Tag Archives: aardvark

Far From Dead: The Surprising Biodiversity of Bare Ground

Occasionally, biodiversity might just be thriving beneath our feet.

Karin Sternberg

bare hard ground at sunset — The deflation hollow which is home to so much diversity

The resilient Karoo landscape

During my explorations of the Wolwekraal Nature Reserve, in the arid Karoo region of South Africa, a seemingly desolate stretch of land consistently caught my attention. This area, characterised by hard, ancient sediment, served as a shortcut from the jeep tracks to a wild colony of honeybees nesting in an aardvark (antbear) burrow. The flora surrounding this bare ground is a stark reminder of the Karoo’s remarkable resilience, showcasing a rich tapestry of species that thrive in one of the world’s extreme climates. Over centuries, the vegetation here has adapted to withstand dramatic temperature fluctuations, from severe winter frosts to scorching summer heat at times exceeding 50°C, often enduring prolonged periods of drought.

Yet, amid this tenacity, certain areas of the landscape remain barren and hardened. Recently, I buried a wild hare—a tragic victim of roadkill—in an aardvark dugout; a deep, empty cavity, in an area of hard ground I could never have dug myself. My sister, with her characteristic humour, had remarked, “Everyone needs an aardvark.” As I reflected on the hare’s untimely death, I was once again captivated by the number of solitary bees nesting in holes on the inner edges of these burrows. Like the wild honeybees in these landscapes, many species are dependent on the :aardvark for their nest sites; a reminder of nature’s interconnectedness. All around the dugout vibrant yellow swathes of Gazania lichtensteinii were in flower, their annual beauty enhanced by early winter rains.

Top row left to right, solitary bees living on the edge of this aardvark dugout: Samba female, Colletes female, and a Patellapis female.

Misconceptions of bare ground

The seemingly lifeless stretch of ground, a wind-scoured deflation hollow, was located close to this dugout. Deflation hollows form where vegetation is lost allowing wind to remove sandy topsoil and expose a hard subsoil comprising desert dust cemented with calcium carbonate. They are often associated with stone age human settlements of hunter-gatherers and herders. At this particular deflation hollow, there are various stone tools made from chert including a stone arrowhead. Standing on this hardened ground I was struck by a common misconception: that bare earth signifies death. Often dismissed in environmental assessments, this apparently barren, hard ground was, in fact, teeming with life and intrigue. Initially mistaking the sounds I was hearing for a drone congregation area – where honeybee males dart through the sky waiting for a queen – I quickly realised that the sound was emanating from the ground. A closer look revealed a fascinating gathering of male Tetraloniella cf. brevikeraia bees. These short-horned longhorn solitary bees were eagerly vying for a chance to mate with a female as she emerged from her underground nest. Although solitary by nature—females work alone in building nests and provisioning food—these bees form dense aggregations in favourable environments. The apparent barrenness of the ground belied its role as a prime breeding ground, and I counted an astonishing 114 nests in the vicinity.

The author documenting the diversity on the deflation hollow; it is so unassumingly rich in life (photo: Collette Hurt)

The evolutionary journey of bees

The evolutionary journey of bees, stretching back around 100 million years, began with solitary, predatory mud-dauber wasps, coinciding with the rise of flowering plants. Today, bees exhibit remarkable diversity, particularly in arid regions such as the Karoo where solitary species thrive. They range in size from a mere 2mm to 39mm and come in various forms, from densely hairy to smooth and shiny, often adorned with striking colours, masks, stripes and patterns. Most species of solitary bees prefer to nest in the ground, often using plant materials or resin to line their nests. On this hard bare ground, the thriving community of Tetraloniella served as a vivid testament to the vibrant life hidden beneath the surface.

Dynamics on the deflation hollow

The deflation hollow measured 24 m by 13 m, with nests concentrated in a mere twelve square meters. The spacing of the nests varied, with some holes nearly touching while others were separated by more than 20 cm. The solitary male bees, have one primary role: to mate. Males are remarkably specialised, with their entire existence revolving around this singular task. To prepare for mating in the earlier hours of the day with temperatures in the lower teens, the males press their bodies against the sun-warmed sand. In September, when daytime temperatures can reach 28°C, the ground can heat up to a hot 44°C. Males dart close to the surface in circular and zigzag patterns, seeking the radiated warmth that boosts their speed. I counted 26 males on this day, but their numbers waned with each subsequent day. I could only imagine how busy this aggregation had been at the beginning of mating season. Many of the males were covered in bright yellow gazania pollen from hasty sips of nectar essential for their energy needs.

A small section of the *Tetraloniella* nest aggregation

Top row: Shortly after 9 a.m., the first male Tetraloniella bees make their appearance on the deflation hollow, braving air temperatures below 15°C. Seeking warmth, they press their bodies against the sun-soaked sand, where ground temperatures already reach the mid-20s. Middle + bottom row: Males congregating around the nest holes, waiting for the females to emerge

Coexisting species: The diversity of life

In addition to the Tetraloniella bees, there were other bees thriving in this environment. Among them were various species of leafcutter, dauber and mason bees (Megachilidae) that make their nests in pre-existing burrows. Initially chased by the males, they started inspecting holes abandoned after the females emerged. These bees possess unique nesting techniques and have the broadest range of nesting behaviours. Unlike honeybees that collect pollen on their hind legs, the Megachilidae collect pollen on tufts of red hairs on the underside of their abdomen, known as a scopa. When this is fully packed with pollen it is a bright patch of colour.

Leafcutter bees construct thimble-like cells lined with leaves or petals to protect their young from moisture and predators. For their nests they were using both leaves of krimpsiektebos (Lessertia annularis) as well as gazania petals. Both of these plants contain extremely bitter compounds that possibly serve to deter parasites and provide beneficial antimicrobial properties. Another of the females (Hoplitis sp.) used chewed, reddish-pink plant pulp together with a mouth secretion to line her burrow. The source of the plant was not established but was similar in colour to bellbush (Hermannia grandiflora) flowering nearby. Similarly diverse are the materials used for plugging the entrances, with some bees choosing a combination of leaf pieces and mud, while others used mud and stones. The collected pollens for the provision of larvae with food came from plants distinct from those used for nesting materials, possibly from honeybush (Melobium candicans) or the brightfig (Rushia bijliae), both in flower and in range of the nest site and on which the bees were sighted. Each female completed one burrow per day.

Megachilid bees with their diverse nesting techniques, utilising burrows abandoned by Tetraloniella bees

Further careful study of the ground revealed a Camponotus rufopilosis (balbyter) ant carrying a dead conspecific. With mandibles featuring 5 to 7 teeth, these ants defend themselves by spraying formic acid when threatened. Amidst the male Tetraloniella bees, this ant dropped its prey and assumed a defensive stance. Larger, robust dauber bees (Megachile nasicornis) were also sighted, distinguished by their different, deeper sounds, and by their striking, singular patches of black and white coloration. They were also on the lookout for abandoned Tetraloniella nests to use for their own reproduction.

Balbyter ants (Camponotus rufopilosis) and the larger, more robust, dauber bees (Megachile nasicornis) on the deflation hollow

While documenting these interactions, a brown-and-white striped fly (probably in the genus Parisus) scraped her abdomen along the ground and then hovered above several bee nest holes. This Bombyliidae fly is known to parasitise a range of insects including bees. Hovering above a nest, the fly deposited 33 eggs in less than a minute. To lay eggs in this way, some Bombyliidae have a chamber near the ovipositor filled with sand which they stick to the egg, giving it enough weight to shoot deeper into the host nest and helping to prevent the egg from drying out too much. This observation might represent a new host record, and underscores the intricate relationships between host and parasite.

Top row left to right: A Bombyliid fly filling her ovipositor with sand granules, then hovering over a nest burrow to lay eggs. Bottom row left to right: A male Tetraloniella bee investigating the fly; the fly shooting an egg into the burrow (spot the egg!)

A climax

The climax of my observations came when a chaotic scrum formed around a single nest hole, where male bees gathered in a frenzied attempt to mate with the emerging virgin female. In this state where the males were fixated on the hole and seemed vulnerable to predation, I wondered if the female released a pheromone to signal her arrival. As mating commenced, the male produced a sound known as “piping,” a result of the vibrations created by the wing muscles. The male, mounted on the female, used his antennae to possibly release a volatile pheromone, engaging in a behaviour known as antennal fanning. He fans his antennae near hers without direct contact. Research indicates that a courtship pheromone may exist in bees, which is believed to induce receptiveness in the female. Clasped tightly to her, other males attempted to dislodge him, displaying a complex mating struggle. Uniquely, the female grasped a red stone during copulation, remaining mostly still amidst the chaos around her. After more than 3 minutes of mating the primary male was dislodged, and the female executed an intense spinning motion to escape, eventually flying off to establish a new nest elsewhere. (To watch the incredible mating video, click here.)

Top: A scrum of males around the hole where the female is about to emerge. Top right and middle: a tussle ensues as one male battles another for the opportunity to mate with the female. Bottom: the mating pair.

I was unable to establish the mode of excavation of the nests, or whether this species use pre-existing nest cavities as the Megachilidae do, though did note that no turrets or soil mounds were present. Similarly, I could not locate the males at night, though these are thought to form sleeping clusters hanging from a branch.

A rich tapestry of creatures

While at the study site, I encountered numerous other creatures. Among them were a rock agama, Namaqua sand lizards, cryptic Sphingonotis grasshoppers, beetles, robber flies (Asilidae), and a wingless female mutillid wasp (velvet ant). This ant-mimicking wasp was intriguing as she used her abdomen to push aside stones to enter the nest of a solitary bee—they are parasites of the larvae of ground-nesting bees. I also heard barking geckos and, with much patience, managed to photograph one in its burrow. Overhead many kinds of birds flew by, including two pale chanting goshawks. Beyond this deflation hollow, I discovered an extraordinary mud nest in the shallow of a stone; a Chalicodoma mason bee builds her nest in a hollow on a rock, sealed over by sand cemented with a secretion from her mouth.

The hidden life beneath our feet

This study illuminated a critical lesson: even the most unassuming, barren stretches of land may be far from lifeless. They may harbour intricate ecosystems, teeming with life that defies initial perceptions. The conservation of these natural nesting habitats is crucial for the survival of solitary bees and other species. Therefore, these often-overlooked spaces must be included in environmental impact assessments (EIAs). Bare ground is too rich in life to be dismissed; recognising such ecosystems is essential for maintaining biodiversity and ecological resilience, while still allowing for erosion control and restoration efforts such as reseeding rehabilitation and replanting on damaged lands or vacant erven as a means to enhance ecosystem health. Remember, biodiversity might be thriving unseen beneath our feet.

From top to bottom: Wingless female mutillid wasp (in contrast, the males can fly) entering a nest burrow of a solitary bee; Sphingonotis grasshopper and a frantic surface beetle; leafcutter bee and a pale chanting goshawk; Chalicodoma bee and a barking gecko

ACKNOWLEDGEMENTS:

Dr Sue Milton-Dean of Wolwekraal Nature Reserve

Dr Connal Eardley and Dr Michael Kuhlmann for their help with bee identifications

Dr John Mark Midgely for his assistance with fly identification and behaviour

Prof Ben-Erik van Wyk for his ID of Lessertia annularis and his extensive knowledge of plant compounds

Dr Geoff Tribe and Collette Hurt for their assistance with other species and stone artefacts

REFERENCES:

Batra, S.W.T (1984) Solitary Bees, Scientific American Vol. 250, No. 2, pp. 120-127. Scientific American, a division of Nature America, Inc., 8 pgs

Fuchs, M., Kandel, A.W., Conard, N.J., Walker, S.J. and Felix-Henningsen, P. (2008).

Geoarchaeological and Chronostratigraphical Investigations of Open-Air Sites in the Geelbek Dunes, South Africa. Geoarchaeology.

Gess, S.K. and Gess, F.W. (2014). Wasps and bees in southern Africa, SANBI Biodiversity Series 24.

Michener, C.D. (2007). The Bees of the World, The Johns Hopkins University Press.

Packer, L. (2023). Bees of the World. A Guide to Every Family, Princeton University Press.

Romani, R., Isidoro, N., Riolo, P., and Bin, F. (2003). Antennal glands in male bees: structures for sexual communication by pheromones? Apidologie 34 (2003) 603-610.

Skaife, S.H. (1963). Strange Adventures among the insects, National Boekhandel.

Slingsby, P. (2017). Ants of Southern Africa. The ant book for all, Slingsby Maps.

Honeybees and Gomphocarpus filiformis (lammerlat): A source of propolis in the Great Karoo

Karin Sternberg

Karoo landscape with Lammerlat (Gomphocarpus filiformis)

Wild honeybees and propolis

The wild honeybees of Southern Africa are renowned for their propensity in the use of propolis which enhances their survival in the wild. The vast amount of propolis collected and deposited in and around a wild colony attests to its value to the honeybees. But where do the bees collect the waxes, resins and plant exudates that form the basis of propolis, and in such large amounts? Individual honeybees are occasionally seen scraping waxes from buds of Protea species or resin oozing from a wound on the trunks of Vachellia karroo, but most sources of propolis are largely unknown. Although the topography and hence plant species composition may vary greatly between regions, the honeybees appear to have little difficulty in locating a source.

Recorded here is an observation of honeybees collecting the exudate from an oviposition puncture caused by a tephritid fruitfly whose larvae feed on the seeds of a plant widespread in the Karoo.

Extensive use of propolis in a wild honeybee nest — The extensive use of propolis in a wild honeybee nest.

Lammerlat (Gomphocarpus filiformis)

Gomphocarpus filiformis, a plant commonly known as lammerlat (an Afrikaans word, lammer = lambs, lat = stick, often used as a stick to chivy lambs when herding), is widespread across Namibia and the western arid interior of South Africa primarily in Desert, Nama-Karoo and Succulent Karoo habitats. Honeybees were first documented on lammerlat early in December 2023 at KRAAL, a garden in the Prince Albert municipality, where they were collecting resins on horn-like seed pods. The horns indicate that it belongs to the Asclepiadaceae into which family the stapeliads are prominent. There is a fruitfly species which lays its eggs in the stapelia pods where the fly larvae consume the seeds as they develop. A limited survey showed that 98% of the seeds on several Hoodia gordonii plants were entirely consumed (G. Tribe, unpub.). Was this happening on the horn-like seed pods of lammerlat?

Gomphocarpus filiformis (lammerlat), is found primarily in arid habitats.

A honeybee collecting resins on a seedpod of Gomphocarpus filiformis (lammerlat).

Adaptive significance of plant resins and cardiac glycosides in defense and medicinal contexts

Resins are a defensive mechanism of plants and have a physical function (expelling an organism or encasing it) and a chemical antibiotic function (especially for fungi but also insects). For especially mammalian predators, there are heart poisons called cardiac glycosides (also in Erythrina seeds), hydrogen cyanide, etc. Yet porcupines feed without consequence on a wide variety of poisonous bulbs that are deadly to other animals. Nomadic peoples eat locusts or saturniid caterpillars by first removing the guts for they may contain poisonous plant material. Fireflies make cardiac glycosides and they have evolved warning colouration. Toads also possess such compounds. In very small doses these cardiac glycosides may stimulate the heart and are thus used in the treatment of congestive heart failure and arrhythmia, but at higher doses can cause havoc and death.

When injured, lammerlat oozes a milky sap-like resin, a latex, as a defensive response against pathogens. This sap contains cardiac glycosides that are likewise toxic to herbivorous animals. But some insects, like the monarch butterfly and locusts, incorporate it as a defence mechanism and thus become toxic to their predators (S. Milton-Dean, pers. com., Dec. 2023). Thus a defence strategy evolved by a plant to avoid being eaten can be co-opted by another organism so that it too can avoid being eaten. Most early medicines used by humans involved the same principle in plant-based medication when taken at the correct dosage rate.

Honeybee collecting milkweed resins. — When injured, lammerlat oozes a milky sap-like resin. Here a honeybee is collecting the resins.

Defensive resin response of Lammerlat seed pods to Tephritid flies

When its seed pods are punctured, lammerlat immediately exudes a resin to seal the pod and protect the seeds within. The puncture is usually a sign that eggs have been laid by the tephritid fly. Seed pods were collected and examined. The larvae pupate in the pod after completing feeding. At Wolwekraal Nature Reserve (113ha) on the outskirts of Prince Albert are several populations of lammerlat where honeybees were immediately observed on the lammerlat collecting resin, but there were also milkweed bugs Spilostethos, muscid flies, and allodapine bees at various locations on the plant. The allodapines collected mostly nectar from the flowers together with a male Coelioxys kleptoparasite bee.

An Allodapine bee foraging on the lammerlat flower. — A male Coelioxys kleptoparasite bee.

Then a fly which initially looked very wasp-like was spotted on the seed pods. Sue Milton-Dean who offers guided walks on a trail through the nature reserve had studied tephritid flies in Pteronia seeds. One of the conclusions of this study was that flowering and number of seeds containing tephritid fly embryos, were positively correlated with annual rainfall. Sue had a keen eye for these flies. This tephritid fly which was later identified as most probably Dacus bistrigulatus, was laying an egg into the seed pods. We collected a number of seed pods with visible resin and later dissected them under a microscope. Inside each seed pod a larva was found which Sue recognised as a tephritid larva. In seed pods where all of the seeds had been eaten, the biggest mature larvae were found prior to pupation.

A tephritid fly laying an egg into the seed pod.

Tephritid fly larva consumes the seeds as it develops. — The fly larva consumes the seeds as it develops.

Role of resins in honeybee nest construction

The bees collecting the exudate possibly originated from the two wild honeybee nests located in aardvark burrows on the reserve. At these nests honeybees were seen preparing the surface of the burrow for the application of propolis, enabling the colony to either increase the number and/or length of combs, thereby expanding the size of the colony. Once the surface had been cleaned by worker bees, resins were brought in by the resin-collecting foragers to be used as a sealant. Many of the resins used within a honeybee nest are the main components in propolis. These resins often have beeswax added to it to be more pliable, but can also consist of pure plant exudates in outer structures where it adheres tightly to the substrate, even if the substrate is partly loose.

The resins of Vachellia karroo being collected by a resin-collecting honeybee.

Once the propolis is adhered to the substrate, comb building begins and the colony is able to expand to the outer edges of the adhered propolis. Elsewhere in the nest architecture, propolis may incorporate sand grains or plant material to strengthen it. Its thickness depends on where the propolis is being applied and its purpose. Resins play an important and essential role in honeybee nests, far beyond being a sealant. Being defensive chemical exudates of plants, propolis has many anti-bacterial and anti-fungal properties and is aromatic and health-giving with its essential oils. Lammerlat resin as propolis with its cardiac-glycosidic properties could perhaps be beneficial for honeybees in ways that are not yet known, possibly also as a defence mechanism against predators of honeybees, or ants, wax moth larvae and the like. An interesting aspect to consider would be whether the use of propolis for human consumption containing lammerlat resins could be toxic if taken in high doses.

Honeybees preparing the surface and applying resins in a cavity dwelling situated in an aardvark burrow.

In a second cavity situated in an aardvark burrow honeybees prepare surface soils and apply propolis with lammerlat resins. — Honeybees preparing the surface and applying resins in a cavity dwelling situated in an aardvark burrow.

Ecosystem dynamics of Lammerlat

Recently on one of Sue’s nature walks at Wolwekraal, both Rufous-eared warblers and the Karoo eremomelas were seen eating tephritid larvae on the lammerlat. It has also been found that the larvae of these flies are themselves parasitised by a small wasp. The ecological cycle around this arid shrubland species is both complex and remarkable.

A Rufous-eared warbler ((Malcorus pectoralis) photographed here on a Vachellia karroo tree.

SELECTED REFERENCES:

Bruyns, P.V. (2002). The Stapeliads of Southern Africa and Madagascar Volume 1 pg 57.Umdaus Press, 329 pgs
Ellis J.D. Jr and Hepburn, H.R. (2003). A note on mapping propolis deposits in Cape honeybee (Apis mellifera capensis) colonies. African Entomology 11(1): 122-124.
Ghisalberti, E.L. (1979) Propolis: A review. Bee World 60(2):59-84.
Iannuzzi, J. (1983). Propolis: The most mysterious hive element. American Bee Journal 123(8): 573-575.
Iannuzzi, J. (1983). Propolis: The most mysterious hive element Part II – Conclusion. American Bee Journal 123(9): 631-633.
Milton, S.J. (1995), Effects of rain, sheep and tephritid flies on seed production of two arid Karoo shrubs in South Africa, Journal of Applied Ecology 32, 137-144.
Tribe G.D., 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
Whiteman, N. (2023), Most Delicious Poison, Little, Brown Spark.

The Karoo is a tough place to be a bee!

Sue Dean and Karin Sternberg

Surviving the Karoo: resilience in a harsh environment

Being a bee on the Karoo plains is challenging. The Karoo is a boom and bust environment with short periods of spectacular productivity and long periods of drought and famine. Plants survive the droughts as seeds in the soil, or as long-lived small shrubs that are able to reduce their water needs to the minimum by discarding leaves, storing water and desisting from flowering and grow for months or years as need be. Nomadism is/was the preferred option for many birds and larger mammals, whereas many reptiles and invertebrates wait out the tough times in underground burrows reducing their activities to the minimum to save energy and water. Populations of small mammals follow boom and bust cycles in unison with the weather with numbers dwindling in drought and growing exponentially in the good times.

Honeybees as cavity dwellers

Honeybee colonies in more stable environments may persist for many years in hollow trees and cavities in rocks. On the Karoo plains there are no trees and rarely any rock cavities. Accommodation, in common with food supply, is ephemeral and honeybees need to be mobile and opportunistic. From the North African deserts comes the 2000 year old biblical tale of the bees that colonised a lion carcass¹. In the Karoo the deep dens and foraging excavations of aardvark offer a somewhat more hygienic place to build a nest – but underground accommodation is temporary and risky.

Beneath the surface: termites, aardvark and honeybees

Aardvark feed on Harvester Termites which build their nests 1-2 m below the soil surface. The long-snouted aardvark digs down to the nest and uses its sticky tongue to extract its food. Aardvarks eat a portion of the termite workers at night but seldom if ever wipe out the colony. The termites immediately start to repair the damage by filling the aardvark foraging hole with soil and their droppings. Aardvarks also dig deeper, wider burrows or dens in patches of deep soil and use these as a daytime retreat where they sleep. After a few months they move on to find a new source of food, and the abandoned den is quickly occupied by porcupines, bat eared foxes, mongooses, meercats, shell duck or honeybees.

The downsides of making a nest below ground in a termite colony are threefold: flooding during heavy rain, attacks by the termites wishing to reclaim their territory, and unwanted interest from potential predators of termites, particularly Aardvark, Bat-eared Fox, Yellow Mongoose and Meercat. Dealing with these challenges is time consuming and costly for bees. After flooding, the workers clean the mud out of their nest by carrying mudballs out one by one and dumping them above ground. Bees injured or killed by soldier termites need to be carried out of the nest by fellow workers, and unwanted visitors such as mongooses chased away. All this defence and maintenance work reduces the workforce and eats into the time needed to gather the nectar and pollen resources needed to build combs and grow the swarm.

This is probably why the small dark Cape Honey bee (Apis mellifera capensis) with its multiple false-queens, small colonies and mobile lifestyle is much better at exploiting patchy and unpredictable food resources in the Karoo than the larger and more productive yellow race² (Apis mellifera scutellata) from the summer rainfall region of southern Africa.

Camera trap footage from Wolwekraal Nature Reserve taken at the wild honeybee nest site:

Footnotes

Lyle’s Golden Syrup tin boasted the now famous logo depicting Samson’s ‘lion and the bees’ (from the Old Testament, Judges 14:8). It was registered as Lyle’s trademark. Just as the bees produce honey inside the lion’s carcass, rich sweet syrup pours forth from the well-loved tin. Apparently the subject was raised at a beekeeper’s meeting in Pretoria – asking why this should be so? One farmer answered that when animals were slaughtered on the farm, honeybees would come and collect the moisture from the carcass (G. Tribe, personal communication, October 25, 2023).
They are the same species, but from different geographical races of that same species. There are many such geographical races throughout the distribution of Apis mellifera that naturally inhabits Africa, much of Europe, and some of the Middle East.

The author at work:

Wild Bees

Field Notes on the Conservation of Wild Bees and their Natural Habitat in a Small Karoo Town in South Africa