By Geoff Tribe & A. David Marais

Of the three aardvark burrows found on the farm Zoethoek in the Succulent Karoo north-east of Touwsrivier, two were inhabited by honeybees and the third was still in use by an aardvark. In contrast, none of the 17 aardvark holes inspected recently in mountain fynbos vegetation on Aurora Mountain above the town of the same name (32° 41’ 04’’S 18° 32’ 10’’E) contained honeybee nests. This is because the topography, vegetation and climatic conditions of the two sites differ greatly.

Autumn foraging by the aardvark colony

The honeybee nest in the aardvark hole on the plateau was first discovered in May 2013 (Fig. 1a). Exposed combs could easily be seen near the bottom of the burrow (Fig.1b). On a subsequent visit in January 2015, the combs were completely covered with bees and the swarm was actively foraging (Fig.2). The nest was inspected again on the 26^th of April 2015. In the interim a propolis wall had been built in front of the combs (Fig. 3). As a result of 20mm of rain having fallen four weeks previously, the bees were actively foraging and white pollen was being brought to the nest – the origin of which was never discovered.

The driest period of the year in the Succulent Karoo is from January through February into March when the number of plants in flower is minimal and accessible water is hard to find. Although Hessea stellaris (Fig. 4), Ornithoglossum undulatum (Fig. 5), and an Oxalis species were in flower, no honeybees were seen to visit them.

Honeybees were soon attracted to water from a tap which was allowed to drip continuously near the shearing shed about a kilometre away (Fig. 6a). Presumably the odours released from the patch of soil dampened by the water indicated its presence to the bees. The fighting amongst the bees indicated that they were from at least two colonies (Fig. 6b); the attacked bees being vastly in the minority.

Carrion flowers and their deceptions

Honeybees however, were not involved in the pollination of five plant species of the carrion flower group which were in flower. Belonging to the Stapelieae, their flowers release foetid odours which mimic their oviposition substrates and thus attract flies for pollination. The most important pollinators of stapeliads belong mainly in the Calliphoridae (blowflies), Sarcophagidae (flesh flies) or Muscidae (houseflies). It is interesting to note that these succulent plants that extend from this semi-arid region into very arid regions, evolved to attract the ubiquitous flies that may be more prevalent than bees in such barren areas. Unlike bees which sense light better in the ultraviolet region, these flowers are a deep red that may be mistaken for meat by flies. The presence of fur-like projections on some flowers such as Stapelia hirsuta (Fig. 7a) may further imitate the appearance of a wounded or dead animal. Some of these flowers may even have yellow or white markings that further improves the resemblance by suggesting fat. In this way, Huernia zebrina (Fig. 7b) attracts blowflies. Flies which breed in dung invariably lay their eggs in clumps in crevices in the dung from which white larvae hatch. Stapelia glanduliflora (Fig. 7c) for instance, has its flowers fringed by vibratile white cilia which move in the slightest breeze and are thought to resemble that of fly maggots. Flies are believed to be attracted to this movement as they are gregarious when depositing eggs. In especially Stapelia species the flies are so deceived that they lay their eggs on the flower, only to have them predated by ants. The flies are attracted by both the appropriate colouration of the plant and the odour which act in concert, the odour profiles being species specific and independent of generic affiliation (Jὔrgens et al. 2006).

Intricate pollination mechanism

All these features may be attractive to flies but the final conviction comes with the odour the plants emit. The chemicals in these odours are not unique to the Stapelieae: they have been identified in some malodorous arums and orchids. Chemical analyses have even shown that there are different blends that conform to odours from cadavers, carnivorous faeces, herbivorous dung and urine. Bees would not be attracted to these flowers but flies are. There may be some selection according to their detection of the chemicals and the structural features of the plant. Only the right size of insect will successfully collect and transfer the pollen because a certain amount of force is needed to remove the pollinarium (Meve & Liede 1994). Probably the results of a low insect count, these plants, in a similar fashion to orchids, place their 200-300 pollen grains in a sac (pollinium). Two such sacs are connected to a central node to form the pollinarium with the two thin rods forming an inverted V-shape. The fly, exploring the flower towards the ‘nectar’ opening, is deployed as the vector for pollination when its proboscis or other part of its anatomy dislodges the sticky pollinarium. The fly may even have been fooled in laying eggs on the flower with the maggots having no hope of maturing. The pollinarium is carried to the next flower where it is detached in specialized grooves as the fly once again probes for liquid at the nectar opening.

Stapeliads in flower on Zoethoek

The five species in flower (i.e. Quaqua acutiloba, Quaqua mammillaris, Huernia barbata, Piaranthus parvulus, and Stapelia surrecta identified by Dr Peter Bruyns) have relatively inconspicuous flowers and only mild odours within this family of large and colourful flowers (Figs 8.a-e).

One species on the farm, but not in flower at the time of this visit, does have a strong carrion odour: Hoodia gordonii (Fig. 9) whose attractant consists of 94 compounds (Jὔrgens et al. 2006) which presumably have the potential of attracting a variety of fly species.

Though quite spiny, it had been partly consumed by porcupines (Fig.10); presumably because there was little else on which to forage. The Quaqua mammillaris had been partly consumed by baboons which rejected many portions as they too are spiny. Baboons and porcupines appear to have a special liking for the roots of Euphorbia rhombifolia (Fig. 11) which is dug out and consumed over the entire farm.

Ecology of stapeliads

The ecology of the stapeliads is also interesting. After the pollinarium is lodged on the complex central structure of the flower, two seed pods are produced. These eventually dry and split open to reveal small brown to black seeds that are attached to a very fine parachute. The seeds are released and dispersed by wind. The heat generated on the soil surface during the day (where temperatures of 41°C have been recorded) results in strong winds at night. These seeds are blown up against the bases of spiny Ruschia paucifolia bushes together with other debris. Here, in response to rain they germinate within the debris and grow within these spiny bushes which protect them from predators. When conditions, typically in late summer along with some rain, are favourable, these plants flower. Owing to their growth under bushes or in crevices, they need to attract their pollinators. The (mal)odour may not be sensed by flies from afar but the flower may be seen. The Quaqua mammillaris is a larger plant and bears its flowers directly on the fleshy and spiny stems on which the pollinator can see them. The Stapelia surrecta makes its flower visible by placing it on a long pedicle that projects beyond the canopy of the bush.

Migration of animals

Stapeliads are in synchrony with their environment. They respond to sufficient rainfall by flowering from 3 to 4 weeks later. When animals could still migrate in days of old, herds of antelope would follow the rain and the fresh grazing that it produced. No doubt this would support the growth of flies and the mimicry of the smell of dung would be useful for the pollination of the carrion flowers. The phenomenon of a migrating herd was described by George Mossop in 1877 in his book “Running the Gauntlet” on the Transvaal Highveld near the present day town of Davel. One day while out hunting with an elderly Boer by the name of ‘Ghert Visajie’, Mossop saw many thousands of game on the plain. They suddenly began to trot in opposite directions, leaving an open lane of two miles wide as far as the eye could see. He then heard the distant low rumblings of what appeared to be thunder although it was a perfectly clear day. ‘Visajie’ shouted a warning and spurred his horse up the side of a kopje (hillock) where they watched a huge cloud of dust, about two miles wide, rushing towards them. This great cloud of dust came rushing up with the thunder of hoofs making the earth tremble. Then a line of wildebeest came into view, followed by a mass of game of all kinds which took an hour and a half to pass. ‘Visajie’ explained that their grass had been grazed to the ground and now they were moving on to where it had rained in the distance. The game in possession of the grazing made the lane open for them to pass through to new grazing lands further on. This phenomenon would be repeated again and again, with those now in possession of grazing eventually becoming the migrating herd and being let through by the other herd until an annual circle had brought them back again.

Chemicals used in attraction

With such animals are the constant hoards of flies of various species which pester them. The antelope in turn are trailed by predators, especially lions, which follow in their wake. These flies may be biting flies which feed on the blood of their mammalian hosts; feeding on the liquids such as around their host’s eyes or sweat; on the carcasses of the prey brought down by predators; or those flies which breed in the dung of the various mammalian species. The chemical nature of the odours which attract flies consist of oligosulphides (which mimic carrion) and phenol, indole and p-cresol (which mimic faeces). The stapelia attractants can be divided into four groups – those that mimic herbivore faeces (high in p-cresol content but low amounts of polysulphides); carnivore/omnivore faeces or carcass (high polysulphides but low amounts of p-cresol); carnivore/omnivore (high amounts of heptanal + octanal); and urine (hexanoic acid) (Jὔrgens et al. 2006). At this time, several weeks after the rain has fallen, as the animals migrate through the now green region, the stapeliads are in flower and they virtually ‘borrow’ these flies for pollination. Only flies are attracted, for despite the huge diversity and abundance of dung beetle species in southern Africa whose primary attraction is to dung (Tribe and Burger 2011), they are not attracted to stapeliad flowers.

Two divergent pollination systems

Within this Succulent Karoo there are thus two entirely divergent systems at play involving specialized pollinators with completely different attractants – that of a scented flower with a reward of sweet nectar and the other of foul smelling carrion. In the former system there appears to be mutualism in that the flowering plants and the pollinator benefit from each other. Honeybees have a well-developed communication system which is able to immediately recruit large numbers of foragers to a transient nectar source unlike that of flies. In the case of the carrion flowers, the flies are exploited – there is no benefit to the flies and their survival clearly depends on other factors but is nevertheless essential for the carrion flowers. Stapeliad flowers are considered as deceptive flowers because they defraud the flies while imitating a substrate for oviposition (Meve & Liede 1994). The ecology of both categories of pollinators is intricately linked to their environment which determines their behaviour in all respects.

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!

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

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.