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Swarming Bees and Pseudoscorpions

By Karin Sternberg and Jenny Cullinan

The chelifer found in South Africa is mostly Ellingsenius fulleri and is believed to be a predator of small mites, wax moth larvae and other arthropods found in the nest debris. They often cling onto the legs of bees and are believed to be spread in this way to other colonies (Geoff Tribe).

When bees swarm, thousands of bees pour out of a nest only to collect a short distance away in a cluster, often on a branch, but otherwise on any other structure. In September 2017 we were watching bees on the move, temporarily clustered under a concrete table, with scout bees heading out to look for possible new nesting sites and, on their return, performing dances on the surface of the cluster (on other bees) as to the location of the nesting sites found. We watched and waited over a couple of days as slowly the number of possibilities and therefore dances diminished, as the colony came closer to a consensus as to the location of their new nesting site. On the third day of watching this intriguing behaviour and to our utter amazement, we noticed that we were not alone in our waiting.

Pseudoscorpions emerging

From the edge of the first layer of bees in direct contact with the table, we spotted a number of pseudoscorpions emerging. They appeared to be restless and hungry as they moved out and away from the hanging colony, using their pincers which had fine and relatively long hairs to sensitively feel for food in the cracks and gaps of the table undersurface.

They did not get very far as certain (dedicated?) bees seemed concerned and actively encouraged them back. There was a very clear communication between these two species and they were continually touching each other; the pseudoscorpions using their pincers either in a waving motion or by clasping at the bee, and the bees using their antennae and legs to touch and usher the pseudoscorpions back into the cluster.

From all of the fussing, one could tell that the pseudoscorpions were crucial to the bees. With colony activity and communication between the bees increasing as the colony prepared to leave for their final nesting site, the bees kept a close eye on their fellow-travellers. As more and more surface bees stopped dancing and started almost buzz-running and whirling like dervishes on the surface before pushing their way into the middle of the colony as paths clearly opened up for them, the vibrations and sounds of the bees increased and activity peaked. No doubt this was also a cue completely understood by the pseudoscorpions. For when the colony finally departed for their new nesting site, remarkably not a single pseudoscorpion was left behind. 

Holes opening in the cluster

 

These observations showed us an extraordinary interdependence between bees and pseudoscorpions, and highlighted how vital each are to the other that these wild bees on the move should take the pseudoscorpions along with them. The pseudoscorpions are absolutely necessary to the health and well-being of a colony and are very much part of the bees’ hygiene. We would be very interested to hear if this has ever been documented before?

A pseudoscorpion attaching itself to the leg of a bee

Swarming bees departing for their new nesting site

(All photos are copyrighted and are thus the property of the authors. If you wish to use any, please contact us at ujubeeconservation@gmail.com)

The authors at work:

Honeybees and The Great Fire of 1869 extending from Swellendam to Uitenhage

By Geoff Tribe

The devastating fires of 7 June 2017 extending over a distance of 125 kilometres from George to beyond Plettenberg Bay resulted in the loss of life of seven people, thousands of animals, and of much property.  On 6 June the speed of the hot Berg wind blowing from the north-west was recorded between 90km/h and 100km/h with gusts exceeding 110km/h which were responsible for fanning the fire which can superheat it in excess of 2000°C (Preston 2017). The first fire was reported near Knysna following in the wake of a fierce hot wind with over 50 fires following this and resulting in more than 10 000ha reduced to ash.  It will take many years for this region to recover, a region which relies heavily on tourism of its scenic attractions. But this is not the first time this region has experienced a devastating fire, and then over a much larger area. As we know from back then, the wild bees will survive after a fire, even if they are forced to abscond.

The Great Fire of 1869

Between the years 1862-1869 large parts of South Africa were experiencing a severe drought in which hundreds of thousands of sheep and other stock died (Du Preez). In early February 1869, following several weeks of exceptionally hot weather, a fierce hot bergwind blowing from the north fanned bushfires which had started all over the area from Swellendam in the west to Uitenhage in the east. The fires swept through the mountains, gorges and lower coastal plateau, one branch swept down a gorge and raced through the hills towards Knysna but by a miracle the wind changed and the town was saved from certain destruction (Van der Merwe 1998). During this fire 27 people died in the Humansdorp district alone and many elegant homes were razed to the ground while their occupants took refuge in dams and rivers, covering themselves with blankets against the falling cinders.

The belt of dense forests along the upper coastal plateau was hardly touched by the Great Fire, for fire seldom penetrates deep into moist forest (Van der Merwe 1998). Dry coastal forest, wooded valleys and isolated mountain forests were however totally destroyed.

  The Eastern Province Herald reported this disaster of unimaginable proportions:

In February 1869 the Herald reported that: “A correspondent in Knysna mentioned that the sun had just risen … when we had the sense that something unusual was going to happen. Between 9 and 10 o’clock a strange wind, unknown in these parts, started blowing. It was such a hot wind that a person could hardly go outdoors. A few hours later it appeared that our feeling had come true, because between 12 and 1 o’clock Plettenberg Bay was covered in thick smoke, soon we could see a tremendous fire; it looked as if the whole of Plettenberg Bay stood in ligte laaie [basically, as smoky as anything].

“The fire came from all sides so that in a moment Wittedrif, Ramdorings River and the whole area was one huge inferno, At Wittedrif the houses were fortunately saved but everything else was burnt. It was the same story everywhere, and people were only too relieved to have escaped with their lives. It was moving to hear the weeping and wailing of the women and to see the great confusion which reigned. The valleys, forests and caves were covered in such thick smoke that one didn’t know where to flee. Particularly pathetic was the sight of pigs, dogs, geese and chickens and even doves which had died in the flames. The intense heat forced birds to tumble out of the sky like leaves of a tree. Sheep died by the hundred as did buck in great numbers.

Some people who fled towards the sea were rescued by the wind changing direction. Jan Groenewald ran to the river with his wife and children where their lives were saved by sitting in a boat. The next day the whole world wore a huge black cloak. It was painful to see how earthly possessions were destroyed in just one day. It was fortunate that the fire did not break out at night because then it would almost certainly have occasioned loss of human life. For this reason many of cried out as did Job, ‘The lord giveth and the Lord hath taken away. Blessed be the name of the Lord’. Knysna was in great peril, at one stage all the forests around the town were burning fiercely. Then, suddenly, the wind changed and the town was saved”.

The huge loss of life and the destruction of property and the aftermath of the fire is vividly portrayed in other newspaper reports at that time where the fire was reported to have originated at Bedford where a farmer named Dixic was injudiciously burning rank grass during a high wind, which carried the flames along with fearful rapidity (see Papers Past).

Outeniqualand before the Great Fire

When the 1869 Great Fire swept through Outeniqualand there were no pine and eucalyptus plantations and no ploughed land except around certain homesteads, the forests being surrounded by great swathes of fynbos vegetation. The density of the forest and the many deep gorges across the coastal plateau with the rockbound sea coast caused early travellers in the area to instead use a more inland course through Pampoenkraal (Saarsveld) and into the Langkloof. Elephant trails were initially used to penetrate the forest but the Great Fire served to facilitate greater access to the region because it cleared the way for the completion of the coastal road system which created the Garden Route.

An indigenous forest

Historical records recount hundreds of elephants and buffalo which grazed on the grass in the coastal valleys and used the forest as shelter (Skead 2011; Van der Merwe 1998). Local memory recounts that elephants sought refuge in the sea during the fire, yet this could not be substantiated from records. The large animals were decimated over two centuries of hunting and farm expansion, with the last buffalo shot in 1883 (Van der Merwe 1998). No information appears regarding the presence or nesting localities of bats, of which the Egyptian fruit-bat is essential for the regeneration of forests by eating only fleshy fruit such as that of yellowwood where the fleshy part is removed and the pip is dropped, thus dispersing the seed.

South Africa is poorly endowed with natural forests with only 0.3% of the land afforested. These forests represent a relic of large coastal forests which dominated the Cape about five-million years ago under a tropical climate. The Mediterranean climate became established and has persisted for the last two million years when the tropical forests slowly gave way to sub-tropical thicket, grasslands and fynbos species (Newton 2009). Fires driven by hot, desiccating winds are the major agents that keep forests in check; forests shelter on the lee side of steep ridges or in narrow gorges where eddies branching from the main wind prevent the fires from burning down the lee slopes (Van der Merwe 1998). Such eddies do not develop on the gradual slopes of rounded hills which are consequently covered with fire-adapted fynbos. Dr John Phillips maintained that the extensive areas of Kuistervaring or Ystervaring (Gleichenia polypodioides) found in the Deepwalls forests are to be attributed to honey-hunters [burning out nests] and also to incendiaries aiming at burning portions that they might report the damage done, and thereafter buy the burned trees at a tariff less than normal (Skead 2011). The biomass of these Kuistervarings within the Pinus plantations, where they form a dense mat several meters deep, requires that each tree needs to be excavated to its base before it can be felled.

Preston (2017) explains the phenomenon of the ‘thermal wave’ as a sine wave flow of super-heated air associated with fires such as these. As heat from the fire rises it is blown horizontally by the wind over distances of 300m to 1000m before it touches down and ignites a new fire and then again bounces off downwind. As the superheated air descends, it heats everything before it which then erupts into flame spontaneously before any flame reaches the area. The immense pressure and heat of the descending air forces down the roof of a house and melts the glass and disintegrates the bricks, leaving a pile of rubble. Because the wave is able to jump over valleys and rivers, the effect appears random as single houses explode into flames while others remain unscathed.

The forests were under constant attack long before the early explorers arrived there with fire having played a major role in reducing their area, resulting in patches of isolated forest surrounded by grasslands or dense fynbos (Skead 2011). Dias, Da Gama and others have recorded that in the fifteenth century great smoke banks were seen from their vessels, the sun appearing as if veiled in a grey cloud; undoubtedly the Outeniquas were to some extent responsible for the first burning of some of the larger ‘eilands’ now existing – a work in which they were later assisted by elephant, buffalo and honey hunters (Skead 2011).

Origin of the name Outeniqua

The earliest records show that this region was inhabited by the semi-nomadic Outeniqua clan. According to Raper (2004), Outeniqua means ‘men who carry honey’ from ‘tou, t’hou, ou, recorded in 1752 for ‘honey’; teni, ‘carry’; qua, ‘men’. Tsitsikamma means ‘waters begin’ from tsoa-tsoa, ‘begin’, kamma, ‘water’ due to the high rainfall and the occurrence of many rivers and streams. The name Knysna is of Khoi origin and probably means ‘ferns’ or ‘fern leaves’. There are a number of other Quena names of places associated with honeybees which have survived (Tribe 1982; 1997).

However, Hromnik (2009) in a series of articles in the George Herald further elucidates on the origin of the name Outeniqua. In 1766 Jan Willem Cloppenburg recorded that “… the name Houteniquas, means houtini – to carry a bag, quas – men or people; because the people that live there carry in bags honey from the forests”. François le Vaillant in 1780-85 reported that the name “Auteniquoi” meant ‘men loaded with honey’ and confirmed that the local forests were full of honeybees. Hromnik’s interpretation is that the word Outeniqua consists of three component words: Ou-teni-qua (i.e., ‘/Hao-teni-qua’) meaning ’People Living United or in Harmony with Honeybees’. These Honeybee People, the Outeniquas, associated themselves with the honeybee as a symbolism of Mother Earth as found in other civilizations from India to Egypt.

Importation of English honeybees

The early settlers in Outeniqualand regarded the indigenous Cape bee as ‘… indolent, [and] thus good, muscular, wise and hardworking bees were sent for from England” (Du Preez). Replacing the indigenous honeybees of Southern Africa with docile European races (mainly the Italian bee) had been advocated and attempted from 1925 to 1942 as a government program which was finally abandoned only in 1965. This bee breeding station with Italian bees (Apis mellifera ligustica) was situated just below the Union Buildings in Pretoria. However in the 1970s on the removal of wild nests in Pretoria and the taking of cell measurements, no influence of these Italian bees could be discerned in the wild suburban population.  The presence of their genes in a milieu of Apis mellifera scutellata swarms was completely smothered. The rationale behind this was to breed a less aggressive and more productive race of bees. Yet all these attempts failed to establish European honeybee races in South Africa because they were outcompeted by the indigenous bees. It is now accepted that the indigenous races are adapted to the conditions of Africa. For example, the smaller size of the African bee which is linked to a shorter development period from egg to adult is an adaptation to meagre and erratic rainfall (resulting in short and erratic nectar flows) which may be taken advantage of by the local race having a faster developmental period in synchrony with the flow.

Henry Barrington of Knysna is first documented as importing bees, the Black English bee (Apis mellifera mellifera), in 1871 to his farm Portland.  This was not a success because “The English bees imported at the Knysna with Nutt’s hives, at great expense, finding the climate so genial – no winter, the flowers all the year round – refused to make honey, preferring a life of enjoyment to work” (Du Preez). It was probably more a case of insufficient forage needed for a much larger bee than laziness of behalf of the bees! This also indicates that he must have hived and kept the Cape bee as well. Presumably his bees also died in the inferno of the Great Fire which consumed his house and farm which he described as ‘complete’. Barrington imported two more hives of bees from London in March 1869 after the fire and continued multiplying his black bees until his death in 1882 (Du Preez). Because of the difficulty in transporting hives of bees by ship from England to Cape Town (a journey of at least 64 days) and on to Mossel Bay, then by cart to George and finally carried the 50 kilometres to Portland through dense undergrowth by two men (Du Preez), meant that only a limited number of hives must have been imported during this period.

Disappearance of forest ecotype of the Cape bee?

Thunberg in November 1772 passed through the Southern Cape and recorded that it was rich in honeybees and honey. In much later years, the presence of numerous wild honeybee colonies and their potential for commercial beekeeping was used in a prospectus to lure British settlers to the Outeniqua region. Yet today this region is not renowned as an exceptional area for honeybees even despite the many exotic eucalypts grown there. An intriguing theory for this discrepancy was recounted to me by Hennie Steyl, a forester and beekeeper from George. He suggests that after the Great Fire that the locally adapted ecotype of the indigenous Cape bee (Apis mellifera capensis) within the forest was destroyed and later replaced by the ecotype from the surrounding fynbos which moved into the area as the forest slowly regrew. Hence the noticeable incompatibility of the honeybees seen today within this region.

People living in harmony with Honeybees

The 2017 fire destroyed many hives of honeybees which will be replaced mainly by the time honoured South African way of placing out trap boxes for migrating swarms. Should these swarms originate mainly from the fynbos on the periphery of the forest, will this reinforce this incompatibility? More so, over time will the bee finally adapt to the forest biome even though today it is largely disjointed and does no longer cover the same area when the Outeniqua people collected honey to trade in times gone bye.

 

The intricacies of a forest system:

The author at work:

Geoff Tribe

References

Du Preez, F.M. (no date) A History of Beekeeping in South Africa. Office 444 Govan Mbeki Avenue, Port Elizabeth. pp201.

Hromník, C.A. (1997) Quena and the Kung: aka the Hottentots and Bushmen. Cape Times 29 September, pp8.

Hromník, C. A. (1999) The ethnonym Quena: The true name of the Hottentots. In: Actas del XX Congreso Internacional de Ciencias Onomásticas, Ed: Ana Isabel Boullón A Coruna, Galicia: Biblioteca Filolóxicca Galega, 202, pp1463-1480.

Hromník, C.A. (2007) Free the Ottentotu from the ideologues. Sunday Times 15 April 2007.

Hromnik, C.A. (2009) Outeniqua Quena & Mountains in the realm of Dik!areb. George Herald 18 June pp37; 23 July pp24; 27 August pp52; 24 September pp48; 29 October pp43; 28 January pp28; 4 February pp30.

Newton, I (2009) The future of Fynbos. Full Circle 6(11): 70.

Papers Past (internet) The Great Fire at the Cape of Good Hope. – Loss of Life and Destruction of Properties. Daily Southern Cross, Vol. XXV, Issue 3718, 18 June 1869.

Preston, G. (2017) Knysna Fires: Five factors that produced the perfect inferno.

Raper, P.E. (2004) New Dictionary of South African Place Names. Jonathan Ball Publishers, Johannesburg & Cape Town. 421pages.

Skead, C.J. (2011) Historical Incidence of the larger Land Mammals in the broader Western and Northern Cape. (second edition). Centre for African Conservation Ecology, Nelson Mandela Metropolitan University, Port Elizabeth, South Africa. 519pages.

Tribe, G.D. (1982) Bees of the Outeniqua in 1781. South African Bee Journal 54(4): 91.

Tribe, G.D. (1997) Hottentot (Khoekhoen) place names associated with honeybees in southern Africa. South African Bee Journal 69(1): 3-6.

Van der Merwe, I. (1998) The Knysna and Tsitsikamma forests. Chief Directorate: Forestry, Department of Water Affairs and Forestry. 152 pages

Pollination by deception

By Jenny Cullinan and Karin Sternberg

Disperis capensis (Cape witch orchid) which has no nectar or other reward for bees, uses deception to attract the male carpenter bee to its flowers for pollination.

Mild winter days of late July, bring the first flowerings of Disperis capensis. The witch orchid times its display in this section of Cape Point Nature Reserve with the similarly coloured Muraltia (purplegorse). Overcast days make the purple of both Muraltia and the orchid stand out in an otherwise flower-barren patch. The orchid has a gentle, but beautiful sweet scent, reminiscent of both a component of Serruria villosa’s fragrance as well as Wurmbea hiemalis. Muraltia has little to no fragrance perceivable to the human nose.

Xylocopa rufitarsis visits Muraltia for nectar and sometimes mistakenly visits the delicately-scented orchid. Realising that there is no nectar to be had, he immediately flies off, the sticky viscidium adhering to the visiting bee and a pollinarium is withdrawn; it becomes immediately coiled so that the pollen massulae (individual pollen grains) become outwardly orientated so as to be correctly positioned to break off onto the stigmatic surface of the next Disperis visited by the bee. These are visible as individual grains on the sticky orchid stigma (Bill Liltved). The carpenter bee seems quite irritated with the pollinaria stuck under his thorax, but continues collecting nectar from Muraltia in a methodical way, only to make the same mistake with another orchid depositing the pollen in this way. 

Once D. capensis is fertilised it fades from its purple-pinks to a burnt orange and her bonnet folds in on itself.

It was previously thought that Disperis capensis only mimicked the nectar-secreting shrublet Polygala bracteolata, (Johnson 1994; Pauw & Johnson 1999), but these observations show how fascinating the unknown is and how much there still is to discover.

In a completely different biome in Cape Point Nature Reserve, we have found pockets of D. capensis resembling none of the other flowers surrounding them, neither in colour, shape nor fragrance. The only flowers in close proximity are Metalasia compacta, Diastella divaricata and Lobelias. However, the orchids in this location still have to be visited by a bee.

Disperis capensis and Muraltia. Both displaying similar colour combinations.

X. rufitarsis, realising that there is no nectar to be had, quickly flies off from the orchid carrying the pollinaria under his thorax

The pollen grains are outwardly orientated as he flies from flower to flower sipping nectar

An unpollinated orchid

A pollinated orchid

After fertilisation the orchid’s bonnet folds in on itself and turns a burnt orange

As a small exercise to show how a pollinarium is released, we mimicked a bee’s arrival by touching the sticky viscidium with a sterile tool, as a carpenter bee would make contact with the orchid with its thorax, and slowly withdrew the spring-loaded pollinarium from the anther sac while photographing it. Once released it immediately coiled.

We then took the pollinarium to a separate orchid, touching it on the sticky stigmatic surface as the carpenter bee would come into contact with it. Immediately the pollen grains broke off from the caudicle, the stalk to which the pollen masses are attached, leaving individual grains of pollen on the stigma.

Further reading:

The Cape Orchids (Liltved & Johnson 2012)

 

The authors at work:

When smoke gets in your eyes!

The perception that honeybees can escape an approaching wild fire by absconding in advance of the fire is so well entrenched that no thought appears to have been given to see that it is an utter fallacy. Entire apiaries in the Western Cape have been utterly consumed by fire on a fairly regular basis over the years with not a single swarm issuing from them as the fire bears down on the apiary.

The reason for such thinking is as a result of the well-known behaviour of bees to imbibe honey when a reproductive swarm departs the hive or the colony absconds. This honey stored in the bodies of workers tides the bees over the period in which they found a new colony by creating combs in which to rear brood.  Thus the reasoning that follows is that in responding to smoke by imbibing honey the honeybees are preparing to abscond.

However, a gravid queen is too heavy to fly and honeybees rarely abscond if brood is present. Thus for a swarm to issue from a hive takes preparation in advance – which is impossible with the sudden arrival of a fire. Pheromones are crucial in co-ordinating such a swarm and smoke disrupts and smothers such chemical communication – which in the case of a beekeeper using a smoker, disrupts the alarm pheromone which targets concentrated attack on the perpetrator who is disrupting the hive.

Reaction of wild colonies of honeybees to fire

Such questions regarding the behaviour of honeybees to fire were raised after the devastating wild fire in the Cape Point section of Table Mountain National Park on 4 March 2015 which incinerated 988 ha of fynbos before it was brought under control. How many of the wild honeybee swarms in this burnt area had survived the fire? We realized then that the swiftness of the fire alone would have ensured that no colony could have escaped in advance of the fire. The question then arose as to why the bees always respond to fire by imbibing honey when there is no intention to abscond? An analysis of the 17 nests within the fire zone supplied an explanation.

The fynbos vegetation is adapted to fire which is essential for its maintenance and which occurs at intervals of 15 to 25 years. Analysis of the wild honeybee nests throughout Cape Point revealed that 78% were located under rock outcrops, within clefts in rocks or in cliff faces; 11% were directly in the ground; 8% in cavities in trees and 3%within the intertwined branches of bushes. Of these nests, 68% had their openings entirely enclosed in propolis with small openings within this propolis wall serving as entrances to the nest.

Honeybee colonies within the burnt area

Within the burnt area were 17 wild nests of which 13 were situated under the bases of boulders and 4 in clefts within boulders. Propolis walls enclosed all these nests, of which two walls and adjacent combs had been totally destroyed by the fire and two walls partially destroyed. However, all these colonies survived the fire. The response of the bees to fire was to imbibe honey and retreat to the deepest recess of the cavity.

Fynbos fires are not exceptionally intense but flames tend to be high (2 to 5m) and of short duration where temperatures may reach 550 °C for only 10 seconds. Experimental fires in the fynbos spread at a rate of 0.04 t0 0.89msˉ¹. Once the fire has passed, the landscape is filled with powdery grey sand and the blackened skeletons of the larger shrubs. It is this devastation of their environment which the bees encounter after the fire has passed where neither nectar nor pollen is available to them. This is when the imbibed honey is essential to tide them over this dearth period which is about 2 to 3 weeks long before the fire-loving ephemerals sprout from underground bulbs or rhizomes and flower in profusion, having been relieved of competition from other plants. However, the surviving swarms were considerably weakened because of the suspension of foraging which was possibly followed by the eating of existing eggs and larvae which could not be reared further due to such a lack of food.

Firmly established, innate behaviour

The response of honeybees to smoke by imbibing honey which tends to make them less inclined to sting, coupled with the masking of their alarm pheromone is a godsend to beekeepers in their manipulation of hives in extensive apiaries. This behaviour is innate and firmly established. That all honeybees of the genus Apis respond in a similar way by imbibing honey in the presence of smoke indicates an evolution in a fire-prone ecology.

Original publication

Tribe, G., Tautz, J., Sternberg, K. and Cullinan, J. 2017. Firewalls in bee nests – survival value of propolis walls of wild Cape honeybee (Apis mellifera capensis). Sci. Nat. 104:29.

DOI 10.1007/s00114-017-1449-5

http://rdcu.be/p2u4

HOBOS

Acknowledgment: The permission granted by SANParks to locate and analyse the nesting sites of honeybees in the Table Mountain National Park is gratefully acknowledged.

The authors at work…

Carpenter bees indicate pheromone is released by drones in Drone Congregation Areas

By Geoff Tribe, Karin Sternberg and Jenny Cullinan

Fig. 1 Male Xylocopa caffra carpenter bee at his patch of Pelargonium cucullatum busy challenging the photographer.

Fig. 1. Male Xylocopa caffra carpenter bee at his patch of Pelargonium cucullatum busy challenging the photographer.

Patrolling his patch!

Ever wonder about the antics of the yellow-haired carpenter bee hovering around a flowering shrub (Fig. 1), then darting off, only to return seconds later to hover briefly again? This is the male Xylocopa caffra which is distributed throughout South Africa. The females are unlike the males in that they are black and hairy with two bands of yellow hair (Fig. 2).

Fig. 2. The female Xylocopa caffra carpenter bee does not resemble the male.

Fig. 2. The female Xylocopa caffra carpenter bee does not resemble the male.

What the males are doing is to patrol a patch of flowers to which females are attracted out of necessity whilst foraging in order to mate with them. A patrolling male will aggressively chase away intruding males and will even attempt to discourage you from coming too close by mock diving at you. Stretch out your arm and point your finger at the carpenter bee and it will often approach the finger directly and will follow the finger as it is moved slowly up and down – as if it is an intruder.

Xylocopa caffra males make quick circuits of an area of several square meters and females that are receptive allow themselves to be seized in flight (Watmough, 1974). The receptive female will vibrate her wings and help the male carry her in flight, a successful mating flight ending 50 meters or so up in the air about a kilometre away.

Exposing interstitial membranes

What is most fascinating is that the normally completely yellow male, when hovering around its patch of flowers, lowers its abdomen and exposes two of its interstitial membranes which appear as two black bands on the abdomen (Fig. 3). The most likely explanation for this behaviour is that the male is releasing a sex pheromone, both as a species specific chemical signal and female sexual attraction. When the male momentarily darts away, the membranes are less exposed when compared to when it hovers.

Fig. 3. Male Xylocopa caffra with his interstitial membranes exposed while patrolling his patch of Pelargonium.

Fig. 3. Male Xylocopa caffra with his interstitial membranes exposed while patrolling his patch of Pelargonium.

For semi-social carpenter bees which nest in tunnels they construct within dead branches of trees or dried Aloe inflorescences, this method of patrolling patches of flowers that females must visit for the collection of pollen and nectar, is obviously suffice for the sexes to meet. The success of these encounters is enhanced by the permeation of a sex pheromone released by the male while patrolling his patch of flowers. Males of the carpenter bee Xylocopa hirsutissima have a different strategy and fly to the top of the mountain where they spread mandibular gland secretion over the ventral surface of their abdomen while hovering in the air awaiting the female (Velthuis and Camargo, 1975).

Drone Congregation Areas

For highly specialized social insects like honeybees, a more intricate and highly efficient behaviour has evolved to bring virgin queens and drones together. Mating in honeybees takes place in the air at considerable distance from the hive. These are called drone congregation areas (DCA) where thousands of drones congregate in certain locations in the air where they await the arrival of a virgin queen. Drones from as many as 240 colonies have been recorded in a DCA at one time. The phenomenon of DCAs is still little understood but certain characteristics pertaining to them are known.  Both drones and queens independently find these locations, some of whose locations have been known for hundreds of years and are therefore persistent from year to year (Zmarlicki and Morse 1963). Drones and queens from hives brought in from outside the region are immediately able to find these DCAs.

Thousands of drones milling about in a DCA greatly reduce the chance of a queen being eaten by alpine swifts (Fig. 4a), bee-eaters, redwinged starlings (Fig. 4b) or other avian predators.

Swallows in Perth, Western Australia were found to have up to 19 drones in their stomachs (Tribe 1989). Even spider’s webs may prove a hazard, even within a DCA (Fig. 5). A virgin queen always leaves on her mating flight during a worker orientation flight which persists until the queen returns – thus further reducing the chance of predation.

Fig. 5. Drones caught in a spider’s web between two tall trees in a pine plantation at Grabouw, Western Cape. The web was eventually shredded by comets of drones attracted to those caught in the web.

Fig. 5. Drones within a DCA caught in a spider’s web between two tall trees in a pine plantation at Grabouw, Western Cape. The web was eventually shredded by comets of drones attracted to those caught in the web.

Advantages of a Drone Congregation Area

Obviously the DCA must serve an important function, especially if one considers the resources entailed in rearing hundreds of drones in each honeybee colony each year. The amount of drone comb and the number of adult drones present is positively correlated with the number of workers in the hive and represent a maximum of 14% of the total brood at any time. The number of drones kept in an active colony is restricted to about 1000. Because it takes 24 days from egg to emergence (compared with 19 days for an African worker) the larger drones consume abundant pollen. The cessation of the rearing of drone brood is in response to pollen shortage, while the killing or expulsion of drones by workers is mostly the result of a shortage of nectar and may occur at periods throughout the year (Currie 1987).  Because the mating flights of drones and virgin queens are not random but concentrated into distinct areas, mating takes place in the shortest possible time. In times of very low drone population density, queens have a reasonable chance of being mated in a DCA. The lifespan of a drone is between 13-59 days.

The main advantage of a DCA appears to be to lessen the chance of a virgin queen mating with a related drone which is detrimental to the colony. With the sometimes thousands of drones drawn from diverse colonies in the area, the possibility of mating with a related drone is much reduced. In addition, queens of European races mate with an average of 8 drones and up to 17 (Woyke, 1962) which further reduces the level of inbreeding if she inadvertently mates with a related drone. By using DNA fingerprinting techniques, Moritz et al. (1996) determined that Apis mellifera capensis queens of the same population will have mated between 24 and 44 times.

Although the spermatozoa from one drone (12.7million) is suffice to fill the spermatheca of the queen, as the spermatozoa move from the oviduct past the spermatheca, fractions of the sperm of each drone is absorbed into it.  Only about 370 000 spermatozoa (3%) are retained in the spermatheca.  On the eversion of the aedeagus of the drone (like a glove blown inside out) (Fig. 6), the clump of sperm is followed by mucus and following the dissection of a recently mated queen the number of drones with which a queen has mated can thus be calculated.

The mated queen determines whether she must lay a fertilized or un-fertilized egg by measuring the cell width with her forelegs before commencing oviposition. At the height of summer a huge number of drones are present in a DCA, the majority of which will never mate – an estimate that only 4% of drones mate naturally. This huge investment in the transfer of genes indicates the importance of DCAs.

Characteristics of Drone Congregation Areas

DCAs vary greatly but most appear to have some form of relief in the form of trees or mountains near which they are established. Usually they occur high above the ground and are discerned from the noise the drones make whilst flying which sounds like a huge swarm of bees about to settle. Years back in Pretoria an irate grounds manager of a rugby club phoned to ask if we could remove a huge swarm of bees that interfered with their rugby matches on Saturday afternoons. It was quickly ascertained that no one had ever been stung, nor had any bees been observed but that the swarm ‘hovered high above the ground’. The rugby field was below a DCA and was flanked by high Eucalyptus trees. A DCA may expand or contract in size throughout the year but there is always a ‘core’ area which persists from year to year.

DCAs in Europe are recorded located at heights of 15-25m above ground (range of 8-40+m) over open ground or on summits, often in areas demarcated by buildings or rows of trees. They were 50m to 5km from the apiary and their individual sizes fluctuated from 30 to 200m in diameter but there was always a ‘steady centre’. Researchers found that drones of European races did not follow queens out of DCAs but always remained within its limits and could not be attracted to ground level with queen pheromone lures. Certain DCAs were more attractive than others and the number of drones visiting a DCA varied between sites and on different days. The sun was not used to orientate to DCAs. And of course there were no dances among the drones to indicate the location of a DCA! Successful matings from 10 to 16km distant have been recorded but the usual distance is from 5-7km. By placing drone-less colonies on islands or in desert areas, it was shown that to prevent mating an isolation of at least 15km from the nearest hive was required.

Drone Flight

Drone flight in Pretoria during the summer months began at about 12h00 and ended after 17h00 with peak flight times between 14h30-15h45. The average number of flights undertaken by flight mature A. m. scutellata drones in Pretoria was 3.7 flights/day (n=23) with a range of 3-5 flights. Individual marked drones made multiple flights in an afternoon with a mean duration of 21min 30sec (range 12min 15sec to 33min 53sec).  Using 8m/s as the flight speed, an A. m. scutellata drone is able to travel a distance of 10.3km in 21.5min with a maximum of 16.4km. When visiting a DCA no further than 1 to 1.5km distant (in ±3min), a drone could be cruising within the DCA for 45min on each flight. Between flights, drones would spend an average of 4 minutes feeding on uncapped honey.   With three flights in an afternoon, including feeding intervals between flights, drones on average would spend 72min/day on mating.

From limited data it appeared that the older the drone, the longer the duration of the mating flight. The African bee produces and maintains larger numbers of drones even in resource-scarce conditions than do European races, which accounts for the huge numbers found in DCAs.

Queen Flight

The first orientation flight of an Apis mellifera scutellata queen would take place on the third day after emergence. Usually there were orientation flights on two successive days before the virgin queen departed on a mating flight. The queen would only leave the hive during a worker orientation flight and such orientation flights would persist until the queen returned to the hive. The queen would fly once or several times in the same afternoon or on successive days until she was fully mated.

Gary (1971) recorded queen flight at 340m/min (5.6m/s), enabling a queen to take 2min 56sec to fly 1 000m. On Sylt Island (Germany) where the wind hardly ever stops blowing, matings took place at windspeeds of up to 5m/s (Tiesler 1972). The mean duration of a queen flight in Pretoria was 13 minutes 17 seconds (range 6min 11s – 21min 58s) (Fletcher and Tribe, 1977). Thus the A.m. scutellata queen could fly 4 515m in 13.28min or a return journey of 2 257m. Two further queen flights in November 1979 gave a duration of 19min 49sec and 26min 34sec which gives a maximum range of 9km.  Drones evert within 1-6 seconds on mounting the queen. Upon eversion, the drone falls backwards and the resulting pressure within the aedeagus causes the non-chitinized section to rupture, the drone falling to the ground while the queen flies off with the ‘mating sign’.

Flight experienced workers appear to determine if and when the queen departs on her mating flight. They orientate in front of the hive in ever widening circles, possibly gauging if weather conditions are suitable for flight. In an observation hive, a virgin queen primed for a flight can be seen preening herself on the comb. Ever more workers vacate the hive on their orientation flight, and the cue for the queen to leave happens after several of the orientating workers return to the hive and run ‘randomly’ around on the comb. The queen, while trying to find the exit (because the cover is off the observation hive), invariably ‘jumps’ onto the glass window and then quickly follows the bees out of the entrance.

Behaviour within the Drone Congregation Area

Fig. 7. Honeybee drones attracted to a strip of cloth attached to fishing gut and a helium filled balloon which had been lowered to near ground level within a drone congregation area in Pretoria.

Fig. 7. Honeybee drones attracted to a strip of cloth attached to fishing gut and a helium filled balloon which had been lowered to near ground level within a drone congregation area in Pretoria.

Drones form comets within the DCA of several hundred individuals which can dissipate as fast as they may be formed (Fig.7). Comets may be formed even in the absence of a queen when they orientate to any object that may enter the space such as butterflies, or even to another drone. Despite the literature recording that drones of European races of honeybees never descend near the ground (Gary 1962), in October 1986 in Floreat Park, Perth, Western Australia drone comets were observed flying at head height in an open park surrounded by trees (Tribe 1989b). Within the DCA of about 100m x 50m, individual drones were flying at knee height.

The queen is approached from below where she is silhouetted – hence the function of the abnormally large eyes of the drones. Because of its small visual acuity, a drone must fly within 1m of an object the size of a queen in order to see it (Butler and Fairey 1964). Queens may return fully mated on their first flight or may undertake subsequent mating flights on the same day or subsequent days.

Types of DCAs

How do drones and queens independently locate DCAs? Olfaction, especially pheromones, plays a crucial role in the life of the honeybee and no doubt this extends also to the formation and function of DCAs. Pioneering research into DCAs in Pretoria showed what appeared to be three types of DCAs which were used interchangeably in response to varying weather conditions: ‘barrier’, ‘sheltered’ and ‘convectional’. The most regularly visited DCA was situated downwind from a ridge which formed a barrier (e.g.  A in figure 9, the most consistent DCA). After consulting weather bureau personnel, it was determined that a breeze passing over the ridge on an otherwise relatively still day would cause an eddy downwind. The height of the ridge and the velocity of the wind would determine the strength of the eddy and its distance from the ridge. Drones fly in the afternoons on hot days and ground that bakes in the sun during the day results in late afternoon breezes as cooler air is drawn in as the hotter air rises which often results in showers of rain.

Fig. 8. Map of the situation of drone congregation Areas around the apiary on the University of Pretoria Experiment Farm.

Fig. 8. Map of the situation of drone congregation Areas around the apiary on the University of Pretoria Experiment Farm.

Eight DCAs were located around the apiary situated on the University of Pretoria Experimental Farm in 1975 with an average distance from the apiary of one kilometre (Fig. 8). By monitoring the wind speed at the entrance to the hive, it was determined that queens would not fly if the wind speed ≥5m/s, and drones at ≥7m/s. On extremely windy and usually overcast days, a DCA which normally attracted a smaller number of drones would supplant the barrier DCA in numbers. It occurred in the sheltered lee of a kopje where the air within was relatively calm compared to the gusts of wind all around it (D in figure 9). On Lion’s Rump in Cape Town there is such a DCA which can be looked down upon where the drones can be observed flying. Here again there is relatively calm air while all about the easterly rages.

At the height of summer in Pretoria with its oppressive heat with nary a breeze, the air is filled with the sound of drones. Huge convection currents were initiated by the air above the hot soil attracting in cooler air with the DCAs expanding considerably in size in response to this.

When comparing DCAs in Europe with those in Africa, it must be remembered that in Europe most honeybee colonies are hived and relatively few are feral, whereas in Africa the opposite is true and drones within a DCA are mostly from wild swarms in natural nesting sites. The late Beowulf Cooper when visiting the Pretoria DCAs related that DCAs in the United Kingdom were perceptibly warmer within them than without and regarded this as a distinctive feature for their formation in Britain. Cooper (1977) proposed a thermal vortex of warmer air within the DCA contributing to its formation.

Pheromone plume

This is what appears to be happening. The drones exiting their hives on mating flights appear to fly mostly upwind or alternately downwind until they reach an area of mild turbulence where they congregate.  Here they fly around randomly within the limits of the eddy. Drones from comets caught in nets in DCAs (Fig. 9) were transferred to plastic bottles where they were marked by dabbing them with ‘tippex’ of different colours according to their DCA location. As they emerged between the fingers of the hand placed over the mouth of the bottle, a distinct musty smell could be detected (which incidentally attracted the occasional worker bee which would not leave). This odour could be a pheromone which not only assists the queen in finding the DCA but helps create the comets. Guard bees have been recorded in prolonged lapping over much of the dead body of a drone, especially near its thorax, apparently to salvage some highly desirable substance (Australian Beekeeper 1979, 80(8): 174). Crushed drones are highly attractive to worker bees and may produce a substance which is attractive to workers in summer, enabling a drone to drift to other colonies with immunity (Holmes and Henniker 1972). Another indication of a substance produced by drones is when drones and workers were returned to their queenless colony they were accepted, but the workers when confined to a cage with their queen and drones and returned to their colony are killed – but not the queen or drones (Orὅssi-Pál 1959). Drones could be attracted in DCAs with drone extracts as efficiently as with queen extracts – head extracts being the most successful (Ruttner H. 1972). In the presence of queen pheromone the drones will form comets as one drone follows the other. They will attempt to mate with any object silhouetted above them, a butterfly or stone thrown into the air.

A queen flying into a DCA releases queen pheromone (9-oxodecenoic acid) which results in the immediate formation of comets which zigzag after her, following her pheromone plume from at least 420m downwind of her. Drones are attracted by 9-oxodecenoic acid from distances of 50m and more while the queen tergite gland’s pheromone is effective only within short distances (less than 30cm) and increases copulation activity (Renner & Vierling 1977). A pheromone is also produced from the abdominal tergites in virgin queens 8 days or older and in mated queens, probably in the glands described by Renner and Baumann (1964) which are most active at the time of mating (Butler 1971). Production of a chemical from the abdominal sternites shows that it is restricted to nubile virgin queens because ‘wipes’ of newly emerged and very young laying queens had none of the perfume (Boch, Shearer and Young 1975).  Several comets may be seen simultaneously within the DCA, dissipating as they lose the scent and reforming at will.  They approach from below the queen and mate in the air, each drone in turn removing the previous ‘mating sign’ before inturn mating with her. Thus the reason why DCAs form in certain areas appears to be to facilitate through pheromones, the fast and efficient mating of the queen by following the pheromone plume.

Of interest is the question of why the multitudes of drones within a hive do not attempt to mate with their own mated or virgin queen who is continually secreting queen pheromone? Presumably the pheromone ‘bouquet’ released by a virgin as opposed to that of a mated queen is perceptibly different. Yet if mating within the hive were to occur, it would negate the major function of a DCA to prevent in-breeding. The difference between an inactive drone within the hive and that of a drone in a DCA is one of flight. Thus presumably flight changes the physiology of a drone and makes it responsive to queen pheromone. This could be a result of the accumulation of carbon dioxide in their tissues caused by exercise.

Sound

Could sound play an integral part in the formation of a DCA? Quietly sitting in a meadow, one of the most harmonious sounds is that of honeybees going about their business. Yet we are all familiar with the raised, high-pitched sound of an angry bee. Sound plays almost as important a role within the hive as that of pheromones. The piping of queens, the moaning of bees besieged by banded bee pirates (Palarus latifrons), the distress calls of worker bees in a queenless A. m. capensis colony, and many more sounds are familiar to the beekeeper. In addition, the male semi-social carpenter bee Xylocopa hirsutissima is known to raise its flight tone when it perceives the female approaching the top of the mountain that it is patrolling (Velthuis and Camargo, 1975).

Sounds have frequencies which are distinct, and in some instances the frequency or vibration may be more important than the sound that we hear. For example, following the departure of the old queen in a reproductive swarm, several virgin queens cut their way out of their queen cells. They soon detect the presence of the other queens and are further agitated by the workers which goad them on by harassing them. To shake off the harassing workers, the queen pipes with her wings. This high pitched sound causes the workers around her to freeze, and she scoots away temporarily before they again catch up with her. In an observation hive it is possible to follow the path of the queen as she pipes on the opposite side of the comb by observing the bees ‘freezing’ in the absence of the queen on this side. The sounds/ vibrations are carried through the comb.

The sound of drones returning to their hive after a mating flight is distinctive and cannot be confused with that of a worker bee. The screeching sound of a Stuka fighter aircraft in a bombing dive was deliberately built into the plane to terrify the enemy on the ground. Surely then, the loud and distinctive sound of a drone in flight also has an important purpose? The sound (and vibrations in the air?) of several thousand drones in a DCA could serve to make the locating of the DCA easier for both drones and virgin queens. Sound could also assist, besides sight and pheromones, in the creation of a DCA and the formation of drone comets and also to help distinguish a drone from a queen within the DCA. While marking drones in a DCA several would accidentally have ‘tippex’ splattered on their wings. This would result in a different sound being produced as it flew off which immediately attracted other drones to it. A major function of a DCA is to facilitate the complete mating of a virgin queen in the shortest possible time and a combination of sound, sight and pheromones may serve to accomplish this.

Evolution of male bee pheromone glands for mating?

While monitoring the number of times marked drones flew each afternoon and the duration of their flights, it was observed on many occasions that returning drones had the two interstitial abdominal membranes exposed – in exactly the same position as that of Xylocopa caffra males. Although dissections of drones were made to discover any underlying pheromone glands, they were so small that the equipment used could not detect them. If this is the source of a mating pheromone, it appears that it may be present in many bee species from solitary, sub-social and social species. Besides different flight times, the comparison of the composition of this pheromone could possibly help explain the sexual isolation of the different species of Apis and their phylogenetic linkages.

The authors at work:

References

Boch, R., Shearer, D.A. and Young, J.C. 1975. Honey bee pheromones: field tests of natural and artificial queen substance. Journal of Chemical Ecology 1(1): 133-148.

Brὔckner, D. 1979. Effects of inbreeding on worker honeybees. Bee World 60(3): 137-140.

Butler, C.G. 1971. The mating behaviour of the honeybee. Journal of Entomology 46: 1-11.

Butler, C.G. and Fairey, E.M. 1964. Pheromones of the honeybee: biological studies of the mandibular gland secretion of the queen. Journal of Apicultural Research 3: 65-76.

Cooper, B.A. 1977. Have you heard a drone assembly? British Isles Bee Breeders’ Association, 9pp.

Currie, R.W. 1987. The biology and behaviour of drones. Bee World 68(3): 129-143.

Fletcher, D.J.C. and Tribe, G.D. 1977. Natural emergency queen rearing by the African bee, A. m. adansonii, and its relevance for successful queen production by beekeepers. In African Bees: Taxonomy, Biology and Economic Use, ed. D.J.C. Fletcher. Pretoria: Apimondia. Part I, pp. 132-140; II pp. 161-168.

Gary, N.E. 1962. Chemical mating attractants in the queen honey bee. Science NY, 136: 773-774.

Gary, N.E. 1971. Observations on flight-experienced queen honeybees following extra-apiary release Journal of Apicultural Research 10(1): 3-9.

Holmes, F.O. and Henniker, N.H. 1972. Attractiveness of drones to worker honeybees. Gleanings in Bee Culture 100(10): 297.

Johannsmeier, M.F. (Ed.) 2001. Beekeeping in South Africa. Third Edition, Revised. Plant Protection Research Institute Handbook No 14, Agricultural Research Council, Pretoria. 288pp.

Moritz R.F.A., Kryger P. and Allsopp, M.H. 1996. Competition for royalty in bees. Nature 384: 31.

Orὅssi-Pál, Z. 1959. The behaviour and nutrition of drones. Bee World 40(6): 141-146.

Renner, M. and Baumann, M. 1964. Ueber Komplexe von subepidermalen Drὔsenzellen (Duftdrὔsen) der Bienenkὅnigen. Naturwissenschaften 51: 68-69.

Renner, M. and Vierling, G. 1977. Die Rolle des Taschendrὔsenpheromons beim Hochzeitsflug der Bienenkὅnigin. Behavioral Ecology and Sociobiology 2: 329-338.

Ruttner, F. 1968. The life and flight activity of drones. Australia Beekeeping 69(4): 279-284.

Ruttner, H. 1972. Neue Versuche  ὔber die Flugbahnen der Drohnen ὔber den Alpen. Apimondia Science Bulletin, Bucharest, pp 79-81.

Tiesler, F.K. 1972. Mating stations in the islands north of Germany. Apimondia Science Bulletin, Bucharest, pp. 91-95.

Tribe, G. 1982. Drone mating assemblies. South African Bee Journal 54(5): 99-100, 103-112.

Tribe, G.D. 1989a. Drones caught in a spider’s web within a drone congregation area. South African Bee Journal 61(5): 110-111.

Tribe, G.D. 1989b. A drone congregation area in Perth, Western Australia. South African Bee Journal 61(4): 83-86.

Velthuis, H.H.W. and Camargo, J.M.F. de 1975. Further observations on the function of male territories in the carpenter bee Xylocopa (Neoxylocopa) hirsutissima Maidl (Anthophoridae, Hymenoptera. Netherlands Journal of Zoology 25(4): 516-528.

Watmough, R.H. 1974. Biology and behaviour of carpenter bees in southern Africa. The Journal of the Entomological Society of Southern Africa. 37(2): 261-281.

Woyke, J. 1962. The hatchability of ‘lethal’ eggs in a two sex-allele fraternity of honeybees. Journal of Apicultural Research 1: 6-13.

Zmarlicki, C and Morse, R.A. 1963. Drone congregation areas. Journal of Apicultural Research 2(1): 64-66.

Flowering Gums: Honeybee Smorgasbord

Fig. 1

By Geoff Tribe

Australia’s gift to the world was the gum- or Eucalyptus tree now found growing throughout the world where it has been planted for its timber, fire-wood, honey resource and as an ornamental. In southern Africa, eucalypt plantations not only provide hardwood timber and half the paper-pulp needs of the region, but are also found scattered throughout the landscape. Almost everywhere there was European habitation in the past and present, the ubiquitous eucalypt is bound to have been planted. At most wind pumps in the arid Karoo or the Kalahari Desert, a few eucalypts may be found growing nearby as a source of shade for the stock.

Origins of Eucalyptus in South Africa

South Africa is poorly endowed with natural forests, with only 0.3% of the land area afforested. Exploitation of these indigenous forests began with European settlement at the Cape of Good Hope in 1652 and gradually extended eastwards as the local resources became exhausted. Timber was required for shipbuilding, housing, ox-wagons, furniture and fuel. The early Cape governors realized the necessity for the importation of fast-growing exotic tree species and the first introductions were the common oak (Quercus robur) followed by cluster and stone pines (Pinus pinaster and Pinus pinea). By 1847, attempts were made to halt the exploitation and conserve what remained of the indigenous forests by restricting access. Increased demand for timber arose in the 1870s for railway sleepers, telegraph poles and props for mines. The first timber plantations consisting of eucalypts was established at Worcester in 1876 to provide firewood for railway locomotives. However, it was only during World War II when timber imports were disrupted and prices escalated that a boom in afforestation began and continued after the war with a total area of commercial plantations in South Africa now exceeding 1.5 million hectares, of which slightly less than half is under eucalypts.

Much of South Africa’s honey production relies on the nectar from these eucalypt plantations and woodlots throughout the country. Commercial eucalypt plantations, however, are not found in the Western Cape, but a variety of spectacular flowering gums have been planted as ornamentals (Fig. 1a,b,c,d). Many of these originate in the winter rainfall region of Western Australia and so are well adapted to the climate of the Cape. These exotic trees are able to grow rapidly and are able to outperform those in their country of origin because they are not subjected to the depredations of the many pests and diseases that afflict them in their natural environment.

Cape Town ornamental gums

The most striking of the Christmas flowering gums is the Red-flowering gum, Corymbia (Eucalyptus) ficifolia (Fig.2) which is extremely attractive to honeybees (Fig. 3) and many other insect species. There are colour varieties from a deep crimson to almost orange (Fig.4a,b,c,d,e,f) and some may be hybrids between the White-flowering gum, Corymbia calophylla (Fig. 5) as seen in the red tinges (Fig. 6). The profusion of clumped flowers is available to bees over a period of several weeks. Both nectar and pollen are produced in abundance and the honey of the red-flowering gum is distinctive in that, when the honey is extracted or a comb broken, the honey forms long ‘strings’. Another spectacular tree which flowers in late autumn is the swamp messmate Eucalyptus robusta (Fig.7).

Also flowering around Christmas and into the next year is the prime honey producer of the Western Cape, the Sugar-gum, Eucalyptus cladocalyx (Fig.8). The sugar-gum grows to impressive heights and is possibly the most important gum in the Western Cape because it tides the bees over the crucial dearth period of January-March when not much forage is available in the indigenous fynbos and temperatures soar to 35°C. It also produces the premium honey in the Western Cape – a honey which may take 10 years or more to crystalize if from pure source. All Eucalyptus species in the winter rainfall areas contribute to the wellbeing of the honeybees and thus safeguard the fundamental economy of the region.

There are many other less spectacular species of eucalypts growing in Cape Town and surroundings because many species were introduced into the Arboretum at Tokai during the early days of the Commonwealth in order to select those which showed promise as plantation species. The following list is of some of these species and their rating in nectar and pollen production out of a maximum of 4 according to Johannsmeier (2001):

                                                        Nectar             Pollen            Months            Origin

Eucalyptus ficifolia*                         3                         2                   12-2              WA (south-western)

Eucalyptus calophylla*                     3                         2                   12-5              WA (south-western)

Eucalyptus cladocalyx                      4                         1                    1-2                South Australia

Eucalyptus lehmannii**                  3                         2                    9-11             WA (south-western)

Eucalyptus diversicolor                    3                         2                    2-3                 WA (south-western)

Eucalyptus globulus                          2                         2                    7-10              Tasmania

Eucalyptus gomphocephala           3                          4                     3-4               WA (south-western)

Eucalyptus robusta                          3                          3                     4-6               NSW + Queensland

Eucalyptus leucoxylon                    3                          1                     5-9                South Australia

*Genus of blood-woods and ghost-gums recently reclassified as Corymbia.

**Species present in South Africa now confirmed as Eucalyptus conferruminata.

Features of eucalypts

Most eucalypt species carry three sets of reproductive stages – the ‘fruits’ (seeds) of the previous year, those presently in flower and the buds beginning to form for the following year. It usually takes a full year for the buds to mature and thus the weather conditions of the previous year have a direct effect on the number and profusion of flowers in the present year. Initially drought conditions may stimulate the tree to produce more buds as opposed to new growth, and a bumper honey flow may be experienced following this. But if the drought persists for several years, then the tree ceases both growth and bud formation. This curtailing of both growth and bud formation may also be induced by the action of pests.

Trachymela tincticollis

Trachymela tincticollis.

The arrival of the Eucalyptus tortoise beetle (Trachymela tincticollis) in the Western Cape which severely defoliated all concolorous (similar shade of colour on both sides of the leaf) eucalypt species caused the trees to die back and as a result, also stopped the formation of buds. The introduction of the egg parasitoid, Enoggera reticulata resulted in a 96% parasitism rate (Tribe and Cillié, 2000) which was subsequently followed by a massive flowering of Eucalyptus gomphocephala trees, the weight of the flowers causing several branches to break.

Many insect pests of eucalypts that have arrived in South Africa have had a devastating effect on the monospecific and contiguous plantations. The success of Enoggera reticulata in controlling the eucalyptus tortoise beetle was largely due to the exclusion of its two hyper-parasite species which together accounted for 88% of its population in Australia. Freed from its own parasitism, it was most effective in parasitizing the eggs of its primary host and preventing the emergence of the highly destructive larval stage.

Eucalypts in Australia

Honeybees were absent in Australia until introduced by European settlers and before then eucalypts were pollinated exclusively by a host of indigenous insects, birds and mammals such as possums. Their exposed flowers which gave easy access of their pollen and nectar to a wide variety of organisms attest to this. Although most flowers of eucalypt species are white to cream coloured and therefore more attractive to insects, red flowering gums (presumably more attractive to birds) also attract honeybees and many other insects. Perhaps the primary reason for this unusual attraction to red flowers is the incredible melliferous scent emanating from the eucalypts when in full flower.

The amount of nectar secreted by eucalypts is immense. In Yuraygir National Park in northern New South Wales it was possible in the mornings to gently move the sand away from under where a cluster of flowers had dripped over-night, leaving a loosely nectar-bound core of sand the size of a small bucket. Honeybees were excluded from the park due to the controversy raging at that time on the possible negative effect of alien honeybees on indigenous pollinators.

Eucalypts as ‘invaders’

Several Eucalyptus species have been placed on the invasive list of the Department of Agriculture including the River red-gum, Eucalyptus camaldulensis, whose seeds are discharged into water courses and add to the many other exotic species clogging the rivers. However, it is not common to see a myriad seedlings sprouting around established eucalypts. This is mainly a consequence of the fire-ecology of natural eucalypt forests in Australia. When visiting the endemic Ludlow Tuart Forest (Eucalyptus gomphocephala) south of Perth, one is struck by the non-random distribution of the trees – as if they had been planted in rows. The reason for this is that after a fire progresses through the forest and burns fallen trees, dehiscence occurs and seeds falling into the ash germinate and grow. Because the ash occurs in strips, this results in rows of seedlings following the outline of the burnt trunks. Apparently without this ash few seeds would germinate and eventually grow to maturity. This phenomenon is utilized by foresters where, following the felling of sections of mature natural forests, seeds are collected from the now open capsules of felled trees and then temporarily stored. The logs are removed and the debris is then burned and soon thereafter the stored seeds are spread over the area by helicopter into the ash for successful germination.

Fig 9. The spider gum, Eucalyptus conferruminata in flower – their dry gum nuts are often placed on fires to supply an aromatic flavour to the meat.

Fig 9. The spider gum, Eucalyptus conferruminata in flower – their dry gum nuts are often placed on fires to supply an aromatic flavour to the meat.

In paddocks bordered by eucalypt windbreaks such as E. lehmannii (now identified as E. conferruminata) (Fig.9) few if any seedlings survive as they are eaten by antelope, sheep, goats and cattle and therefore pose no danger of spreading.

Other attributes of eucalypts

Eucalyptus species such as the white stemmed Corymbia (Eucalyptus) papuana ghost gum of the outback growing in their natural environment are aesthetically beautiful. The texture and colour of the bark is a reflection of the habitat in which they occur and can also add to their beauty as ornamentals as in suburbs of Cape Town. Stringybark species are water and fire resistant and grow in regions inundated with water for months of the year followed by fires. White stems resulting from peeling bark reflect sunlight, an adaptation to fierce heat (much like kokerbooms, Aloe dichotoma now Aloidendron dichotomum in arid areas of southern Africa). Dwarf, multi-stemmed mallee eucalypt species in fire prone areas of Australia rely on an underground woody rootstock (lignotuber) in order to re-sprout after the fire has passed through. The blood-woods if wounded ooze a red resin which is dried and powdered and used as medicine (Fig. 10).

Fig 10. Kino from gums known as blood-woods such as Corymbia ficifolia which has medicinal properties.

Fig 10. Kino from gums known as blood-woods such as Corymbia ficifolia which has medicinal properties.

Eucalypts as integral to the proliferation of honeybee colonies in the Western Cape

Not only are the eucalypt species in the Western Cape highly attractive as ornamentals, but are essential to the wellbeing of honeybee colonies and thus to the agricultural base of the economy of the region. Does the presence of alien eucalypts distort or negatively influence the survival of the Cape Bee and other pollinators from flies to beetles and birds which visit them? Available evidence shows that eucalypts are in fact possibly responsible for an increased number of colonies in the region due to an increased amount of nectar and pollen. Such healthy honeybee colonies are able to produce a greater number of reproductive swarms each year than would have occurred naturally in the fynbos, and so maintain or increase the natural capacity of the area.

The author at work:

Dr Geoff Tribe

Dr Geoff Tribe

References

Boland D.J., Brooker M.I.H., Chippendale G.M., Hall N., Hyland B.P.M., Johnston R.D., Kleinig D.A. and Turner, J.D. 1987. Forest Trees of Australia. CSIRO, Australia. 687pp.

Johannsmeier, M.F. (Ed.). 2001. Beekeeping in South Africa. Plant Protection Research Institute Handbook No 14, Agricultural Research Council of South Africa, Third Edition, Revised.288pp.

Tribe, G.D. and Cillié, J.J. 2000. Biological control of the Eucalyptus-defoliating Australian tortoise beetle Trachymela tincticollis (Blackburn) (Chrysomelidae: Chrysomelini: Paropsina) in South Africa by the egg parasitoid Enoggera reticulata Naumann (Hymenoptera: Pteromalidae: Asaphinae). African Entomology 8(1): 15-22.

Feral capensis outsmarting American Foulbrood?

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Geoff Heathcote-Marks, Dominique Marchand and Geoff Tribe

American Foulbrood (Paenibacillus larvae) is an exotic bacterial disease which appeared in South Africa some 20 years ago and to which our indigenous honeybees had not before been exposed. After its initial discovery in the Cape Peninsula where it wreaked havoc amongst several commercial beekeepers, the disease spread throughout the Western Cape where sporadic outbreaks were reported over the intermediate years. Then in 2015 there was again an upsurge in the disease in which major losses were inflicted on mainly commercial beekeepers which raised major concerns.

The economy of the Western Cape is underpinned by the export fruit industry which in turn is reliant on pollination by honeybees. With the expansion of the industry in recent years, there is already a shortage of pollination units. This is now exacerbated by the presence of American Foulbrood (AFB) which is only contained either by incinerating infected hives or by radiation treatment which adds to the cost. Why commercial beekeepers are more adversely affected by American Foulbrood as compared with that of hobbyist beekeepers appears to be the greater mobility of hives of the former and the higher infection rate experienced at the depot where honey is extracted due to intermingling of hive parts and the drifting of bees.

Hobbyist beekeepers in Pinelands

The recent discovery of American Foulbrood in the Cape Town suburb of Pinelands has raised some interesting questions. Several hobbyists keep hives within the suburb and there are many wild swarms to be found both within trees and in air vents etc. in houses. Swarms are trapped or removed within and in the surroundings of the suburb but there is no commercial activity where hives are taken to orchards for pollination purposes. The suburb provides many flowering plants for the bees to utilize including ornamental eucalypt species such as the red flowering gum, Corymbia ficifolia (Fig.1), the sugar gum Eucalyptus cladocalyx and many other tree species such as the Brazilian pepper tree. Garden flowers and indigenous plants in many open spaces provide both nectar and pollen especially in spring, but there is always something flowering throughout the year.

Fig. 1. The ornamental gum tree Corymbia ficifolia lining the streets of suburbs in Cape Town.

Fig. 1. The ornamental gum tree Corymbia ficifolia lining the streets of suburbs in Cape Town.

Several incidences of AFB infected hives have been recorded in Pinelands both in hives and in wild swarms. The current case has been well documented. The bees took up residence in an owl-box at a height of 6 metres from the ground in late November 2014. Here they flourished for about a year. However, they were observed to abscond on 30 December 2015, settling in a tree for a brief time before disappearing in a swirl of bees. They left behind about 8 sturdy combs about 22 cm deep and wide, of which 4-5 had been brood combs. All the honey had been consumed by the departing bees. Some diseased brood which had the typical sunken appearance and perforations in the cappings together with the characteristic scattered brood pattern (Fig.2) remained to show the extent of the disease. The ‘matchstick’ test confirmed the presence of AFB (Fig. 3).

Fig. 2. The scattered pattern of brood cells with depressions and perforation in the cappings which are typical of AFB infection.

Fig. 2. The scattered pattern of brood cells with depressions and perforation in the cappings which are typical of AFB infection.

Fig. 3. The ‘matchstick’ test whereby the entire contents of a cell are reduced to a sticky goo.

Fig. 3. The ‘matchstick’ test whereby the entire contents of a cell are reduced to a sticky goo.

Questions

What raised many questions were the following observations. Although there were two hives on the property, no robbing of the vacated owl box was observed – which raises the question whether the smell or sliminess (Fig. 4) of the infected combs act as a deterrent to potential robbers? If this were so, it would serve to help contain the spread of the disease to a great extent. This foul odour which is symptomatic of the disease is foreign to African bees, and if it acts as a deterrent, then it must contain some interesting compounds. African bees are not adverse to collecting water from urine, from animal dung, or from making their nest in a tree frequented as a sleeping place for baboons which foul the whole area, yet show no adverse reaction to such powerful odours when foraging.

Fig. 4. The ‘sliminess’ covering the comb is another indication of the presence of AFB.

Fig. 4. The ‘sliminess’ covering the comb is another indication of the presence of AFB.

Another interesting observation was that despite the nest having been vacated about a month ago, the indigenous small hive beetle, Aethina tumida, had not consumed the combs which, although devoid of honey, had plenty of pollen stores and dead brood on which to feed. Several small hive beetles were observed when the owl box was dismantled, but only a single larva was seen (Fig. 5). The small hive beetle belongs to a family of scavengers who nearly always are present in a colony but flourish if the colony should begin to falter through starvation or disease. The small hive beetle is highly adapted to living within a honeybee colony as it is one third the size of a worker bee, has a round, smooth dome and when confronted it merely pulls in its appendages and holds tightly to the substrate. Hence it is able to enter worker cells where it feeds on eggs, pollen and honey.  In a strong hive the small hive beetle hides away in crevices where the bees cannot access them. The bees’ response is to confine them in a propolis jail where they are prevented from mating or laying eggs. However, the small hive beetle confined as such is able to solicit food from its captors. This normal reaction where one worker bee may solicit food from another by antennal contact is mimicked by the confined beetle, which is then fed by the misled bee.  Should the swarm abscond, the small hive beetle breeds rapidly and their larvae within a short while are able to consume the entire nest and then exit to pupate in the soil in front of the nest. In this way, much like hyenas, they act to control the spread of disease.

Fig. 5. A single small hive beetle (Aethina tumida) larva was observed.

Fig. 5. A single small hive beetle (Aethina tumida) larva was observed.

The small hive beetle recently found its way to North America and Australia where it has overwhelmed hives because the European races of honeybees on those continents were unfamiliar with it and were unable to contain or expel it. The prolific use of propolis by the African bee may in part be a consequence of containing the small hive beetle where wild nests in cavities may be enveloped in a propolis sheath which denies the beetle places in which to hide (Tribe 2000).

Similarly, wax moth larvae were present only in a small section of the honey-crown (possibly where the lowest titre of diseased spores would be found) (Fig.6) but had not also consumed the brood combs. Were they perhaps also deterred by the presence of the disease?

Fig. 6. The wax moth had only become established in a small section of the honey-crown.

Fig. 6. The wax moth had only become established in a small section of the honey-crown.

The above observations are limited to the colonies inspected and it is not known if the above applies to most colonies infected with AFB.

How is AFB spread to wild swarms?

How did this owl-box swarm become infected with AFB? Had they brought the disease with them as a trace of spores when they took up residence and which then took a year to overwhelm the colony? The two hives on the property showed no signs of AFB but will continue to be monitored. Absconding was most definitely as a result of the disease, a behaviour which is consistent with African bee races when faced with adverse conditions (Hepburn & Radloff 1998). The honey containing AFB spores that the absconding bees ingested before departure would be consumed within a few days and in theory they would then have rid themselves of the disease and be free to begin elsewhere again. This is one method that beekeepers use to rid their hives of the disease by shaking the bees into a new hive, burning the infected hive, and starving the bees for about a week to rid them of the spores. Could the owl-box swarm have absconded once before due to the disease but not entirely rid themselves of the disease which slowly built up to overwhelm them?

Natural health of African bees

Beekeepers in southern Africa have adapted their methods to tie in with the ecology of the African bee. The underlying basis of beekeeping in South Africa relies on the trapping of migrating, absconding or reproductive swarms to replenish their ‘stock’. Absconding is ubiquitous in the African races and is induced by dearth, predation or deterioration in nest quality (Hepburn 1993). To those in Europe, Australia or the Americas (the latter two continents having been devoid of honeybees before European colonists arrived) who work with European races of honeybees, this would seem fairly primitive. What is so different in southern Africa is that because they are indigenous, more than 80% of honeybee colonies are still to be found in the wild. Even those that are hived are never really domesticated – they as easily abscond and may again at some stage be re-captured by a beekeeper in a trap-box. However, the great advantage here is that the African bee is still being subjected to natural evolutionary pressures and can be regarded as being extremely healthy genetically. The Varroa destructor mite from Asia which wrought havoc in those countries farming with European honeybees, despite great apprehension initially, was brought under control by the African bee because of two main traits – that of having a shorter life cycle, thus the mite not being in full synchrony with that of its host, and of being more aggressive and physically biting and removing them from the hive. Could we hope that the African bee has the means in its ‘repertoire’ of behavioural traits to neutralise AFB?

Absconding as a defence mechanism?

American Foulbrood appears not necessarily to cause the death of a honeybee colony, which if strong enough after detecting the disease, will abscond before being overwhelmed. If the honey engorged before they absconded is used within a few days and the newly constructed combs are not contaminated with AFB spores, then the colony has a good chance of surviving and ultimately thriving.

The owl box

The owl box

References

Fletcher, D.J.C. 1975-1976. New perspectives in the causes of absconding in the African bee (Apis mellifera adansonii L.) South African Bee Journal I & II. 47(6): 11-14; 48(1): 6-9.

Hepburn, H.R. 1993 Swarming, absconding and migration in southern African bees. South African Bee Journal 65(3): 61-66.

Hepburn, H.R and Radloff, S.E. 1998. Honeybees of Africa: 5. Swarming, migration and absconding. Springer –Verlag, Berlin Heidelberg.

Tribe, G.D. 2000. A migrating swarm of small hive beetles (Aethina tumida Murray). South African Bee Journal 72(3): 121-122.

Ambushed! The Hazards of Foraging Honeybees

By Karin Sternberg, Jenny Cullinan and Geoff Tribe

Philanthus

Like all living creatures, the honeybee faces many dangers in trying to survive – from environmental hazards such as fires and drought, to the many organisms which wish to feed off their honey and nutritious brood. Those colonies which survive and prosper will be the ones which send out many drones and reproductive swarms which will disperse their genes to the advantage of the species. Because at least 80% of honeybee colonies in Africa are wild (Fig. 1) and relatively few have been hived, the evolutionary pressures acting on the species is being maintained. Even those hived are never domesticated – they have a strong tendency to abscond, for reasons such as starvation or an excess of parasites, or to migrate to seasonal honey flows in adjacent regions. These swarms will in turn be hived again because beekeeping in southern Africa is based on the annual trapping of wild swarms, whether migrating or reproductive, for ‘making increase’ – bringing the number of hives up to optimum again.

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Fig. 1. Wild honeybee colonies, clockwise: Apis mellifera scutellata nest hanging under the branch of an exotic pine tree in Pretoria, Apis mellifera capensis swarms hanging under a branch in Stellenbosch and c. in a small cave in the Cape Peninsula.

Another of the dangers not often pondered are the ambush predators, the robber flies and wasps, many of them generalist predators of soft-bodied insects such as flies, but the diet of several species consists largely of honeybees. The banded bee pirate Palarus latifrons (Fig.2) can be a major problem for beekeepers in the dry, hot and sandy regions of southern Africa. Foraging bees are captured as they leave the hive and are paralyzed by the female wasp which makes a cavity in the soil in which the bee is placed. On this bee the wasp lays an egg which hatches into a larva and consumes the bee.

Fig. 3. The female banded bee pirate, Palarus latifrons.

Fig. 2. The female banded bee pirate, Palarus latifrons.

As many as 80 bee pirates have been seen in front of a hive at the Heuningberg near the town of Porterville on the West Coast. The bees become so intimidated that they cease foraging – only pouring out as the sun sets and the wasps have departed as it cools and they become inactive. The bees fill the entrance with their bodies and create a ‘moaning’ sound which is quite distinctive. The wasps alight on the entrance board and try to entice a bee away from the massively defended entrance. Often the only solution is for the bees to abscond because they are starving.

Fig. 2. Asilid robber fly with a captured honeybee in the Tanqua Karoo.

Fig. 3. Asilid robber fly with a captured honeybee in the Tanqua Karoo.

Robber flies (Fig.3) regularly capture honeybees in flight usually away from the nest where they sit on the sand or perch on rocks or twigs from which they make forays at foraging bees or any passing soft-bodied insect. Around Vachellia (Acacia) karroo trees in flower in the Tanqua Karoo, they tend to perch on nearby rocks and capture the many flies which visit the flowers. There is no information on the numbers of robber flies in any area or any quantifiable data on their detrimental effect on honeybee populations.

The wasps of the genus Philanthus are well known predators of honeybees but will also prey on a wide range of bee and wasp species. The yellow bee pirate Philanthus triangulum which preys regularly on honeybees has another strategy: it ambushes the bees on the flowers on which they are foraging (Fig.4).

It is widely distributed and is common in Europe where it is known as the ‘Bee Wolf’. The wasp stings the bee in the throat which it then malaxates, feeding on the honey which is forced from its crop. The paralysed bee is taken to a burrow excavated in the sand where it is stored in a cell with others to provision the larvae with food in the same way as the banded bee pirate.  While observing a bee wolf out foraging on a flower, its behaviour changed when a honeybee came into range. It later dug a nest in a sandy bank and then flew off only to return 12 minutes later with a honeybee it had captured (Fig.5).

Fig. 5. A Philanthus wasp returning with a honeybee it had just captured.

Fig. 5. A Philanthus wasp returning with a honeybee it had just captured.

Recently vast numbers of wasps of the Bembix genus were observed in the vicinity of honeybees drinking water in seepage beside a stream in the Cape Point section of the Table Mountain National Park. With temperatures as high as 36°C a number of bees were collecting water (Fig. 6).

Tracking Bembix in the late afternoon light, we found an aggregation of about 50 nests located in soft soil on the bank above the stream and many Bembix furiously and almost chaotically digging at the surface at intense speed creating new nesting sites (Fig.7). Bembix wasps do not have it all their own way. Adult wasps are preyed on in turn by some birds, lizards and antlions, Neuroptera and probably also crab spiders, robber flies and mantids; while bombyliid flies are known parasitoids of their larvae, and chrysidids, cuckoo wasps, mutillids (velvet ants) and true ants are known to rob Bembix nests. One of the Bembix observed was carrying a winterschmitiid mite (Fig. 8), attached to the thorax with its suctorial plates. Many of the mites are phoretic, travelling on the body of adult insects without being a parasite.  (S. Gess, pers. comm).

Fig. 7. An aggregate nesting site of Bembix wasps in a sandy bank besides the stream.

Fig. 7. An aggregate nesting site of Bembix wasps in a sandy bank besides the stream.

Fig. 8. Bembix carrying a winterschmitiid mite.

Fig. 8. Bembix carrying a winterschmitiid mite.

The alien European wasp, Vespula germanica (Fig. 9), is now firmly established in the south-western Cape and with time will migrate up the eastern coast into other provinces. It nests in the ground, as opposed to the other invasive wasp, Polistes dominulus, also from Europe which makes grey ‘mache’ nests the size of a football under the eaves of houses. Vespula germanica feeds on soft bodied insects including honeybees at flowers and is able to raid hives, collecting both adults and brood to feed to their larvae. The mild climate in southern Africa allows them to build massive nests in the ground, to persist throughout the year, and to invade the fynbos.

Fig. 9. An unusual photo of a pair of Vespula germanica mating on a shrub in Tokai.

Fig. 9. An unusual photo of a pair of Vespula germanica mating on a shrub in Tokai.

There is a great variety of organisms which feed on honeybees, of which those which have a close association are recorded and their biology mostly unraveled. But there appear to be yet many more opportunistic species of predators of honeybees which are only rarely recorded when they are chanced upon. They occur in diverse environments from fynbos to semi-desert biomes and their slow attrition on the numbers of foragers must ultimately have an effect on the well-being of the honeybee colony.

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Philanthus triangulum

References

Pulawski, W.J. and Prentice, M.A. 2008. A revision of the wasp tribe Palarini Schrottky, 1909 (Hymenoptera: Apoidea: Crabronidae). Proceedings of the California Academy of Sciences, Series 4, 59(8): 307-479

Acknowledgement

We are grateful to Dr Sarah Gess of the Department of Entomology and Arachnology, Albany Museum for the information supplied concerning these wasps.

The authors at work:

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Karin Sternberg

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Jenny Cullinan

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Dr Geoff Tribe