Concentrating on carbon …

On the other side of Ennerdale Water I could see plenty more submerged stones, all covered with green filaments but these belonged to different genera to those that I wrote about in my previous post.   Both are genera that we have met previously – Mougeotia, which has flat, plate-like chloroplasts which rotate around a central axis in order to control its rate of photosynthesis – and Spirogyra.  When light levels are low, Mougeotia’s flat chloroplast is perpendicular to the light in order to capture as much energy as possible, but in bright light it rotates so that the plate is parallel to the direction of the light, in order to slow the photosynthesis mechanism down and prevent internal damage (see “Good vibrations under the Suffolk sun” for another approach to this problem).

However, too much sunlight is the least of an alga’s problems in the Lake District.   This post looks at a different challenge facing freshwater algae and our starting point is the spherical nodules, “pyrenoids”, that you should be able to see on the chloroplasts of both Mougeotia and Spirogyra in the images below.   Photosynthesis involves a reaction between water and carbon dioxide to make simple sugars (turning fizzy mineral water into “pop”, in other words).   A submerged alga does not have a problem obtaining the water it needs, but what about carbon dioxide?   Gases are not very soluble in water, so this presents a much bigger problem to the algae.   Explaining why also presents a big problem to a blogger who conscientiously avoided physics and chemistry from age 16 onwards.  Here goes …

Mougeotia from the littoral zone of Ennerdale Water, April 2017.  Scale bar: 20 micrometres (= 50th of a millimetre).

The concentration of a gas in a liquid depends upon the concentration of that gas in the surrounding atmosphere.   As far as we know (and this is still an area of contention amongst geologists), concentrations of carbon dioxide in the deep past were much higher than they are today, in part because there were no land plants to suck it out of the atmosphere for their own photosynthesis.  So the earliest photosynthetic bacteria and, subsequently, algae, lived in water that also had higher concentrations of carbon dioxide.   As land plants spread, so the carbon dioxide concentration in the atmosphere dropped as they used it to fuel their own growth.  As a result, carbon dioxide concentrations in the water also dropped, thus depriving the algae of an essential raw material for photosynthesis.

However, carbon dioxide is not the only source of carbon available to aquatic organisms.   There is also carbon in many rocks, limestone in particular, and this can mineralise to carbonate and bicarbonate ions dissolved in the water.  Aquatic plants can get hold of this alternative carbon supply via an enzyme called carbonic anhydrase.   By concentrating the carbonic anhydrase activity in a small area of the chloroplast, the algal cell can boost the activity of the Rubisco enzyme (which evolved to function at a higher concentration of carbon dioxide).   This whole process is one of a number of forms of “carbon concentrating mechanism” that plants use to turbocharge their photosynthetic engines (see “CAM, CAM, CAM …” on my wife’s blog for more about a terrestrial version of this).

A two-chloroplast form of Spirogyra from the littoral zone of Ennerdale Water, April 2017.  Scale bar: 20 micrometres (= 50th of a millimetre).

Pyrenoids are widespread amongst algae, though a few groups (notably red algae and most chrysophytes) lack them.   Cyanobacteria (blue-green algae) use an organelle called a “carboxysome” for a similar purpose.   The only group of land plants with pyrenoids are the hornworts, relatives of mosses and liverworts.   About half of all hornworts have pyrenoids and a recent study has suggested that the ability to form pyrenoids has evolved up to five times in this group during their evolution.   The appearance of pyrenoids in distinct evolutionary lineages of algae also suggests that there may have been several evolutionary events that precipitated their formation.  And, it is important to stress, some algae which lack pyrenoids have alternative methods of concentrating carbon to enhance Rubisco activity.

So let us end where we started: in the littoral zone of Ennerdale Water on an April morning, gazing at a fine “fur” of filamentous algae clinging to the submerged rocks.   Back in October last year, I talked about how Ennerdale fitted into a pattern of increasing productivity of Cumbrian lakes first noticed by Pearsall in the early part of the 20th century (see “The power of rock …”).   Now we can start to understand that pattern in terms of basic biochemical processes: getting enough carbon from a combination of atmospheric carbon dioxide and the surrounding rocks for Rubisco and the other photosynthetic enzymes to convert to sugars.   In Ennerdale Water, one of the least productive of the Cumbrian lakes, we can see these algae during the winter and spring because the amount of biomass that those biochemical reactions produces is still just ahead of the amount that grazing invertebrates such as midge larvae can remove.  In a month or so, the grazers will have caught up and the rock surfaces will be, to the naked eye at least, bare.

Rubisco is the enzyme whose gene, rbcL, we use for molecular barcoding, subject of many recent posts (see “When a picture is worth a thousand base pairs …”).  My early desire to avoid physics and chemistry at school translated into as little biochemistry as possible whilst an undergraduate and, over the past few-years, I’ve developed a frantic urge to catch-up on all that I missed.   Just wish that those lectures explaining the Calvin cycle had been a little less … tedious …

References

Giordano, M., Beardall, J. & Raven, J.A. (2005).  CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution.   Annual Review of Plant Biology 56: 99-131.

Villareal, J.C. & Renner, S.S. (2012).  Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years.  Proceedings of the National Academy  of Science of the USA 109: 18873-18878.

 

Spring in Ennerdale …

My latest trip to Ennerdale Water, in the Lake District, has yielded its usual crop of spectacular views and intriguing questions (see “Reflections from Ennerdale’s far side”).   This time, my curiosity was piqued by lush growths of green algae at several locations around the lake shore.  The knee-jerk reaction to such growths is that they indicate nutrient enrichment but I am always sceptical of this explanation, as lush green growth are a common sight in spring (see “The intricate ecology of green slime …”) and these often disappear within a month or two of appearing.

Two points of interest: first, the lake seems to be lagging behind the River Ehen, which flows out of Ennerdale Water.   We often see these lush growths of algae on the river bed in winter but by this time of year the mass of algae there is lower than we saw in the lake littoral.   Second, the lake bed looks far worse (see photograph below, from the north-west corner of the lake) than the actual biomass suggests.

Filamentous algae (Ulothrix aequalis) smothering cobble-sized stones in the littoral zone of Ennerdale Water, April 2017.

Under the microscope, this revealed itself to be unbranched filaments of a green algae, whose cells each contained a single band-shaped chloroplast lapping around most of the perimeter.   This is Ulothrix aequalis, a relative of Ulothrix zonata, which I wrote about a few times last year (see link above).   Like U. zonata, this species is very slimy to the touch and, I suspect, the payload of mucilage adds to the buoyancy of the organism and means that we look down on a fine mesh of filaments which trap light and add to the unsightly appearance of the lake bed at this point.   That this part of the lake shore is close to a tributary stream draining some improved pasture triggers some suspicions of agricultural run-off fuelling the algal growths but, looking back at my notebook, I see that the lake bed was almost clear of green algae when we visited this location in July last year.  I suspect that a return visit this summer would also show a clean river bed.  Appearances can often be misleading (see “The camera never lies?”).

Ulothrix aequalis from the littoral zone of Ennerdale Water, April 2017.   Scale bar: 10 micrometres (= 1/100th of a millimetre).

This was not the only site that we visited that had conspicuous growths of green algae, though the mass of algae was greatest here.   All of the sites at the western end had these growths (see “A lake of two halves” for an explanation of geological differences within the lake) but, curiously, the genus of alga that we found differed from site to site.   In addition to Ulothrix aequalis in this corner of the lake, we found Mougeotia on the south side and Spirogyra close to the outfall.  This diversity of forms is, itself, intriguing, and I have never read a convincing explanation of what environmental conditions favours each of these genera.   I see both spatial and temporal patterns of green algae in the River Ehen too and, again, there is no satisfactory explanation for why the species I find can differ along short distances of the river and between monthly visits.

The Mougeotia and Spirogyra both have another story to tell, but that will have to wait for the next post …

Desmids on the defensive …

ennerdale_bog_pool_jan17

I made a short diversion back to the car after sampling at Ennerdale’s south-eastern end (see “Reflections from Ennerdale’s Far Side …”) crossing the boggy land behind the gravel spit and dipping into one of the pools to pull out a handful of submerged Sphagnum in the hope of finding some desmids, a group of algae that I have not looked at for some time (see “Swimming with desmids …” for my most recent post on this group).

Squeezing the water from a handful of Sphagnum from a bog pool into a vial and allowing the contents of this water to settle is usually a reliable way of collecting desmids; however, on this occasion the haul was rather meagre.  There were plenty of diatoms, but desmids were sparse and limited to a few Pleurotaenium and Euastrum species and some rather impressive cells of Xanthidium armatum.

The distinctive feature of the genus Xanthidium is the bristling armoury of spines around the margins.  The arrangement of spines varies between species and X. armatum has one of the most impressive collections, with bundles of three or four short spines at each angle.   The photograph below does not really capture the depth of the cell, and it is also not possible to see that there are two “decks” of marginal spines, but also bundles of spines on the top surfaces as well as at the margins.   This is truly a man-of-war amongst desmids.

xanthidium_armatum_ennerdal

Xanthidium armatum from a boggy pool at the south east end of Ennerdale Water, January 2017.  Scale bar: 10 micrometres (= 1/100th of a millimetre).  The photographs at the top of this post show the pool from which the sample was collected.

I’m intrigued by desmids but do not claim great competence with the group, so this is a good place to advertise a field meeting organised jointly by the British Phycological Society and the Quekett Microscopical Society.   We will be using the Freshwater Biological Association beside Windermere as our base but heading out to various desmid-rich locations in the Lake District over the course of the weekend.  There will be opportunities to look at other groups of algae too, but desmids will be the main focus of our weekend.  David John of the Natural History Museum will be helping with this group, but there will be experts on other groups available too.  If you are interested in coming, let me know and I will keep you informed as the programme evolves.

Reflections from Ennerdale’s Far Side …

ennerdale_far_end_170105

Ennerdale Water is, as I have described in earlier posts, is a lake of two halves, with a south eastern end influenced by granite and the north western end by softer mudstones and sandstones.  That has a big effect on the algae that we find in the littoral zone, with Cyanobacteria (blue-green algae) abundant in the south-east end and Chlorophyta (green algae) more conspicuous at the other end.   Diatoms are conspicuous in the littoral zone all around the lake, although there are some differences in the types of species encountered.  That is a story for another day, but I did find one species in some of the samples I collected from the south-eastern end that point to one other influence on the ecology of Ennerdale’s littoral zone.

Look at the photograph at the start of this post.  It was taken as I walked up to the south-eastern end (circa NY 127 140) and shows the view up the lake, with Angler’s Crag visible on the left hand shore in the distance.   The River Liza enters the lake on the right hand side (just out of the frame) and the low lying area between the River Liza and the raised ground where I was standing is an area of wet heath with a range of Sphagnum species and several boggy pools.   The shoreline of the lake itself is formed by a shingle spit which acts as a barrier between the wet heath and the lake itself.

ennerdale_gravel_bar_170105

The shingle spit separating the wet heath at the south-east end of Ennerdale from the lake itself.   Photographed in January 2017.

Several of the diatoms that I found at this end of the lake were species that I associate with acid conditions although, curiously, the limited chemical data that we have does not show a lower pH here than elsewhere in the lake.   I suspect that the proximity to the acid Sphagnum heath may lead to occasional pulses of acid water entering this area and exerting a subtle effect on the attached algae before being diluted by the water of the lake as a whole.   Of the species that I found, the most intriguing was Stenopterobia sigmatella, a long, sigmoid diatom with a single plate-like chloroplast.

The genus Stenopterobia fulfils most of my criteria for a genuinely rare diatom (see “A “red list” of endangered British diatoms”).   I only have 11 records in my dataset of 6500 samples, and in only one case did Stenopterobia constitute more than one percent of the diatoms in the sample.   These samples are all from acid habitats (mean pH: 6.1), with low nutrient concentrations (never more than 2 mg L-1 reactive phosphorus).  Those for which we have location information are plotted below.   The record in East Anglia needs further investigation (meaning: “I don’t believe it … but I haven’t had a chance to track down the slide for a closer look”). If we ignore this, the distribution is confined to mountainous regions of western Britain, and these Ennerdale samples also fit this trend, although the lake has soft water and is circumneutral rather than acid.

Stenopterobia sigmatella is another diatom with a sigmoid outline, and this brings me back to a question that I have posed before (see “Nitzschia and a friend …”): what advantages does a sigmoid outline confer on a diatom?  I cannot think of any other genera of algae that has species with a sigmoid outline, which only adds to the mystery. All of the diatoms that are sigmoid are motile, so I guess that the explanation may be linked to movement, but I don’t know for sure what the reason may be.   For all of the rich diversity that we see in diatoms, there is still, to pick up on a phrase from my biography of Humboldt, a “poverty of meaning” …

stenopterobia_sigmatella_en

Stenopterobia cf sigmatella from Ennerdale Water, October 2016 and January 2017.  Scale bar: 10 micrometres (= 1/100th of a millimetre).

stenopterobia_distribution_

A distribution map of records of Stenopterobia in Great Britain.   S. curvula is a synonym for S. sigmatella (see taxonomic note below).  Map prepared by Susannah Collings (see “Why do you look for the living among the dead?” for more details of how this was done)

stenopterobia_densestriata_

A valve of Stenopterobia densestriata.  Photograph from the ADIAC database (photographer: Micha Bayer).  Scale bar: 10 micrometres (= 1/100th of a millimetre).

Taxonomic note

I have used the name “Stenopterobia sigmatella” in this post, but this still needs confirmation as there is a closely-related species, S. densestriata (Hustedt) Krammer 1987 (see image above).  S. sigmatella has < 24 striae in 10 micrometres whilst S. densestriata has > 26 striae in 10 micrometres.  S. densestriata also has slightly smaller overall dimensions.

David Mann made the following comment about Stenopterobia sigmatella on the website Common Freshwater Diatoms of Britain and Ireland (predecessor to the new Diatom Flora of Britain and Ireland: “A nomenclatural mess. For most of the 20th century, this species was referred to (wrongly) as S. intermedia. Ross (in Hartley, 1986) stated that there is an earlier name, sigmatella, that could be applied to this species and made a new combination S. sigmatella. Unfortunately, this was wholly ignored by Krammer (in Lange-Bertalot & Krammer, 1987; and see Krammer & Lange-Bertalot, 1988) who made the new combination S. curvula. However, Nitzschia curvula of W. Smith is preceded by N. sigmatella of Gregory (1856, 1854, respectively).”   The references can all be found on the Common Freshwater Diatoms website.

 

A bigger splash …

Ennerdale_from_nr_Croasdale

This post continues my occasional series on insignificant black or dark brown spots on submerged stones (see “Both sides now …” for another recent episode).  I found these particular specimens on a cobble in Croasdale Beck in Cumbria, close to my regular haunts around the River Ehen and Ennerdale Water and thought that, with algae grabbing headlines for the wrong reasons yet again, I should write something positive about them.   What kind of weird world do we live in when people think it strange that algae thrive in a warm, well-lit water body, whilst simultaneously lauding other people who devote four years of their lives to practising jumping into a swimming pool?

Chamaesiphon_fuscus_Croasda

Colonies of Chamaesiphon cf fuscus (mostly 2-3 mm in diameter) growing on a submerged cobble in Croasdale Beck, Cumbria, August 2016. 

There was something about the regularity of the outlines of the dark brown / black spots on some of the more stable stones in this flashy beck that attracted my attention.   I’ve scraped a lot of dark smears and smudges off rocks in the past and often been disappointed when all I find are inorganic iron or manganese deposits.  Over time, one gets an eye for what is and is not an algal growth (or, for that matter, a submerged lichen) and even, in some cases, for the type of alga that formed the growth.   In this case, I had a good idea, straight away, that I was looking at a member of the genus Chamaesiphon, a cyanobacterium (blue-green alga).

Members of this genus are unicellular and form dense mats of cells that can be difficult to photograph.   I could not get a really clear view of individuals within this particular colony so, instead, have included some of Chris Carter’s photographs of another member of the genus.   You can see the short, club-shaped cells, each in a sheath and many topped by small “exospores” which bud off from the mother cell to propagate the colony.   The sheath has a brown tinge, presumably to the “sun-screen” compounds that we have met before in cyanobacteria.   Most of the members of the genus live on submerged rocks, but a few live on other algae (see “More from the River Ehen”).   Most of the rock-dwelling species indicate at least good conditions in rivers, but one species, C. polymorphus, is tolerant of more enriched conditions, which complicates use of a straight genus-level identification for rapid assessments.

Chamaesiphon-polonicus-Cald

Chamaesiphon polonicus from Caldbeck, Cumbria, photographed by Chris Carter.  Top left: looking down on colony; other images: side views showing cells in their sheaths and, in a few instances, with exospores. 

Oddly (to me at least) press coverage of the Olympic diving pool story has only used the word “algae”, never telling us what sort of alga is responsible for the problem.   This is equivalent to the commentators saying that “animals” have just made a perfect leap off the 3 metre springboard, leaving the audience to work out whether the subsequent splash was made by a slug or a human.

But I should end on a positive note: better, perhaps to compare the algae not with the divers but with the judges who assign the final scores.   That’s because a few minutes mooching around a stream or beside a lake can usually reveal enough from the types of algae that live there to give some insights into the health of the stream.   My visits to Croasdale Beck over the past year or so have shown me enough to suggest that this little Cumbrian stream probably deserves the algal equivalent of an Olympic medal.  But I doubt that we’ll get much press coverage for saying that…

‘Signal’ or ‘noise’?

Ehen_15107_musselsI’ve been visiting the River Ehen now for three years and this is my 32nd post on this small Cumbrian river.   You might think that, after about 40 visits to each of four locations, I should be beginning to understand the biology of the Ehen. I sometimes find myself being lulled into this false sense of complacency myself: I have a fairly good idea of where in each reach particular algae can be found, and when, in each year, they will be most abundant.   It was no great surprise, last week, for example, when Maria finished measuring the biomass with her BenthoTorch and announced that it was higher than the measurements she made last month. We’ve seen this trend of a sharp increase in the quantities of algae at this time in previous years.   Similarly, we were expecting (and therefore looked for) the pink blushes of the red alga Audouinella appearing on the rocks at the lowermost site. Again, these had been a common sight in the river during the cooler months throughout the period of our visits.

Yet, in some other ways, the River Ehen has changed over the course of our visits. Most noticeably, the uppermost site, just below the outfall from Ennerdale Water, had some lush growths of the alga Nitella flexilis when we visited last week.   I’ve recorded this from the Ehen before (see “Finding the missing link in plant evolution”) but not from this particular location, and not in such quantities.   Growths of the submerged angiosperm Myriophyllum alterniflorum were also more conspicuous at this site than on previous occasions.

A few kilometres below the outfall, at the lowermost site that we visit routinely, I also noted that the mats of Phormidium autumnale, a cyanobacterium (blue-green alga) that is an ever-present at this site also seemed to be more conspicuous than on any of our previous visits.   The mats of this alga were generally most obvious at the stream margins, where they were periodically exposed to air (see “In which the spirit of Jeremy Clarkson is evoked …”). However, last week, they were also prolific at some permanently submerged locations.

Nitella_flexilis_Ehen_SC_15

Nitella flexilis growing in the River Ehen, about 400 metres downstream from the outfall from Ennerdale Water, October 2015. The clump is approximately 25 cm in length.

Are these changes in the distribution of alga in the Ehen telling us something about how the river itself is changing or are they within the range of “natural variation”?   My suspicion is that, even after three years close observation we have not seen every nuance of the river’s behaviour. Yet three years is a long time by the standards of many ecological studies.   We also know that the river has changed over the period that we have been visiting.   In particular, Ben Gill, a tributary stream that had been redirected to flow into Ennerdale Water in the 19th century, has recently been reconnected to the River Ehen. This should mean that the flow regime in the river is now more natural but we’ve noticed a lot more fine sediment in the river on occasions since this happened.   The lake acts as a huge sediment trap so maybe this sediment itself is a ‘natural’ feature of the stream?   There is a temptation to define ‘natural’ in terms of our own experience, which can make it hard to evaluate the significance of events that happened more than a lifetime ago.

Phorm_autumnale_Ehen_0b_151

A mat of Phormidium autumnale on the bed of the River Ehen, about five kilometres from the outfall from Ennerdale Water.   The scale bar indicates approximately one centimetre.

Indeed, I would not even be writing about the Ehen today had I not been called in to look at the river due to the excessive growth of algae.   This brings in another facet to the story: my colleague in this study, Ian Killeen, is an expert on the ecology and conservation of pearl mussels. He had seen enough rivers with healthy pearl mussel populations to know that the quantities of algae that he could see in the Ehen were unusual, and he then got in touch with me.   We have to be aware, as applied ecologists, that we often do not start collecting data until someone perceives a problem.   That, too, creates difficulties when trying to understand the ‘natural’ or ‘baseline’ condition of a river.

These are not new themes for this blog. I’ve talked about the need for broadly-skilled, observant field-based biologists as the foundation for any effective environmental management process (see “Slow science and streamcraft”) and pointed out the limitations of pursuing highly-specialised tech-based approaches (see “Replaced by a robot?”).   On the other hand, I am also realistic enough to recognise that the luxury of having a biologist look at the same stream on a monthly basis is way beyond the means of most regulators.   So we need to find a compromise and, in the process, we need to agree on the non-negotiable elements of any compromise.   Suffice it to say, ensuring that experienced biologists have enough time to visit the sites that they are expected to assess would have to be part of any package.   However, don’t take that for granted: the line has, I am afraid, already been crossed by some environmental regulators.

More from Loughrigg Fell

As I do not pretend to great expertise on the desmids, I sent photographs of the specimens I collected during my visit to Loughrigg (see “A visit to Loughrigg Fell”) to Dave John who, in turn, passed them to David Williamson, to confirm their identities.   David Williamson co-authored the most comprehensive work on British desmids currently available, so I’m pleased to have his views on these specimens. To be honest, I was a little disappointed that I found so few desmids at a location from which so many had been recorded in the past. But then I am not a desmid expert, and may not have been looking in the best places.

Lily_Tarn_desmids_May15

Desmids from the margins of Lily Tarn, Loughrigg Fell, Cumbria, May 2015. a. Netrium digitus var. latum; b. Closterium dianae; c. Closterium dianae var. minus; d. Closterium directum (e. shows an entire cell of C. directum, photographed at lower magnification). Scale bar: 25 micrometres (= 1/40th of a millimetre).

I also found several cells of Eremosphaera viridis in squeezings from submerged Sphagnum at the edge of Lily Tarn.   At first, I thought that this was a colony of small cells but it is, in fact, a single large cell containing numerous small chloroplasts around the edge, giving it a very distinctive appearance. Like the desmids, it is a member of the Chlorophyta, or green algae, but it belongs to a different order, the Chlorellales rather than the Zygnemetales. That means that they are as different to one another as a rat is to a human.   By contrast, Euglena mutabilis, which we met in the previous post, is as different from a desmid as a human is from a slug.

I can recommend the desmids to anyone interested in microscopy.   They are, in many ways, much more amenable to amateur study than the diatoms. Desmids are generally about an order of magnitude larger than diatoms, which means that you can study them with a medium-power objective, rather than an expensive oil-immersion objective.   There is, in addition, a good English-language guide available whereas much of the key literature on diatoms is in German.   There are also plenty of sources of information available online. The only drawback with desmids is that their habitats are less widespread. Alternatively, I could put a positive spin onto this and remind you that a fascination with desmids will take you to some of our most spectacular landscapes.

Eremosphaera_viridis_Lily_T

Eremosphaera viridis from submerged Sphagnum at the margin of Lily Tarn, Loughrigg Fell, Cumbria, May 2015. Scale bar: 25 micrometres (= 1/40th of a millimetre).

Reference

Brook, A.J. & Williamson, D.B. (2010): A Monograph on some British Desmids. Ray Society, London.