I recently contributed a short piece for The Conversation. It is a shameless love letter / advertisement for one of the most striking Eucalypts in Australia and the Great Western Woodlands in which it lives.
I recently contributed a short piece for The Conversation. It is a shameless love letter / advertisement for one of the most striking Eucalypts in Australia and the Great Western Woodlands in which it lives.
Australian flowering plant diversity is legendary. Within an hour trip outside of our major metro centres anyone can quite easily witness unique Australian plant diversity in subtropical forest (Brisbane), grassland (Melbourne), and sandstone heath (Sydney). The diversity close to home is fairly well catalogued, and while it is hard to discover a new plant species, merely spending time around our native plants is very likely to reveal something that has never before been documented.
Something like 90% of our native plants rely on animals for pollination in order to set seed. Despite this, we simply do not know what pollinates most of our Australian native plants. The fact that the private lives for many of our native plants remains mysterious is due to their great diversity and the limited time and resources available to document what’s going on every day in the bush.
And these uncharted interactions are totally critical for the functioning of our native ecosystems. Pollination underpins production of seed for the next generation, builds seed banks for post-fire regeneration, and also produces fruits and seeds that are critical food resources for our native animals.
Our ignorance of native pollination networks is therefore vastly out of step with their importance. This is illustrated in the example of bee declines, where we have all heard about the threats impinging on honeybees and pollination service for food crops, yet when it comes to Australian native bees, we lack the basic benchmark data needed to make a solid judgment about whether they too are declining*. It is therefore imperative that we commit effort to recording native pollination networks now, before they are lost to us. While it is hard for long term ecological monitoring projects to attract funding, ongoing development of automated imaging of flower visitors and large scale citizen science projects offer some promise for increased capability in filling this ecological blind spot.
But our ignorance here can also be thrilling. This means that every time you are in the bush, and witness an insect or bird taking nectar or pollen from a flower, there is a reasonable chance it has never been documented before. In my work with University of Melbourne I have been studying several native shrubs to understand their pollination, and for many of these species, it is gratifying to know that my work will be the first documented evidence of what is visiting them. But you don’t have to be a trained scientist to do this, you just need some patience, luck, and some fine weather. And while discovering and photographing an unusual native bee pollinating one of our native flowers won’t win you a Nobel Prize, I guarantee it will provide any enquiring mind with a hit of electric discovery every single time.
Links for pollinator observations:
*But given native bees need native habitat, and native habitat is being cleared at astonishing levels, we can, with a high degree of confidence, say that native bees are declining too.
The flowers on one of these plants conceal drops of sticky nectar. The other is a cheating orchid, presenting empty flowers and false promises. Can you tell which is which? Even if you knew which one carried nectar, how can you tell the difference between them? The two plants might look a bit different to human high-res optics, but now try blurring your eyes. Pretty similar, huh?
What about this pair?
If it’s difficult for our brains and eyes to discern the difference between the flower with the reward and the one that’s falsely advertising, then what hope does a nectar-hunting fly with low resolution compound eyes and a smear of a central nervous system have?
Specifically, I’m talking about this fly…
Until now, you probably thought lion, or elephant, or rhino were the most impressive animals roaming the grasslands of southern Africa. Well you’re wrong, and it’s ok to change your mind after seeing the majestic long-proboscid fly of South Africa. There are several species of these magnificent beasts, and this one is named Prosoeca ganglbaueri.
That giant proboscis hanging from its face is a tool crafted by evolution for sucking nectar from the bottom of long flower tubes, and it can grow as long as 5 cm (which is longer than the fly’s own body length). Unlike butterflies who coil their proboscises, the long-proboscid flies simply hinge the instrument down, tucking it away underneath their bodies to trail out behind them. And this species isn’t even the most extreme: proboscises in Moegistorhynchus longirostris get up to 8 cm!
Sometimes handling that long instrument can be a challenge…
In some areas of South Africa, P. ganglbaueri is the only creature capable of extracting nectar from flowers with very long floral tubes, and because of this it has become the exclusive pollinator for 20 species of plant. Altogether, the long-proboscid flies as a group bear the great responsibility as the only pollinator for approximately 130 species of plant, making them a truly important creature for the ongoing survival of many South African plants.
An interesting fact about flowers that are pollinated by long-proboscid flies, is that most of them are pink, or white, or some variation in between (with one blue exception). This strong colour preference is a critical feature directing the evolution of the cheating orchid flowers introduced earlier. For a deceptive orchid to attract this fly, the orchids’ flower colour must match the flies’ colour preference, or the mimicry simply won’t work.
In my recent paper, we asked whether the colour preference of flies was something that they learned, like we learn to associate that perfect golden-brown hue of fried food with a mouth-watering culinary experience, or if it was instead a more hardwired innate response, like a moth drawn to a lamp. The answer is important for understanding ultimately what is driving the evolution of false advertisement signals in mimic orchids. So, for example, if flies had an innate bias to pink or white, then cheating orchid flowers would evolve to match that bias, in the same way that any good advertisements are designed to appeal to the fundamental desires of its audience. On the other hand, if flies learned to associate nectar reward with certain colours, their preference should be determined by the colour of their local nectar diet. Under the learned scenario, orchids should be evolving to match local flowers’ colours, not any intrinsic bias of the fly.
To test this, I took advantage of just how easy it is to bamboozle these flies. With a home-made artificial flower, painted to match the pink and white flowers visited by the fly, anyone can fool a fly into attempting to feed. So I mounted a pink and a white model to my “interview stick”, and travelled across the rugged Drakensberg Mountains to interview various populations of flies. In each location, I recorded whether the local flies preferred probing the pink or white model flower, as well as the colour and species of flower that the flies were using for nectar there.
This tells us that the flies are very flexible in their preferences, and the strong implication is that these flies are learning to associate colour and reward. A further result showed that as the variation of colours flies fed from increased, this made them less choosy in the pink-white preference choice. So the bottom line is that the colour of their local nectar-buffet strongly controls a fly’s colour preference.
What does this mean for orchid cheats? Well, the colour of nectar cheats is all important, and what matters most for the success of a deceptive orchid is the colour composition of the surrounding nectar-rich floral community.
Still wondering about which flowers in the opening images were cheats, and which had nectar?
In both cases the deceptive orchid is on the left. The first image features Disa nivea (left), and Zaluzianskya microsiphon (right), the second features Disa pulchra (left) and Watsonia lepida (right).
Peaceful woodlands of widely spaced gnarled Eucalypts lie in mosaic with spiny, scratchy, shrubby heath on the sand-plains north of Perth. They form one of the most floristically diverse regions on earth, with estimates of over 60 species of plant per 0.01 ha (an area smaller than half an an IMAX screen).
With so many species packed on top of one another, it is perhaps not surprising that in the effort to co-exist, some plants have been forced to flower outside the traditional Spring-flowering window. Winter in the sand-plains, while often wet and cloudy, is therefore anything but dull. While daily insect activity is very low, resident birds and honey possums must still feed, and so there are a comparatively high number of vertebrate-pollinated species in full flower at this time of year.
Plants mate. In a manner far more elegant than our own mammalian shenanigans, and far more important for the ongoing survival of the Earth’s ecosystems, plants are out there constantly having sex. And it is a deeply interesting thing involving insects, and wind, and stigmas, and stamens, and enough puzzling evolutionary biology to fill journal articles and occupy a small handful of academic careers.
My latest paper is about plant mating, and rather than wade through meadows of blooms to collect the data for this effort, I remained desk-bound in Milwaukee, wading through 30 years of plant mating literature with the intention of assembling a dataset to help us see plant mating in a new light.
As you may know, the flowers of many plant species are hermaphrodite, i.e. they bear both male and female sexual organs. This means plants can have sex with themselves. It’s called self-pollination, or “selfing”, and it can happen in two ways. First, pollen can move from the male parts of a flower to the female parts of the same flower. Second, on a single plant, pollen can move from the male parts of one flower to the female parts of a different flower.
“But isn’t this inbreeding??” I hear you ask, recoiling in horror at the moral and population genetic gutter down which I have so suddenly led you. Yes! Seed fertilized in a selfed flower is about as inbred as it gets, even more so than sibling mating. But you see, inbreeding is not always a bad thing—in fact inbreeding can actually be beneficial in some circumstances—and here’s where things get messy.
Genes are selfish. As such, they will do whatever it takes to get themselves propagated into another body. Consider then the selfish genes of a mother plant, which want to get into the next generation, and into as many individuals as possible. If a mother plant mates with a genetically different plant (an “outcross” mating event), its seeds each inherit approximately 50% of the mother’s genetic variation. This is because they combine with (and are diluted by) the genes of the pollen donor during pollination and sexual reproduction. On the other hand, if a mother self-fertilizes its own seeds, it transmits closer to 100% of its genetic legacy into each offspring. In the eyes of natural selection, this is a huge difference, and offers a great advantage to selfing over outcrossed reproduction.
So why aren’t all plants selfing all the time? This is because the huge advantage in transmitting genes via selfing is offset by the drawbacks of inbreeding. You can’t often get away with inbreeding without cost, and the cost is that inbred offspring are commonly less fit than their “outbred” siblings. Called “inbreeding depression”, this occurs because breeding from related individuals vastly raises the probability of combining rare genetic variants that harm the individual they are in. In the long run, inbreeding also reduces genetic variation that is essential for adapting to changing environments.
Evolutionary biologists have been pondering this tension for decades, and it led to the hypothesis that plants should be driven by natural selection into two polar opposite strategies: selfing plants should be favoured by natural selection when inbreeding depression is weak, and outcrossing plants should be favoured by natural selection when inbreeding depression is strong. Anything in the middle should not be adaptive, and should therefore be rare in nature. Sounds sensible, except numerous studies have now measured selfing/outcrossing across hundreds of plant species, and there is a curious and difficult-to-explain preponderance of plants that are neither exclusively selfing or outcrossing. These plants are having it both ways, seemingly hedging between strategies, and we call them the “mixed maters”.
Now for the problem my study addresses… Over the last 30 years, loads of studies have been measuring the selfing/outcrossing rate of plants in the wild. There have also been important studies which collect all these outcrossing estimates into big global datasets and generate observations like the one above: that mixed-mating is inexplicably common. For 30 years however, much of this discussion on global patterns was centred around average outcrossing per species, and using this to classify a species as a “selfer”, “outcrosser”, or “mixed mater”. We know evolution doesn’t work on a “species level” though. What is more appropriate is what is happening in a population context. And perhaps by averaging away all the variation within each species, my co-authors and I thought we might be missing an important perspective on the data.
What my co-authors and I did then was to collect all the outcrossing estimates from published papers containing three or more population outcrossing estimates. Going back 30 years, we collected data for 105 species and measured the variation in outcrossing within a species, among populations.
What we found was huge variation! There was commonly so much variation in mating within a species, that species averages felt inadequate for expressing where mating system variation lies. The data also showed that variation was difficult to predict. For example, there was an old hypothesis floating about that wind-pollinated plants were less variable in their outcrossing/selfing rate than animal pollinated species. The reason being that animals were thought to fluctuate more in their abundance and service between sites and seasons, while wind was a more consistent, reliable force for pollination. For the first time we were able to test this, and our analysis did not support the hypothesis. We also tested whether mating variation was evolving in a predictable fashion, but found that the relationship of plant species had no bearing on the variation we found in those species’ mating patterns.
Ultimately, our study can’t solve the mystery of why we have so many mixed-mating plants. What it does do though is present a new way to look at the known range of variation in plant mating. There are other analyses waiting to be done with the data collected here, and we have highlighted where more studies are needed to answer interesting questions. For example, do different kinds of animal pollinators result in more or less variable outcrossing? Or do populations on the fringe of a species’ range experience more or less variable outcrossing?
As the body of knowledge on plant mating systems continues to grow, this dataset will grow too, and this population-level perspective on plant mating will hopefully provide the basis for the next insights into evolution’s influence on plant mating.
Goodwillie C, Kalisz S, Eckert CG. (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu. Rev. Ecol. Evol. Syst., 36:47-79.
Schemske, DW and Lande, R. (1985) The evolution of self‐fertilization and inbreeding depression in plants. II. Empirical observations. Evolution, 39:41-52.
Barrett, SC and Harder, LD. (2017) The Ecology of Mating and Its Evolutionary Consequences in Seed Plants. Annual Review of Ecology, Evolution, and Systematics, 48:135-157.
I’m thrilled to share this never-before seen sequence of birds feeding on Astroloma stomarrhena, a winter-flowering shrub endemic to Western Australia.
Earlier this year, I decided A. stomarrhena looked like a perfect candidate for my new study on pollinators and gene flow. What I needed was a bird-pollinated species of plant, closely related to an insect-pollinated species. This one seemed to match all the criteria I needed, except there was no evidence that it was bird-pollinated. But with those long, tapered corolla tubes, and that pink-red coloration, I believed that birds absolutely had to be the pollinator.
The danger was, that while birds might be visitors, the plant could be somewhat “generalized”, and also use insects. This is pretty common, especially in places like Australia where European Honeybees (Apis mellifera) have invaded ecosystems that evolved in their absence, and honeybees will visit absolutely everything whether the plants are adapted to bees or not.
By deploying a new camera-trapping method that I am developing to record insect visitation, I was able to gather several days of pollinator observations, despite some very bad weather. After initially being baffled as to what honeyeater might visit such a low ground-hugging shrub, I got my answer after day one, when I captured video of my new favourite bird: the Tawny-crowned Honeyeater (Gliciphila melanops) feeding on the flowers. Furthermore, the recordings of honeybee fly-bys are sufficient to rule them out as pollinators.
This little result is a win on two fronts: a successful trial of new pollinator-monitoring cameras, and vindication of predicting pollinators from flower morphology.
Rare plants nurseries are like second hand bookshops. It’s always so tempting to browse on the off chance you find that little treasure. I recently visited a charming rare plants nursery in Mt Macedon (boutique-y town outside Melbourne, Australia) where I discovered these for sale:
The last time I saw this elegant iris, it was flowering on stream banks 10,000 km away in the Drakensberg Mountain range in South Africa. There in its natural habitat, it is pollinated in some areas by a very special butterfly: the Mountain Pride (Aeropetes tulbhagia). In other places, it is pollinated by the amazing long-tongue fly (Prosoeca ganglbaueri). The two forms are a wonderful example of “pollination ecotypes”, where different populations are undergoing adaptation to their unique pollinators. The fly-serviced ones are a pink hue with narrow petals, while the butterfly-pollinated ones are much redder with broader petals.
Fast forward two weeks, and I’m home walking the dog in my quite unremarkable Melbourne suburb, when who should I see?
It’s winter here, with very little in flower, but these brilliant little pink blooms volunteering themselves from underneath a fence in suburban Melbourne really made my day. The last time I saw a Diascia, it was growing amongst the boulders on creek beds and on cliffs in the Drakensberg Mountains. These are Diascia, or “twinspur” and its this common name that alludes to their fascinating pollination story.
Diascia have two spurs on the back of the flower, which is distinct from the usual arrangement of a single nectar-spur. The difference is that these flowers don’t reward pollinators with sugary secretions, instead they provide oil to specialised oil-collecting bees in the genus Rediviva. The bees use this oil to line their nests and provision their young. In order to collect the nectar, they must reach deep into the twin spurs with their lanky forelimbs, and comb it out. In so doing, they effectively hug the reproductive parts of the Diascia flower and effect pollination.
In Spring, I plan to take some cuttings from this little Diascia. Keeping species with special personal significance is a deeply satisfying part of cultivating plants. A plant can be kept like a souvenir or memento marking a time in one’s life, just like a photo or trinket. But plants have an advantage over these inanimate reminders. Because biological reproduction requires the physical donation of part of the mother’s cells to the daughter cells, my keepsake plant can be viewed as a physical part of the plant that appears in my fond memory. If I could see in four dimensions, I could literally look down the line of cell-divisions all the way back to where the Hesperantha in the nursery physically intersects as the same individual with the Hesperantha I observed flowering in the Autumn sun of the Drakensberg Mountains in South Africa.
To be born an orchid is a most unlikely thing. First your parents must be pollinated, which is difficult. Orchids are both rare, and rarely pollinated due to the bizarre and dishonest means by which they go about attracting pollinators. Added to that, orchids often rely on a single species of pollinator to do the job.
Let’s say, however, that your orchid parents do manage to achieve fertilization. Your orchid mother will produce many thousands of tiny dust-like seed, which will be jettisoned into the wind. Unlike most seeds, you have no maternal energy investment to power your germination and first days as a seedling. Instead, you must rely on blind luck to land you within reaching distance of a strand of soil fungus. This fungus is the wet nurse to bring you into the world, invading the seed coat and hooking the young orchid up to a network of fungal strands that pervade the soil. Tapping into this network provides you with the first sips of carbohydrate and nutrient you need in order to build your first green leaf and begin to stand on your own roots. But it is not enough to land near any fungus. Many orchid species require fungal partnership with a specific species of fungus for this to occur at all. Multiplied together, it is a wonder that orchids ever overcome these odds to propagate themselves into the next generation.
The southwest of Western Australia is rightly famous as a global biodiversity hotspot. The area is particularly rich in orchids, and the spider orchids (Caladenia) are some of the most impressive and diverse of the region’s main orchid groups. In 1967, University of Adelaide researcher John Warcup discovered in association with Caladenia a new genus of fungi. Today those fungi are called Serendipita, and although we have known of them for around 60 years, there have been less than a handful of species discovered and described.
Although related to mushrooms, Serendipita fungi have not been observed producing the conspicuous spore-bearing fruit bodies we usually use to find and identify them. This makes them largely invisible, and I have therefore never observed them in the wild. Despite that, recent research using DNA sequencing has found them to be absolutely everywhere. Inside all kinds of plants, outside all kinds of plants, and distributed from the equator to Antarctica. It is clear then that there must be a hidden biodiversity of these species siting, waiting to be discovered.
My study took a wide sample of southwest WA spider orchid samples and assayed them for the presence of Serendipita fungi. We then sequenced the DNA of all the fungi we found, and used a new analytical technique for dividing that DNA sequence diversity into units that are probably species. This is currently the only way to sensibly identify Serendipita fungi, as they all look completely alike and do not produce spores in the lab.
We found a total of eight species of Serendipita fungi, including the original species discovered by Warcup back in the 60s. These came from a total of 18 species of orchid. At some sites where we sampled multiple orchid species, we found six species of Serendipita, meaning that the fungi were as diverse as the orchids!
Although we have chosen to study these Serendipita in association with orchids, their wide host association has got other researchers interested in their role in plant health and application to agriculture. For example, Warcup’s species and one other have been used in experiments (and patent applications) showing inoculation with Serendipita results in profound benefits for the host plant, including:
These proven benefits make Serendipita a potentially powerful tool to enhance plant productivity and stress tolerance in crops. Furthermore, application of Serendipita fungi could be an organic alternative permitting growers to lower the application of unsustainable and ecologically harmful synthetic fertilizers. Our knowledge of plant-Serendipita associations in the wild suggests that these relationships are more prevalent in nutrient poor soils such as those in southwest WA. They are probably one factor that allows our plant diversity to thrive in such weathered, poor soils. This means that species of fungi that have evolved with the nutrient poor soils (like those discovered in this paper) might be untapped tools to enhance agriculture taking place in those very same soils.
(Erratum: This story was edited to replace the figure attributed to Ray and Craven (2016). The first image I used was one showing Arabidopsis capability for mycorrhizal association. Arabidopsis is typically thought to be a non-mycorrhizal plant, which is why this is interesting. The image however showed slower growth in the mycorrhizal treatment. A related Serendipita has been shown to enhance root growth in Arabidopsis however. I have now updated the post with a more appropriate image of root growth gains in wheat. Thanks to Pawel Waryszak (@PWaryszak) for pointing this out.)
Whitehead, M. R., Catullo, R. A., Ruibal, M., Dixon, K. W., Peakall, R., & Linde, C. C. (2017). Evaluating multilocus Bayesian species delimitation for discovery of cryptic mycorrhizal diversity. Fungal Ecology, 26, 74-84.
Weiß, M., Sýkorová, Z., Garnica, S., Riess, K., Martos, F., Krause, C., … & Redecker, D. (2011). Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. Plos one, 6(2), e16793.
Weiß, M., Waller, F., Zuccaro, A., & Selosse, M. A. (2016). Sebacinales–one thousand and one interactions with land plants. New Phytologist, 211(1), 20-40.
Ray, P., & Craven, K. D. (2016). Sebacinavermifera: a unique root symbiont with vast agronomic potential. World Journal of Microbiology and Biotechnology, 32(1), 16.
Bokati, D., & Craven, K. D. (2016). The cryptic Sebacinales: An obscure but ubiquitous group of root symbionts comes to light. Fungal Ecology, 22, 115-119.
I recently began a brand new project with the University of Melbourne. The beginning of a new project is filled with equal parts excitement and trepidation—excitement at the novelty, the blank canvas, the potential, and trepidation at not wanting to put a foot wrong in critical early decisions that will affect the outcome of a career-defining opportunity.
Here the photos from a first foray into East Gippsland, surveying sites for bird-pollinated Prostanthera walteri.
Seduction. Pollination. Deception.
I recently wrote an article for Wildlife Australia about Australian sexually deceptive orchids, their evolutionary biology, and historical and current research about them. You can download and read the article here: PDF. Thanks to Carol Booth for her collaboration and editorial guidance.
The latest of Australia’s sexually deceptive orchids that I have seen (below) are Caleana major, the Flying Duck orchid (left), and a spider orchid Caladenia clavigera (right). Both were photographed last week in Brisbane Ranges NP, Victoria.
Flowering this year is one of the best seasons of recent times both east and west of the country. So if you’re in Australia, don’t miss the chance to get out bush and enjoy it.