Category Archives: Apocynaceae

“Weighted” nestedness and “classical” nestedness analyses do not measure the same thing in species interaction networks

This post resulted from a question I posed on Twitter last week and hopefully summarises the issue as I see it and the results of the discussion with colleagues that followed.  Let me know if you disagree or if I have missed anything.


The use of network approaches to understanding how plants and their flower visitors interact has revolutionised the study of these and other mutualistic assemblages of species.  It’s a subject I’ve discussed on the blog before, highlighting some of the work we have published – for instance, see Plant-pollinator networks in the tropics: a new review just published and Local and regional specialization in plant–pollinator networks: a new study just published as two recent examples.

One of the recurring patterns that we see in mutualistic species networks (but not in antagonistic ones such as host-parasite and predator prey) is “nestedness”.  In a nested assemblage of species, generalists with lots of links to other species interact with other generalists and with specialists (those species which have few links to other species)Conversely, specialists tend only to link to generalists: specialist-specialist interactions are rare.  In nature, when we rank species in a network from most to least generalised, this sort of relationship looks like this:

South Africa nested

The rows are plants and the columns are pollinators, in this case from an assemblage of asclepiads and their pollinators we studied in South Africa.  A filled cell in the matrix indicates an interaction between that particular plant-pollinator combination.  It’s not perfectly nested by any means, but statistically this is not a random pattern and it comes out as nested when analysed.  There are a few ways of doing this but the most commonly used is the Nestedness metric based on Overlap and Decreasing Fill (NODF) developed by Almeida-Neto et al. (2008).

I first saw nestedness discussed in relation to plant-pollinator interactions in a presentation by Yoko Dupont of her PhD research at a SCAPE meeting in Sweden in 2001.  It was one of those “A-HA!” moments in science when the light bulb switches on and you realise that you are seeing an important new development which adds significant understanding to a field.  Yoko subsequently published her work as Structure of a plant–flower‐visitor network in the high‐altitude sub‐alpine desert of Tenerife, Canary Islands.

The nested pattern of interactions is conceptually derived from earlier work on island biogeography and species-area relationships and was initially developed to apply to interaction networks by Jordi Bascompte and colleagues in Spain and Denmark – see: The nested assembly of plant-animal mutualistic networks.

What was so exciting about this idea to me was that it provided a way to formally analyse what many of us had been observing and discussing for some time: that mutually specialised plant-pollinator interactions between species are rather rare, and that specialists tend to exploit generalists.  This makes perfect sense because specialist-specialist interactions may be more likely to go extinct, though why it does not also apply to host-parasite interactions is far from clear (and in fact the best known specialist-specialist interactions tend to derive from seed parasitism interactions such as fig-fig wasp and yucca-yucca moth relationships).

Fast forward 20 years and the plant-pollinator networks literature has exploded and our methods of analysis are much more sophisticated than they were in the late 1990s and early 2000s.  Every few months researchers are coming up with new ways in which to analyse these networks, mainly using the R environment for statistics and graphing.  Anyone entering the field would be forgiven for being bewildered as to which approaches to use: it’s bewildering enough for those of us who have been following it from the start!

One thing has been particularly bewildering me for a few years now, and that’s the introduction of “weighted” nestedness.  “Weighted” in this sense means that the abundance or interaction frequencies of the species in the network is taken into account in the analyses.  Visually it could look something like this if we code the cells in the network above to represent abundance or frequency (the darker the cell, the more abundant or frequent):

South Africa nested weighted

I’ve just mocked up the network above, it’s not the actual data.  But quite often networks look like this when we weight them: generalist interactions and/or species tend to be more frequent than specialist.  So far, so obvious.  But here’s the thing: networks that are statistically significantly nested when analysed by NODF tend to be not significantly nested when analysed by a new set of weighted metrics such as wNODF or WINE – see the documentation for the bipartite package for details.   And I don’t understand why.  Or rather I don’t understand why we should be using weights in an analysis of nestedness which is, at its heart, an analysis of presence-absence.  Species are either there or they are not, they are either interacting or they are not.  Their frequency or abundance is immaterial to whether a network is nested.  Indeed, assessing frequency of interactions in plant-pollinator networks is fraught with difficulties because (a) there are so many ways in which to do it; and (b) interactions between plants and pollinators in a community can vary HUGELY between years and across the geographical ranges of the species involved.

This should concern the interaction network community because recently I’ve had reviewers and co-authors saying things like: “don’t analyse for nestedness using NODF because wNODF/WINE is The Latest Thing, use that instead”.  But as far as I and the colleagues who commented on Twitter can tell, nestedness and weighted nestedness are different concepts and are not inter-changeable.  Indeed, many of us are struggling to really define exactly what weighted nestedness analyses are actually measuring.  I can define nestedness in simple terms as a verbal concept, without using the word “nested”, as you saw above.  I can’t do that with weighted nestedness, and I have yet to encounter anyone who can.

So the consensus from the Twitter discussion seems to be that:

  • for any study we should use only those analyses that are relevant to the questions we are asking rather than simply running every available analysis because there are lots to choose from.
  • weighted interaction networks that include abundance or frequency are not necessarily superior to binary presence-absence networks.  Again, it depends on the question being asked.
  • we should not treat weighted nestedness as an upgraded or superior version of classical nestedness.  If you are interested in nestedness, use a binary analysis like NODF.

My thanks to the colleagues who contributed to the Twitter discussion:  Nacho Bartomeus, Pedro Jordano, Pedro Luna, Marco Mello, Chris Moore, Timothée Poisot, and Kit Prendergast.  If you want to follow the Twitter discussion, start here:  https://twitter.com/JeffOllerton/status/1159377089319047168

 

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Are these first photographs of a living specimen of a rare African butterfly?

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Earlier this year my colleague at the Royal Botanic Gardens Kew, David Goyder, tweeted a link to a new book about the biodiversity of Angola which you can download for free by following this link.  David’s an authority on Apocynaceae, the family of plants on which I’ve also worked for many years (see this recent post), and has been sorking in Angola in recent years on a large biodiversity project.  So I was interested to see what was in the chapter  he had co-authored called “The flora of Angola: Collectors, Richness and Endemism“.  I was immediately struck by one of the images in Figure 5.3 showing an unnamed butterfly feeding on the flower of a species of Apocynaceae (Raphionacme michelii).

I made a note to myself to talk to David about adding the record to our Pollinators of Apocynaceae Database. But before I had a chance to do that, another apocynologist colleague, Ulrich Meve in Bayreuth, forwarded the chapter with a similar idea in mind.

We emailed David about the image and he sent us originals, but confessed he didn’t know what the insect was.  So I uploaded it to an African Lepidoptera forum on Facebook.  At which point a wave of excitement broke, because after some discussion as to whether it might be a new species, it turned out that the most likely candidate was an exceptionally rare butterfly called Acraea mansya in the family Nymphalidae.

According to Dominique Bernaud, an authority on the group, this species is hardly known beyond a few collections and he has never seen a photograph of a living specimen: if you follow this link you will see that the known distribution of the species does not include Angola,  and indeed it is not listed in the chapter on butterflies in the Angola biodiversity book.  So this is a new country record and (we think) the first images of living insects: so a double first for a beautiful species.

Here’s links to collection information for the plant and to David’s checklist of plants from the region, which gives details of the vegetation and the habitat.

An unanswered question, of course, is whether the butterfly is a pollinator of this species of plants.  Raphionacme belongs to a subfamily of Apocynaceae that have hardly been studied from the perspective of pollination ecology, so we simply don’t know.  Hopefully someone in the future will visit this remote region of Africa and find out!

Thanks to David for sending the images (a complete set of which is below), the National Geographic Okavango Wilderness Project, and the Wild Bird Trust, Parktown, South Africa.

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Tantalising evidence for a new type of pollination system in Madagascan Apocynaceae

cynanchum obovatum with wasp_madag -angavokely_meve 1

As I recounted in my post last summer, the plant family Apocynaceae contains species with a very wide diversity  of pollination systems – see:  The evolution of pollination systems in one of the largest plant families: a new study just published – download it for free.  Confirmed pollinators include bees, birds, moths, butterflies, flies, beetles, and wasps of a dizzying diversity.  So I was intrigued to receive an email earlier this week from my colleague Prof. Dr Ulrich “Ulli” Meve of the University of Bayreuth with the subject line “Wasp expert needed”.  Ulli is an authority on Apocynaceae taxonomy, also has an interest in their pollination biology, and is a co-author of the study last year.

Attached to the email were a couple of images showing a wasp visiting flowers of Cynanchum obovatum, an endemic species of Apocynaceae from northern and eastern Madagascar.  Ulli had taken the photographs during field work there in preparation for the Flora of Madagascar project.  Here’s the global distribution of the species according to GBIF records:

cynanchum obovatum from gbif

I was excited because Madagascar has a very rich diversity of Apocynaceae (between 500 and 1000 species).  However we have flower visitor observations for only a small fraction of them, fewer than 20 species, and good evidence that the visitors are pollinators for only a couple of those.

I didn’t immediately recognise the family to which the wasp belonged: it didn’t look like either Vespidae or Pompilidae, two groups that are known pollinators of Apocynaceae.  So I uploaded the shots to the Hymenopterists Forum on Facebook and within minutes had received an answer:  it was a species of Scoliidae, commonly referred to as scoliid wasps.  The distinctive wing corrugation found in this family is clearly visible on this image:

cynanchum obovatum with wasp_madag -angavokely_meve 2

Scoliids are parasitoids of beetles and are some of the world’s largest wasps, but it’s not a very diverse family, with only about 560 described species, and only a single species in the UK (on the Channel Islands).  Compare that with the Pompilidae and Vespidae, both of which contain c. 5,000 species worldwide.

Ulli tells me that when he saw the scoliid on C. obovatum “the wasp knew what to do with the flowers”, something I’ve experienced with vespid and pompilid wasp pollinated species in Africa: these wasps are really familiar with the flowers, they know how to work them to get a reward as they are regular and committed visitors.  We believe that this is likely to be the legitimate pollinator of the plant, in which case it’s one of the few records for Scoliidae pollinating Apocynaceae, and the first for Madagascar.  Other examples are mainly in South America, India and South Africa, and usually as one of a broad set of other wasps and/or bees visiting generalist flowers.

It’s interesting that this species of Cynanchum is one of the few in which the corona which covers the gynostegium (the fused sexual parts) is closed over:

cynanchum obovatum_madag - angavokely_meve

That means it requires quite a strong, large insect to get inside and access the nectar.  So the prediction is that the pollen masses (pollinaria) will be found on the mouthparts of these wasps.  Intriguingly, a very closely related species C. repandum has no such closed corona, begging the question of whether it might be pollinated by a different type of insect:

cynanchum repandum sl 2867_low

For now this record will go into the Pollinators of Apocynaceae database as pollinator unproven, but i would be great if someone working in Madagascar could confirm the status of this pollination system.

My grateful thanks to Ulli for sharing his pictures and allowing me to tell the story of what may be a whole new Madagascan pollination system for our favourite family.  Apocynaceae is full of surprises!

cynanchum obovatum with wasp_madag -angavokely_meve 3

 

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The evolution of pollination systems in one of the largest plant families: a new study just published – download it for free

Figure 1 JUNE revision

Interactions between flowering plants and the animals that pollinate them are known to be responsible for part of the tremendous diversity of the angiosperms, currently thought to number at least 350,000 species.  But the diversity of different types of pollination system (bird, bee, moth, fly, etc.) is unknown for most large, related groups of plants (what systematists term “clades”) such as families and subfamilies.  In addition we know little about how these interactions with pollinators have evolved over time and in different parts of the world.  Only a handful of groups of flowering plants have been studied with respect to questions such as:

How much do we currently know about the diversity of pollination systems in large clades?

How is that diversity partitioned between the smaller clades (e.g. subfamilies, tribes, genera) of a family, and what are the evolutionary transitions between the major groups of pollinators?

Do these pollination systems vary biogeographically across the clade’s range?

These sorts of questions have been addressed for the massive, globally distributed Apocynaceae (one of the top 10 or 11 largest angiosperm families with more than 5,300 species) in a study just published using a new database of pollinators of the family.  What’s more, the work is open access and anyone can download a copy for free.  Here’s the citation with a link to the paper:

Ollerton, J., Liede-Schumann, S., Endress, M E., Meve, U. et al. [75 authors in all] (2019) The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study. Annals of Botany 123: 311–325

In this study we have shown that (among other things):

  • The family is characterised by an enormous diversity of pollination systems involving almost all of the major pollen vectors and some that are nearly unique to the Apocynaceae.
  • Earlier diverging clades have a narrower range of pollination systems than those that evolved later.
  • Transitions from one type of pollination system to another are evolutionarily constrained, and rarely or never occur, whereas others have taken place much more often, e.g. between wasp and beetle pollination.
  • There is significant convergent evolution of pollination systems, especially fly and moth pollination, by geographically and phylogenetically distinct clades.

You’ll notice that there are 75 (!) authors on this paper.  That’s because we’ve pulled together a huge amount of previously unpublished data and used some state of the art analyses to produce this work.  It was a monumental effort, especially considering that my colleague Sigrid Liede-Schumann and I only decided to push ahead with this project about a year ago when we chatted at the International Botanical Congress that I posted about at the timeIn truth however the origins of this paper go back over 20 years to 1997 when when Sigrid and I published a study of what was then known about pollination systems in the Asclepiadaceae (the asclepiads).

In that paper we said that the research “is intended to be ongoing…[we]…hope to re-review asclepiad pollination within the next decade”.  At the time I didn’t think it would actually take more than 20 years!  However over that period a lot has changed.  For one thing the Asclepiadaceae no longer exists, broken up and subsumed within a much larger Apocynaceae.  Also, I’ve done a lot of work in the field and in the herbarium on some of the smaller groups within the family, such as CeropegiaOthers, including many of my co-authors, have also been working on different groups in various parts of the world.  Finally the level of sophistication of the analyses we are now able to do has increased beyond recognition compared to what we could achieve in the mid-1990s.  All of this means that now is the right time to produce this study.

Having said all of that, this is still a work in progress.  Our Pollinators of Apocynaceae Database contains a sample of just over 10% of the species in the family.  So lots more data on plant-pollinator interactions needs to be collected before we say we fully understand how pollination systems have evolved in this most remarkable family.  I’d be happy to talk with anyone who is interested in the family and being involved in future data collection.

The database will be freely available to anyone who wants to use it – lots more can be done with this information and, once again, I’m happy to chat with potential collaborators.

I was recently interviewed about the study, and about plant-pollinator interactions and the Apocynaceae more generally, for the In Defense of Plants podcast – here’s a link to that interview.

Finally, I’d like to express my sincerest thanks to my co-authors on this study – I really couldn’t have done it without you guys!

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Academic job interviews: don’t feel obliged to do everything you said you’d do

Interview transparencies 2018-07-17 17.14.59

Last month I cleared out my office in preparation for our move to the University of Northampton’s new Waterside Campus.  Going through files I’d not opened in decades was a cathartic and occasionally emotional experience.  In one file I came across a box of OHP transparencies from the presentation I gave at my job interview in 1995!  (For younger readers, OHPs were just like PowerPoint, but you carried them around in a box….)

Anyway, the presentation (see photo above) at what was then Nene College of Higher Education set out what my research plans were going to be if I was offered the job. It’s interesting to look back on these research themes and consider whether I did actually do what I said I was going to do (go to my Publications page for details of the papers I’m referring to):

Flowering phenology” – This was a large part of my PhD, which I had completed two years earlier.  At Northampton I did a bit of work,  including a big meta analysis with Mexican colleagues Miguel Munguia-Rosas and Victor Parra-Tabla, but nothing further, though I do have a lot of unpublished data that one day may see the light of, err, day….

Pollination systems in the Asclepiadaceae” – I’ve done a lot of work on this plant family, including field work in South America and Africa, particularly with my German colleague Sigrid Liede-Schumann.  However Asclepiadaceae no longer exists as a separate family (it’s now a subfamily of Apocynaceae).  I have a large paper in press at the moment which assesses the diversity of pollination systems in the Apocynaceae; more on that when it’s published.

Specialisation and generalisation in pollination systems” – yes, done lots on this too, including contributing to the Waser et al. (1996) Ecology paper that’s now racked up >1550 citations, plus assessing latitudinal trends in specialisation.  Still a major focus of my research, it’s an area where there are lots of questions still to be answered.

Reproductive output [in plants]” – very little done since my doctoral work, though questions of annual variation in reproductive allocation were a big part of my PhD.  Has fallen by the wayside rather.

Seed predation” – ditto – it was a major component of my PhD and I published a couple of things but then hardly touched the topic.  A shame in some ways as I still think it’s a fascinating topic.

Pollinator behaviour” – I’ve done some work, mainly on birds and bees rather than the butterfly model system I proposed at the time, which was to work with Dave Goulson on a follow-up of a paper we published on floral constancy in Small Skipper butterflies.  This field has moved on hugely though, with some extremely sophisticated work being done with captive bumblebee colonies for instance.

Overall I think I’ve worked on about 50% of what I said I would do, which I’m more than comfortable with.  Because I’ve also done a whole bunch of stuff I never mentioned at interview, including work on pollinator conservation and interaction network analyses, both of which were hardly thought about in 1995.  There’s also research on the history of science that I was thinking about in the early 90s but which I didn’t present as a major research theme.

The moral of this story for anyone preparing for a job interview for an academic position is: Don’t think that you have to do all of the research that you say you’re going to do in the presentation.  Opportunities come and go, and interests wax and wane.  What is currently seen as exciting research may well, in 10 years time, be seen as old hat or a dead end, or have evolved in ways that provide you with fewer opportunities to contribute.  Prepare to be flexible, but don’t lie about your intentions.  In fact, as recently highlighted on the Dynamic Ecology blog, don’t lie about any aspect of getting an academic job!

One other thing: be realistic.  In retrospect I was too ambitious in the range of areas in which I wanted to do research, though they were all linked.  But over the course of 23 years it’s impossible to say how your research career will develop.  I’m looking forward to the next 23…. 🙂

 

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Something for Blue Monday – the only known blue flowered asclepiad

Tweedia caerulea - OBG 2014-11-06 11.33.14

Today is Blue Monday – reckoned to be the most depressing day of the year, though I’m in a very good mood: just back from a great 9am seminar with my final year students taking the Biodiversity & Conservation module.  They presented some really interesting, diverse and thought provoking papers as part of their assessment for this module; it’s a great group to teach.

But if you are suffering from the blues this morning, here is a photograph to cheer you up.  As far as I am aware Tweedia caerulea (also known as Oxypetalum coeruleum)  is the only known blue flowered asclepiad (that’s to say, a member of the family Apocynaceae subfamily Asclepiadoideae – what used to be the family Asclepiadaceae*).

No one is sure why blue is such a rare colour within the asclepiads (and indeed the Apocynaceae as a whole) and it may be connected to the pollination system of this plant.  However we don’t know what pollinates Tweedia caerulea in the wild so it’s hard to test that idea; other species within this group are variously pollinated by wasps, bees, flies, moths, etc.  Truly blue flowers (as opposed to some shade of purple or violet) are relatively uncommon generally amongst the flowering plants and the source of much interest and excitement in those groups where they do occur, for example the Himalayan Poppies (Meconopsis).

Tweedia caerulea is easy to grow from seed but not so easy to get through the winter in the UK, so in the past I’ve grown it as an annual in the garden.  Apart from the colour, one of the other reasons I like this plant is that it’s named after the 19th century plant collector John Tweedie whose life I’ve been researching over the past 20 years or so – see this paper for example.

 

 

*The asclepiads are my favourite group of plants, and one that I’ve published quite a bit of research on, so I was a bit miffed when the taxonomic rank of the family was relegated to subfamily.  But it makes evolutionary sense and now gives me a much larger family of plants on which to research, so every cloud etc. etc.

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Pollinator biodiversity and why it’s important: a new review just published – download it for free

P1110763

In a new review paper that’s just been published in the Annual Review of Ecology, Evolution and Systematics I have looked at the question of just how diverse the pollinators are, and why pollinator biodiversity is ecologically important and therefore worthy of conservation.  I’ve taken a deep time and wide space approach to this, starting with what the fossil record tells us about when animal pollination evolved and the types of organisms that acted as pollinators in the past (the answer may surprise you if you’re unfamiliar with the recent paleontological literature on this topic).  Some of the most prominent biogeographical patterns have been highlighted, and I have tried to estimate the global diversity of currently known pollinators.  A conclusion is that as many as 1 in 10 described animal species may act as pollen vectors.

As well as this descriptive part of the review I’ve summarised some recent literature on why pollinator diversity matters, and how losing that diversity can affect fruit and seed set in natural and agricultural contexts.  Extinction of pollinator species locally, regionally, and globally should concern us all.

Although I was initially a little worried that the review was too broad and unfocused, having re-read it I’m pleased that I decided to approach the topic in this way.  The research literature, public policy, and conservation efforts are currently moving at such a fast pace that I think it’s a good time to pause and look at the bigger picture of what “Saving the Pollinators” actually means and why it’s so important.  I hope you agree and I’d be happy to receive feedback.

You can download a PDF of the review entitled Pollinator Diversity: Distribution, Ecological Function, and Conservation by following that link.

Pollination ecologists should also note that in this same volume of Annual Review of Ecology, Evolution and Systematics there’s a review by Spencer Barrett and Lawrence Harder called The Ecology of Mating and Its Evolutionary Consequences in Seed Plants.  If you contact those authors I’m sure they’d let you have a copy.

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Fly pollination in the trap flower genus Ceropegia: a new study just published

Flies on C. arabica from Sage Reynolds

Pollination of flowers by flies (the insect order Diptera) has long fascinated me, in part because it often subverts the idea of what “normal” flowers should look like, but also because it is much less well studied, and appreciated, compared to bee pollination.  This is despite the fact that fly pollinated flowers are at least as frequent as bee pollinated flowers in many plant communities, as I show in a forthcoming review in the journal  Annual Review of Ecology, Evolution and Systematics (more on that in November when it’s published).

Over the past decade I’ve been studying the large plant genus Ceropegia in the family Apocynaceae (subfamily Asclepiadoideae).  The flowers of these species temporarily trap their fly pollinators, releasing them after a period, during which pollination takes place and/or pollen is picked up.  The latest study from this work has just been published in the journal Flora, in collaboration with colleagues from eight different countries.  The title is:

Diversity of Diptera families that pollinate Ceropegia (Apocynaceae) trap flowers: an update in light of new data and phylogenetic analyses

If you follow that link you can download the PDF for free for the next 50 days.

One of the main findings from this new study is that the diversity of fly families that pollinate Ceropegia spp. is much greater than we had previously realised.  The total now stands at 16 different families, including some that rarely, if ever, pollinate other plants (as far as we yet know).

Another important finding is that this clade, which may contain as many as 1000 species in total, seems to have diversified despite that fact that all species are apparently fly pollinated.  This is unusual: diversification of plant clades often involves shifts to very different groups of pollinators, e.g. bee to bird or bat pollination.

There’s still lots to discover about this group of plants and this is just the latest output from what is an ongoing project focused on Ceropegia and the Apocynaceae more generally.

Here’s the abstract:

“Pollination by flies (Diptera) has been important to the diversification and ecology of the flowering plants, but is poorly understood in contrast to pollination by other groups such as bees, butterflies and birds. Within the Apocynaceae the genera Ceropegia and Riocreuxia temporarily trap flies, releasing them after a fixed, species-specific period of time, during which pollination and/or pollen removal occurs. This “trap flower” pollination system shows convergent evolution with unrelated species in other families and fascinated Stefan Vogel for much of his career, leading to ground-breaking work on floral function in Ceropegia (Apocynaceae). In this new study we extend the work of the latest broad analysis published by some of the authors (Ollerton et al., 2009 − Annals of Botany). This incorporates previously unpublished data from India and Africa, as well as recently published information, on the diversity of pollinators exploited by Ceropegia. The analyses are based on a more accurate phylogenetic understanding of the relationships between the major groups, and significantly widens the biogeographic scope of our understanding of fly pollination within Ceropegia. Information about the pollinators of 69 taxa (species, subspecies and natural varieties) of Ceropegia is now available. Twenty five families of Diptera are known to visit the flowers of Ceropegia, of which sixteen are confirmed as pollinators. Most taxa are pollinated by species from a single family. Overall, there were no major biogeographic differences in the types of Diptera that were used in particular regions, though some subtle differences were apparent. Likewise there were no differences between the two major clades of Ceropegia, but clear differences when comparing the range of Diptera exploited by Ceropegia with that of the stapeliads. This clade, one of the largest in the Asclepiadoideae, is a fascinating example of a species radiation driven by an apparently relatively uniform set of pollinators.”

Photo credit: flies on flowers of Ceropegia arabica in cultivation by Sage Reynolds.

 

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