Pollination ecology and the functional significance of unusual floral traits in two South African stapeliads.

Abstract

Carrion and dung mimicking plants often exhibit unusual floral traits which are believed to attract necro- and coprophagous insects as pollinators. Our understanding of these unusual traits and their functions is very limited. Stapeliads (Apocynaceae: Asclepiadoideae: Stapeliinae) are a monophyletic group of some 400 species of stem-succulent plants, many of which emit foul odours and exhibit unusual morphological traits that have anecdotally been assumed to represent adaptations to enhance the flowers’ resemblance to carrion or dung. This study looked at the pollination biology of two stapeliads, Orbea variegata and Stapelia hirsuta var. hirsuta, and explored the functional significance of some of the floral traits commonly associated with carrion or dung mimicking flowers. Further, odours emitted by both species were compared to the odours of putative models to explore the chemical basis for the assumed mimicry. Orbea variegata attracted flies from the families Muscidae, Calliphoridae and Sarcophagidae (at sites near Scarborough and Clifton, Western Cape) and individuals from each of these families were found carrying pollinia. The scent of O. variegata flowers was found to be dominated by dimethyl disulphide, dimethyl trisulphide as well as phenol. The presence of both these compounds suggests mimicry of both carrion and dung, although an ANOSIM analysis indicated that the odour of O. variegata shared more similarities with dung. This suggests that O. variegata is fairly generalist and explains the attraction of various flies that are associated with carrion or faeces by the flowers of this species. In experiments testing the importance of black versus yellow colouring and the importance of patterning, flies were found to prefer black coloured models in the presence of O. variegata odour, whereas the presence and size of blotching on the corolla lobes had no significant effect on fly visits. The colours of the black blotching and yellow of the corolla lobes showed minimal chromatic contrast when interpreted using the Troje (1993) fly vision model, although background rocks showed chromatic contrast, suggesting flies can distinguish between the flowers and the background. In an experiment testing the importance of odour for attracting flies, significantly fewer flies were able to locate concealed flowers compared to visible flowers, suggesting an important role for visual cues for flies to locate the odour source. Stapelia hirsuta var. hirsuta was found to exhibit two floral colour morphs at Swellendam (Western Cape). The yellow morph was rarer than the maroon morph. These flowers attracted flies belonging to the Muscidae, Calliphoridae and Sarcophagidae families, although only Calliphoridae and Sarcophagidae were found to carry pollinia. The odour composition of these two morphs differed slightly, where the odour of the maroon morph was dominated by dimethyl disulphide, dimethyl trisulphide and p-cresol and the yellow morph was dominated by dimethyl disulphide, dimethyl trisulphide and limonene. The ANOSIM analysis of odours emitted by S. hirsuta var. hirsuta in relation to that of various fly oviposition substrates suggested that these flowers are dung mimics rather than carrion mimics, although the presence of sulphides suggests possible mimicry of both. The yellow morph had higher fly visitation rates than the maroon morph. In experiments testing the role of floral trichomes, the removal of floral trichomes significantly decreased the visitation rates to the flowers, as well as the amount of time visitors spend on the flowers. Again, visual cues were shown to be of importance, as visible flowers received more visits than concealed flowers. Analysis of colours of different floral morphs, using the Troje (1993) fly vision model, suggests that flies cannot perceive chromatic colour differences between morphs. In these studies, I have shown that O. variegata and S. hirsuta var. hirsuta are visited and pollinated by carrion associated flies, and the flowers emit odours associated with both carrion and dung. This work sheds light on some of the floral features that are often associated with carrion and dung mimicry by flowers and the roles they play in the attraction of flies.