PlantLife Volume 50.7 December 2020. Aloe pretoriensis

 

Aloe pretoriensis at Skuilkrans Kopje Nature Reserve - its pollinators and predators

Text by Glynis Cron, photos by Glynis Cron, Kaylee van den Bosch and Cynthia Shibanda

 

Skuilkrans Kopje Nature Reserve is an ‘island’ in the midst of suburbia on one of the rocky outcrops in Pretoria East, Gauteng (https://sites.google.com/site/friendsofskuilkrans/home/). This 9 hectare reserve harbours a wealth of indigenous flora – including Protea caffra, Combretum molle, Searsia lancea, Helichrysum kraussii, and Afrocanthium gilfillanii. The vegetation type is best described as ‘Mountain Bushveld’ (Mucina & Rutherford, 2006) and the reserve serves to preserve this small habitat fragment for both local flora and fauna. On the southwest-facing ridges of the kopje, amongst the rocks, grows the elegant Aloe pretoriensis, named for the city of Pretoria. Increasing urbanisation over the last century has resulted in a drastic decline in its population, with only 10% of its original range in Pretoria and the surrounding region now occupied by A. pretoriensis. Fortunately, the aloe has a wider distribution across the northern regions of South Africa, in Limpopo and Mpumalanga, where it is not yet threatened by loss of habitat. The species is not endemic to South Africa and is also found in Swaziland, along the Lebombo Mountains, as well as in north-eastern Zimbabwe.

 

Figure 1. Aloe pretoriensis at Skuilkrans Kopje Nature Reserve, Pretoria East

The slender, pointed leaves of Aloe pretoriensis are a light bluish-green colour, usually with red tips and a pale, yellow leaf sap. The leaf rosette gives rise to a tall branching inflorescence that can grow to 3 m high. Like many of the aloes in the South African Highveld, Aloe pretoriensis is winter-flowering—its bright red (rarely red-orange), tubular flowers visible between May and June. The aloe flowers provide not only colour to an otherwise somewhat dreary, brown landscape but also valuable resources to both birds and insects in the form of nectar and/or pollen. Most winter-flowering aloes are bird-pollinated, either by specialist nectarivores (like sunbirds that feed only on nectar), or generalist omnivores (such as bulbuls, weavers and mousebirds) that feed on nectar when it is available but have a diverse diet. Flowers pollinated primarily by generalists have large amounts (40 −100 μL) of very dilute nectar (8−12% w/w sugar with 0−5% sucrose of total sugar) per flower, whereas smaller amounts (about 10−30 μL) of concentrated hexose-rich nectar (15−25% w/w with 40−60% sucrose) attract the specialist pollinators (Johnson & Nicolson, 2008). Despite birds being the main pollinators of winter-flowering aloes, insects (notably honeybees) have also been shown to contribute substantially to pollination and fruit set in some, for example, the small, spotted Highveld aloe, A. greatheadii var. davyana (Human & Nicolson, 2008).

 

Figure 2  - Aloe pretoriensis

Figure 3 – Aloe pretoriensis – a single raceme

In 2016, research into the relative effectiveness of birds and insects (mainly bees) as pollinators of Aloe pretoriensis was carried out at Skuilkrans Kopje Nature Reserve by Honours student Cynthia Shibanda, at the University of the Witwatersrand. In addition, the effect of inflorescence size (height/length and number of branches) on frequency of bird visitation was investigated—the expectation being that the larger, more showy inflorescences would attract more visits and therefore have a greater pollination success rate (in terms of fruit set relative to number of flowers produced).

Direct observations and camera traps revealed that only specialist nectarivores visited Aloe pretoriensis flowers—mainly the Amethyst sunbird (Chalcomitra amethystina) and less frequently, the White-bellied sunbird (Cinnyris talatala).  A territorial male Amethyst sunbird ensured that most of the time only he and female Amethyst sunbirds had access to this treasure-trove of aloe nectar. The relatively small amounts of nectar produced (7–28 μL) and its high sucrose concentration (11.5–25% w/w) reflected this specialist nectarivore pollinator syndrome. The length of the inflorescence and the number of branches both very strongly influenced the number of avian visitors per hour to the aloe plants—the aloe with the largest inflorescence had three times as many visits per hour (on average) than the smallest one.

 

Figure 4: Camera trap photographs of sunbirds feeding on Aloe pretoriensis nectar: A: Male White-bellied sunbird; B: Male Amethyst sunbird.

 

The exclusion trials set up to assess the relative contributions of birds versus bees (using Tremnet cages preventing bird-access to the flowers) revealed that both birds and bees play an important role in pollinating Aloe pretoriensis. Average fruit set for the open treatments (i.e. both birds and bees could visit the aloe flowers) was 15–20% greater than when birds were excluded (i.e. only insects could access the aloe flowers). The main insect visitors pollinating the aloe flowers were honeybees, although small wasps and solitary bees were also observed to visit the flowers (but not necessarily for nectar or pollen and therefore unlikely to be pollinators). Thus bees are very effective pollinators of Aloe pretoriensis, with specialist nectarivores, the sunbirds, enhancing fruit production. It is quite likely that the territorial male Amethyst sunbird, by limiting access by other sunbird species and conspecific males, reduced the effectiveness of the bird pollinators on fruit set in this aloe.

 

Figure 5: Exclosure around Aloe pretoriensis prevents birds from accessing the inflorescences.

The reason for the small wasps observed visiting the aloe’s flowers was revealed when Cynthia noticed holes in the aloe seeds and photographed a tiny wasp (later identified as Eurytoma aloineae) emerging from one of them. In a follow-up study, Kaylee van den Bosch (also an Honours student at the time) found that six wasp species and a fruit fly (Apenthecia sp.) were developing within the aloe’s fruit or seeds. Very little was known about predation and parasitism of aloe fruits and seeds until Kaylee’s study. The only mention in the literature was of the wasp Eurytoma aloineae having been found when seeds of seven aloes (Aloe africana, A. ferox, A. globuligemma, A. lineata, A. microstigma, A. striata and A. variegata) were shipped to the United States of America. The wasps were found to have emerged from the seeds when they arrived (Burks, 1958). Prinsloo (1980) also recorded this same wasp predating seeds of Aloe ferox. Thus, five of the six wasp species that emerged from seeds and fruit of Aloe pretoriensis were associated with utilisation of aloe fruits and/or seeds for the first time (Van den Bosch et al., 2019).

 

Figure 6: The tiny wasp Eurytoma aloinae emerging from Aloe pretoriensis seed – as seen under a dissecting microscope. Photo credit: C. Shibanda.

 

Figure 7: Insect larva inside fruit of Aloe pretoriensis (as viewed under a dissecting microscope) – note the absence of seeds which have been eaten. Photo credit: K. van den Bosch.

On average, 29% of the fruit sample from this population of Aloe pretoriensis was used by the wasps and/or fruit flies (range 7–68% per plant ) and an average 21% of the seeds were predated on (range 0–51% per plant). Considering that each fruit produced about 23 seeds, insect phytophages and seed predators can impact the reproductive output of aloes quite significantly (Van den Bosch et al. 2019). Subsequent studies on Aloe petricola and Aloe reitzii (Payne et al. 2019), as well as Aloe lettyae (Kremer-Köhne et al. 2020), have also shown extensive utilisation of their fruit and seed by insect phytophages and parasitoids feeding on the phytophages.

The importance of aloes in supporting local fauna (birds and insects) is thus clear—in the form of nectar and pollen for birds and bees but also as a brood-place for wasps and fruit flies in aloe fruit and seeds. Similarly, the important role played by a protected reserve in the middle of an urban landscape in conserving the local flora and fauna should not be underestimated—as revealed by our studies on Aloe pretoriensis at Skuilkrans Kopje Nature Reserve in Pretoria East, Gauteng.

 

Acknowledgments

Our thanks extend to the NRF for funding towards these projects, Adelene Marais (Tshwane Nature Conservation) and Friends of the Skuilkrans Kopje (FoSK) for permission to conduct these two studies on Aloe pretoriensis at the Skuilkrans Kopje Nature Reserve, to Trempak Company for their generous donation of the enclosure netting, and to Dr Simon van Noort (Iziko Museum, Cape Town) for his assistance with wasp identifications.

  

References/Further reading:

Burks, B.D. 1958. A new Bruchophagus from a liliaceous plant with a host plant list for the genus (Hymenoptera, Eurytomidae). Proceedings of the Entomological Society of Washington 59: 273–277.

Human, H. and Nicolson, S.W. 2008. Flower structure and nectar availability in Aloe greatheadii var. davyana: an evaluation of a winter nectar source for honeybees. International Journal of Plant Sciences 169: 263–269.

Johnson, S.D., and Nicolson, S.W. 2008. Evolutionary associations between nectar properties and specificity in bird pollination systems. Biology Letters 4: 49–52.

Kremer-Köhne, S., Harrison, J du G.,Thompson, D.I. & Witkowski, E.T.F. 2020. Arthropods associated with Aloe lettyae, an endangered South African Woodbush Granite Grassland plant endemic. African Entomology 28: 8–18.

Payne, S.L. 2019. Aloe pollination: Floral visitors, reproductive output and gender expression. Unpublished PhD Thesis, University of the Witwatersrand, Johannesburg, South Africa.

Prinsloo, I.G.L. 1980. Annotated records of economically important Chalcidoidea (Hymenoptera) from South Africa. Phytophylactica, 12: 159–163.

Shibanda, C. 2016. The birds versus the bees – the role of pollinators in seed formation in Aloe pretoriensis. Unpublished Honours Research Report, University of the Witwatersrand.

Van den Bosch, K. 2017. Parasitism of Aloe pretoriensis and the effect on fruit and seed production. Unpublished Honours Research Report, University of the Witwatersrand.

Van den Bosch, K., van Noort, S. and Cron, G.V. 2019. Predation of fruit and seed of Aloe pretoriensis – A little known effect on reproductive output in aloes. Austral Ecology 44: 621–634.

 

About the authors: Glynis Cron is an associate professor in the School of Animal, Plant & Environmental Sciences at the University of the Witwatersrand. Her interests include plant systematics and biogeography, patterns and drivers of speciation (especially in the Drakensberg region) and the reproductive ecology of a variety of species, including aloes. Kaylee van den Bosch is an MSc student currently working on the reproductive ecology of the pepperbark tree. Her Honours study looked at fruit and seed predation of Aloe pretoriensis, following a study by then Honours student Cynthia Shibanda on the breeding system and pollinators of this aloe species.