. 4) had just begun to flower as a result of the heavy coastal fog which envelops the mountain in the early morning (Fig. 5). However, around the farmhouses (32° 41’ 04’’S 18° 32’ 10’’E) were some ancient Eucalyptus globulus trees which were in flower. A commercial beekeeper had placed hives (Fig. 6) in groups of three at four localities within the fynbos vegetation. They were placed on recycled plastic containers filled with sand and strapped down to prevent the honey badger from accessing them – the mountain still inhabited by leopards, lynxes, mongooses, and various antelope including klipspringers and exotic fallow deer.

Figure 5. The morning coastal fog seen through the ‘vensterklip’ which can completely envelope the mountain.

Figure 5. The morning coastal fog seen through the ‘vensterklip’ which can completely envelope the mountain.

Figure 6. Beehive placed on top of a sand-filled container and strapped down to prevent access by the honey badger.

Figure 6. Beehive placed on top of a sand-filled container and strapped down to prevent access by the honey badger.

At this time of year the fynbos was drab and the prickly undergrowth showed very few natural resources on which the bees could forage. During the hikes around the outer rim of the mountain, no natural honeybee nests were discovered – not even in the 17 aardvark holes that were inspected. However, in several small secluded valleys there was a Restio species, Elegia tectorum, growing in thick clumps which reached to one’s elbows and which released clouds of pale yellow pollen as one pushed through it. It was here that the bees were encountered in large numbers collecting pollen (Fig. 7).Only pollen collectors were observed. No bees were visiting the female flowers (Fig. 8). It was observed that pollen was not available early in the morning, especially not until the mist had lifted, but became available only during the hotter part of the afternoon when the inflorescences were dry.

Figure 7. A honeybee collecting pollen from male Elegia tectorum flowers.

Figure 7. A honeybee collecting pollen from male Elegia tectorum flowers.

Figure 8. Female Elegia tectorum flowers not visited by honeybees.

Figure 8. Female Elegia tectorum flowers not visited by honeybees.

Elegia tectorum, or Cape thatching reed (as its name tectorum = ‘roofing’ implies), may grow to over 3m in height and occurs naturally in marshes and seeps on deep sand from Clanwilliam to Port Elizabeth. Male and female flowers occur on separate plants; the flowers are small and borne in compound branched inflorescences and flower in autumn (from March to April) which lasts for about four weeks. Large areas of several metres in diameter of either just male or female plants were observed on Aurora Mountain in close proximity to each other. Small black seeds are produced with smoke greatly increasing their germination rate.

Honeybees will be found in even the most desolate desert areas throughout southern Africa in which they find the means to survive. Within the mountain fynbos of the West Coast, restios appear to play an important, if unacknowledged, role in supplying pollen to honeybees at a time of year when such resources are in short supply. More than 400 species in about 40 genera of the Restionaceae family occur in the winter rainfall regions of South Africa and Australia, with outliers in Africa, Madagascar, Indo-China and Chile. There are about 168 restio species in South Africa which are confined mainly to the fynbos biome. They appear to play a far more important role in the ecology of the Cape honeybee than that of a wind pollinated species might warrant.

References

http://www.plantzafrica.com/plantefg/elegiatectorum.htm

127 (2)

A harvester termite nest found at Aurora.

The prehistoric looking 'koringkriek' or corn cricket, Hetrodes pupus, active on the mountain

The prehistoric looking ‘koringkriek’ or corn cricket, Hetrodes pupus, active on the mountain.

The presence of rock art in caves on the mountain indicates that it has been inhabited for many centuries

The presence of rock art in caves on the mountain indicates that it has been inhabited for many centuries.

 

Rock Art Paintings of Honeybee Combs in the Western Cape

By Geoff Tribe

068 fig 6b

Wild honeybee nests in southern Africa have been robbed for millennia by Bushmen (San) who were the original inhabitants of the sub-continent before the arrival of the Bantu tribes from the north and the European settlers from the south. Honey was possibly the only sweetness known to them which was obtained not only from honeybees but also from stingless Trigona bees. Bee brood was also a much relished source of food. Honeybee nests were marked in some way and individually or tribally owned and were robbed at the appropriate season when the combs were full of honey. Being nomadic, the San travelled vast distances following the availability of food according to the seasonal cycle.

There are many thousands of paintings on the walls of caves or rock overhangs in southern Africa which are thousands of years old, with some extending into the early colonial period. The San (Bushman) painters covered a wide variety of subject matter, the interpretation of some of them fill many scholarly books. Honeybees also played an important role in their mythology (e.g. Pager 1974; Lewis-Williams & Dowson 1989).

One painting that occurs in many parts of southern Africa and which was initially thought to depict a necklace was subsequently shown to represent combs of honeybees. Necklaces were worn by the San and were made out of small pieces of ostrich egg shells in which a hole was drilled and then strung together with a piece of string. However, a Zululand commercial beekeeper, Robin Guy, on visiting the preponderance of paintings in the Natal Drakensberg identified these ‘necklaces’ as depicting hanging honeybee combs within a honeybee nest.

Fig. 1

Fig. 1 The hanging combs of a nest of Apis mellifera scutellata hanging under the branch of a pine tree in a suburb of Pretoria.

There is no mistaking their resemblance to the combs of a wild honeybee nest (Fig. 1). This was further confirmed where at some of these sites, the catenary combs were accompanied by dots or bees with red bodies and white wings (Fig. 2a & b).

Frequently the artists made use of the varied surface relief of the walls of the cave to incorporate certain blemishes or imperfections into their paintings. Examples include the painting of an eland around an inclusion in the wall which is used to represent its eye, or a procession of antelope which appear to be emerging from a crack in the wall. The figure of a woman may be painted around a hole in the wall to represent a female’s abdomen or womb (Anderson). In this painting (Fig. 2a) it appears as if the bees are flying out of a crevice in the wall – very much as they would in the wild where many colonies make their nests within rock crevices. The large number of bees, especially concentrated at the lip of the crack and spreading outwards, indicates either an orientation flight or an absconding swarm. Botha’s Shelter contains 899 magnificent paintings including that of combs painted below the stomach of an eland and a bird associated with the bees which in the context could represent a honeyguide (Pager 1971).

Rock art depicting honeybees appears to be rather scarce along the western seaboard of southern Africa as compared with that of the eastern seaboard. And the West Coast paintings most often depict hanging combs which occur in such places as overhangs along the Oorlogskloof Hiking Trail (Fig. 3); on a farm in the Swartruggens Mountains overlooking the Tanqua Karoo (Figs 4 & 5); and in a cave in the Aurora Mountains above the town of that name (Fig. 6). Here again (Fig. 4) the artist has made use of the natural shape of the cave wall to incorporate the convex bump on which to paint the catenary combs. This gives a more realistic three dimensional effect of what a real nest would look like if viewed from below. Similarly, honeybee nests are often found hanging under projecting rocks, and the artist (Fig. 3) has made use of the small projection from the cave wall under which to paint the combs – simulating what occurs in nature.

Rock art depicting the robbing of bee nests occurs more frequently along the eastern seaboard of South Africa. For example, a painting in Eland Cave in the Drakensberg Mountains depicts a honey hunter with a bag on his back climbing a forked ladder to reach a honeybee nest around which bees are flying in agitation (Pager 1973). Similarly, three bees’ nests with ladders giving access to them may be seen in Anchor Shelter (Crane 1983). Near Bergville in KwaZulu-Natal, there is a ladder in close association with two bees’ nests depicted in a painting in Tugela Shelter (Crane 1983). In the Brandberg Mountains of Namibia a swarm of 376 bees are depicted in a painting. Yet the only depiction of a honey hunter in the Western Cape appears to be in a high overhang on a farm near De Hoek at the foot of the Swartbergpas 10km from the Cango Caves in the Oudtshoorn District. In this now faded painting, a man appears to be lowered from above with both hands gripping the rope above him and dots, presumably bees, all around his head. Attached to his body is what appears to be a flaming torch. In this ‘cave’, known as Buck krantz, because it also depicts antelope plummeting over the cliff, there are several honeybee nests in its walls even to this day. These nests are in holes in the wall which are entirely covered with propolis except for several tiny entrances through which the bees forage (Fig. 7).

Fig. 7

Fig. 7 Propolis covered entrances to honeybee nest in cavities in the wall of the Buck krantz rock overhang where a painting depicts the robbing of these same nests.

Also in the Klein Karoo is a painting of a swarm of bees amongst a group of dancing figures – the droning in the ears when in an altered state during a trance dance is recognised as the potent humming of bees (Rust & Van der Poll 2011). Here the bees are again depicted with red abdomens and white wings.

Why honeybees and robbing activity in rock art is more frequently encountered along the eastern seaboard could be because of a variety of reasons. Possibly the most important difference is that the eastern seaboard is much wetter and more rugged and thus honeybees are more prolific with many more and varied nesting sites available. In contrast, the fynbos and succulent Karoo of the western seaboard is far drier, with most honeybee nests located in outcrops of rocks or in the ground. At Buck krantz the depicted scene of the honey hunting can easily be visualized as occurring in the overhang – as with the antelope being chased over the cliff above the ‘cave’, but do single depictions of combs in the other caves, not always associated with other paintings, indicate a nest nearby and its ownership?

Selected references:

Anderson, G. (no date). Bushman Rock Art: South Africa. Art Publishers. 64pp.

Crane E. 1983. The Archaeology of Beekeeping. Duckworth, London. 360pp.

Crane, E. 2005. The rock art of honey hunters. Bee World 86(1): 11-13.

Guy, R.D. 1972. The honey hunters of southern Africa. Bee World 53(4): 159-166.

Lewis-Williams, D & Dowson, D. 1989. Images of power: understanding Bushman rock art. Johannesburg: Southern Book Publishers.

Pager, H. 1971. Ndedema. Akademische Druck- u. Verlagsanstalt, Graz/Austria. 375pp.

Pager, H. 1973. Rock paintings in southern Africa showing bees and honey hunting. Bee World 54(2):   61-68.

Pager, H. 1974. The magico-religious importance of bees and honey for the rock painters and Bushmen of southern Africa. South African Bee Journal 46(6): 6-9.

Rust, R. & Van der Poll, J. 2011. Water, Stone and Legend: Rock Art of the Klein Karoo. Struik. 128pp.

Tribe, G.D. 2000. A Bushman painting of a honey-hunter in an Oudtshoorn cave which still contains honeybee nests in its walls. South African Bee Journal 72(2): 84-87.

Woodhouse, B. 1984. When Animals were People: A-Z of Animals of Southern Africa as the Bushmen saw and thought of them and as the camera sees them today. Chris van Rensburg Publications. 120pp.

Dr Geoff Tribe

Dr Geoff Tribe

Why do honeybees react the way they do to smoke?

By Geoff Tribe (after a discussion on smoke with Jenny Cullinan and Karin Sternberg)

Fire at Cape Point Nature Reserve

The 11km fire at the Cape of Good Hope Nature Reserve, March 2015

While viewing the aftermath of the recent fire that cut a swath of devastation through Cape Point Nature Reserve before it was extinguished, we wondered whether any of the wild swarms we were monitoring there had survived the blaze.

after the fire 1 after the fire 2, The question then arose as to what benefit the innate behaviour of imbibing honey in the presence of smoke could be? How did it contribute to the survival of a swarm whose nesting site is enveloped in fire?

The adage that it is better to work honeybees with a smoker and without protective clothing than vice versa is easily confirmed in practice. The earliest record of the use of smoke to control honeybees is from a tomb painting in Egypt from c. 1450 BC where a kneeling beekeeper is removing combs from the back of a stack of horizontal hives, while smoke was used to drive the bees off these combs towards the flight entrance at the front (Crane, 1999). The use of smoke to subdue honeybees has obviously been known for millennia, because a hieroglyph of the honeybee was part of the titular of the King of Egypt from 3100 BC, the honeybee being of importance in Egypt long before this time. But why should the bees behave the way that they do in the presence of smoke unless it had evolutionary benefits? Various materials may be used in a smoker to subdue honeybees, each beekeeper vouching for the merits of the material that he uses in calming the bees. These may include burlap sacks, dry pine needles and dry herbivore dung – all of which have the same effect on the bees despite what material is used as fuel. Historical records show that dagga was used by the Khoesan (Quena) to smoke the bees but without any comment on any added effects that it may have had on them!

Smoke consists of many compounds, and since all fuels are equally successful in subduing honeybees on whatever continent, they are possibly reacting only to one or more of the chemical components of smoke. These components are as yet unknown, and neither are the receptor sites on the bee where this recognition is facilitated. Another suggestion is that the receptors of the honeybees are reacting to a certain size of smoke particle.

What is not disputed is that smoke causes honeybees to imbibe honey and with their distended abdomens they are less inclined to sting. Honeybees have first to grip the target before the sting can be brought into play by bending the abdomen, a distended abdomen making this procedure more difficult. Smoke also disrupts the chemical communication of the bees. Bees protect their valuable honey stores from mammals by a concentrated mass attack on the intruder after it has been marked by a guard bee whose stinging apparatus is ripped out and the alarm pheromone is released in quantity. Hence the practise by beekeepers of smoking the area that has been stung to smother the odour and to confuse the bees. The Western honeybee (Apis mellifera) inhabits temperate areas which are subject to regular fires which are part of their ecology. Savannah grasslands and fynbos need fire to survive as such.

Honeybees however are unable to escape fire by flight as witnessed by entire apiaries being burnt to cinders and all swarms perishing. Honeybees only react to smoke if it wafts into their hive, which gives them little warning of impending disaster. Observation hive studies have shown that honeybees which abscond do so after consensus has been reached within the hive – which takes many days. By overcrowding an observation hive with bees it is possible to force the swarm to abscond. As the bees prepare to abscond, perhaps six dances indicating six potential nesting sites may occur initially. Over a few days this number is narrowed down to one dance and consensus has been reached. The swarm leaves the hive after the number of vibratory dances (an inhibitory dance where one worker places its head on another and shakes it by a dorso-ventral abdominal movement) (Fletcher, 1978) per unit time reaches zero. exposed nestThere would not be time to organise a mass evacuation of the hive in the event of a fire. In any case, smoke would disrupt all chemical signals involved in coordinating swarming and absconding. Exposed wild colonies would perish , the selection of secure nesting sites in fire-prone vegetation thus having primary survival value.

Nest under a rock

A wild nest deep under a rock

Laying queens would be unable to leave with a swarm escaping a fire because she would be too heavy to fly and, like the workers, would not be inclined to desert her brood. A swarm preparing to swarm or abscond first starves their queen and prevents her from laying eggs by not preparing cells for her in which to lay eggs. Absconding occurs soon after most young bees have emerged from their cells and the stores have been consumed – except that which is needed to establish the swarm at the new nesting site and is carried in the bees’ stomachs. This preparation again takes several days. Absconding usually takes place when conditions are adverse and there is an ‘awareness’ of this throughout the hive due to the ‘feedback’ mechanism in operation within the hive, where for example, the lack of incoming food causes a reduction or cessation in egg-laying.

Honeybees are therefore unable to escape by absconding in the face of the fire and exposed colonies would perish. The innate behaviour of honeybees to smoke must thus have become entrenched in those swarms which did survive the fire. The bees are therefore not trying to escape the fire by fleeing – so what is the value of imbibing honey? The value appears to be in the survival of those swarms which escaped the initial fire.

Natural fires in southern Africa in days of yore would burn over a vast area. For example, the fire that started in Riviersonderend in February 1869 that was driven by a hot Berg wind burnt the indigenous forest all the way from Swellendam to Humansdorp, driving elephants and other game into the sea for refuge. Swarms surviving such fires would emerge to find a ‘lunar’ landscape devoid of plants to sustain them and thus would be forced to abscond. Smoke causes bees to imbibe honey and retreat to the far recesses of the nest cavity. Bees will imbibe any honey flowing from melted combs and so function as living storage units. Under such conditions, to sting and die would cause the loss of this crucial honey store. Hence also a reason why they are then less inclined to sting. It appears that the innate behaviour of honeybees to imbibe honey in the presence of smoke has survival value in that it allows the eventual escape by migrating from a devastated landscape after the fire has passed. The honey stored in the bodies of the bees would allow the bees to survive the initial calamity and then to organise a migration out of the area and rebuild comb in the new nest site. This behaviour has become innate, which presupposes that the Western honeybees (and Apis species in general) have been subjected to fire for many millennia and have evolved to survive it.

The Heuningberg

The Heuningberg in the foreground dwarfed by the Groot Winterhoekberge behind them

A natural indication of the value in imbibing honey was recorded by O.F. Mentzel in 1787 at the Heuningberg (Fig. 4) where honey was bartered with the Khoesan. The translation records: “A few miles towards the east lie the Honig Bergen. These derive their peculiar name from the bees which find abundant nourishment in the many wild flowers and store their harvest in the crevices of the rocks. The Hottentots clamber up these mountains…to look for honey which they discover the sooner because the sun often makes it fluid, so that it runs onto the rocks, is again collected by the bees and carried back but in this way the storerooms are soon discovered”(Tribe, 1996). Temperatures in summer in this region exceed 40°C and the rock faces are blisteringly hot. Here the bees’ reaction is to heat and the melting of the comb but in the absence of smoke.

Do other organisms have innate reactions to fire? There appears to be none with the same innate response as that of honeybees. Various predatory birds are attracted to fire to capture escaping insects and rodents, but smoke is just a learned signal indicating a meal.

Anyone who has tried to remove a nest of the alien European wasp (Vespula germanica) which has invaded the fynbos and which forms massive multi-queen colonies because the African climate is so conducive to them, will rue the fact that they do not respond to smoke as do honeybees. The mass attack by these wasps soon results in the veil becoming completely covered in wasps with stingers extended and the odour from their stings becoming overpowering. With no response to smoke such as retreating from it, presumably because they nest in the soil and are not unduly affected by fires, they have no comparable reaction to that of honeybees. Even so, there is no honey stored in the wasps’ nests, their brood being fed progressively with regurgitated protein from soft bodied insects killed by their foragers.

The innate behaviour of honeybees to smoke has allowed people to effectively control them, making modern beekeeping including the movement of hives to pollinate crops possible.

survival

Crane, E. 1999. Recent research on the world history of beekeeping. Bee World 80 (4): 174-186.

Fletcher, D.J.C. 1978. Vibration of queen cells by worker honeybees and its relation to the issue of swarms with virgin queens. Journal of Apicultural Research 17(1): 14-26.

Tribe, G.D. 1996. Heuningberg: past and present. South African Bee Journal 68(2): 39-47.

Images by Geoff Tribe, Jenny Cullinan and Karin Sternberg

 

Leafcutter Bees of the Tribe MEGACHILINI

By Geoff Tribe (Images by Jenny Cullinan and Karin Sternberg)

leafcutter bee 8

Megachile frontalis (Identified by Dr Connal Eardley, National Collection of Insects, Pretoria)

This large and abundant tribe known generally as leafcutter bees, even though nests may be lined with various materials besides leaves, is found in every continent where the majority of the species belonging to this tribe are solitary. Unlike other solitary or sub-social bee groups, secreted cell linings are absent. Material for cell walls and linings is instead brought in from outside and, depending on the species, includes pieces of leaves, chewed leaf material, resin, mud, or pebbles.

The distinguishing feature of the family Megachilidae is that the females of non-parasitic species carry pollen by means of a scopa on the venter of the abdomen instead of on the hind legs. The following genera are included in the Megachilini: Chalicodoma, Chelostoma, Heriades, Hoplitis, Megachile and Osmia.

Leafcutter bees in southern Africa are stoutly built, brown or black bees up to the size of a honeybee, hairy and with a conspicuous yellow tuft of hairs on the underside of the abdomen where the pollen grains are collected on this special apparatus. The female leafcutter bee seeks out a tube or tunnel that is of the correct dimensions which is dry and sheltered. Such cavities include hollow stems, holes in a wall, deserted cavities constructed by wood-boring beetles and even man-made holes in buildings.

leafcutter bee 4 leafcutter bee 5

The female Megachile venusta cuts a fairly thin oval piece of leaf from a smooth-leaved plant and carries it between her forelegs to the selected nesting site. The leaf segment is pressed into position with her head at the base of the tube. This process is repeated until both the base and walls are lined with overlapping leaf segments. The first small cup about 10mm deep is then filled to three-quarters with a yellow paste of pollen and honey. On this she lays a single egg before sealing the cup with leaf segments and then repeats the process with one cell on top of the other until the tube is filled with such cup cells containing brood. Finally the entrance is stuffed with assorted pieces of leaf of different shapes and sizes before being sealed with a plug of chewed leaf cemented with saliva. There appears to be just one generation per year.

The fully grown larva spins a cocoon which lines the inside of the cell and after excreting, coats the inside with the excrement which dries to form a water-proof varnish. Here it remains for several months until the following season, after which it pupates and emerges two or three weeks later.

A number of the Megachilidae have become ‘cuckoo’ bees where they lay their eggs in the nests of related bees, their larvae feeding on the honey and pollen paste stored by the host which results in the starvation of the host larva.

The related tribe of Anthidiini is much smaller and less abundant than the Megachilini and use the same materials as above for lining their nests except for mud. Genera include: Anthidium, Trachusa, and those with Anthidium as the root. The communal carder bees (Immanthidium) are included here. As their name implies, various cottony fibres which they strip from hairy plants are used to construct the nest. One such carder bee nest made out of a cottony material and the size of a fist was discovered in the hills above Pietermaritzburg in 1972 built within a huge discarded concrete water pipe. Here it was protected from rainfall and the entrance hole to this mass of ‘cotton’ was streaked with yellow pollen. Inside were several individual cells provisioned with a honey and pollen paste.

References:

Michener, C.D. 1974. The Social Behavior of the Bees. Belknap Press, Massachusetts, 404pp.

Skaife, S.H. 1979. African Insect Life. Struik, Cape Town, 279pp

leafcutter bee 2 leafcutter bee 6 leafcutter bee 7 leafcutter bee 1

 The Author…

Geoff Tribe

Geoff Tribe

Getting the shots…

at the beach

Jenny Cullinan

bee paradise

Karin Sternberg