The strange case of the migrant diatom …

Ach_tepidaricola_Elia_near_Vyzakia_190313

I’m taking time during lockdown to catch up on some papers that I had been meaning to write for some time.  One of these, for a special issue of the journal Ecological Indicators, is about the diatoms of Cyprus, a subject that I’ve touched upon in a few earlier posts (see “Diatoms from the Troodos Mountains”).  Writing about Cyprus, even via the dry prose of an academic paper, reminded me how much I had enjoyed earlier visits, and when I might be  able to return.

Most of the hard work to produce the data in this paper was, I have to admit, done by Marco Cantonati and, in the process, he has found several species that had not previously been described, which makes us wonder if the endemism for which the higher plant flora of Cyprus is well-known also extends to the diatoms.  There has been a vigorous debate about the extent to which diatoms are cosmopolitan rather than restricted to particular geographic areas in recent years, with evidence now to show that some species definitely seem to be cosmopolitan whereas others are much more localised in their distribution.  The diatom flora of an island such as Cyprus ought to be a valuable test case for this.

One species that we had not seen before but which, after searching the literature, Marco was able to match with a previously-described species was Achnanthidium tepidaricola – shown in the picture at the top of the post.  Achnanthidium is a large genus of small diatoms, and we have only really started to appreciate the diversity within the genus over the past 20 years or so (see “Quantifying our ignorance …”).  This particular species, however, has a story to tell.  It was first found growing on a wet stone wall in a greenhouse in the National Botanic Garden in Meise, Belgium by Bart van der Vijver a few months after the wall had been constructed.   Finding the same species in Belgium and Cyprus ought to be a hint that it is relatively cosmopolitan.  However, our story has an interesting twist …

The twist is that the wall that Bart sampled in the greenhouse in Meise was built with stones that had been imported from Turkey.  Suddenly, A. tepidaricola is looking less Flemish and more like a migrant.   Turkey is, of course, the nearest mainland country to Cyprus, and shares the same arid climate of the eastern Mediterranean.   Many of the streams in this part of the world will, naturally, dry out in the summer and the diatoms will have to be prepared to survive in these conditions.   Suddenly, A. tepidaricola growing both in Cyprus and on that one particular wall in Belgium is looking less like evidence of endemism and more like a hint that, even if not endemic to Cyprus, this species may be characteristic of the eastern Mediterranean.  It may be more widespread than that, but this is certainly where it is being recorded at the moment.

That’s the trouble with biogeography: the distribution of species is forever shifting, and our modern joined-up world only accelerates this process.  Dump a pile of stones from Turkey almost anywhere else in Meise and the Flemish climate would probably have sent Achnanthidium tepidarociola to the Great Biofilm in the Sky.  But these particular stones were put into a greenhouse where they were able to thrive and, eventually, to be noticed by Bart.   Humans helping previously unknown bugs to move across the world?  Where else have I heard about that before?

The photo at the top of this post was taken by Marco Cantonati and shows a population of Achnanthidium tepidarocola from Vyzakia, Cypris in March 2019.

Reference

Van der Vijver, B., Jarlman, A., Lange-Bertalot, H., Mertens, A., de Haan, M. & Ector, L. (2011).  Four new European Achnanthidium species (Bacillariophyceae).  Algological Studies 136/137: 193-210.

 

Some other highlights from this week:

Wrote this whilst listening to: 1980s Bob Dylan (probably not his greatest period): Empire Burlesque and Knocked Out Loaded.  Also an elderly, rather scratchy recording of Rachmaniov’s first two piano concertos with Rachmaniov himself on piano.   And Scottish singer-songwriter Siobhan Wilson’s There Are No Saints.  Well worth checking out, if you have never heard her before.

Cultural highlights:  Jojo Rabbit.   This one split the critics but was a box office hit.  There were too many negative reviews when it first came out for us to make the trip out to see it but our son persuaded us to give it a try.  Glad we did.   Very clever soundtrack.

Currently reading:   HG Well’s War of the Worlds.

Culinary highlight:   Caesar Salad, from a Felicity Cloake recipe in The Guardian.  We also found some pumpkin lurking in the depths of the freezer and turned it into a pie.   Ate both whilst sitting in the garden: a rare treat in our climate.

The dark side of the leaf …

Whites_Level_lower_epiphytes

Having mentioned in my previous post that the epiphytes on the top and bottom surfaces of a Potamogeton polygonifolius leaf were different, I have produced a companion piece to the painting I showed in that post.   The new painting is of the lower surface, and shows a greater number of diatoms than are present on the upper surface.  In order to explain why this is the case, it is helpful to look at the structure of the Potamogeton leaves.  The first image, therefore, shows a section through a leaf. It is quite a thick section but we can see the upper epidermis, the palisade mesophyll cells below this, which have plenty of chloroplasts in order to capture the sunlight that the plant needs for photosynthesis.  Below this, we can see parenchymous tissue arranged to create some large internal air spaces which contribute to the leaves buoyancy. Finally, at the bottom, there is a single layer of epidermal cells.   All this is crammed into a thickness of about half a millimetre.

Potamogeton_polygonifolius_leaf_section

Part of a section of a leaf of Potamogeton polygonifolius.  The leaf vein is on the left, thinning to the leaf blade on the right.  The leaf blade is about half a millimetre thick.   The picture at the top of the post shows an artist’s impression of diatoms and Chamaesiphon cf. confervicolus on the lower surface of a Potamogeton polygonifolius leaf. 

 Viewed from the underside, these parenchymous tissues create polyhedronal chambers, ranging from about 100 to 200 micrometres (a tenth to a fifth of a millimetre) along the longest axis.  There are also a few stomata scattered across the leaf surfaces (see the right hand image below).

With this in mind, take a look at my impression of the epiphytes growing on the lower surface of a Potamotgen polygonifolius leaf.   There are a number of cells of Chamaesiphon cf confervicolius, as seen on the upper surface, but there are several cells of the diatom Achnanthidium minutissimum, growing on short stalks, plus a few long, thin cells of Ulnaria ulna, growing in small clusters on the leaf surface (there were a few other species present, but such low numbers that I have not included them here).    It might seem strange to think of two surfaces of a leaf having such different communities of epiphytes but that’s because we’re thinking like large land-dwelling organisms, not like algae.   The longest alga visible in the image of the leaf underside is Ulnaria ulna, at about a 10th of a millimetre in length.  Therefore, to get a realistic impression of the two images, we really need to put a distance of five of these between them, and then pack the gap with chloroplast-rich mesophyll cells inside the Potamogeton leaf.   Allowing for foreshortening, this distance is about five times the height of the image.

Pot_polygonifolius_leaf

The structure of a Potamogeton polygonifolius leaf viewed from the underside.  The left hand image (100x magnification) shows a leaf vein running diagonally across the lower right hand side along with the polyhedron-shaped chambers; the right hand image (400x magnification) shows the outline of one of these chambers superimposed behind the epidermal cells with a stomata with two guard cells visible just above the centre.   Scale bar: 20 micrometres (= 1/50th of a millimetre). 

The epiphytes on the upper surface of the leaf get first dibs at the meagre Pennine sunlight, which then has to pass through the upper layers of the Potamogeton leaf, where the mesophyll cells will continue to feast on the tastiest wavelengths, leaving relatively meagre pickings for the epiphytes that hang around on the underside of the leaf.

Chlorophyll, the molecule that makes plants green, absorbs light over a relatively narrow range of wavelengths – predominately red and blue – and this means that there are plenty of other wavelengths awaiting an organism with different pigments.   Diatoms have chlorophyll, but they also have some carotenoids (principally fucoxanthin) that grabs energy from the green part of the visible light spectrum (which is reflected, rather than absorbed by chlorophyll) and passes it to the cell’s photosynthetic engine.  Having this capability means that they can survive in relatively low light, which is why we see more diatoms on the underside of the Potamogeton leaf than on the top.

And that, best beloved, is the story of how Potamogeton got its epiphytes …

 

Some other highlights from this week:

Wrote this whilst listening to: more Bob Dylan.   I’ve got to the mid-70s, which means the live version of Like a Rolling Stone on Before the Flood plus the great Blood on the Tracks.  Also, as I was reading Ian Rankin, I listened to John Martyn’s Solid Air.

Cultural highlights:  we’re watching the BBC adaptation of Sally Rooney’s Normal People

Currently reading:  Ian Rankin’s Rather be the Devil.

Culinary highlight:   A rather fine vegetarian chilli, from Felicity Cloake’s column in The Guardian last week.   Served with corn bread, using a recipe we got from a hand-me-down American housekeeping magazine during our time in Nigeria.

 

Not quite a coral reef …

Fold_Sike_March2020

Working on the principle that we usually pass only a handful of people during our walks in Upper Teesdale we decided that this counted as “social distancing” and headed off to the hills.  Whether this is still deemed to be acceptable behaviour this week is another matter, but I can report that Teesdale in midweek was certainly far less crowded than the tourist honey-pots that were the focus of so much bad press over the weekend.   But I digress.

Our regular beat follows the Pennine Way for a long stretch with the River Tees on our left and the looming cliffs of Falcon Clints on our right.   Just before the Pennine Way gets to this section, however, the valley is broader, with a flat floor that is used as grazing land by Widdybank Farm.  A small stream, Fold Sike, flows off Widdybank Fell and crosses the Pennine Way at an oblique angle before joining the River Tees.   I’ve walked past it many times, mentally noting prolific growths of a broad leafed Potamogeton as I press on, but little else.  Today, however, my eyes were caught by light-coloured crusts on many of the basalt stones just below the surface of this shallow stream.   If you look closely at these crusts you’ll see that they are not homogeneous: there are distinct nodules on their surfaces and they are more prominent on the edges, rather than the tops, of the stones.  You’ll also see a distinct green tinge in some areas.

Fold_Sike_with_Potamogeton

Potamogeton and Homoeothrix crustacea growing in Fold Sike, Upper Teesdale (NY 834 292) in March 2020.   The photograph at the top of the post shows the view looking back down the valley from Fold Sike with Widdybank Farm in the distance.

Homoeothrix_crustacea_Fold_Sike_March20

A basalt cobble from the bed of Fold Sike showing the surface nodules and the greenish tinge to the crust.  

This crust is distinctive: I know from previous encounters that it is formed, primarily, of the cyanobacerium Homoeothrix crustacea, a member of the Oscillatoriales (see “Shuffling the pack”).  I also know that it is a beast to photograph, having very narrow filaments and, in this case, also is extensively calcified.  I describe the process of calcification of Chara in “Everything is connected” and the same principles are likely to apply here too.   the I did try to dissolve away the calcite with some vinegar, but without much success in this case.  I’ve included some photographs of another species below, and you can see yet another species of Homoeothrix in “Algae from the Alto Duoro”.   The microscopic image shows the characteristic tapering filament combined with the absence of a heterocyst.  In the far past, Homoeothrix was thought to be a heterocyst-free relative of Calothrix, rather than a tapering relative of Oscillatoria and Phormidium.

Homoeothrix_images

Some images of Homoeothrix: a. Homoeothrix crustacea encrusting a boulder (approximately 40 cm across) from a calcareous stream in Cumbria, UK; b. filaments of H. fusca from a crust on Whitbarrow tufa stream, Cumbria (scale bar: 100 micrometres, 0.1 millimetre); c: close-up of a single trichome from the same stream. Note the distinctive tapering and absence of a heterocyst (scale bar: 10 micrometres, one hundredth of a millimetre).

The greenish patches on the surface of the crust were mostly composed of the green alga Bulbochaete (discussed in more detail in other posts – see “A winter wonderland in the River Ehen“) and I also saw a number of diatoms, principally Achnanathidium minutissimum and Delicata delicatula.  The latter, formerly included in Cymbella, is a common species in streams hereabouts, though relatively uncommon in the UK as a whole.  I also saw a few trichomes of a member of the Rivulariaceae, though did not find any intact colonies.  Were this a warm, shallow maritime environment a few dominant calcifying algae that create a habitat for a range of other species would be called a “reef”.  That word stretches the imagination when applied to a small windswept sike in upland County Durham, but the processes are the same even if scale and context are very different.   However, what with all the travel restrictions and closed borders at the moment, this might be the closest any of us will get to a coral reef for quite some time …

Delicata_delicatula_FoldSike

Delicata delicatula (?) from Fold Sike, March 2020.   Scale bar: 10 micrometres (= 1/100th of a millimetre).

Some other highlights from this week:

Wrote this whilst listening to: Bob Dylan’s first two albums.  One of my projects for the next weeks is to listen to all Bob Dylan’s albums sequentially.  Tony Allen and Hugh Masekela’s latest album, Rejoice, is also well worth a listen.

Cultural highlights:  The Perfect Candidate.  A Saudi film about a female doctor battling misogyny to get elected to the local council.   Under normal circumstances we would probably have ventured up to the Tyneside Cinema in Newcastle to see this.  Instead, we streamed it via Curzon Home Cinema.

Currently reading:  Still ploughing through Hilary Mantel’s The Mirror and The Light.  Oddly, despite the enforced isolation, I don’t seem to be finding much time to read at the moment.

Culinary highlight:   The bad news is that Durham Indoor Market has finally succumbed to the inevitable and closed its doors, taking with it most of our opportunities to buy non-supermarket food.   That means that the risotto we cooked with a stock made from the leftovers from last weekend’s prawns probably wins the “culinary highlight” this week, if only because it may be some time before we can make another.

 

 

Disagreeable distinctions …

When you look at an organism, how do you know what it is?   That’s a big question that hovers over many of the posts that I write.   I tell you the names of organisms and you believe me. Sometimes I do too.   The truth is that we take the way that our brains process the constant stream of signals that our eyes send us as we observe the natural world without a second thought.   The subject intrigues me, but I only manage to scratch the surface in the posts that I write (see “Abstracting from reality …” and “Do we see through a microscope?” for some of these speculations).

The plate below offers a case study in this process.  It shows a diatom we encountered in a recent ring test, and which most us agreed was either Fragilaria austriaca or something quite similar.   In binary terms, though, we have to be blunt: either it is Fragilaria austriaca or it is not which may have implications for subsequent recording and interpretation (see “All exact science is dominated by the idea of approximation”).   How come a group of experienced analysts can look at the same population of diatoms and reach different conclusions?   I’ve got two suggestions: the first is that we differ in how we process the images, and the second is that there are sources of systematic error which confound our attempts to seek the right answer.

Fragilaria_austriaca_Foreshield

Fragilaria austriaca” from Foreshield Burn, Cumbria, May 2019.

There are three basic strategies that we use to name an organism:

  • Probabilistic reasoning, through the use of keys which, in theory at least, have a logical structure that guides a user to the correct identity of an unknown specimen. In practice, this is not quite as straightforward as it sounds (see “Empathy with the ignorant …”) and, at some point, many of us will abandon the formal structure of a key and switch to …
  • Pattern recognition, which amounts to flicking through images until we find one that matches our specimen. We can then corroborate this preliminary match by checking the written description.  In practice, we will probably switch from probabilistic reasoning to pattern recognition and back again as we home in on the identity of an unknown specimen. Repeating this process several times will lodge a schemata of this species in our memories, leading to a third strategy:
  • Recall. In practice, most of us probably have seen many of the common and even less-common species so often that we can by-pass these first two steps completely because we recognise the species without recourse to any books.

Disagreements, then, arise partly because we use different books as part of our naming process, our prior experiences differ and because our discipline in checking measurements of our own specimens against descriptions is not always as good as it should be.   In many cases, especially with modern understanding of diatom species, boundaries between species are frequently being redrawn and descriptions of newer species can only be found in obscure journal articles, often behind paywalls, and knowledge of these often diffuses through the community of diatomists more slowly than it should.   However, our discussions about the identity of the mystery Fragilaria also revealed a further issue, which I’ve illustrated in the graph below.

When we switch from “pattern recognition” to “probabilistic reasoning” we often base decisions on categoric distinctions of continuous variables such as length and width.  In this case, the literature quotes a maximum width of four micrometres for F. austriaca, and this was an important factor contributing to decisions about the correct identity.  However, there were differences in our measurements which means that some decided that the population was too broad to qualify as F. austriaca whilst others decided that it fell within the correct range.   The likelihood, based on these graphs, is that at least some of us were making incorrect measurements but, at this stage, we don’t know who they are.

FAUS_measurements

Measurements of width, stria density and length of the population of “Fragilaria austriaca”.  Six analysts were involved in total, using either the eyepiece (“E”), an image projected onto a screen (“S”) or a measuring program (“P”) to make measurements (some used more than one approach). The dashed lines show the upper and lower limits for each parameter.

But that, itself, brings me to another point: do we know the correct size range of Fragilaria austriaca?  In order to be sure, we would need measurements of both initial cells (the largest in a cell cycle) and cells at the point where they are about to undergo sexual reproduction (the smallest in the cell cycle), ideally from several populations.  As this is rarely the case, we actually have three problems: first, is the description reliable? Second, are your measurements accurate? Third, we are using a point on a continuous scale as a criterion for a categorical judgement which implies perfect knowledge of the size range of the target population.  Even if you are sure of your microscope’s calibration, the best you can say is that the largest valve that you saw in the sub-sub-sub-sub-sub-sub sample of the population that lived in the stream you sampled exceeds (or not) the largest valve that the original author measured in the sub-sub-sub-sub-sample that s/he examined.   Several of our measurements just tip over four micrometres, the maximum width quoted in the literature for Fragilaria austriaca but, given these other factors, is that enough to drive a decision?   Statisticians are more comfortable predicting means, modes and medians than predicting extreme values.   Taxonomists, by contrast, seem to have undue reverence for maxima and minima.

Molecular biologists are approaching similar questions with considerable vigour.   The arrival of metabarcoding and high throughput sequencing means that they have had to write complicated computer code (“bioinformatics pipelines”) to sort the millions of sequences that emerge from sequencers, matching as many as possible to sequences from organisms whose names we already know, in order to turn those sequences into data that biologists can use (see “When a picture is worth a thousand base pairs …”).   We are conscious that decisions about software and settings within packages contribute to variations in the final output for reasons that we cannot always answer to our satisfaction.  But, whilst engaged in these discussions about cutting-edge technology, I’m conscious that old-school biologists such as myself each perform our own private “bioinformatics” every time we try to name an organism and we don’t always agree on the outputs from these thought processes.   Molecular biology, in a roundabout way, holds up a mirror to the way that we’ve been used to operating and should make us ask hard questions.

Some other highlights from this week:

Wrote this whilst listening to: my elderly vinyl copy of Mike Oldfield’s Tubular Bells

Cultural highlights:  Milton Jones at Newcastle City Hall

Currently reading:  Hilary Mantel’s The Mirror and The Light

Culinary highlight: polenta served with a mushroom and cheese sauce.

Finally, breaking news: I’m going to be live at the Green Man festival this August.  More details of our event “Slime Time”, and all the other performers at Einstein’s Garden can be found here

GM2020_EINSTEINS GARDEN (1)

And the Oscar for best alga in a supporting role goes to …

Low_Force_022006

I know that the focus of this blog can meander, depending on what takes my fancy week-to-week.  My core business is, however, writing about the hidden world of algae so, having written about Sam Mendes’ use of the River Tees Upper in his film 1917 in my previous post, I thought that I ought to take a trip up Teesdale to take a closer look at what is growing in the river at this time of year.   With Storm Ciara looming ominously on the forecast, I knew that if I did not sacrifice my Saturday morning it might be a while before I had another opportunity (there’s a graph at the end of this post which confirms this hunch).  And so I found myself buffeted by the wind with clouds scudding across the sky and the peaty water of the Tees thundering across the sequence of cascades that make up Low Force.

The main river was, even after a period without much rain, too deep and fast-flowing for me to venture far in so my activities were confined to the margins.   The rapid current, however, means that there were few of the small and medium-sized stones that I would normally remove and inspect.  Most had been picked up and transported further downstream leaving wide expanses of the Whin Sill bedrock.   In the shallow areas towards the edges that were not exposed to the full force of the current, there were dark green patches that I picked at with a pair of forceps.   When I was able to look at these under my microscope, I saw that they were Ulothrix zonata, a common inhabitant of northern British streams during the winter, and an alga that I have written about previously (see “The intricate ecology of green slime …” and “Bollihope Bhavacakra” amongst others).

Ulothrix_zonata_Tees_200208

Ulothrix zonata growing on Whin Sill in the River Tees at Low Force, Teesdale in February 2020.   The upper and central pictures on the left hand side show vegetative filaments and the lower picture shows empty cell walls after zoospores had been released, to which a germling is attached.  Scale bar: 20 micrometres (= 1/50thof a millimetre).   

The rocks were very slippery, even when not covered by green patches of Ulothrix zonata.   My usual approach to collecting specimens is to remove the whole stone and scrub the top surface with a toothbrush.  That, however, was impossible here so I had to resort to brushing the surface of the Whin Sill and hoping that enough of the slippery film remained attached to my toothbrush, which I then agitated in a bottle containing some stream water to shake the gunk off before repeating the process.  The small amount of material that I did manage to transfer from the rocks imparted a chocolate-brown hue to the water that signifies that diatoms were present.

Sure enough, when I did get a drop of the suspension under my microscope, there were diatoms aplenty, mostly wedge-shaped cells of Gomphonema growing at the end of long, branched mucilaginous stalks.  These, like Ulothrix zonata, are very common in northern British streams at this time of year.  I described similar assemblages from the River Wear at Wolsingham although, in that case, the Gomphonema shared their habitat with motile Navicula species as well (see “The River Wear in January”).   The Gomphonema in the River Tees is most likely G. olivaceum or a relative but I will need a closer look to be sure.  If I used an old Flora such as Hustedt’s 1930 Süsswasser-flora Mitteleuropas, I would have been able to be more assertive in naming this “Gomphonema olivaceum” but we now know that diatom systematics are more complicated than was thought to be the case in Hustedt’s days.

Gomphonema_Tees_200208

Gomphonema olivaceum-type colonies growing on Whin Sill in the River Tees at Low Force, Teesdale, February 2020.  Scale bar: 20 micrometres (= 1/50th of a millimetre).   

The sequences of 2017 were filmed in June not January so George Mackay would not have found the bedrock of the Tees to be quite as slippery as it was on my visit.   As the water warms up, grazers become more active and, as a result, the biofilms in the summer are much thinner than those in January.  That means that fewer slippery, slimy polysaccharides are produced, making it easier to keep your balance when walking at the edges of the river.

As I mentioned in my previous post, the sequence in 1917 involves George Mackay falling into a river in Picardy but crawling out of a river in Upper Teesdale.   I know less about the rivers of Picardy than I do about those in northern England, but a combination of low relief, extensive canalisation and the presence of heavy industry and coal mining in the area will mean that the algae found there will be very different to those in the Tees.   However, if 1917 can get 10 Oscar nominations (including for best sound editing) despite having the call of a Great Northern Diver echoing over No-man’s Land, then we can be fairly sure that the Wrong Sort of Algae is a level of detail that Sam Mendes and Roger Deakins thought they could safely ignore.

References

You can find some information about the diatoms of Picardy rivers in this paper:

Prygiel, J. & Coste, M. (1993).  The assessment of water quality in the Artois-Picardie water basin (France) by the use of diatom indices.  Hydrobiologia 269: 343-349.

This week’s other highlights:

Wrote this whilst listening to:  Michael Kiwanuka and other acts who will be playing at the Green Man festival in August.   I’ll be there too, talking about slimy algae, at Einstein’s Garden, the on-site science festival, along with (I hope) a gang of volunteers from the British Phycological Society.

Cultural highlight:   Two picks this week.  The first was Monteverdi’s Vespers performed at Durham Cathedral.  The cavernous interior of the cathedral joins the choir and orchestra as part of the experience, providing resonances that raise the experience beyond anything that a CD can offer.   The second is Bong Joon-ho’s film Parasite, a strong contender, along with 1917, at this evening’s Oscar Awards Ceremony.

Currently reading:  John le Carré’s Mission Song

Culinary highlight: a Napoli pizza cooked with locally-grown flour (www.gilchesters.com), part of a push this year to source more of our ingredients locally.  There’s obviously more to a Napoli pizza than can be grown in the UK but it is a start.

Tees_Middleton_levels_200208

River levels at the Tees at Middleton-in-Teesdale (x km downstream from Low Force) in the week from 3 to 9 February 2020. The arrow shows the time of my visit; note the steep rise in level a few hours later, coinciding with Storm Ciara moving through the region.  Graph from the excellent https://riverlevels.uk website.

Quantifying our ignorance …

Petta_Water_May19

I am fairly sure that I am not a popular person after my latest choice of slide for the “ring test”, the regular calibration exercise that UK and Irish diatomists perform.   I had noticed a few taxa that we had not seen in previous ring tests in a sample I collected during my visit to the Shetland Islands back in May 2019 (see “Hyperepiphytes in the Shetland Islands”) but, on closer examination, the sample proved to be both highly diverse and very challenging.  The seven experienced analysts who provide the benchmark analyses for the ring test found, between them, over 150 different species: some we could name with confidence, but others we could match to no published description.  Amongst those was the species of Achnanthidium photographed below.   It might be Achnanthidium digitatum or possibly A. ertzii but, then again, it does not quite match the characteristics of either of these so, once again, we have left it unnamed (you can find the original descriptions of both these species in the reference list).

According to Algaebase there are 116 species of Achnanthidium that are currently accepted but descriptions of these are scattered through the literature so it is really hard to be confident that you have found a new species during a routine survey.  This is particularly the case when we only have light microscopical analyses with which to work, as the small size of Achnanthidium species means that you really need a scanning electron microscope to see the fine details clearly.  This, however, assumes that the pool of unnamed Achnanthidium species is finite and that the 116 species on Algaebase is a significant proportion of the total number of Achnanthidium species.  A recent study by Eveline Pinseel and colleagues based on samples from Arctic regions offers hints that there is still plenty of diversity within the genus that cannot be linked to named species

This may, however, be a naïve assumption.   My colleague Maria Kahlert, who works in Sweden, comments that she is quite happy looking at samples that I send her from polluted sites in the UK as she can name most of the species (Achnanthidium and otherwise) from her own experience.   It is the samples from pristine habitats that fox her because so many of the forms are different to anything she has encountered in Sweden.  We have, in other words, a neat reversal of the opening line of Anna Karenina (“All happy families are alike, each unhappy family is unhappy in its own way”), with very high beta and gamma diversity of diatoms (probably other microalgae too) as a characteristic of regions with low population density (see “Baffled by the benthos (2)”).  We often miss this in our enthusiasm to fit all that we see down the microscope to published descriptions, but when we take time to look hard, that diversity – and those differences between sites – start to mount up.

Achnanthidium_Petta_Water_May19

The unknown Achnanthidium species from Petta Water, Mainland, Shetland Islands (pictured at the top of the post).  Scale bar: 10 micrometres (= 1/100th of a millimetre).   Photographs: Lydia King

Let’s think of this as an ecological experiment to understand the diversity of Achnanthidium, following the capture-mark-capture approach.   Capture-mark-recapture is a technique used by ecologists to assess the size of a population.   As it is rarely possible to count all individuals, a portion of the population is collected, marked (a dab of paint on a snail’s back, for example) and released.   Some time later, the population is sampled again, and the proportion of those that bear the mark in this second sample is used as an indicator of the proportion of the population captured by the original sample.   Though devised for population biology, some have used the same principles to understand diversity in other contexts too so might it work as a means of understanding the yet-to-be discovered diversity of diatoms?

What we have in the scattered taxonomic literature is a record of all the Achnanthidium species that have been “captured” (i.e. observed) and “marked” (i.e. described) by taxonomists.   Suppose we now go some locations not previously visited by taxonomists, take some new samples and see 1) how many different forms of Achanthidium we can see and b) how many of these are “recaptured” (i.e. forms that align with previously described species).   Or, thinking about the problem in a different way, the number of named species could be compared with the number of distinct “operational taxonomic units” (“OTUs”) detected by metabarcoding.   More relevantly, how many extra OTUs are added when more lakes and streams are added to the dataset?   There are well-established methods for deriving “rarefaction curves” that might be useful in understanding regional diversity of diatoms, and modifications of “capture-mark-recapture” have been used to understand taxonomic diversity in palaeobiolgoical contexts, so why not in contemporary ecology too?

The Shetland Islands would make an ideal test ground for such a study as they are geologically-diverse habitats providing the types of conditions where Achnanthidium species thrive (low population density and agricultural intensity.   The diatoms of the region were studied about 40 years ago by my late mentor John Carter and although one of his samples yielded the type material for Achnanthidium caledonicum there have been so many developments in Achnanthidum taxonomy subsequently that this archipelago represents a tabula rasa for a modern taxonomist.   Its many remote lochs and streams offer the setting for a natural experiment which sets out, to put it bluntly, to quantify our ignorance.

Achnanthidium_caledonicum_Osgaig

Achnanthidium caledonicum from Loch Osgaig, Highland Region, Scotland.   Originally described as Achnanthes microcephala f. scotica Carter & Bailey-Watts 1981 (Scale bar: 10 micrometres (= 100th of a millimetre).  Photographs: Lydia King.

References

Carter J. R., Bailey-Watts A. E. (1981). A taxonomic study of diatoms from standing freshwaters in Shetland. Nova Hedwigia. 33: 513-630.

Pinseel, E., Vanormelingen, P., Hamilton, P. B., Vyverman, W., Van de Vijver, B., & Kopalova, K. (2017). Molecular and morphological characterization of the Achnanthidium minutissimum complex (Bacillariophyta) in Petuniabukta (Spitsbergen, High Arctic) including the description of A. digitatum sp. nov. European Journal of Phycology 52: 264-280. https://doi.org/10.1080/09670262.2017.1283540

Van der Vijver, B., Jarlman, A., Lange-Bertalot, H., Mertens, A., de Haan, M. & Ector, L. (2011).  Four new European Achnanthidium species (Bacillariophyceae).  Algological Studies 136/137: 193-210.

Liow, L.H. & Nichols, J.D. (2010). Estimating Rates and Probabilities of Origination and Extinction Using Taxonomic Occurrence Data: Capture-Mark-Recapture (CMR) Approaches.  The Paleontological Society Papers 16: 81-94).

This week’s other highlights:

Wrote this whilst listening to: Sheku Kanneh-Mason’s recording of Elgar’s Cello Concerto.   Taking me back to his performance at the proms on a warm evening last summer.

Cultural highlight: Sam Mendes’ film 1917 which, coincidentally, uses the River Tees (as featured sporadically in this blog) as one of its locations

Currently reading: I have just finished Good Economics for Hard Times by Abhijit V. Banerjee and Esther Duflo, which I mentioned a couple of weeks ago.  It left me with the feeling that, had both Boris Johnson and Jerermy Corbyn read it and taken on its messages, the election campaign and the UK political landscape might have been very different.

Culinary highlight: OK Diner on the southbound side of the A1 near Grantham.  Felt like we were walking into the opening scene from Pulp Fiction (the one where Tim Roth jumps up onto a table and attempts to rob all the customers).   Escaped with wallet intact.

 

Hooray for hippo dung …

Pygmy_hippo_Jos_1990

I’ve only seen hippopotami in the wild once in my life, and then only at a distance in the Yankari game reserve in northern Nigeria.   I took some photos, but these were taken with only a moderately-powerful telephoto lens and crocodiles basking a few metres from where our Land Rover was parked were a more pressing concern.  In any case, the prints from that holiday (years before digital cameras) are now lost.   The photo at the top of this post is, in fact, a pygmy hippopotamus – a different genus to the common hippopotamus (Hexaprotodon liberiensis rather than Hippopotamous amphibious) – taken at smaller wildlife park (a glorified zoo, really) near Jos but it will do for my purposes. 

A couple of years ago, I wrote about the role that bears may play in the transfer of essential nutrients from the ocean to the forests of north-western North America (see “Ecology’s bear necessities”).  I recently came across a paper that described a situation where hippos were responsible for a significant movement of nutrients in the opposite direction: from land to water.   We think of hippopotami as beasts that wallow in muddy water, but that is because they are filmed and photographed when there is enough light.   Hippos are actually nocturnal animals, coming out of the water to feed on the savannah grasslands when it is dark, and resting in pools during the day.    As they rest in their pools, the grass that they eat during the day is slowly digested (hippos are “pseudoruminants”) and, eventually, passes out of their colons as faeces.   That is an important source of carbon, nitrogen and phosphorus for the river, but also of silicon, an essential nutrient for diatoms.   Diatoms form the base of the food chain in Lake Victoria so, consequently, depend upon a constant supply of silica from the surrounding catchment, and the hippos are inadvertent vectors for this.

There is plenty of silicon in the natural environment (it is the second most abundant element on earth, after oxygen) but most is tightly-bound in particles and so is not in a form that is accessible to other organisms.   Some plants, especially grasses, however, use silicon as a means of strengthening and supporting their cells.  In the process, they also provide a measure of protection (as anyone who has been cut by the sharp edge of a grass leaf will know).  The silicon is taken up by the plant’s roots, but is then laid down in the cells as structures called “phytoliths”.  When these phytoliths are released back into the environment via a tortuous path through the hippo’s digestive system, the silicon they contain is in a much more accessible form than when it was trapped into minerals in the savannah soil.

The phytoliths released by the hippos form about three quarters of all the biologically-available silicon in the hippo pools and, when these have made their way down the stream, may also have an effect on the ecology of Lake Victoria.  At this point, the paper gets rather speculative, but noting that there has already been a significant decline in hippo numbers in recent decades, the authors suggest that this may have had an impact on the ability of diatoms to compete with other algae, contributing to the greater dominance of cyanobacteria that has been observed in recent years.

Even allowing for a little academic hyperbole, this is a useful reminder that trying to keep ecology neatly compartmentalised is never a good idea.  Everything is connected to everything else: lakes, rivers, terrestrial systems.  We sort of know this instinctively but, at the same time, scientists spend so much time absorbed by their specialisms that they often forget this too.   The hippopotamus seems to be an unlikely benefactor of tiny diatoms, but maybe that is the fault of our imagination rather than of nature.

Reference

Schoelynck, J., Subalusky, A. L., Struyf, E., Dutton, C. L., Unzué-Belmonte, D., Van De Vijver, B., Post, D.M., Rosi, E.J., Meire, P. & Frings, P. (2019). Hippos (Hippopotamus amphibius): The animal silicon pump. Science Advances 5: https://doi.org/10.1126/sciadv.aav0395

baboon_Yankari_1990

A baboon, photographed at Yankari game reserve in 1990.  The photograph at the end of the post shows a waterbuck, photographed on the same visit.

And, once again, some notes on what else I have been up to this week:

Wrote this whilst listening to: Keith Jarrett’s Köln Concert

Cultural highlight: Keith Jarrett’s Köln Concert is so good that I am prepared to enter it under two headings.  Worth listening to Tim Harford’s Cautionary Tales Podcast (Episode 7: Bowie, jazz and the unplayable piano) to learn more about this remarkable piece of music.

Currently reading: Raynor Winn’s The Salt Path.  I’m in south-west England so a book about walking the South West Coast Path seems appropriate.

Culinary highlight: yet to happen.  I’m at a conference at the University of Plymouth, subsisting on breakfast from a chain hotel and lunch from a university catering service that offers few options for those who are lactose-intolerant.

waterbuck_Yankari_1990

 

 

Reflections from Castle Eden Burn

As 2019 draws to a close, I have looked back at all the data I have collected from Castle Eden Burn over the past twelve months.   I chose this location precisely because it was different to my usual haunts and, despite having visited this Dene and others along the Durham coast for over thirty years, I realised that I had never had a look at the algae.  Dry river beds are not the most obvious hunting grounds for aquatic biologists, after all.   This year, I put that right over the course of a number of visits between January and November and in this post I am summarising what I found.

I found a total of 77 different diatoms in the six samples that I collected, not to mention green and yellow-green algae (see “When the going gets tough …”) and mosses (see “A thousand little mosses …”).   Of these diatoms, 48 were rare and infrequent, only found in one or two samples, and never forming more than one percent of the total number of diatoms present.   Of the remainder, only two were found in every sample (Humidophila contenta-type and Achnanthidium minutissimum) whilst another eight formed at least ten percent of the total on one occasion.  Numbers of each species waxed and waned over the year: Humidophila contenta-type was abundant in the sample from my first visit in January 2019 but relatively scarce thereafter.  In comparison, Luticola frequentissima was very abundant on two occasions (more than 80% of individuals), quite abundant on three other occasions but absent from the sample from my final visit in November.

Some of these differences are due to the variable flow regime: the stream was dry on three occasions, ponded on one and flowing on just two occasions.  Those occasions when there was no running water were those when the proportions of diatoms that are tolerant to desiccation (see “Life out of water …”) were most abundant, forming from 20 to 97 percent of all individuals.  When there was running water, it was motile Nitzschia  species that dominated.    In fact, there was a strong negative correlation between proportions of desiccation-tolerant and motile taxa in the samples, indicating that the diatoms responded rapidly to the changing pressures experienced in the stream.  There was also a relationship between the proportions of desiccation-tolerant diatoms and the number of taxa recorded – the latter is a good measure of the level of physiological stress experienced in a stream.

What of the diatoms themselves?  Humidophila contenta-type was one of the two ever-presents.  It is, however, very small (few of those in our samples were more than a 100th of a millimetre long), making it difficult to photograph and, indeed, to discern many of the features of the valve.   This species sometimes forms short chains though I did not see any in the Castle Eden Burn samples.  It is strange to think that, when I first started to identify diatoms, this was considered to be part of the genus Navicula.   Since then, it has moved into the genus Diadesmis before finally being transferred to the new genus Humidophila by Rex Lowe and colleagues in 2014.    Some recently-described Humidophila species cannot be differentiated from H. contenta without a scanning electron microscope, so I have referred to this as “Humidophila contenta-type”. Humidophila_contenta

Humidophila contenta ag. from Castle Eden Burn, Co. Durham, January 2019.  Scale bar: 10 micrometres.   Photograph: Lydia King. 

The most abundant diatom in samples collected during the dry periods was Luticola frequentissima.  I started the year referring to this as “Luticola mutica” but was gently corrected by colleagues more au fait with recent literature than me.   Luticola mutica is larger (length: 11-28 µm; breadth: 6-9.5 µm) and has more widely-spaced striae (16-18 / 10 µm) than L. frequentissima (length: 7 – 13.8 µm breadth: 4.8 – 6.8 µm; striae: 20 -24 / 10 µm).  The specimens in the plate below all fit the description for L. frequentissima.  Some of the large specimens have size ranges that overlap with L. mutica (though even the largest specimen as a striae density consistent with L. frequentissima).   L. mutica is associated with more brackish habitats whilst L. frequentissima prefers freshwaters.

Luticola_frequentissima

Luticola frequentissima from Castle Eden Burn, Co. Durham, January 2019. Scale bar: 10 micrometres (= 1/100th of a. millimetre).  Photographs: Lydia King.

Simonsenia delognei is another characteristic species of habitats that dry out periodically.   This species, which is in the same family as Nitzschia, is quite small and only lightly silicified so easily overlooked.  It was common early in the year, but rare thereafter.  Whether this is a real characteristic of the species or an artefact of the conditions in Castle Eden Burn this year is difficult to tell as it is not a particularly common species so there are few other records against which this trend can be compared.

Simonsenia_delognei_CEB

Simonsenia delognei from Castle Eden Burn, Co. Durham, January 2019.  Scale bar: 10 micrometres (= 1/100thof a millimetre). Photographs: Lydia King.

Two other species of Nitzschia were common: I illustrated N. clausii in “Out of my depth …” and have included photographs of N. sigma here.   I’m intrigued that two of the most conspicuous Nitzschia in this sample are sigmoid in outline.  I’ve visited the question of sigmoid diatoms before, and still don’t have any good explanation why a few diatoms have this outline (see “Nitzschia and a friend …”).  Note, too, that Nitzschia species can be sigmoid in valve view (i.e. looking down from above) or girdle view (i.e. looking from the side), although the great majority of species are straight in both planes.

Nitzschia_sigma

Nitzschia sigma from Castle Eden Burn, Co. Durham, January 2019.  Scale bar: 10 micrometres (= 1/100th of a millimetre).   Photographs: Lydia King.

Finally, one more relative of Nitzschia that was found in a couple of samples, but never in large numbers, was Tryblionella debilis.  The genus Tryblionella was treated as part of Nitzschia for much of the 20th century.   As it appears to form a natural group with some distinctive characteristics, it is now generally treated as a distinct genus, although the molecular evidence indicates a complicated evolutionary history.   The principle characteristic of the genus is a longitudinal undulation on the valve face that is most clearly manifest on those species in the genus which have visible striae.   T. debilis is a small species with striae that are not resolvable with the light microscope; however, the undulations are just apparent as faint longitudinal lines running along the valve face.

Tryblionella_debilis

Tryblionella debilis from Castle Eden Burn, Co. Durham, January 2019.  Scale bar: 10 micrometres (= 1/100th of a. millimetre).  Photographs: Lydia King.

That’s a lot of diatoms from a stream that is not always a stream.   I am sure that someone with interests in other groups of algae could probably make similarly long lists for some of those, and a more thorough exploration of habitats within the stream could add to the number of diatoms.  That’s before suggesting a molecular study, which might well reveal cryptic diversity (i.e. significant taxonomic variation that is impossible to discern with a light microscope) within the species I have already described.   The greater our capacity to unravel the mysteries of the microscopic world, the more, it seems, we discover we don’t know.

Reference

Lowe, R.L., Kociolek, P., Johansen, J.R., Van de Vijver, B., Lange-Bertalot, H. & Kopalová, K. (2014).  Humidophilagen. nov., a new genus for a group of diatoms (Bacillariophyta) formerly within the genus Diadesmis: species from Hawai’i, including one new species.  Diatom Research 29: 351-360.

Castle Eden Dene in November

Castle_Eden_Burn_Nov19

For the first time this year, I heard Castle Eden Burn before I saw it.  Walking down from the car park, the distant roar of water was apparent almost as soon as the canopy of largely leafless branches closed over me.  A few trees still held their leaves – spectacularly golden on beech and birch, in particular, and the Dene’s famous yews were still green, of course – but the forest was dressed for winter now, much as it was on my first visit this year, back in January (see “Castle Eden Dene in January”).  Then, I was surprised that there was no water in the Burn.  On this trip, however, I wore my chest waders.  Back in August, I had compared Castle Eden Burn to a wadi (see “The presence of absence in Castle Eden Dene”) so the heavy rain of the previous few weeks had led me to suspect that today would be different.

The water surging through the Dene was very turbid, so collecting stones to examine involved feeling around on the river bed with my hand until I located one that was not sufficiently bedded into the substratum to remove.   That’s not ideal, but needs must and I got the five cobbles I needed, each with a distinct biofilm, slimy to the touch.  This is the first time, after eleven months, that Castle Eden Burn’s substratum has looked and felt remotely like the substratum from most of the other rivers I know in this part of the world.

Under the microscope, I see lots of particulate matter but also plenty of algae.   Apart from a few filaments of the cyanobacterium Phormidium, these were mostly diatoms.   The green algae I described in “When the going gets tough …” back in May were not obvious.  The diatoms were mostly largely motile cells of Navicula, with a few sigmoid cells of Nitzschia clausii and some smaller cells whose identity I will need to confirm once I have cleaned the sample and prepared a permanent slide.  The Navicula species, in particular, are typical inhabitants of local rivers during winter and early spring, all tolerant to a wide range of conditions.   I suspect that the rainfall has washed a lot of fine particulate debris from the industrial estates in the upper catchment into the river, and these diatoms will have the resilience to cope with such types of pollution.  A large storm sewer overflow also empties into the burn about a kilometre upstream of where I was standing and this, I suspect, has been flowing over the past month or two.

I also saw a few cells of Achnanthidium minutissimum, which I generally associate with cleaner conditions.  I suspect, however, that numbers will be relatively low compared to its more pollution-tolerant brethren.   Again, I can give a more authoritative answer once I have cleaned the sample and performed a full analysis.

CEB_diatoms_Nov19

Diatoms from Castle Eden Burn, November 2019.  a., b.: Navicula trpunctata; c. – e.: Navicula lanceolata; f., g.: Rhoicosphenia abbreviata; h., i.: Nitzschia clausii; j., k.: Navicula gregaria; l. Achnanthidium minutissimum.   Scale bar: 10 micrometres (= 1/100thof a millimetre).   The photograph at the top of the post shows Castle Eden Burn just downstream from the point I sampled.

I originally set out to visit Castle Eden Burn six times during 2019 and this was the last of those. I’ve written about most of these visits already but not about my September visit.  There was, on that occasion, little new information to justify a separate post but I will include the sample I collected in my final overview of the algae of Castle Eden Burn, just as soon as I get this final sample cleaned and analysed.   Before then, I have one more post to write about the diatoms, based on some more detailed observations of a few of the species, and then it will be time to think about where to focus my observations during 2020.

Diatoms from the Troodos mountains

Troodos_snowscape_Apr19

Back in April, I wrote two posts about the algae from a stream draining a chromite mine in the Troodos mountains in Cyprus (see “Survival of the fittest (1)” and “Survival of the fittest (2)”).  I also planned to write a post about the diatoms growing in the stream but the slide I prepared has been sitting on my desk over the summer whilst I was distracted by other things.  However, I have just started looking at some samples from metal-enriched streams in the northern Pennines and, curious to see whether a Cypriot chromite mine had similar effects, I blew the dust off the slide and slipped it under my microscope.

The principal effect of toxic pollution is to reduce the number of species found and, in this respect, my sample from the outflow of the Hadjipavlou mine outflow was true to form, containing just eight species.  The most abundant of these was Meridion circulare, accounting for one in four of all the cells.  What is more, many of the cells were visibly distorted (see images a., c. and d., in particular, in the plate below).  This is quite a common phenomenon in metal-polluted streams (see “A twist in the tale”) though I have not seen it quite so obviously in Meridion circulare before. My own pet theory is that one of the enzymes involved in laying down the silica cell wall has a metal co-factor that is displaced by heavy metals.

Meridion_circulare_Hadjipavlou_Apr19

Meridion circulare from thepebbles from the stream draining Hadjipavlou chromite mine in the Troodos mountains, Cyprus, March 2019.  Scale bar: 10 micrometres ( = 1/100th of a millimetre).   The photograph at the top of the post shows snow on the Troodos mountains near the mine.

The only other diatom that was at all common in the sample was Hantzschia amphioxys, which also occurred alongside a smaller population of Hantzschia abundans.  I’ve not come across Hantzschia in metal-enriched streams before: it is a species that is most often associated with habitats that are not permanently submerged.  That may be the case at Hadjipavlou but the water that flows from mines comes from groundwater rather than rainfall so would not be subject to the strong seasonal variations that we associate with Mediterranean streams.  It is hard to draw a firm conclusion from a single visit.   Unlike Meridion circulare, however, neither population of Hantzschia showed any obvious distortion, perhaps due to the Hantzschia cells being more heavily silicified than those of Meridion circulare.

The extent to which cellular distortions are obvious does vary between species, as can be seen in “A twist in the tale …”  which compared three different representatives of the same genus in a metal-polluted stream.  I chose the word “obvious” with care as I do think that these phenomena are more easily seen in long thin cells than in shorter ones.  In the same Pennine streams where distorted Fragilaria are common, for example, I can also see distorted cells of smaller diatoms such as Achnanthidium minutissimum.  But you need a keen eye to spot these reliably.   Some other people have used fluorescent stains to look at other cellular irregularities, such as the position of the nucleus and damage to the nuclear membrane, but these require specialist approaches whereas distortions to cell outlines can be spotted from a standard analysis.

Hantzschia_spp_Hajipavlou_Apr19

Hantzschia abundans (k., l.) and Hantzschia amphioxys (m. – p.) in the from the stream draining Hadjipavlou chromite mine in the Troodos mountains, Cyprus, March 2019.  Scale bar: 10 micrometres ( = 1/100th of a millimetre). 

A few years ago I was involved in a study of diatoms from streams in Cyprus and I dug out some of these data in order to put the Hadjipavlou sample into context.  One immediate surprise was that many of the “reference” (i.e. pristine or near-pristine) samples in that survey also had relatively low diversity.   The 45 samples in this subset had, on average, nine species, and a mean Shannon diversity index of 1.7, compared to eight species and a Shannon diversity index of 1.42 for the Hadjipavlou sample.   I’ve never been a fan of diversity indices as measures of ecological quality (see “Baffled by the benthos (2) and links therein”) although I suspect that average diversity at Hadjipavlou measured over a period of time will always be low whereas average diversity at unimpacted sites is more likely to fluctuate. Equally, low diversity coupled with a second strand of evidence, such as distorted valves, is a useful sign to an ecologist that something untoward is happening.

diversity_indices

Number of taxa (left) and Shannon diversity (right) recorded in 45 samples from “reference” sites (i.e. minimal evidence of anthropogenic alteration) in Cyprus.  The arrows indicate the location of the Hadjipavlou stream within this dataset. 

The irony of writing about a heavily-polluted stream in the Troodos mountains is that the geological conditions which created the metal-rich veins hereabouts also create conditions for many plants endemic to Cyprus.   The serpentine and other ultramafic rocks create metal-rich soils within which few plants can survive (more about these here. I suspect that few of the plant enthusiasts drawn to Cyprus will ever cast more than a cursory glance at the green flocs adorning the abandoned mines of the Troodos mountains.

References

Licursi, M., & Gómez, N. (2013). Short-term toxicity of hexavalent-chromium to epipsammic diatoms of a microtidal estuary (Río de la Plata): Responses from the individual cell to the community structure. Aquatic Toxicology 134-135: 82-91.  https://doi.org/10.1016/j.aquatox.2013.03.007