The challenging ecology of a freshwater diatom?

amp_pedi_pollybrook

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.

aped_v_p

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”.

References

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.

Hard science in hard water?

Having started to think about the ecology of small Fragilaroid diatoms in a recent post (see “When is a diatom like a London bus?”), I thought that it might pay to look in more detail at the habitats that these taxa do like, in the hope that this will help us to understand why they occur together so often.   I am just looking at two “species” in this post: “Staurosirella pinnata” (which we suspect to be a complex of several species) and “Staurosira construens” (which is also a complex, as the records in my database merge a number of varieties, most of which have subsequently been raised to the status of species in their own right).

One problem has to be confronted at the outset: these taxa also share a propensity to form chains which remain intact even after we’ve made slides.   This means that we often encounter aggregates of five or more cells, which violates the assumptions of random distributions of diatoms that underpin our statistical methods.   No-one, to my knowledge, has found a satisfactory means of dealing with this, but it should be borne in mind when considering the graphs which follow.

The first graph shows the distribution of records of these species in my database along an alkalinity gradient, and generally confirm the preference of both species for hard water.   I have highlighted two outliers on the chart for Staurosira construens. These samples are from the same location, the upper reaches of the River Wey (South) in Surrey, which receive a mixture of soft water, flowing off the Greensand, and harder water from the surrounding areas.   I have encountered anomalies between diatoms and water chemistry in this area before, which are probably the result of the complex hydrology of the area.

Staurosira_versus_alkalinity

The distribution of Staurosirella pinnata (left) and Staurosira construens (right) along an alkalinity gradient. Records from the “DARES” dataset.   Two outliers from the River Wey (South) are highlighted.

The next two graphs show the distribution of records along phosphorus and nitrogen gradients and these show opposite responses: both seem to be most abundant when phosphorus is low and nitrogen is high. Again, we have the problem of the two outliers from soft water sites confusing the view for Staurosira construens but we can generalise and say that neither species is likely to be abundant (meaning > 10 per cent of all valves) except when these conditions are met.

The horizontal red lines on these graphs show the range of phosphorus and nitrogen measured in a single river, the River Wylye, during a study in 2011-2012. I have included these lines to give a rough idea of the precision that we should expect when defining the preferences of a diatom.   The River Wylye is a chalk stream, which tend to have relatively stable hydrology, so the range of nutrient concentrations measured in these streams is probably lower than is the case for many rivers.

Staurosira_versus_PO4-P

The distribution of Staurosirella pinnata (left) and Staurosira construens (right) along an reactive phosphorus gradient. Records from the “DARES” dataset.   Vertical lines represent the approximate position of high (blue), good (green), moderate (orange) and poor (red) status boundaries.   The horizontal line shows the range of concentrations encountered in the River Wylye, Wiltshire in 2011-2012.

Staurosira_versus_nitrate

The distribution of Staurosirella pinnata (left) and Staurosira construens (right) along a nitrate-N gradient. Records from the “DARES” dataset.   Vertical lines represent the position of the (Irish) high (blue) and good (green) status boundaries.   The horizontal line shows the range of concentrations encountered in the River Wylye, Wiltshire in 2011-2012

Ecological assessment using diatoms is largely based on indices that calculate the relative position of a sample along a quality gradient based on a combination of the known ecology of the species and the representation of that species in the sample.   This means that the result is most strongly influenced by the most common species and anything that occurs below about five per cent has little influence. These charts suggest that Staurosirella pinnata and Staurosira construens will both be good indicators of a combination of low phosphorus and high nitrogen in hard water; however, there are a “tail” of records that extend into other types of water.   One valid question is whether the individuals responsible for these occurrences outside the “optimum” are the same species as those that are abundant at low P / high N / hard water.   Given what I wrote above about both of these taxa probably being complexes, this is a possibility.   However, the generally low numbers means that solving taxonomic riddles will be unlikely to lead to a great increase in precision in ecological assessments.

Personally, I lean towards the options I suggested in Baffled by the benthos (2) – that diversity within samples may be controlled by a wide range of factors unrelated to anthropogenic pressures and that interspecific diversity may give insights into ecological resilience. The problem is that this hypothesis is easier to propose than it is to test. It is not impossible to test; however, the hegemony of taxonomically-inclined diatomists over those with a genuine interest in functional ecology means that will probably remain no more than a theory for some time to come …

Michael McCarthy: Nature Studies

Here’s a link to an interesting article in today’s Independent about the state of England’s chalk streams.   They are not, says Environment Editor Michael McCarthy, in a very good condition, pointing to the problems of “diffuse pollution” (a catch-all phrase for all the pollutants that find their way into our rivers across the land, rather than via industrial or sewage effluents).   Principal amongst these is the run-off of agricultural chemicals, particularly nutrients.   This leads, says McCarthy, quoting members of the Salmon and Trout Association, to the growth of “blanket weed”, filamentous algae such as Cladophora glomerata.  Blanket weed smothers the gravel on the river bed which, in turn, makes life difficult for the bugs on which the trout and salmon feed.

Wylye_KD_110510_1_squeezed

The River Wylye at Kingston Deverill: a classic example of an English chalk stream. photographed in May 2010.

All this forms a narrative that has been repeated many times by river users and environmental scientists, including many in the Environment Agency.  The condition even has a name: Chalk Stream Malaise.   The problem is that there is no “smoking gun” to link the run-off to the decline of salmon and trout beyond reasonable doubt.   I had to research the literature on this as part of a study a few years back and was surprised about how little hard evidence I could find.  The circumstantial evidence is strong, so long as you cast your net wider than just English chalk streams, but I could not find one paper in a peer-reviewed literature that demonstrated an unambiguous link between nutrients and blanket weed, or between blanket weed and salmon and trout populations, specifically in chalk streams.   The reality is that there is much else happening in the surrounding catchments, including over-abstraction by water companies, which also affects stream ecology.   Nor are nutrients the sole consequence of increased agricultural production: silt and pesticides also enter the rivers and have their own effects, all of which are difficult to disentangle from one another. The result is a plot of interweaving motives and alibis that would make Hercule Poirot blanch.

See also streams of consciousness, my post from 21 August.

Fertile speculations …

The River Browney does not give up it’s secrets gracefully.   To reach the lower stretches of this tributary of the River Wear, just a few kilometres outside Durham City I had to push through thick growths of Himalayan Balsam, stinging nettles, brambles and what looked suspiciously like Giant Hogweed.   The bankside luxuriance continued in the river itself, the bed of which is almost completely covered with either submerged water crowfoot or algae.   The river has wound its way down from the foothills of the Pennines, collecting the wastewater from small towns and, just a couple of kilometres upstream from where I stand, from a sewage works serving a large village on the outskirts of Durham itself.   The algae and plants all thrive in the steady supply of dilute manure that these works provide.

Browney_Low_Burnhall

The River Browney at Low Burnhall Nature Reserve, just below the A167 Bridge.  Photographed in September 2013.

Many of the stones in the margins were coated with brownish filaments, waving gently in the current.  When I pick up one of the stones, these filaments collapsed into amorphous slimy masses but, under the microscope, they resolved themselves into a tangle of chains of algal cells.  Two types predominated, both with the yellow-brown colouration typical of diatoms.   The most abundant of these was chains of cylinder-shaped cells.  This was Melosira varians, a very common diatom in nutrient-rich rivers and which often forms these long brown streamers during periods of low flow during the summer.   The other type of cell was cigar-shaped when seen from above (as in fig. d, below) but rectangular when seen from the side (as in fig. c.).  These cells were mostly joined at the corners to form zig-zag chains.  You can also see, in fig. d., the transverse ribs of silica which are characteristic of this genus of diatoms.

Browney_Melosira_#1

Filamentous growths of diatoms on stones in the River Browney, County Durham, September 2013 and (inset) one of the growths on a stone removed from the stream bed.

Browney_diatoms

Microscopic views of diatoms (and a few desmids) from the River Browney, September 2013.  a. low power view of the filaments; b. part of a chain of cells of Melosira varians photographed at high magnification.  Note the large number of small brown chloroplasts inside each cell (scale bar: 10 micrometres = 1/100th of a millimetre); c. zig-zag chain of Diatoma vulgare photographed at medium magnification; d. a single cell of D. vulgare at high magnification (scale bar as for b.)

These masses of cells are the microscopic equivalent of the bankside vegetation that I had to push through in order to reach the river in the first place.  The surprise was that I did not find a large number of insect larvae feasting on this abundance, as I have described from cleaner rivers such as the River Ehen.  The answer, suggested by some recent papers, is that the normal relationship between algae and their grazers breaks down in these enriched rivers.   The dense diatom growths can suck the oxygen out of the water at night when there is no sun to generate photosynthesis so the insects that would normally be feeding on the algae cannot survive.  This, in turn, will reduce the food supply of fish, as well as smothering the areas where they would normally lay their eggs.   We see, in other words, a “domino effect” as the consequences of artificially high nutrients clatter through the different groups of organisms leading, in some cases, to consequences for the way in which we are able to use these ecosystems.