Follow this link to find a guest post that I have just written for Luca Marazzi’s blog, describing the biology of Navicula lanceolata.
Whilst looking at some samples from an experiment conducted on mesocosms beside a chalk stream, Candover Brook in Hampshire for Mark Ledger and colleagues, I came across a diatom that I had not seen before and which, at first glance, was out of place. As the images above show, it is a diatom whose cells join together to form chains which, in turn, means that they typically present their sides to the viewer rather than the valve face, which is the way that the writers of identification guides generally assume that we can see. It took some time to track down a couple of cells that were lying face-upwards so that I could try to name the species and some of the few that were lying this way were damaged (see left hand image), perhaps itself a consequence of the naturally strong links between the cells.
Naming the genus was relatively straightforward: the valve shape, fine striae and very narrow axial area (the gap along the median line of the valve face between the two rows of striae) coupled with the tendency to form chains all pointed to Fragilariforma. However, most of the Fragilariforma that I encounter are in soft water, often acid habitats whilst this sample was from a flume beside a chalk stream in southern England. After scratching my head a little more, and sending images to my friend Lydia in Germany, I eventually decided that Fragilariforma nitzschioides was the most likely name for this diatom. Searching through my records, I found only one other record for this species: from the River Itchen (into which Candover Brook drains) in the mid-1990s. That must be more than coincidence. Interestingly, Hoffman et al. (2011) describe the species as “rare” and say that its ecological preferences are “difficult to define”.
The limited records that we have show that this species does not behave in the same way as most other representatives of the genus. The weighted average of pH for the genus is 6.6 (see graph below), but there are plenty of records extending into more acid waters. By contrast, the River Itchen population was recorded at pH 8.1 and the pH in Candover Brook will be very similar. Most of the records for the genus came from relatively soft water, in contrast to the very hard water found in a chalk stream. The scarcity of records of a species that is well described in the literature also suggests that this might be a genuinely rare diatom (see “A “red list” of endangered British diatoms”).
One other peculiarity of this species is the name itself. Fragilariforma was one of a number of genera split away from Fragilaria by Dave Williams and Frank Round in 1986, originally as “Neofragilaria”. Fragilaria nitzschoides, was not formally transferred at the time, presumably because the authors did not have access to the type material. They presented good evidence for this new genus but a few people – notably Horst Lange-Bertalot – have continued to group these species under Fragilaria. This is the situation in Diatomeen im Süsswasser-Benthos von Mitteleuropa but, curiously, for Fragilaria nitzschoides, he created the new combination of “Fragilariforma nitzschoides” purely as a synonym (see p. 268). The good news is that the next version of this book (see “Tales of Hoffman”) does use these new names.
The relationship between Fragilariforma spp and pH (left) and alkalinity (right) in UK rivers, based on the mid-1990s dataset described in “The challenging ecology of a freshwater diatom”. Vertical lines show the boundaries for high (blue), good (green), moderate (orange) and poor (red) status classes based on current UK standards and the arrows show the location of the River Itchen population of Fragilariforma nitzschoides along these gradients.
Hofmann, G., Werum, M. & Lange-Bertalot, H. (2011). Diatomeen im Süßwasser-Benthos von Mitteleuropa. A.R.G. Gantner Verlag K.G., Rugell.
Williams, D.M. & Round, F.R. (1987). Revision of the genus Fragilaria. Diatom Research 2: 267-288.
Williams, D.M. & Round, F.R. (1988). Fragilariforma nom nov., a new generic name for Neofragilaria Williams & Round. Diatom Research 3: 265-267.
Writing the previous post led me to contemplate how much things had changed over the time that I have been working in this field. Back in the early 1990s when I first set out to look at the response of diatoms to nutrients in streams, few in the National Rivers Authority (NRA, predecessor to the Environment Agency) regarded phosphorus as a serious pollutant in rivers, and most biologists thought about ecological quality solely in terms of organic pollution and invertebrates. In order to investigate the effect of nutrients, I wanted to visit sites where organic pollution was not a problem.
I was helped in this task by the work done by biologists at the then Institute for Freshwater Ecology (now Centre for Ecology and Hydrology) who had just developed the early versions of RIVPACS (“River Invertebrate Prediction and Classification System”) which established the principle of expressing ecological quality as the observed quality / expected quality. This, in turn, required an ability to predict the “expected” condition for any stream. The work that had developed these equations started from a dataset of invertebrate and environmental data collected from a wide range of “unpolluted” running water sites which, in those far off days, was compiled by asking biologists working for the Regional Water Authorities (predecessors to the NRA) for their recommendations of sites that were of “good” or “fairly good” quality. Nowadays, screening sites to be used for calibrating ecological methods is a much more rigorous procedure but this was the first tentative step on a long journey and “expert judgement” was as good a place to start as any.
The paper that emerged from this exercise (see reference below) analysed data from these “unpolluted” sites and classified them into eight groups. Each of these groups consisted of sites that shared similar invertebrate assemblages which reflected similarities in the habitat, from upland, fast flowing becks to deep, wide slow-flowing rivers in the lowlands. The authors included a useful table that listed the physical and chemical characteristics of each of these groups and I noticed that the phosphorus concentrations reported for these spanned a very wide range. This meant that I could use these as the basis for putting together a sampling program that spanned a long gradient of nutrient pressure without the complications of organic pollution. The outcome of that work was the first of the two papers referenced in my previous post.
Time has moved on and I thought it would be interesting to revisit these “unpolluted” sites to see how they would be classified using the UK’s current standards for phosphorus. This highlights a striking difference between the prevailing idea of “unpolluted” in the early 1980s and the present day, as all of these groups had average concentrations that equate to substantial enrichment by modern standards; in half the groups this average concentration would be classified as “poor status” whilst the maximum concentrations in three groups equates to “bad status”. Whatever way you look at it now, these sites were far from “unpolluted”.
Classification of TWINSPAN end-groups of unpolluted river sites in Great Britain based on Armitage et al. (1984) along with average and maximum phosphorus concentrations recorded in each group and the phosphorus status based on current environmental standards. M = moderate status; P = poor status; B = bad status.
I am not being critical of the approach taken by Patrick Armitage and colleagues. In many ways, I regard the work of this group as one of the most significant contributions to the science of ecological assessment in my lifetime. I am just intrigued to see how the thinking of ecologists and regulators has moved on in the thirty years or so since this paper was published. I know from my own early conversations with NRA biologists that inorganic nutrients were not perceived as a problem in rivers until the early 1990s. It was probably the European Community’s Urban Wastewater Treatment Directive (UWWTD) that started to draw the attention of biologists in the UK to these problems, and which led to the development of stricter environmental standards for nutrients, though not without opposition from several quarters.
This, then is a situation where good legislation provided the impetus needed to start the process. There were places in the UK – rivers in the Norfolk Broads, for example – where nutrients were already being regulated, but these were special circumstances and nutrient problems in most rivers were largely ignored. Indeed, as I said in my previous post, phosphorus was not even measured routinely in many rivers. I heard via my professional grapevine that it was the Netherlands who had made the case for the clauses in the UWWTD concerning regulating nutrients, as their stretches of the lower Rhine were subject to numerous problems caused by unregulated inputs of nutrients from countries upstream. I do not know if this is true, but it is certainly plausible. However, once the need to control eutrophication in rivers was codified in UK law, then the debate about how to evaluate it started, one of the outcomes of which was more funding for me to develop the Trophic Diatom Index (referenced in the previous post). And, gradually, over time, concentrations in rivers really did start to fall (see “The state of things, part 2”). I’d like to think the TDI played a small part in this; though this might also mean that I am partially responsible for the steep increase in water charges that everyone endured in order to pay for better water quality …
Armitage, P.D., Moss, D., Wright, J.F. & Furse, M.T. (1984). The performance of a new biological water quality score system based on macroinvertebrates over a wide range of unpolluted running-water sites. Water Research 17: 333-347.
Amphora pediculus from Polly Brook, Devon, December 2016. Scale bar: 10 micrometres (= 1/100th of a millimetre).
The images above show one of the commonest diatoms that I find in UK waters. It is a tiny organism, often less than 1/100th of a millimetre long, which means that it tests the limits of the camera on my microscope. In recent months, however, it is not just the details on Amphora pediculus’ cell wall that I am struggling to resolve: I also find myself wondering how well we really understand its ecology.
The received wisdom is that Amphora pediculus favours hard water, does not like organic pollution and is relatively tolerant of elevated concentrations of inorganic nutrients. This made it a very useful indicator species in a period of my career when we were using diatoms to identify sewage work s where investment in nutrient-removal technology might yield ecological benefits. There were many nutrient-rich rivers, particularly in the lowlands, where any sample scraped from the upper surface of a stone was dominated by these tiny orange-segment-shaped diatom valves. Unfortunately, twenty years on, many of those same rivers have much lower concentrations of nutrients (see “The state of things, part 2”) but still have plenty of Amphora pediculus. Did I get the ecology of this species wrong?
The graph below shows some data from the early- and mid- 1990s showing how the abundance of Amphora pediculus was related to phosphorus. The vertical lines on this graph show the average position of the boundaries between phosphorus classes based on current UK standards. Records for A. pediculus are clustered in the “moderate” and “poor” classes, supporting my initial assertion that this species is a good indicator of nutrient-enriched conditions, but there are also samples outside this range where it is also abundant, so A. pediculus is only really useful when it is one of a number of strands of evidence.
The relationship between Amphora pediculus and reactive phosphorus in UK rivers, based on data collected in the early-mid 1990s. Vertical lines show the average boundaries between high and good (blue), good and moderate (green), moderate and poor (orange) and poor and bad (red) status classes based on current UK standards and the two arrows show the optima based on this dataset (right) and data collected in the mid-2000s (left).
If we weight each phosphorus measurement in the dataset by the proportion of Amphora pediculus at the same site (i.e. so that sites where A. pediculus is abundant are given greater weight), we get an idea of the point on the phosphorus gradient where A. pediculus is most abundant. We can then infer that this is the point at which conditions are most suitable for the species to thrive. In ecologist’s shorthand, this is called the “optimum” and, based on these data, we can conclude that the optimum for A. pediculus is 154 ug L-1 phosphorus. The right hand arrow indicates this point on the graph below. However, I then repeated this exercise using another, larger, dataset, collected in the mid-2000s. This yielded an optimum of 57 ug L-1 phosphorus (the left hand arrow on the graph), less than half of that suggested by the 1990s dataset. There are, I think, two possible explanations:
First, the 1990s phosphorus gradient was based on single phosphorus samples collected at the same time that the diatom sample was collected (mostly spring, summer and autumn) whilst the mid-2000s phosphorus gradient was based (mostly) on the average of 12 monthly samples. As phosphorus concentrations, particularly in lowland rivers, tend to be higher in summer than at other times of the year, it is possible that part of the difference between the two arrows is a result of different approaches. (For context, in the 1990s, when I first started looking at the effect of nutrients in rivers, phosphorus was not routinely measured in many rivers, so we had no option but to do the analyses ourselves, and certainly did not have the budget or time to collect monthly samples).
However, another possibility is that the widespread introduction of phosphorus stripping in lowland rivers in the period between the mid-1990s and mid-2000s means that the average concentration of phosphorus in the rivers where conditions favour Amphora pediculus have fallen. In other words, A. pediculus is tolerant of high nutrient conditions but is not that bothered about the actual concentration. My guess is that it thrives under nutrient-rich conditions so long as the water is well-oxygenated and, as biochemical oxygen demand is generally falling, and dissolved oxygen concentrations rising (see “The state of things, part 1”), this criterion, too is widely fulfilled. I suspect that both factors probably contribute to the change in optima.
But the second point in particular raises a different challenge: We often slip into casual use of language that implies a causal relationship between a pressure such as phosphorus and biological variables whereas, in truth, we are looking at correlations between two variables. Causal relationships are, in any case, quite hard to establish and the effect that we call “eutrophication” is really the result of interactions between a number of factors acting on the biology. All of these simplifications mean that it is useful, from time to time, to look back to see if assumptions made in the past still hold. In this case, I suspect that some of our indices might need a little fine-tuning. There is no disgrace in this: the evidence we had in the 1990s led us to both to a conclusion about the relative sensitivity of Amphora pediculus to nutrients but also fed into a large-scale “natural experiment” in which nutrient levels in UK rivers were steadily reduced. When we evaluate the results of that natural experiment we see we need to adjust our hypotheses. That’s the nature of science. As the sign on the door of a friend who is a parasitologist reads: “if we knew what we were doing, it wouldn’t be research”.
The 1990s dataset (89 records) is mostly based on data used in:
Kelly M.G. & Whitton B.A. (1995). A new diatom index for monitoring eutrophication in rivers. Journal of Applied Phycology 7: 433-444.
The mid-2000s dataset (1145 records) comes from:
Kelly, M.G., Juggins, S., Guthrie, R., Pritchard, S., Jamieson, B.J., Rippey, B, Hirst, H & Yallop, M.L. (2008). Assessment of ecological status in UK rivers using diatoms. Freshwater Biology 53: 403-422.
For the past five years or so the constant companion on my desk whilst I stare down my microscope has been a thick tome (2.8 kg) entitled Diatomeen im Süßwasser-Benthos von Mitteleuropa by Gabi Hofmann and colleagues. It serves as my aide-mémoire when I am analysing freshwater diatoms, jogging my memory when I see a diatom that I recognise but whose name I have forgotten. Before this was published, I used a French publication Guide Méthodologique pour la mise en oeuvre de l’Indice Biologique Diatomées which was free to download (I cannot find a link on the web any longer, unfortunately). Neither of these is the last word in diatom taxonomy, but that was not the point: a lot of the time, I just need a gentle reminder of the right name for the species I am looking at, and I don’t want to have to pore through a pile of books in order to find this.
One of the strong points of both books is that they are copiously illustrated, and the plates are arranged very logically so that similar-shaped diatoms are together, making it easy to pick out differences. For most routine identification, this is exactly what is needed: we may pretend that we are logical people but, in truth, pattern matching beats using a key nine times out of ten. The 133 plates in Diatomeen im Süßwasser … act as a visual index and, to make life even easier, the species descriptions are arranged alphabetically and cross-referenced in the plates. Having found an image that resembles the diatom I am trying to identify, it is straightforward to flick to the description to check the details.
There is just one problem: Diatomeen im Süßwasser-Benthos von Mitteleuropa is in German, and quite technical German at that. I tell people not to worry because all the images are in English but, in truth, I worry that I may lose some of the nuances due to my linguistic limitations. I was delighted, then, to be asked by Marco Cantonati to help produce an English version of the book. Marco is half-German so reads and speaks the language fluently, and I was able to work on his first drafts in English to produce the final text. Conscious that translating a German book into English is only a partial solution for the almost 70% of the EU who have neither as their first language, we also unpicked the prose in order to put the information about each species into a series of “bullet points” so that it was more accessible and we also took the opportunity to update some of the taxonomy. A large part of last weekend was spent poring over the proofs so it should not be long now before it is available to purchase.
The great irony for me is that I am putting the finishing touches to this book at the same time as I am helping the Environment Agency to move away from using the light microscope to identify diatoms altogether. I am just finalising the last of the regular competency tests that I organise in which, Environment Agency staff will participate, after which routine samples will be sent off for Next Generation Sequencing rather than being analysed by light microscope. I’ve written about the pros and cons of this before (see “Primed for the unexpected …”) but there is a funny side. After over a decade of struggling with identification literature in a language that almost none of them spoke my dedicated band of Environment Agency analysts get the book they dreamed about two months after their last diatom slide is packed away. My sense of timing is, as ever, impeccable …
Hofmann, G., Werum, M. & Lange-Bertalot, H. (2011). Diatomeen im Süßwasser-Benthos von Mitteleuropa. A.R.G. Gantner Verlag K.G., Rugell.
Prygiel, J. & Coste, M. (2000). Guide Méthodologique pour la mise en oeuvre de l’Indice Biologique Diatomées. NF T 90-354. Cemagref, Bordeaux.
Some part-time sleuthing on a sample that I was sent a couple of weeks ago have resulted in a new addition to the UK freshwater diatom flora. The slide came to me from an Environment Agency laboratory with a question mark over a small diatom that was quite abundant but which did not match any of the species with which they were familiar. It was a small diatom, only about 10 micrometres (1/100th of a millimetre) long, with very fine features, but there were enough features visible for me to realise that it was not something that I had seen before either. I sent images off to a couple of colleagues and we decided that it was a species of Nupela, probably N. neglecta.
Nupela was only established in 1991. Before that, species that we now place in this genus were spread between Achnanthes and Navicula, as people struggled to understand its characteristics. If you look at diatom keys written before Nupela was established (and several written subsequently – including my own), the presence of a raphe on either or both valves is seen as an important distinguishing characteristic, and the small number of genera that have a raphe on just one valve were generally assumed to be related. Nupela, however, has some representatives that have a raphe on one valve (formerly placed in Achnanthes) and representatives that have a raphe on both valves (formerly placed in Navicula). Nupela neglecta has a raphe on both valves, but one of the valves has raphe slits that only extend for about half the total length. Stir in the small size and morphological details that are barely visible with the light microscope and there is ample scope for confusion.
Valves of Nupela cf neglecta with a full raphe. Scale bar: 10 micrometres (= 1/100th of a millimetre). The double lines indicate a single valve at different focal points. Photographs: Chris Carter.
Valves of Nupela cf neglecta with a short raphe. Scale bar: 10 micrometres (= 1/100th of a millimetre). The double lines indicate a single valve at different focal points. Photographs: Chris Carter.
The sample was collected from the River Stor, a tributary of the River Arun, in West Sussex, downstream of Storrington sewage works (NGR: TQ 0681 1641). This is a small hard water stream (average pH: 7.9; average alkalinity: 170 mg L-1 CaCO3) with very high concentrations of nutrients (average dissolved reactive phosphorus: 0.99 mg L-1; average total oxidised nitrogen: 5.0 mg L-1). These observations are similar to those made by Marina Potapova and her colleagues for habitatas where they found N. neglecta in the USA. And this raises an interesting paradox: normally, the presence of a rare and exotic organism is considered to be a reason for conserving a habitat. In this case, however, the rare species seems to be associated with a polluted habitat and, as a result, the Environment Agency will be doing their best to drive any organism that thrives here (however rare) to extinction. Discuss.
Krammer, K. & Lange-Bertalot, H. (1991). Süswasserflora von Mitteleuropa2: Bacillariophyceae; 4. Teil: Achnanthaceae, Kritische Ergänzungen zu. Achnanthes s.l., Navicula s. str., Gomphonema, Gesamtliteraturverzeichnis Teil 1-4. Spektrum Akademischer Verlag, Heidelberg. (see p. 440 for account of Nupela)
Potapova, M.G., Ponader, K.C., Lowe, R.L., Clason, T.A. & Bahls, L.L. (2003). Small-celled Nupela species from North America. Diatom Research 18: 293-306.
Vyverman, W. & Compère, P. (1991). Nupela giluwensis gen. & spec. nov. A new genus of naviculoid diatoms. Diatom Research 6: 175-179.
Amidst the dreary nothingness of the sample that prompted the previous post, I stumbled across the diatom in the photograph above. This image gives a misleading impression as it is a relative large diatom with considerable variation in three dimensions and my first thought was that I was looking at a fragment of vaguely diatom-like structures amidst a unfocussed blur. Careful use of the fine focus control revealed the twisted nature of the structure and I was able to create this semi-focussed image from a “stack” of images of the individual focal planes using Helicon Focus software. The scale bar is 10 micrometres (= 1/100th of a millimetre). As there are relatively few diatoms with a frustule with such a contorted form, it was relatively easy to identify it as Surirella spiralis Kützing 1844.
Surirella spiralis is one of a small number of diatoms whose outline is twisted. There are diatoms that show considerable curvature within a single plane (see Stenopterobia sigmatella in “Reflections from Ennerdale’s Far Side”) but few where this curvature occurs between planes. The only other diatom with this feature that I have written about in this blog are Entomoneis (see “A typical Geordie alga …”) and Cylindrotheca (see “Back to Druridge Bay”). These twisted diatoms, like sigmoid diatoms such as Stenopterobia, typically have motile habits. In my post on Stenopterobia I wondered what advantage a sigmoid outline conferred on a diatom and we really need to ask the same questions when thinking about twisted diatoms. I have the germ of an idea, but want to think it over some more before unleashing it onto the world.
Surirella, Stenopterobia and Entomoneis are all members of an order of diatoms, the Surirellales, that are the subject of a recent paper by Elizabeth Ruck, from the University of Arkansas, and colleagues. They compared morphology and genetic differences amongst members of this order, along with a related order, the Rhopalodiales, two of whose members are Epithemia and Rhopalodia, both of which I have also written about in this blog. Their conclusion is that current generic limits need an extensive shake up with long-established genera that seemed to be based on sensible criteria when viewed with the light microscope split apart and reassembled, based on ultrastructural and genetic characteristcs.
The main changes relevant to a freshwater ecologist are as follows:
- Campylodiscus: some freshwater species retained in Campylodiscus, some moved to Iconella; marine species moved to Coronia. The Fastuosae group of Surirella are now included in Campylodiscus;
- Cymatopleura: now included in Surirella
- Entomoneis: no change
- Epithemia: all species now merged into Rhopalodia;
- Rhopalodia: now includes Epithemia;
- Stenopterobia: now included in Iconella;
- Surirella: now limited to the Pinnatae group of Surirella, plus former Cymatopleura species;
- The genus Iconella has been re-established for a group of former Surirella species (section Robusta) along with some freshwater Campylodiscus species and Stenopterobia. Of particular relevance to this post, Surirella spiralis is now Iconella spiralis (Kützing) Ruck & Nakov in Ruck et al. 2016; and,
- The order Rhopalodiales has been subsumed into Suriellales.
It will be interesting to see whether or not, and how quickly, these names diffuse through the community of scientists who study diatoms. Taxonomy has a dual nature: on the one hand, specialists are driven by a desire to understand how evolutionary forces have shaped and differentiated a group of organisms; on the other hand, taxonomists act as biology’s janitors, sorting and organising information about species so that other biologists can use this for their own purposes. I am the editor and co-translator of a guide to European diatoms that was being finalised just as this paper was published and which, as a result, uses the “old” names. These books often have a ten or twenty year shelf life which will prolong the use of these names, and slow the uptake of new ones. I also know, from many years training people to analyse diatoms, that taxonomic changes, however well justified, sow confusion among beginners. On the other hand, we are entering a new era, when molecular barcoding will be used more widely for routine identification of diatoms and, for this, a correct understanding of the phylogenetic relationships amongst a group of organisms improves the accuracy of the bioinformatics routines that assign names to the diatoms.
For most practical purposes, in other words, Surirella spiralis will remain S. spiralis for some time (and Stenopterobia sigmataella will remain S. sigmatella too), if only because of the innate conservatism of most of the people who work with diatoms. My use of the old name in this post means that the part of my readership who know at least a little about diatoms could place the diatom within a familiar framework, even if Iconella spiralis is the correct name. The term “post-truth” has entered our political vocabulary over recent months; in diatom taxonomy and identification, however, we sometimes have to accommodate “pre-truth” as well.
Ruck, E.C., Nakov, T.., Alverson, A. & Theriot, E.C. (2016). Phylogeny, ecology, morphological evolution, and reclassification of the diatom orders Surirellales and Rhopalodiales. Molecular Phylogenetics and Evolution 103: 155-171.
Ruck, E.C., Nakov, T.., Alverson, A. & Theriot, E.C. (2016). Nomenclatural transfers associated with the phylogenetic reclassification of the Surirellales and Rhopalodiales. Notulae algarum 10: 1-4.