A Drakensberg Crag Lizard (Pseudocordylis subviridis) licking nectar from the “Hidden Flowers” of Guthriea capensis in a terrarium

Little dragons with a sweet tooth pollinate the mysterious “Hidden Flower”

High up in the Maloti-Drakensberg World Heritage Site in South Africa, and unexpected visitor is changing ideas of what animals can be pollinators.

How do you attract pollinators, like bees and butterflies, if you have flowers? Almost 90% of flowering plants use bright colourful floral displays to attract their pollinators. The flowers of Guthriea capensis are different. G. capensis is the “Hidden Flower”. Just as their common name implies, the flowers are hidden at ground level, beneath the leaves of the plant. Also like the leaves, they are green. The flowers are, however, filled with nectar and strongly scented, which suggests that some animal does manage to find and pollinate the “Hidden Flowers”- but what is it?

Researchers from South Africa and the Netherlands, based at the Pollination Ecology Research Lab at the University of KwaZulu-Natal and the Afromontane Research Unit at the University of the Free State, think they have the answer. They have published their discovery in the journal Ecology. The team found staked out a group of “Hidden Flowers” in the Maloti-Drakensberg World Heritage Site in South Africa. After many fruitless hours of human observations, cameras triggered by motion-detectors finally revealed the identity of a shy and highly surprising pollinator. Drakensberg Crag Lizards pick up pollen on their snouts when they visit the flowers to lap nectar.

A Drakensberg Crag Lizard (<em>Pseudocordylis subviridis</em>) licking nectar from the “Hidden Flowers” of <em>Guthriea capensis</em> in a terrarium
A Drakensberg Crag Lizard (Pseudocordylis subviridis) licking nectar from the “Hidden Flowers” of Guthriea capensis in a terrarium (photo Ruth Cozien & Steve Johnson)

“‘Gobsmacked'” is probably the most appropriate word to describe us when we saw the first footage,” said Ruth Cozien, first author of the paper. We were aware lizards occasionally visit flowers on islands, and we knew that lizards are very abundant where Guthriea occurs. They both have a preference for rocky, high elevation habitats. We never put two and two together because it simply never occurred to us that a plant in continental Africa would be pollinated by lizards.”

Flowers like the “Hidden Flower” look like other flowers that use rodents and shrews as pollinators. Ruth Cozien said: “We had strong, preconceived ideas about what we were going to find, to the extent that, based on the expectation that most pollinator activity would be between dusk and dawn (when rodents and shrews are most active), we even initially set most of the motion-trigger cameras to record only during the night, to save battery power and storage space on memory cards which are often major limitations on data collection when working with motion trigger cameras in inaccessible sites. We won’t do that again!”

Lizards are not on the list of suspects, when botanists search for pollinators. Ruth Cozien explained: “Although it has been known for more than fifty years that some lizards do feed on flowers, they are still rarely considered as potential pollinators. Firstly, because they really are unlikely to be visiting flowers, and secondly because they are unlikely to be observed if they do visit! Lizards (like mice and shrews) may even actively avoid humans, so these interactions are really difficult to document. That the lizards have been found now, is down to affordable motion-sensitive cameras.

But using them still isn’t a simple task. Ruth Cozien said: “The first challenge with filming “hidden flowers” is pointing a camera at any flower at all. The flowers lie on the ground, and the line of sight is almost inevitably obscured by the leaves under which the flowers are hidden. To get an angle where flowers were visible, we had to position cameras below the plants. One way was to either by angle them upwards on very steep ground. This involved a lot of re-positioning of rocks at 2700m! Another way was by partly sinking the cameras into the ground.

“In theory that works to get the flowers in view. But you can’t be sure because both tricks make the viewfinder impossible to reach as it’s on the underside of the camera. Worse, you may obscure the motion sensor, which is critical to operate the camera!

“It turns out that to record activity at ground level, it is best to position your motion-trigger camera upside-down for recording in the field, and then use software afterwards to flip the footage back to right-side-up. But this advice does not come with the standard operating instructions!”

Once the team saw the lizards carrying off pollen, they made sure that the lizards really were pollinators. When lizards were experimentally excluded from plants, the number of seeds produced dropped dramatically, by almost 95% percent. Although flower visitation by lizards is not unknown, it occurs almost exclusively on oceanic islands, and the critical role of lizards for reproduction in G. capensis is virtually unprecedented.

Just how lizards find the “Hidden Flowers” is the next riddle to be solved. Most lizards are insectivorous. In the harsh environments of islands, deserts, and high mountains, they may develop a sweet tooth and supplement their insect diets with sips of nectar. Lizards can locate food using only odour, and chemical analysis of the scent produced by the “Hidden Flowers” identified compounds which are almost unique in the plant kingdom. It seems likely that these extraordinary scent chemicals are key to attracting the lizard pollinators.

Intriguingly, at close range, small orange glands are visible at the base of the inside of the flowers, and these glands bear a striking resemblance to the orange colour that male lizards develop in mating season to attract females. This similarity suggests that flowers may be using a colour that the reptiles recognise to enable them to locate the nectar. The unique combination of specialized lizard pollination in a continental setting provides exceptional opportunities for gaining insight into both the ecology of lizards and the function of unusual flower features.

This study shows while insects such as honey bees are for pollination, there are still many unknown and surprising interactions that also need to be conserved. If we want to ensure that plants like the mysterious “Hidden Flower” persist then we will need to make sure that visits continue from the little dragons with a sweet tooth.

Ruth Cozien

Ruth Cozien is interested in why and how the amazing variation among flowers arises, and in particular the role of adaptation to different pollinators in driving variation. Her PhD research focuses on variation in floral colour, morphology and nectar properties among populations of Hesperantha coccinea, a Drakensberg iris. She's investigating the roles of population genetics, riverscape geneflow, mating system, inbreeding depression and siring success in mediating divergence. She's also interested in functional differences among pollinators, as well as pollinator and plant distributions and community composition as proximate and ultimate drivers of pollinator-mediated divergence.

Alex Assiry

Alex Assiry is an editorial assistant in the Annals of Botany Office. When not working, Alex listens for the opportunity to help.

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