Project update: Contrasting bird and insect pollination through use of novel camera and genetic technologies.

I recently put together some material on my work for the University of Melbourne open day. As a teaser for the papers in current preparation, here’s an abstract and some visuals on the project.

While we simply do not know what pollinates many of Australia’s plants, there is good evidence emerging showing Australia to be a global hotspot for bird-pollination. This raises questions about what ecological and evolutionary factors might encourage plant lineages to adapt to use birds as couriers for their pollen. As well, we might ask what the outcomes are when a plant species ties its reproductive fortunes to a bird, rather than an insect.

My project employs custom cameras designed for motion-capture data capture of insect visitors to flowers, in order to demonstrate contrasting bird versus insect visitation in pairs of closely related native shrubs. Fine-scale population genetic analysis in these plants is revealing evidence for systemic differences in the movement of pollen under these different pollinator regimes.

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Styphelia stomarrhena is pollinated exclusively by birds.

The video below shows bird visitation by a number of honeyeater species, as well as the way in which floral morphology excludes bee pollinators from accessing pollen or nectar in Styphelia stomarrhena.

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Styphelia xerophylla is the sister species to S. stomarrhena and has evolved a tight relationship with a single species of native bee: Leioproctus macmillanii.

 

The videos below show motion-captured footage of the native pollinator of Styphelia xerophyllum, a female native bee (Leioproctus macmillani).

However the flowers are also visited by introduced honeybees (Apis mellifera).

 

A quick note on plant names: These species recently underwent taxonomic revision, moving them from genus Astroloma to Styphelia. It is rather new, hence the confusion over these shrubs apparently having two names.

Densey Clyne 1922 – 2019

I must have been around six or seven years old, but I vividly remember being captivated by Densey’s work on late 80’s Burke’s Backyard. Her subjects were mostly invertebrates, the natural history of which she brought to life with superb macro and timelapse filmography. (For classic Densey and awesome 80’s music check out this vid about cicadas). It might not even be too far-fetched to draw a direct line from Densey’s work—  some of my earliest recollections of a natural history fascination—to my life and work now, preoccupied with the flowers and insects she revealed to me so long ago.

Clyne’s clips of flowers blooming in timelapse made a particular impression on me. In a moment of frustration with a bored and annoying child, I remember Mum sending me into the backyard to wait for a flower to bloom. Soaked in the false impressions of timelapse filmography, I stood staring at a Callistemon for what felt an age before finally conceding defeat and coming back indoors.

In the last couple of years I had the desire and embryonic plan to go and visit her, knowing she was getting on, wanting to meet her and tell her the impression she made on me, and perhaps write up an interview to share her experience and wisdom with others. But I never got around to prioritising it, and now that opportunity is gone.

From the tiniest, dankest little crevices in the bottom of my heart; thanks Densey.

(For more information about her life and achievements, the Port Macquarie news have a nice write-up)

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Photos from the field: The Great Western Woodlands.

The Great Western Woodlands (GWW) form the largest tracts of temperate woodlands left on Earth. They hold approximately 30% of Australia’s Eucalypt species, and close to 20% of Australia’s plant species overall. This is truly an overlooked gem of Australian biodiversity. Last Spring I was lucky enough to visit for my work on pollination in our native plants.

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My target there was Eremophila, a genus of approximately 250 species largely confined to arid and semi-arid Australia. The GWW represents one of the centres of diversity for the genus, and so I chose it as a likely spot to set up a new study contrasting bird and insect pollination.

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Eremophila alternifolia was one of about 15 Eremophilas I saw flowering despite the drier than average conditions.

I was joined by perhaps the best kind of field assistant: a trained and accomplished professional ecologist who also happens to be my beautiful wife. After driving 2800km from Melbourne to field sites near Norseman, Western Australia, we spent a little under two weeks observing pollinators, surveying and mapping populations of plants, and collecting samples for population genetics.

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One of the many viewpoints south of the Nullarbor Plain.

I left in awe of the scale of these woodlands, in love with the peace and isolation they offer, and a bit concerned over their insecure future. Fully 60% of the GWW is tenured “unallocated Crown land”, unmanaged and open access. With more visitors, and more appreciation of the value of these vast woodlands, I hope we can find a way to secure more of it into ongoing reserve for future generations.

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The bluebush understory contrasts dramatically with red sand in many areas. Front left is one of my study species Eremophila scoparia.

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The whole region is dotted with salt-pans.

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As predicted from the small, violet flowers, Eremophila scoparia was visited by a host of native bees.

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Eremophila decipiens has characteristic bird-adapted flowers.

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Camera traps being expertly arranged by Samantha. Footage revealed that E. decipiens was being visited by a range of honeyeater species.

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Eremophila calorhabdos

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This spectacular Grevillea hid a massive bloom of flowers underneath it

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The inflorescences are held on stems that grow along the ground underneath the shrub. The very long style with pollen-presenter is suggestive of adaptation to birds, but mammals might not be out of the question.

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Eucalyptus loxophleba with daggy botanist for scale

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Majestic Salmon gum (Eucalyptus salmonophloia) with Samantha for scale.

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The serenity of wandering amongst giant Salmon gums at dusk was magic.

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Gleaming bark on Eucalyptus salubris

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Elevating on Lake Cowan. Photo: S. Vertucci.

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For the second half of the trip I was joined by collaborator and all-round legend Dr. Renee Catullo. I made us walk 10km to collect camp gear following a single poor decision.

Stay tuned as research results emerge. The study should tell us about the way pollen moves under bee and bird pollination, and how those fine scale patterns play out on a grand landscape level.

We don’t know what pollinates most Australian plants.

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.

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Two native bees (Hylaeus (Rhodohylaeus) sp.) visiting flowers of the Broom Bush (Eremophila scoparia) in Western Australia.

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.

 

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Photographed on Mount Buffalo, Ken Walker (Victoria Museum) later identified this bee as the very rare Lasioglossum (Callalictus) callomelittinum. Few photos of it exist. This individual is buzz-pollinating a Fringe Lily (Thysanotus tuberosus).

 

Links for pollinator observations:

Bowerbird: Nature observations database

Wild Pollinator Count

Government pollinators repository

*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 whimsical long-tongue fly and its favourite colour.

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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?

Screenshot 2018-10-30 15.09.50If 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…

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If this fly looks embarrassed, its because it has orchid pollen stuck to its face.

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.

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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…

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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.

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Figure 1 from Whitehead et al. (2018): Prosoeca ganglbaueri feeding from a variety of nectar sources. (a) Zaluzianskya microsiphon, (b) Scabiosa columbaria, (c) Agapanthus campanulatus, (d) Dianthus basuticus.

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.


The results were clear. Flies used to feeding mainly on pink flowers preferred the pink model. Flies that fed mainly on white flowers preferred the white model. And flies that fed on both pink, white, and violet flowers, showed no clear preference between pink and white.

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Figure 3 from Whitehead et al (2018): Pink-white preference for flies at seven sites. The x-axis shows colour preference, with pink on the right, white on the left. Measured preference at seven sites is represented, with the colour of local nectar sources depicted in the small pie charts.

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.

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Post-script:
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).

Reference:

Whitehead MR, Gaskett AC, Johnson SD. (in press) Floral community predicts pollinators’ color preference: implications for Batesian floral mimicry. Behavioral Ecology 

Photos from the field: Northern Sand-plains, WA

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.

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Omphalina chromacea in its diminutive but sulphureous glory

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Bird-pollinated Astroloma glaucenscens excludes insect visitors with a tiny corolla-tube opening

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Pterostylis sanguinea: a sexually-deceptive trap-pollination orchid

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Astroloma stomarrhena, bird-pollinated. This individual has curiously short corolla tubes.

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Calothamnus sanguineus mixed in with Conostephium

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Calothamnus sanguineus

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An early-flowering Caladenia latifolia

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Diuris corymbosa

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Tiny pgymy Drosera

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One of the most common orchids in the area, but I’ve never seen it flower. Pyrorchis leaf.

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Very rare, and while this specimen is a little tired late in the season, the winter-flowering Cleopatra’s Needles (Thelymitra apiculata) is a stunning contrast of hues.

First video of bird pollination in Astroloma stomarrhena

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.

Click here for the full HD video.

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Bumping into old floral friends, and pollination with a hug.

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:

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Hello old friend! (Hesperantha coccinea)

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.

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Hesperantha coccinea at home in South Africa with its pollinator (Prosoeca ganglbaueri).

Fast forward two weeks, and I’m home walking the dog in my quite unremarkable Melbourne suburb, when who should I see?

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Hello old friend! (Diascia sp.)

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.

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Hug-pollination by oil-collecting bee (Rediviva sp.) in Diascia.

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.

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The Drakensberg Mountains, South Africa, Autumn 2014.

 

Photos from the field: East Gippsland, Victoria

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.

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Mt. Elizabeth

 

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Snowy River National Park

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Prostanthera walteri

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Prostanthera hirtula

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McKillops Bridge

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The Snowy River

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The Snowy River

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Prostanthera walteri

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Snowy River National Park

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Gippsland waratah – Telopea oreades

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Floral diversity in Prostanthera

 

Australia’s sexual swindlers.

Seduction. Pollination. Deception.

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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.