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.

 

More algae from Shetland lochs …

Lamba_Water_May19

I’m taking you back in the Shetland Islands for this post, and onto the remote moorlands of northern Mainland.   When I visited this particular loch in 2016, I noticed a lot of slippery filaments of Batrachospermum attached to the sides of the cobbles in the littoral zone (see “Lucky heather …”).   This time around, I explored further around the edge of the loch and, in the south-west corner noticed prolific growths of algae in the shallow peaty water.  Closer inspection showed that these, too, were the red alga Batrachospermum and, though they were not fertile, Dave John suggests that they are likely to be B. turfosum Bory.

Batrachospermum_Lamba_Water_May19

Tufts of Batrachospermum turfosumin the littoral zone of Lamba Water, north Mainland, Shetland Islands, May 2019.   The picture frame is about 15 centimetres across. 

If you have a hand lens you can just about make out a bead-like structure when observing Batrachospermum in the field; however this becomes much clearer with higher magnification.   I think it looks like a bottle-brush when seen under the microscope at low magnification, with whorls of side-branches arising from the central filament.  At higher magnification, these filaments can be seen to have a bead-like structure, with cell size gradually reducing with distance from the centre.

What you cannot do in the field is separate Batrachospermumfrom the closely-related genus Sheathia(see “News about Batrachospermum… hot off the press”).   I usually tell people that, for a general overview of the condition of a stream or lake (for example, as part of the UK macrophyte survey technique), then simply recognising that you have “Batrachospermum” (meaning Batrachospermum or Sheathia) should be enough.   In my experience, the presence of Batrachospermumis usually a good indication that the water body is in a healthy condition.  However, I have been told that Batrachospermumis often found growing prolifically in very enriched conditions in southern chalk streams, which would challenge this assumption.   This may be because the species that are found in southern chalk streams are different to those that I encounter in my more usual haunts in northern England and Scotland.  But it is also possible that the factors I described in “The exception that proves the rule …” pertain in those cases too.

Batrachospermum_turfosum_Lamba_Water

Filaments of Batrachospermum turfosum from Lamba Water, north Mainland, Shetland Islands, May 2019.   The upper photograph shows a low magnification view of a filament (about 350 micrometres, or 0.35 millimetres, wide) whilst the lower image shows a whorl of side branches arising from the main stem.  Scale bar: 20 micrometres (= 1/50thof a millimetre).  

We often run into this dilemma with filamentous freshwater algae: it is reasonably straightforward to identify the genus but we need reproductive organs to determine the species.  As they seem to survive quite happily in the vegetative state our understanding of the ecology of individual species (rather than the genus as a whole) is scant so it is hard to tell whether there is value in that missing information or not.   In a few cases – this is one – better taxonomic understanding has revealed that we may not even be dealing with a single genus but the lists used for applied ecological surveys still persist with the old concepts.

This creates a toxic spiral of consequences: it is hard to split into species so most people don’t bother. Because we don’t bother, our interpretations are based on generalisations drawn from the behaviour of the genus.  This means we don’t generate the data needed to demonstrate the value (or otherwise) of the effort required to go from genus- to species-level identifications.   So we carry on lumping all records to genus (or, in this case, a pair of genera) and accept a few records that our out of line with our expectations as “noise”.  The situation is probably worse in the UK than in many places because there are very few people in universities specialising in these organisms and, as a result, no-one is producing the data that might break us out of this spiral.

We found Batrachospermum turfosum in a few other locations during our visit, but nowhere, even in nearby lochs, was it in such quantity as we saw in Lamba Water.   Chance might play a part in determining its distribution on a local scale but that ought to be the explanation of last resort rather than the go-to answer when we are worryingly short of hard evidence.

 

 

Hyperepiphytes in the Shetland Islands

Gossa_Water_May19

I was lucky enough to spend a couple of days in the Shetland Islands during last week’s spell of warm weather and spent one of my mornings there hiking in shirtsleeves across moorland to a remote loch.   Good infrastructure is a legacy of the Shetland Islands’ association with the oil industry, and this includes a strong mobile network, meaning that I managed to find this particular loch using the Ordnance Survey maps on my smartphone. I would not normally rely upon a mobile signal to navigate across such remote terrain but in Shetland it is often possible.  I would, nonetheless, recommend keeping a paper map and a GPS in your kit just in case, as I did lose the signal on a few occasions during my stay.

Most of the lochs in the northern part of mainland Shetland are shallow, peaty water bodies, with soft water and relatively sparse assemblages of aquatic plants.   Parts of the littoral zone of this particular loch, however, had extensive growths of submerged mosses.  It is a long time since I was proficient at identifying aquatic mosses but these clumps look likeWarnstofia fluitans to me, though I am willing to be proved wrong.  I did try to remove some leaves and have a proper look but that task was complicated by tufts of attached filamentous algae.   In their submerged state, these formed distinct clusters at intervals along the straggly stems of the moss but, once removed, the filaments collapsed to smother the leaves and confound my attempts to run a scalpel blade along the stem.

Warnstofia_Gossa_Water_May19

Submerged colonies ofWarnstorfia fluitans(?) smothered byOedogoniumfilaments in Gossa Water, north Mainland, Shetland (HU 4354 6047). Gossa Water (one of five that share this name in the Shetland Islands!) is illustrated in the photograph at the top of this post.

The filamentous alga proved easier to unmask: the unbranched filaments, reticulate (net-like) chloroplasts and distinctive ‘cap cells’ all identifying it as the green alga Oedogonium.  As is often the case, however, the populations lacked any sexual organs so it was impossible to know which species (see “The perplexing case of the celibate alga“ and, for a rare case of a sexually-mature filament, “Love and sex in a tufa-forming stream”).   Abundant epiphytes can be another feature of Oedogonium: unlike several other filamentous green algae it produces little mucilage which makes it easier for diatoms, in particular, to colonise.  As well as colonies of needle-shaped cells of Fragilaria gracilis there were also several Achnanthidium cells and, entangled around the filaments and the moss, chains of Tabellaria flocculosa.   Given that the Oedogonium was, itself, an epiphyte, these diatoms are ‘hyperepiphytes’, a term that attracts remarkably few Google hits, almost all associated with lower plants.

The ‘cap cells’ are one of the most distinctive features of Oedogonium and results from a distinctive mode of cell division that leaves rings of scar tissue at the point where the two cells split.   That we see four or more of these scars on a few cells whilst the great majority have none suggests that we are looking at a primitive form of specialisation, with a few cells in a filament being responsible for all the cell division.  What is more, these cap cells are also often the ones that form oogonia (see “Love and sex in a tufa-forming stream” for an illustration of this) and asexual zoospores, so there must be something slightly different in the biochemistry within these cells that drives these processes.   However, at this point the formal scientific literature goes strangely silent apart from a single paper published in 1962.  Curiously, the evolution of multicellularity is one of those big questions that attract a lot of top academics (see the reference to a recent paper in Nature Scientific Reports below)  whilst a genus of algae that seem to show some faltering first steps towards specialisation of some cells are largely ignored.  Another case of the “trailing edge” of science?

Gossa_Oedogonium

Oedogonium filaments growing on Warnstofia fluitans in the littoral zone of Gossa Water, north Mainland, Shetland, May 2019.   The arrow on the top image shows the “cap cells”.   Note also the cluster of Fragilaria gracilis(plus a few cells of Achnanthidium) on the lowermost filament and, in the middle image, two of the many cells of Tabellaria flocculosa that were entangled with the Oedogonium filaments and moss stems.  Scale bar: 20 micrometres (= 1/50thof a millimetre). 

Oedogonium_zoospores

A zoospore being released from a filament of Oedogonium.  This series of photographs was taken by me in about 1993 and I have no details of the location from which it came.  The filament is about 40 micrometres (= 1/25thof a millimetre) in diameter.

Reference

Herron, M.D., Borin, J.M., Boswell, J.C., Walker, J., Chen, I-C. K., Knows, C.A., Boyd, M., Rosenzweig, F. & Ratcliff, W.C. (2019).  De novo origins of multicellularity in response to predation.  Nature Scientific Reports 9, Article number: 2328

Rawitscher-Kunkel, E. & Machlis, L. (1962).  The hormonal integration of sexual reproduction in Oedogonium.   American Journal of Botany 49: 177-183.

St_Ninians_tombola_Shetland_May19

Sightseeing in Shetland: the tombolo (sandy isthmus) linking St Ninian’s Isle with Mainland in the Shetland Islands, May 2019.