Some Recent Fun publications

Our publications page has recently been updated! Whilst 2020 and 2021 was a strange year for all of us field biologists, it meant that many scientists holed up and spent the time in lockdown to write. Here are just five abstracts and cool pictures from our 2021 publications.

Sexual deception of a beetle pollinator through floral mimicry. Sexual mimicry is a complex multimodal strategy used by some plants to lure insects to flowers for pollination. It is notable for being highly species-specific and is typically mediated by volatiles belonging to a restricted set of chemical compound classes. Well-documented cases involve exploitation of bees and wasps (Hymenoptera) and flies (Diptera). Although beetles (Coleoptera) are the largest insect order and are well known as pollinators of both early and modern plants, it has been unclear whether they are sexually deceived by plants during flower visits. Here we report the discovery of an unambiguous case of sexual deception of a beetle: male longhorn beetles (Chorothyse hessei, Cerambycidae) pollinate the elaborate insectiform flowers of a rare southern African orchid (Disa forficaria), while exhibiting copulatory behavior including biting the antennae-like petals, curving the abdomen into the hairy lip cleft, and ejaculating sperm. The beetles are strongly attracted by (16S,9Z)-16-ethyl hexadec-9-enolide, a novel macrolide that we isolated from the floral scent. Structure-activity studies confirmed that chirality and other aspects of the structural geometry of the macrolide are critical for the attraction of the male beetles. These results demonstrate a new biological function for plant macrolides and confirm that beetles can be exploited through sexual deception to serve as pollinators.

The functional ecology of bat pollination in the African sausage tree Kigelia africana (Bignoniaceae). Plants often interact with a wide range of animal floral visitors that can vary in their pollination effectiveness. Flowers of the African sausage tree Kigelia africana are visited by bats and bush babies during the night and by birds during the day. We studied
floral traits (phenophases, scent, color, and nectar chemistry) and the visitation frequency and pollination effectiveness of different flower visitors to determine whether K. africana is functionally specialized for bat pollination. We found that flower opening corresponds with bat activity, flowers emit scent dominated by aliphatic esters and alcohols, and that nectar is produced in copious amounts accessible to bats. Pollen deposition on stigmas was twenty-fold greater per visit by bats than it was per visit by birds, likely a result of the close morphological fit between snouts of bats and the flowers. However, bat visits appear to be rare at some sites and the delayed senescence of flowers that are open throughout the morning provides an opportunity for additional pollination by birds. We conclude that K. africana is primarily adapted for bat pollination, but is also able to exploit other animals for pollination.

Fly Pollination of Kettle Trap Flowers of Riocreuxia torulosa (Ceropegieae-Anisotominae): A Generalized System of Floral Deception. Elaborated kettle trap flowers to temporarily detain pollinators evolved independently in several angiosperm lineages. Intensive research on species of Aristolochia and Ceropegia recently illuminated how these specialized trap flowers attract particular pollinators through chemical deception. Morphologically similar trap flowers evolved in Riocreuxia; however, no data about floral rewards, pollinators, and chemical ecology were available for this plant group. Here we provide data on pollination ecology and floral chemistry of R. torulosa. Specifically, we determined flower visitors and pollinators, assessed pollen transfer efficiency, and analysed floral scent chemistry. R. torulosa flowers are myiophilous and predominantly pollinated by Nematocera. Pollinating Diptera included, in order of decreasing abundance, male and female Sciaridae, Ceratopogonidae, Scatopsidae, Chloropidae, and Phoridae. Approximately 16% of pollen removed from flowers was successfully exported to conspecific stigmas. The flowers emitted mainly ubiquitous terpenoids, most abundantly linalool, furanoid (Z)-linalool oxide, and (E)-β-ocimene—compounds typical of rewarding flowers and fruits. R. torulosa can be considered to use generalized food (and possibly also brood-site) deception to lure small nematocerous Diptera into their flowers. These results suggest that R. torulosa has a less specific pollination system than previously reported for other kettle trap flowers but is nevertheless specialized at the level of Diptera suborder Nematocera.

A shift in long-proboscid fly pollinators and floral tube length among populations of Erica junonia (Ericaceae). Macroevolutionary studies frequently emphasize the importance of pollinator shifts for driving speciation within the angiosperms. Pollinators have been identified as a driver of diversification in the mega-diverse genus Erica in the Cape Floristic Region of South Africa, but basic information on pollinator-driven divergence at the initial stages of speciation in this genus is lacking. We focus on two populations of Erica junonia (var. junonia and var. minor) that occur on adjacent mountain ranges separated by c. 10 km and which differ in floral tube length, and ask whether these differences in tube length are associated with a shift between pollinators with different proboscis lengths. In addition, we assess whether the two forms differ in their ability to reproduce in the absence of pollinators. Our findings show that different Erica junonia varieties are visited by different nemestrinid fly species in the genus Moegistorhynchus, and that their floral tube lengths correspond to the proboscis lengths of these flies. Pollinator exclusion experiments show that the short-tubed var. minor is capable of producing seeds in the absence of pollinators, whereas the long-tubed var. junonia depends fully on pollinators. Our study provides an example of pollinator-driven divergence on a small spatial scale and contributes to an understanding of diversification of the genus Erica.

Pollinator Community Predicts Trait Matching between Oil-Producing Flowers and a Guild of Oil-Collecting Bees. The impact of pollinator community diversity on trait matching in plant-pollinator interactions is poorly studied, even though many mutualisms involve multiple interaction partners. We studied 10 communities in which one to three species of oil-collecting Rediviva bees pollinate the long-spurred, oil-producing flowers of Diascia “floribunda” to examine how pollinator diversity affects covariation of functional traits across sites and trait matching within sites. Floral spur length was significantly correlated with weighted grand mean foreleg length of the local bee community but not with foreleg length of individual bee species. The closeness of trait matching varied among populations and was inversely related to pollinator community diversity. For all bee species, trait matching was closest at sites characterized by exclusive pairwise interactions. Reduced trait matching associated with increased community diversity for individual pollinator species but close matching at the community level supports the importance of community context for shaping interacting traits of flowers and pollinators.

And they strike again! Power team Anne and David rediscover Ceropegia rudatisii

Once again, we owe congratulations to power team Anne and David! In the previous lab blog post we presented the amazing discovery of a new Ceropegia species, C. heidukiae, by Dr Annemarie Heiduk and David Styles. Now they have surprised us again with the incredible rediscovery of C. rudatisii, a Ceropegia species which, having not been seen in 100 years, was believed to be extinct. And it even turned out to be the sister species to the newly discovered C. heidukiae. Below, Anne describes how her and David’s combined determination to rediscover this long-lost KwaZulu-Natal endemic Ceropegia led to the ultimate success:

In November 1903, the amateur botanist Walter Jaqcues Haygarth collected an unknown, but remarkable Ceropegia in Hillcrest, inland from Durban. Without much further attention, the specimen was deposited at the Durban Herbarium. Two years later, the same species was collected a little further south near Dumisa by August Gottlieb Hans Rudatis, a German botanist born in Berlin. Rudatis’ collection was sent to Friedrich Richard Rudolf Schlechter, the curator of the Berlin Botanical Museum. Unaware of Haygarth’s previous collection, Schlechter named it C. rudatisii in honour of Rudatis, whom he assumed to be the discoverer. Although a handful of collections were made subsequently, there seemed to be no more observations after 1916.

When looking at herbarium sheets and photographs of other Ceropegia rudatisii collections, I felt the excitement that Haygarth and Rudatis must have experienced on their encounters. C. rudatisii had been assessed as Critically Endangered and Possibly Extinct under IUCN red list criteria, and I wondered if after more than 100 years it was possible to find it again. I also pondered about the corolla lobes which were mounted erect in flowers of the pressed herbarium specimens; somehow, I knew that in a live plant they would instead be dangling from the throat of the tubular corolla, flying in the wind like five little flags.

But it was actually David who drew my attention to this species in particular. David had looked for C. rudatisii years previously and was interested in resuming the search. He has an exceptional knowledge and intuition on suitable habitats for many plant species and identified several localities at which C. rudatisii might yet be found. When we went out to search for it together, we knew the odds were against us. During the hours of driving, we joked about who would spot the first plant.

At one locality we split up to cover more ground and, lucky for me, my direction was the right one. When I first spotted it, I could not believe it. I was still in seventh heaven after my recent discovery of C. heidukiae, and there it was right in front of me. It was not in flower, but I knew that this was the long-lost C. rudatisii. What a magic moment! It took a while for David to arrive at the spot as he was already quite a distance away, but he could also hardly believe it. I do remember him exclaiming: “One can’t take you anywhere, you just keep on finding things!” From that day on I had the nickname ‘Eagle Eyes’. When we at a later stage saw it in flower, I was so excited to see the pendulous corolla lobe tips waving in the wind; I had been right.

Unfortunately, the very small populations of Ceropegia rudatisii only occur in remnants of former habitat where they are severely threatened. KwaZulu-Natal Sandstone Sourveld, the vegetation type in which it occurs, is also Critically Endangered. Due to the paucity of flowering and fruiting material, it took much effort and time to gather enough information for a redescription. But now that this has been achieved, the amazing Ceropegia redatisii, sister species to the recently described C. heidukiae, has been beautifully illustrated and meticulously described.

Text: Annemarie Heiduk and Hannah Butler.

Photos: Annemarie Heiduk.

Article: https://www.biotaxa.org/Phytotaxa/article/view/phytotaxa.498.2.5

Ceropegia heidukiae — a morphologically intriguing and rare novelty from South Africa

Discovering a new species and having a species named after you has been the pursuit of many plant hunters and scientists over the centuries, and if all botanists’ dreams could come true, we would all have a story like this one. We offer our endless congratulations and jealous thoughts to lab members, Dr Annemarie Heiduk and David Styles, on their discovery and description of the morphologically intriguing and rare novelty, Ceropegia heidukiae.

The happy plant, Ceropegia heidukiae.

Ceropegia species (Apocynaceae-Asclepiadoideae) are world-famous for their sophisticated and functionally complex flowers, with five petals fused into a tubular structure which functions as a pitfall for pollinating flies. South Africa is one of the centres of diversity for this genus of plants, but only six new species have been described since the 1980s. Now, a new species and a real gem for South Africa has been discovered by our very own lab members, Dr Annemarie Heiduk and David Styles and is even named after Anne.

Anne joined our lab as a postdoc in 2018 and has been studying the chemical ecology and pollination biology of Ceropegia and related plants for more than 12 years. Her research has made a significant contribution to our understanding of the deceptive pollination strategies in these functionally specialized fly-pollinated plants. In fact, many of us consider her to be the world expert on Ceropegia pollination and scent chemistry!

David joined our lab as a PhD candidate in 2019. He is a well-renowned botanist with much experience and exceptional knowledge on the flora of South Africa, and in particular within KwaZulu-Natal. His fascination for Sisyranthus, a small South African genus closely related to Ceropegia, has driven him to pursue a PhD. He has discovered and described a number of plant species already, some of which bear his name. Thanks to David’s knowledge, the description of Ceropegia heidukiae includes detailed information on vegetation types, habitat and ecology. And thanks to his amazing photography skills, the astonishing beauty of this novel species is wonderfully captured.

The happy scientists, Dr Annemarie Heiduk and David Styles.

One can either find Anne spending a considerable amount of time tinkering with flies and scent chemicals in the lab, or in the field studying the plants in their natural habitat. To spot the many tiny and often inconspicuous Asclepes she works on, she has developed an excellent eye for spotting them. But, of course, it never once crossed her mind that she would find a new species! This completely unexpected discovery may be what can be considered one of the most beautiful Ceropegia species known in South Africa (which is quite a claim considering the other exquisite species in the genus). Discovering such an intriguing and unusual Ceropegia species, and having it named after her, can only be considered an appropriate acknowledgement of Anne’s scientific contribution to our understanding of the evolution of these amazing plants through her hard work and dedication.

From Anne: “I was out in the field with David hiking through the breath-taking landscape of Ngome. When I first spotted the flower, I immediately knew I was looking at something no one had ever seen before. I called David over and he was just as surprised and excited as I was by what was in front of us. It was so special and almost surreal – I will certainly not forget that moment for the rest of my life! I am exceptionally grateful that this beautiful example and flagship species of Ceropegia has been given my name (which was David’s idea) and thereby immortalized me in botanical nomenclature. I personally consider this a highlight of my career.”

Ceropegia heidukiae is not only exceptionally good-looking but is also exceptionally rare as it is endemic to a restricted area in KwaZulu-Natal and its habitat, Northern Zululand Mistbelt Grassland, is considered an endangered vegetation type. Ulrich Meve (specialist in the taxonomy of Apocynaceae-Asclepiadoideae) and David Styles described the species in a recently published article. In their species description, they assessed the conservation status of Ceropegia heidukiae as being Critically Endangered (CR). The publication of this rare novelty will hopefully encourage appropriate conservation measures to preserve this landscape and to ensure that this species can enjoy its glory without being threatened by extinction.

Text: Annemarie Heiduk and Hannah Butler.

Photos: David Styles

Article: https://www.biotaxa.org/Phytotaxa/article/view/phytotaxa.497.1.2

A1 NRF Rating for Steve Johnson

Our very own head of the pollination lab, Professor Steve Johnson, has obtained an A1 rating from the National Research Foundation (NRF). This is the highest rating that the NRF awards to ‘researchers who are unequivocally recognised by their peers as leading international scholars in their field for the high quality and wide impact (ie beyond a narrow field of specialisation) of their recent research outputs.’

Johnson is a professor in the School of Life Sciences on the Pietermaritzburg campus and the Director of the UKZN Centre for Functional Biodiversity. He also holds the South African Research Chair (SARCHI) in Evolutionary Biology.

Johnson’s research is aimed at understanding the reproductive ecology and evolutionary diversification of plants. He has a keen interest in the role of volatiles (chemical elements and compounds that can be readily vaporised) in mediating plant-animal interactions and has established a state-of-the-art laboratory for the study of chemical signals deployed by plants to attract pollinators.

He has a Google Scholar h-index of 73 and has published more than 330 peer-reviewed scientific papers and four books. He has also served as an Associate Editor for five international science journals.

‘The School of Life Sciences is particularly proud to have such a high calibre researcher in our team,’ said Dean and Head of School, Professor Ade Olanarin. ‘His continued contribution to the School, especially in the areas of mentorship and capacity building, through the activities of the NRF-funded community of practice linked to the Centre for Functional Biodiversity is very much appreciated. We wish Steve an ever more successful academic career as he continues to inspire and motivate all of us.’

Dean of Research in the College of Agriculture, Engineering and Science, Professor Neil Koorbanally concurred: ‘Steve, we are proud to have you in our College. You are truly an inspiration for younger researchers.’

‘Being A-rated is a goal achieved by few of us as researchers and academics,’ said College Deputy Vice-Chancellor, Professor Albert Modi. ‘The NRF rating system is a key driver in the NRF’s aim to build a globally competitive science system in South Africa. It is a valuable tool for benchmarking the quality of our researchers against the best in the world. Rated researchers as supervisors will impart cutting-edge skills to the next generation of researchers. Steve, congratulations on this brilliant success! You worked hard with a great team and you deserve this recognition and admiration.’

Text: Sally Frost (UKZN)

Article in Animation – The Blood Flower and the Butterfly

A recent publication by lab members, Hannah Butler (that’s me!) and Steve Johnson, has been turned into an animation by the Linnean Society.

Animation still from the Linneaen Society showing Scadoxus multiflorus subspecies katharinae visited by a male mocker swallowtail.

The original publication “Butterfly-wing pollination in Scadoxus and other South African Amaryllidaceae” has garnered a fair bit of attention since published in March 2020. Whilst scientific articles published in well rated journals are still the main course of action for the long-toothed to the freshly budding scientist, modern technologies and of course the increasing use of the internet is resulting in new ways of publicizing science. Science magazines have been turned into blogs, and even vaguely whimsical blogs such as this one serves to introduce readers to scientific articles and the like.

I feel some might find this somewhat of a conundrum, but personally, I love it! I doubt that the joy of introducing people to the research one has been conducting ever goes away. For this article, I was a mere 21 years of age when I started my research, with many questions and confusions rattling around in my brain. Days of standing in a muddy swamp buzzing with stinging insects and temperatures of over 35 degrees Celsius resulted in the discovery we expected but we hoped would be of interest to the larger scientific community. A great deal of more hot days, terrifying statistics and seemingly endless reading resulted in a published article I will forever be extremely proud of. We had discovered a new case of butterfly wing pollination! Surely someone else would be interested?

Original photo by SD Johnson showing Scadoxus multiflorus subspecies katharinae visited by a male mocker swallowtail.

It turns out that they were. Emails asking me to write a post for other blogs; emails from well-known blogs wanting to publish their own post about it; emails from students and academics alike asking more about it and congratulating me; and then an email from the Linneaen Society about turning the article into a short animation. How exciting! The resulting animation is succinct and beautiful (not least because some of my own illustrations were used). As much as the publicity and interest received for this article thrills the original authors, I am most pleased that it is reaching and hopefully exciting others.

Text: Hannah Butler.

In case you missed the link to the animation: https://www.youtube.com/watch?v=IrNrna62Snc&feature=youtu.be

Pollination Pop-Science from the Plant-Animal Interactions Research Group

PlantLifeSA, an online journal of the KwaZulu-Natal Coastal Branch of the Botanical Society of South Africa features two articles by Pollination Lab members in their latest issue. Check out stories about wonderfully weird Ceropegia flowers and of the discovery of pollination of the Drakensberg’s Hidden Flowers by Crag lizards. Scroll down through that issue for a further article contributed by UKZN horticulturalist, Alison Young, on the botanical highlights of Sehlabethebe National Park in Lesotho, an area which is well known to many lab members from field work in the summer months.

Wonderfully weird – How Ceropegia flowers lure fly pollinators with clever design and evil tricks

If you have half an hour to be fascinated by tales of incredible deception and deceit in the plant world, listen in to this interview with Dr Annemarie Heiduk on In defense of Plants, on her work unravelling the mysteries of Ceropegia pollination.

 

Text: R. C.

New Article in Ecology

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

Most of the almost 90% of flowering plants that rely on animals such as bees and butterflies for pollination, use bright colourful floral displays to attract their pollinators. The flowers of Guthriea capensis, the “Hidden Flower”, however, are just what their common name implies: hidden at ground level, beneath the leaves of the plant and inconspicuous because, 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?

The answer to this puzzle was recently published in Ecology by researchers from South Africa and the Netherlands, based at the University of KwaZulu-Natal and the Afromontane Research Unit at the University of the Free State. In a population 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, which pick up pollen on their snouts when they visit the flowers to lap nectar. 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 Guthriea capensis is virtually unprecedented.

Just how lizards find the “Hidden Flowers” is the next riddle to be solved. Most lizards are insectivorous but, especially in the harsh environments of islands and deserts, and, as this new finding suggests, 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 a 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.

However these lizards find their nectar treats, this study shows that, as indisputably important as 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” will continue to receive the visits from the little dragons with a sweet tooth that are critical for the production of seeds for another generation.

Cozien RJ, Van der Niet T, Johnson SD, Steenhuisen S-L. Saurian surprise: lizards pollinate South Africa’s enigmatic Hidden Flower. Ecology. Doi: 10.1002/ecy.2670.