Cyanobacteria inside their comfort zones …

Last week saw the second presentation of the FBA’s algae identification course for 2023, with another dozen keen participants being introduced to the intriguing world of freshwater algae.  The week starts with sampling in the vicinity of the FBA’s laboratory, first at Windermere itself (see “A hitchhiker’s guide to phytoplankton …”) and then, the following morning, at other sites in south Cumbria.  I usually join the group heading to Cunsey Beck, which flows from Esthwaite Water to Windermere but heavy overnight rain meant that river levels were too high for safe wading.   Instead, we joined Allan Pentecost on a trip to White Scar Quarry, right at the south-eastern tip of the Lake District.   It is an area that Allan knows very well and I always enjoy visiting with him because I learn a lot (see, for example, “Love and sex in a tufa-forming stream …”).

Just at the edge of the quarry, a small seepage flows across a wide bedding plane and, Allan pointed out to us, an impressive range of Cyanobacteria, green algae and moss co-existed side-by-side.   If you look at the photograph at the top of the post, you can see the seepage emptying onto the bedding plane just above the “d.”.   At low flow conditions, there is just a gentle trickle of water running in a narrow band approximately at the centre of the picture.   However, when there is more water coming down the quarry, then the water spreads out further and is also augmented by rainfall landing directly on the bedding plane.  The result is a zonation, roughly akin to what would be seen on a rocky shore, albeit not for seaweeds.  

Following this from the left we have:

1. The driest area, dominated by Nostoc commune whose ecosystem-building capabilities in otherwise adverse environments I’ve described in earlier posts (see “Landscape architects …” for the most recent of these);
   
2. An only occasionally wetted area dominated by dark brown mats of Scytonema.  The colonies described in “Poking around amongst sheep’s droppings …” came from very close to here and will give you some idea of what to expect;
   
3. A slightly wetter area has reddish mats of filamentous cyanobacteria. Schizothrix, Phormidium and Homoeothrix all feature here.  An example of a Phormidium growing at the air-water interface (and, therefore, presumably tolerant of desiccation) is described in “Fieldwork notes, August 2021”)
   
4. The central zone is almost permanently wet and here there is a distinct growth of the green alga;
   Mougeotia, a very common alga in this part of the world.  Recent posts which mention this genus include “Something, somewhere, just for a moment …” and “The man who stares at algae …” (both, incidentally, describe the interplay between green algae and Cyanobacteria in Lake District streams).

From here, the sequence is reversed except, at the right-hand side of the picture frame (e.) we did not see more Nostoc commune but, instead, patches of Rivularia haematites and bright patches of the moss Philonotis fontana.  I last wrote about Rivularia in “Building landscapes …”, based on another excursion that Allan led, this time in the Malham area of Yorkshire rather than in the Lake District.   I wonder, in retrospect, if the moss is, itself, a result of the ecosystem-building properties of Nostoc that I mentioned above and also wrote about in “How to make an ecosystem (2)”.   If I had teased apart those Philonotis clumps, would I have seen colonies of Nostoc lurking at the bottom, perhaps?   We hear a lot about all the problems Cyanobacteria cause in the Lake District at the moment so it is useful, once in a while, to remind ourselves that Cyanobacteria helped to build this wonderful landscape in the first place.

Microscopic views of the zonation at White Scar Quarry, Cumbria, September 2023.  a. Nostoc commune; b. Rivularia haematites; c. Phormidium sp.; d. Mougeotia sp.   No scale bars, I’m afraid, as the images were grabbed ad hoc while I was teaching, but other posts referenced should all have indications of size.

Some other highlights from this week:

Wrote this whilst listening to:  Africa Express Presents … The Orchestra of Syrian Musicians and Guests.  

Currently reading: Maggie O’Farrell’s The Wedding Portrait, set in Renaissance Italy.

Cultural highlight:  Exquisite Korean-American film Past Lives directed by Celine Song.  A love story mostly set against the Manhattan skyline.

Culinary highlight:  It may seem like a minor achievement, but I made the best shortbread of my life this week, following the Ayrshire Shortbread recipe in Cerys Matthew’s cookbook, Where the Wild Cooks Go ….  The vegan haggis that I made from her recipe also went down well a couple of weeks ago.

Patches of Philonotis fontana on the bedding plane at White Scar Quarry, September 2023.

CSI: algae …

My go-to analogy for the type of freshwater ecology that I do is of being a “general practitioner” (family doctor) for lakes and rivers.  I check my “patients” at regular intervals and offer them “prescriptions” to help them recover.  Just occasionally, however, situations demand a different analogy, that of the hard-boiled detective, roused from semi-slumber by the shrill ring of a telephone and summoned to the scene of a crime.  Sometimes there is even blood involved, or at least so it seems.  I am the one who announces to the protagonists assembled in the drawing room that it is not blood at all.   It is … algae.   

Freshwater ecologists have a fairly good idea of what algae grow where, how they wax and wane over the course of the year and how human activities can alter these patterns.  However, we also know that there is a limit to the extent that we can predict, and that there are many occasions when a single species can proliferate to the extent that members of the public can see, and be concerned by, the changes in a local water body.   In most cases, these growths are benign but there are situations – cyanobacteria blooms being the best known – where there are serious implications for human and animal health.

The algae that can cause these problems can come from any one of several groups such that the initial diagnosis necessitates a good general background in algal taxonomy.  We try to provide this background on the FBA course on freshwater algal identification as many of the participants work for regulators and water companies and are “first responders” to calls from concerned members of the public.  On the final day, Bill Brierley gives a talk on “incidents” based on experiences from his long career in the Environment Agency.  

What is striking from this talk is that representatives of all the main groups of algae [see Origin story … ] can be the culprits, along with a few groups that are not algae but which can be confused with algae.   Quite a few have been covered in this blog over the years.  Here’s a quick summary, along with some links.

In the Prokaryotic domain, we have the Cyanobacteria as the serial villains of the freshwater world (see: “A hitchiker’s guide to phytoplankton …”) but other groups can also cause problems.  “There will be blood …” describes a bloom of Chromatium, a purple photosynthetic bacterium, which turned a pond close to where I live an alarming red colour.

However, red-coloured blooms can come from a number of Eukaryotic algal groups as well.  Euglena sanguinea from the Euglenophyceae (Protozoa), in particular, can have a similar effect in standing waters and slow-moving rivers.  One of the key lessons that emerged from Bill’s talk was the need for samples to be examined by a biologist with a broad understanding of algae because it would be easy to jump to the wrong conclusion if a bloom was only viewed from the shore.

A bloom of Euglena sanguinea in a pond in eastern England.  Photograph: Bill Brierley.  The photograph at the top of the post shows an unexplained proliferation of green algae in a river in Cumbria.

Several problem-causing organisms can be found in the Chromista (see “Unlikely bedfellows …“).  The Haptophyta includes some toxin-producing groups including Prymnesium and Chrysochromulina both of which are more common in brackish and marine waters but which can extend inland, especially when salt concentrations are artificially elevated.   In the summer of 2022 a bloom of Prymnesium parvum had catastrophic effects on the River Oder in Poland and Germany, killing about 360 tonnes of fish.  In this case, discharges from salt mines in Poland were responsible for raising the salinity of the river and this, combined with high concentrations of nutrients and low flows, created a lethal cocktail. 

Left hand images: Prymnesium parvulum (note the short, rigid “haptonema, cells about 10 micrometres long); right hand image: Chrysochromulina braunii.  Photographs: Bill Brierley

Both of these genera are widespread in low-lying and brackish lakes in Norfolk and Lincolnshire and the expectation is that the favourable conditions under which they thrive will become more common as climate change continues, leading to more problems in the future.  

The other group of Chromista that are often associated with problems are the diatoms.  Although some marine genera do produce toxins, there is scant evidence for fish kills that are directly attributable to diatoms in freshwaters.  It is more common for mass growths on the beds of rivers to attract attention from passers-by.  The diatom Didymosphenia geminata is a repeat offender in this respect.   Although regarded as an invasive species in some parts of the world, it is native to the UK with records extending back over 150 years (see “Journey to the headwater of the River Coquet”).  Nonetheless, when conditions are right, it can produce massive growths on stream beds that can slough off and float downstream, looking uncannily like untreated sewage.  Members of the public frequently call the Environment Agency about this “problem” but it is one that can be easily diagnosed.

The final major evolutionary lineage which contains algae is the Plantae and, in particular, the Chlorophyta.  As for the diatoms, most of the occasions where the public call in with problems are due to mass growths that are symptoms of a general ecosystem malaise rather than being directly harmful to freshwater life.  Examples include “blanket weed” (Cladophora glomerata), ”gutweed” (Ulva flexuosa – see “Loving the low flows …”) and “water net” (Hydrodictyon reticulatum” – see “Casting the net wide …”) but, in truth, many green filamentous and thalloid algae can form conspicuous growths when conditions are right.  

One green alga that is responsible for fish kills is Botryococcus braunii which is quite widespread in the UK and which can form yellow-orange (sometimes red) growths in standing waters which can be confused with ferrous deposits.   Reports of fish kills are mostly from warmer parts of the world but the potential for similar occurrences in northern Europe will increase as the climate warms. 

Botryococcus braunii in a pond in eastern England.  Photograph: Bill Brierley.

Bill’s talk on algae “incidents” is the last one on our course, and is a good place to finish.  Through the week, we take the students on a journey through the world of algae.  This can be a bewildering experience for a beginner, as so much has changed in recent years.  We speak about insights obtained from molecular biology and the challenges we face when dealing with “cryptic” species.  Each of the tutors brings some specialist knowledge and it is, therefore, important to end with a talk that emphasises the value of being a “generalist”, of knowing enough about what differentiates the major groups to be able to go into an unknown situation and make a tentative diagnosis by themselves. 

The other lesson is that, rather than categorise these as “nuisance” or “problem” algae, we see that most are proliferating due to human-induced circumstances.   For Prymnesium parvum, three separate stressors are involved, all generated by human actions.  Paraphrasing Stephen Sondheim from West Side Story, “Society’s played him a terrible trick, And sociologically [ecologically?] he’s sick”.   Algae, as ever, are misunderstood and are the symptoms, not the reasons, for ecosystem malaise.  

References

Chiang, I. Z., Huang, W. Y., & Wu, J. T. (2004). Allelochemicals of Botryococcus braunii (chlorophyceae) 1. Journal of phycology 40: 474-480.

Edvardsen, B., & Paasche, E. (1998). Bloom dynamics and physiology of Prymnesium and Chrysochromulina. NATO ASI SERIES G ECOLOGICAL SCIENCES 41: 193-208.

Free, G., Van de Bund, W., Gawlik, B., Van Wijk, L., Wood, M., Guagnini, E., … & Stielstra, H. (2023). An EU analysis of the ecological disaster in the Oder River of 2022.  EUR 31318 EN, Publications Office of the European Union, Luxembourg.

Sobieraj, J., & Metelski, D. (2023). Insights into Toxic Prymnesium parvum Blooms as a Cause of the Ecological Disaster on the Odra River. Toxins 15: 403.

Some other highlights from this week:

Wrote this whilst listening to:  Gryphon, early seventies classical-folk-rock fusion.

Currently reading: The Girl who Played with Fire by Stieg Larsson.  Revisiting this book a decade or so after it was written.   It is still a tautly-written thriller but the tech references are now very dated. 

Cultural highlight:  The Barbie Movie.  I have been, I promise you, a fan of Greta Gerwig since I first saw Francis Ha, so don’t judge me.

Culinary highlight:   Delicious ten-course tasting menu at Rebel, new(ish) restaurant in Heaton, Newcastle

Something, somewhere, just for a moment …

Three weeks ago, I speculated that the success of some green algae in rivers may be due to the presence of cyanobacterial mats (see “The man who stares at algae …”) after noticed Mougeotia filaments growing out of darker patches that turned out to be Microcoleus autumnalis.  I’ve followed this up with an illustration, made with Adobe Fresco on my iPad, to show what this may look like in situ, as a complement to the micrograph that I showed in the earlier post.  As I have stressed before (see “Do we see through a microscope?”), many interventions are necessary to observe a stream alga at high magnification, and the result will inevitably be different to the actuality on the bed of the stream.  My illustration is offered as an alternative version of “different to the actuality” and as a thought experiment in how green algal communities may persist in flowing water.

I’ve tried to show the individual filaments of Micocoleus autumnalis wrapping over and around the Mougeotiafilaments which are growing up into the current.   The absence of diatoms is deliberate as neither of these genera typically have many epiphytes when in a healthy state.  

This observation answers the question of how Mougeotia attaches to rock but only by raising a further question: how does Microcoleus autumnalis attach to rock? The literature is quite vague on this question too, with the following explanation based partly on an old study on a completely different cyanobacterium, Pleurocapsa.   This suggested that the outer layer of the cell wall, the “F layer”, is semi-elastic and has a fibrous structure.  When in contact with a surface, it flares out to create a greater area of contact.  Other sources suggest that mucilage production plays a role too (acting as a form of glue) and we also need to consider the roughness of the surface too.   Importantly, a mat like growth form that hugs the contours of the rock exists within a “boundary layer” where it is protected from the current.  A big organism such as myself may be buffeted by the current, but there is a millimetre-thick zone just above the rock surface where friction reduces this current to almost zero, creating a zone where M. autumnalis can thrive.  

I offer this loose association as one example of how algae thrive in rivers.  It is not a universal explanation – it just seems to work for this particular pair of species at this particular location on this particular visit.   For a brief period, the unique properties of one cyanobacterium and one green algae overlap for long enough for them to thrive together.  Then a spate may come, roll the stones and scour everything back.   The next scientist to stare intently at the bed of this river may see something completely different.  And their conclusion is just as likely to be right as mine.  

References

Davey, M. C., Davidson, H. P. B., Richard, K. J., & Wynn-Williams, D. D. (1991). Attachment and growth of Antarctic soil cyanobacteria and algae on natural and artificial substrata. Soil Biology and Biochemistry, 23: 185-191.

Waterbury, J. B., & Stanier, R. Y. (1978). Patterns of growth and development in pleurocapsalean cyanobacteria. Microbiological reviews, 42: 2-44.

Some other highlights from this week: 

Wrote this whilst listening to: Vintage Neil Young.  Harvest and then Zuma.   

Currently reading:   Sweet Cares by William Boyd.

Cultural highlight:  Living Soil exhibition in the John Hope Gateway at the Royal Botanic Garden, Edinburgh.  As the name suggests, the exhibition, based on a residency by Natalie Taylor, focuses on soil but it included a table set with diatom-themed tableware.   

Culinary highlight:   Sichuan hotpot at Happiness 2 in Durham.   A benefit of living in a town with many Chinese students is that we now have two restaurants catering for their tastes.  

Two images of the diatom-themed exhibit from Living Soil at the Royal Botanic Garden in Edinburgh.

The man who stares at algae …

At the risk of writing a post that leads to every reader silently screaming “get a life …”, Lemanea, the subject of my previous post, was not the only alga growing on the stones on the bed of the River Irt.   Alongside the dark brown tufts of Lemanea there are also patches of green algae.   And when you look closely at these, you see that they often arise from dark brown and also that these are a different shade of dark brown from the Lemanea patches on the rock surface itself.  

Unfortunately, you cannot see this clearly in my photographs.  We visited Cinderdale Bridge at the end of a long day, the water was 6 ^oC and the screen on my camera is not very good for assessing the quality of images of small green and brown blobs moving in the current in real time.  You’ll just have to trust me when I tell you this.   

I might not be able to take perfect underwater macro photographs, but I can recognise an excellent stream phycologist from some distance.  So can you.   They have three hands: one to hold the bathyscope that lets them see the stream bed, one to manipulate a pair of forceps underwater and one to hold the sample vial into which a small portion of the algal community will be dropped.  Two-handed people cope by using their knees to support a bathyscope held by the same hand that is gripping a sample vial.  Somehow, I managed to transfer a small piece of this green/brown floc into a vial and get the lid screwed on without disaster.

Mougeotia (green) and Microcoleus autmnalis (brown) from the River Irt in a Petri Dish (approx. 9 cm diameter).   The photograph at the top of the post show filaments of Mougeotia growing out of mats of Microcoleus autumnalis in the River Irt at Cinderdale Bridge, February 2023.   Scale bar: 20 micrometres (= 1/50^th of a millimetre).

Back at home, in my study (rather warmer than the River Irt in February), I emptied the vial into a Petri dish,  teased out a small portion roughly at the border between the brown and green parts and put this under my microscope.  The green growths were filaments of Mougeotia, an unbranched, typically slimy, alga that is common in lakes and streams in this part of the world whilst the brown sections were dense mats of the cyanobacterium Microcoleus autumnalis, also often common in these streams (see “Fieldwork notes, August 2021”.  In this and all earlier posts it was referred to as “Phormidium autumnale”).

Microcoleus autumnalis often lives in habitats where the water level fluctuates and, when exposed, dries into thin, papery layers (“in nuda terra autumno” in the original description – “in the bare earth in autumn”).   That would not be a situation that Mougeotia would enjoy.   However, here in the River Irt, the mats of Phormidiumwere permanently submerged and the Mougeiotia filaments seemed to be growing out from these, their basal sections tangled amongst the interwoven strands of Microcoleus.    I described something similar in the River Liza where Stigonema mamillosum was the host (see “Ever changing worlds …”) and I’ve touched on the idea of cyanobacteria as “ecosystem engineers” on several occasions (see “Landscape architects”).   However, there is nothing in the formal scientific literature about their role in supporting filamentous green algae in streams.   

In fact, the literature devotes very little time to the basic conundrum of how filamentous algae (which don’t have roots) stick to submerged rocks (that are too hard for roots to penetrate anyway).   Old taxonomic works often refer to filaments having “basal cells” or “holdfasts” or, in some genera, putting out rhizoids, but these are never described in great detail, and have not been followed-up in recent years.   We accept the presence of filamentous algae in streams without ever challenging their right to be there in the first place. 

Could it be that cyanobacteria, rather than facilitating colonisation by green algae occasionally, actually play this role quite often but their presence is usually camouflaged by the green algae above them or is simply overlooked by most field biologists?   The interwoven filaments of cynaobacterial mats hug the contours of rocks much more tightly than green algae, meaning that they live in the “boundary layer” where they are protected from the rough and tumble of the stream.   A green algal propagule, or a fragment of a filament, that becomes trapped within this mat, therefore, has a better chance of success than one outside the mat.   I offer this as a hypothesis rather than as a fact.  It might just help us understand why some rivers are greener than others.

References 

The paper explaining why Phormidium autumnale had to be transferred to Microcoleus is: 

Strunecký, O., Komárek, J., Johansen, J., Lukešová, A., & Elster, J. (2013). Molecular and morphological criteria for revision of the genus Microcoleus (Oscillatoriales, Cyanobacteria). Journal of phycology 49: 1167-1180.

Some other highlights from this week: 

Wrote this whilst listening to: The Art of the Fugue by J.S. Bach

Currently reading:   Girl With a Pearl Earring, by Tracy Chevalier.   Getting me in the mood for …

Cultural highlight: Vermeer exhibition at the Rijksmuseum, Amsterdam.   28 of the 37 paintings known to have been painted by Vermeer gathered in one place.  An experience of a lifetime.

Culinary highlight:   Iranian meal kit supplied by Modern Persian Kitchen which started out in Durham but now delivers nationwide.

Looking after their own …

Much has changed in the two months since I was last at the River Irt.  The conspicuous yellow-brown patches of diatoms that attracted my attention in Cold Comforts have gone, but other algae have appeared: clusters of dark brown filaments, each a couple of centimetres long, on the upper surface of boulders.   These tufts are the red alga Lemanea fluviatilis, which I’ve written about before (see“Lemanea in the River Ehen”).   Interestingly, I did not see Lemanea at Lund Bridge, the focus of the posts about winter diatoms, but at Cinderdale Bridge, a few kilometres further downstream.  Lemanea is also not found in the River Ehen close to the outfall of Ennerdale Water but becomes abundant a few kilometres further downstream.  There must be something about proximity to a lake that does not favour this genus.  

Young shoots of Lemanea fluviatilis along with green algae on a boulder in the River Irt at Cinderdale Bridge, February 2023.   The boulder is about 40 centimetres long.    The photograph at the top of the post shows the River Irt at Cinderdale Bridge.

These filaments (which are actually hollow tubes of cells) had some growths which looked remarkably like another red alga common in streams hereabouts, Audouinella hermainii.  But we could also turn that argument around and say that Audouinella looks remarkably like juvenile stages of several red algae (see “The complicated life of simple plants …”).  Unravelling the identities of these simple filaments has kept taxonomists busy for over a century and molecular analyses are still presenting us with surprises.   I’m going to assume that these are young gametophytes of Lemanea until someone convinces me otherwise, simply because of their proximity to so many other young shoots of Lemanea.  

A filament of Lemanea fluviatilis with young epiphytic gametophytes.  Scale bar: 100 micrometres (= 1/10^th of a millimetre).  

Close-up of young gametophytes on a filament of Lemanea fluviatilis in the River Irt, February 2023. 

These were not the only residents on Lemanea.   There were also some thin, unbranched filaments belonging to a cyanobacterial genus Chamaesiphon.   This is a genus with two very distinct habits: some species form dark brown/black crusts on rocks (see “A bigger splash …”) whilst other species live as epiphytes.    I last wrote about the epiphytic forms in “Whatever doesn’t kill you …”.  In that post, I was circumspect about naming the species because I could only see a single “exospore” at the end of filaments.   The population in the River Irt, however, has several filaments with a very characteristic stack of exospores so I can use the name C. confervicola with more confidence.  

A young filament of Lemanea fluviatilis with epiphytic Chamaesiphon confervicola. A stack of exospores is visible on the filament to the left of centre.  Scale bar: 20 micrometres (= 1/50^th of a millimetre).  

The last image in this post is a graph showing the changes in the cover of Lemanea fluviatilis in rivers in West Cumbria over the course of a year.   This shows very clearly that Lemanea is most prolific in winter and spring, becoming very sparse in summer through to autumn.  It is a similar pattern to that shown by Gomphonema.   There are algae that have pronounced summer peaks but we tend not to see these in the very nutrient-poor streams of the Lake Disrict.   My theory is that these small streams tend to be shaded and to have healthy populations of (hungry) invertebrates which are most active in the warm waters of summer.   Consequently, winter offers the best opportunity for an alga to grow relatively unmolested.   And, just as I showed how Gomphonema created a “housing estate” for other diatoms to inhabit, so Lemanea might well be determining the fluxes of the tiny Chamaesiphon confervicola filaments too.  

Seasonal changes in the cover of Lemanea fluviatilis in rivers in West Cumbria, 2019 – 2023.   Cover is expressed on the 9-point scale used for macrophyte surveys in the UK.   Vertical lines separate the twelve months.

Some other highlights from this week: 

Wrote this whilst listening to: In a Silent Way, by Miles Davies.   My favourite of his many records. 

Currently reading:   Animal, Vegetable, Miracle: Our Year of Seasonal Eating by Barbara Kingsolver.  

Cultural highlight: finally got around to seeing BAFTA-winning and Oscar nominated film Aftersun, starring Paul Mescal.  

Culinary highlight:   homemade prawn, crab and fennel cannelloni.   

Memories of last time …

This boulder is to me what madeleines were to Marcel Proust: it stirs memories.   You’ve already read about it in Hunger Games and in some older posts.   When I looked at it on my most recent visit in early December, I not only remembered, but I noticed that it was different.  It is time to take a closer look.   

The first thing to notice is that more of it is exposed than back in October.   The lake must be about twenty centimetres lower.   Second, the zonation of algae is back.   When I visited in August, I commented on the clear distinction between bands of cyanobacteria and green algae (see “More from the splash zone …”).    In October, the green algae had disappeared.  Now, in December, they are back again.   Microscopic examination showed these to be mostly Spirogyra, as in August, along with smaller quantities of Mougeotia, Oedgonium and Klebsormidium.

Third, the growths of Tolypothrix on the side of the boulder are less conspicuous.   I’m guessing that it has been outcompeted by the green algae.  I’m also guessing that it is present, and possibly even serving as a “rooting medium” for the green algae.   It is another example of the “patchiness” in space and time of aquatic algal assemblages (see previous post for more about this).   

Algae below the waterline on the littoral boulder in Wastwater in December 2022.   The photo captures about 20 centimetres depth and cyanobacteria and green algae are both visible.   The photograph at the top of the post shows the boulder with Great Gable in the background.

This drop in lake levels meant that a flat “plateau” of rock on the right-hand side which had been submerged was now largely exposed.   In my earlier post, I had commented on how this had been dotted with Tolypothrix colonies.   Tolypothrix was, on this trip, still conspicuous in depressions on this surface – miniature “rock pools”, as it were, that were rewetted at regular intervals by waves breaking against the boulder.  

I’ll keep this post brief.   It is just an update on a ever-changing situation.  Having made a comparison with Marcel Proust, I need to be mindful of length.   À la Recherche du Temps Perdu spills over into seven volumes and over 3000 pages.   Most of us have heard about it, but almost none of us have read it.   I don’t want that to be my fate too.

The “rock pool” on the right-hand end of the boulder.  It is about 30 centimetres across, and growths of Tolypothrix (up to about a centimetre in diameter) are just visible.

Wrote this whilst listening to:   Phoebe Bridger’s EP of Christmas songs, including her exquisite cover of Merle Haggard’s If We Make It Through December. 

Currently reading:   How to Feed a Dictator by Witild Szabłowski.   Interviews with the personal chefs of Idi Amin, Saddam Hussein and others.  

Cultural highlight: Standing on the Sky’s Edge, new musical set in a brutalist high-rise development in Sheffield.   Features songs by Richard Hawley. 

Culinary highlight:  Christmas dinner, cooked by my daughter at her home in Sheffield.

Hunger games …

My superpower is being able to see bacteria with the naked eye.   This has many advantages, as I am about to show you.  It also comes with a significant downside: confronted with a view such as that looking north-east along Wastwater on a spectacular autumn afternoon, I find myself staring intently at the boulder in the foreground.  If you follow this blog, you will know this boulder well, as it has featured in several posts (most recently “More from the splash zone …”).   Great Gable can wait for another day: there are more intimate landscapes waiting to be explored …

In that earlier post, I wrote about the zonation of algae on this boulder, pointing out a thick layer of green algae below the surface whilst dark crusts of cyanobacteria inhabited the splash zone.   Two months later, the green algae have largely disappeared, apart from a short fuzz on the side of a few stones.   Instead, the area where these were growing is dotted with small brown colonies, most just a few millimetres across.  A close examination, using the macro lens of my waterproof Olympus Tough shows these to be tufts of vertical filaments.

Patches of Tolypothrix distorta var. penicillatus on the side of a granite boulder in Wastwater, October 2022.   The largest are about five millimetres across.  The right hand image shows a close up, with filaments about five millimetres high.

Under the microscope, these tufts reveal themselves to be Tolypothrix penicillatus var. distorta, which I often find in nearby rivers, including the River Irt, which flows out of Wastwater (see “Tangled up under blue skies …”).   I have never seen it growing quite as prolifically in the lake itself.   I always worry, when I make a new discovery, whether it is a genuine new arrival or if I have just missed it in the past.  However, I have stared at this particular boulder on many occasions and am fairly sure that I would not have missed these if they had been there previously.   Whatever happened to remove the green algae presumably created an opportunity for another organism to move in.

The pictures show several of the characteristic features of this genus.   The filaments are composed of rows of cells (“trichomes”) within sheaths, some of which are yellow-brown in colour due to the pigment scytonemin, a natural sunscreen.   You can also see heterocysts (nitrogen-fixing cells) at the ends of several filaments, along with ”false branches”. These occur when a trichome breaks and both sections continue to grow within the same sheath.  

Tolypothrix distorta var. penicillatus from Wastwater, October 2022.   Scale bar: 20 micrometres (= 1/50^th of a millimetre).

The upper image in the second plate shows a filament with what appear to be cyanophycin granules.   These store nitrogen and their presence in some filaments suggests that these cells had recently experienced conditions when phosphorus was scarce.  This meant that the nitrogen obtained by the heterocysts could not be used to fuel growth, so it is stored in these granules (made of amino acids).  Understanding nutrient dynamics in lakes such as Wastwater is difficult because concentrations are so low that you have to push equipment to its limit when measuring nitrogen and phosphorus.  Concentrations of both also fluctuate so that you need a high sampling resolution.   Together, these create serious logistical barriers to understanding what is going on.   

I use the analogy of baking cakes when explaining nutrient limitation to students.   You need everything on the list of ingredients to make a cake.   If you have no eggs, you can’t make the cake with just flour, sugar and margarine, and if you have no flour, you can’t make a cake with just eggs, sugar and margarine.   The same is true for algae: if one nutrient runs out, the algae cannot grow regardless of how much of the other nutrients are present.   In a lake such as Wastwater there will be times when there is enough phosphorus but not enough nitrogen, and other times when there is enough nitrogen, but phosphorus is short.   Having the capacity to capture the nitrogen it needs gives a cyanobacterium such as Tolypothrix a temporary advantage over other algae when phosphorus is available, but when phosphorus is scant, it is not going to let that hard-won nitrogen go to waste.   The cyanophycin acts as a nitrogen larder, ready for whenever the cell needs it.   This can even happen over the course of a day: nitrogen-fixation typically happens at night, because the process is very sensitive to the oxygen produced by photosynthesis.  

Tolypothrix distorta var. penicillatus from the River Irt, October 2022.   Scale bar: 20 micrometres (= 1/50^th of a millimetre).

This fieldworker fully empathises with cyanobacteria.  Long days in the field lead to nutritional fluctuations and I have evolved a strategy when out in the field whereby museli bars, crisps and bananas are secreted around me as human equivalents of cyanophycin granules.   As the habitats I am studying are invariably “hungry” in their natural state, I guess this is a sort of ecological “method acting”.   In an urban setting, I would have ready access to coffee shops, cafes and restaurants.  I would be perpetually saturated with nutritional opportunities, just like an alga in a eutrophic lake.  Out here, I live a more feral existence and my strategies shift accordingly.  So not only do I see bacteria with my naked eyes, I am also beginning to think like them.   Maybe I’ve been doing this job for too long … maybe I need a break …

References

Li, H., Sherman, D. M., Bao, S., & Sherman, L. A. (2001). Pattern of cyanophycin accumulation in nitrogen-fixing and non-nitrogen-fixing cyanobacteria. Archives of microbiology 176: 9-18.

Lu, Z., Ye, J., Chen, Z., Xiao, L., Lei, L., Han, B. P., & Paerl, H. W. (2022). Cyanophycin accumulated under nitrogen-fluctuating and high-nitrogen conditions facilitates the persistent dominance and blooms of Raphidiopsis raciborskii in tropical waters. Water Research 214: 118215.

Watzer, B., & Forchhammer, K. (2018). Cyanophycin synthesis optimizes nitrogen utilization in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Applied and environmental microbiology 84: e01298-18.

Some other highlights from this week: 

Wrote this whilst listening to: Nick Cave’s Murder Ballards, one track on which is Henry Lee, a duet by Cave and PJ Harvey …

Currently reading: Orlam by PJ Harvey …

Cultural highlight:   PJ Harvey reading from Orlam at the Fire Station in Sunderland.  

Culinary highlight:  fish and chips sitting beside the River Eden in Appleby on the way back from fieldwork

Reflections from Lago Trasimeno

There are two types of ecologists: those who can spend a holiday in an apartment overlooking a lake and forget about work, and those who are compelled to scan Google Scholar to find out all they can about that lake.   I’m in the latter group and the lake in question is Lago Trasimeno, in Umbria, central Italy.   I worked on crater lakes in central Italy in the late-1980s (see: “How to make an ecologist #10“) and had assumed that Trasimeno was another of these.   Whilst it is the result of tectonic activity in the region, and has the circular outline that I associate with crater lakes, it does not sit within a crater.  It does, in fact, have an outflow, which is a big clue, as true crater lakes do not (the technical term is “endorheic”).   But therein lies a tale …

As Lago Trasimeno has a very small catchment and is very shallow, it is very vulnerable to rainfall conditions, with both dramatic floods and droughts over the centuries.  There is an outflow in the south-east corner and, at various points in history, this has been lowered to increase the land available for agriculture as well as to alleviate the effect of floods.   Water has also been taken out of the lake for irrigation and this has meant that the water level has often been lower than the outlet, meaning that the lake is effectively endorheic.  Combine this with a gradual warming of the climate leading to greater evaporation, and salt levels in the lake have started to increase too.   The lake, like many in the Mediterranean region, is at risk of becoming brackish at some point in the future unless steps are taken. 

I took a closer look at the lake during a visit to Isola de Maggiore, the only inhabited island in the lake.   There were tufts of Cladophora glomerata on stones in the littoral zone and, tellingly, bleached filaments on exposed stones on the foreshore, suggesting that the lake level at the time of my visit was low.  The presence of Cladophora also suggests that the lake is enriched with nutrients.  This is borne out by a quick scan of the literature, with the phytoplankton suggesting that the lake is moderate or poor status according to WFD definitions.   It still supports a commercial fishery, and we ate fish from the lake in local restaurants.  The enriched nature of the lake means that these are mainly cyprinids such as tench which, to be honest, do not offer not great gastronomic potential.   I did, however, have some very tasty smoked eel with gnocchi at one restaurant in Tuouro sur Trasimeno. 

Cladophora glomerata on stones on the foreshore of Isola de Maggiore, Lago di Trasimeno, September 2022.  Scale bar: 100 micrometres (= 1/10^th of a millimetre).   Isola de Maggiore is on the right hand of the picture at the top of the post. 

Another feature of the lake, which can just be seen in the picture above, is its turbidity.  Fine sediments are very easily stirred up by wind and wave action due to the shallow nature of the lake, and the result is a milky-coloured water that did not look inviting for bathing.  The turbidity is a double-edged sword: on the one hand it stirs up the sediments, releasing their nutrients into the water.  On the other hand, the limited light penetration as a result of all this suspended matter reduces the potential for harmful blooms to form.  

Submerged stones that were within reach had a thick slimy biofilm, and I brought a sample back (preserved with a generous shot of grappa) to examine under the microscope.  There were plenty of diatoms, typical of hard water habitats, and a few that might tolerate mildly brackish conditions.   Epithemia and Rhopalodia were both conspicuous, and suggest nitrogen limitation.   A full account of the diatoms will follow once I’ve had a chance to examine them at high magnification.  I also saw some tapering cyanobacterial filaments which I suspect were once part of Gloeotrichia colonies (see: “Rewriting history at Talkin Tarn …”).  The literature reports that both planktonic (G. echinulata) and epiphytic forms (G. pisum) are present in the lake, and I am not going to speculate which these are.  Like Epithemia and Rhopalodia, Gloeotrichia is capable of fixing atmospheric nitrogen, suggesting that this is the nutrient limiting growth at this time of year.  

Gloeotrichia filaments from the littoral zone of Lago di Trasimeno, September 2022.

The tranquil images that top and tail this post, in other words, are misleading.  This is a lake where there is a lot going on.  There is a history of human habitation dating back to Etruscan and Roman times.  Humans are drawn to lake shores because these can be sources of water, protein and power.   Yet these demands can, in turn, lead to degradation of the lake.   In the case of Trasimeno, tourism also contributes to the local economy but, at the same time, puts yet more pressure onto the lake.   In more recent years, Trasimeno is also having to contend with the impacts of global warming.   This is a widespread problem, but shallow lakes in the Mediterranean region are especially sensitive to this pressure.   I think I knew when I booked the apartment that this was going to turn out to be a busman’s holiday.   I brought back bottles of local wine and olive oil, pictures of the Tuscan countryside, and some broader perspectives on shallow lake functioning.  That’s not a bad haul of mementos, is it?

References

Bresciani, M., Pinardi, M., Free, G., Luciani, G., Ghebrehiwot, S., Laanen, M., Peters, S., Della Bella, V., Padula, R. & Giardino, C. (2020). The use of multisource optical sensors to study phytoplankton spatio-temporal variation in a Shallow Turbid Lake. Water 12: 284.

Gasperini, L., Barchi, M. R., Bellucci, L. G., Bortoluzzi, G., Ligi, M., & Pauselli, C. (2010). Tectonostratigraphy of Lake Trasimeno (Italy) and the geological evolution of the Northern Apennines. Tectonophysics 492: 164-174.

Ludovisi, A., & Gaino, E. (2010). Meteorological and water quality changes in Lake Trasimeno (Umbria, Italy) during the last fifty years. Journal of Limnology 69: 174-188.

Mugnai, M., Angela Margheri, M., Cristina Sili, C., Turicchia, S., Soldati, E., Maffettone, E., … & Ventura, S. (2008). The cyanobacterial community of Lake Trasimeno. Algological Studies, 37-64.

Some other highlights from this week: 

Wrote this whilst listening to: Public Service Broadcasting, who I saw earlier in the week at the Fire Station in Sunderland, as well as lots of Bob Dylan (see below)

Currently reading: Lustrum, part two of Robert Harris’ Cicero trilogy

Cultural highlight:  Girl from the North Country.   Back in January 2020 we had gone to see this musical based around the songs of Bob Dylan, but the production was cancelled 40 minutes before curtain up due to cast illness.   We finally had a chance to see what we missed when a touring production came to the Theatre Royal in Newcastle.

Culinary highlight:  Khai Khai, an Indian restaurant in Newcastle whose vegetarian/vegan food is so good that a flexitarian such as me feels no inclination to look at their meat offerings.  Their Signature Tandoori Broccoli is out of this world.

Lago di Trasimeno from Passignano sul Trasimeno, September 2022.   Mixed media (watercolour/pastel/conté)

 

Fifth columnists …

We managed to tag an extra day onto the fieldtrip that I wrote about in “More from the splash zone …”, and we spent it in the Newlands Valley, ascending the ridge that starts with Cat Bells and walking along as far as High Spy, where we could look down into Borrowdale before descending, again, and walk back along the Newlands Valley to our car.  

The track up the valley was cut into the peat moorland.   At some points, the peat was undercut by a small channel of water that ran down one side.   Where this happened, partially-decomposed Sphagnum hung down in straggly dreadlocks or, if you prefer, “stalactites”.   One of these was decorated with some tiny sundew flowers, exploiting this most unusual habitat.  The Sphagnum provided the framework, around which a peaty-brown ooze clung, providing a rooting medium for the Sundew.   Sundews are fascinating plants well adapted to life in nutrient-poor environments (see “It’s a plant eat insect world out there …”) and their presence here made me wonder what else might be growing within this brown ooze.

Drosera rotundifolia growing on a peat “stalactite” hanging beside the Newlands Valley, August 2022.  Photographs: Heather Kelly.   The photograph at the top of the post shows the view south down Newlands Valley.

I teased out some portions of the peat once we had returned and had a look at it through my microscope and, as I expected, there was a wide range of algae present.  The most common alga was Zygogonium ericetorum, which belongs to the same order as  Spirogyra, which we met in the post mentioned above.  Zygogonium is similar to Zygnema in appearance (see “A day out in Wasdale”) but the two chloroplasts are less obviously star-shaped.  Other features are that the cytoplasm is often pink-purple in colour and that it has thick cell walls, often composed of “H”-shaped segments.   Unlike Zygnema and the other Zygnemetales, it is found mostly in terrestrial habitats, often acid in character.  In this mini-habitat, the tangle of filaments provide an extra level of structure which will both retain water through capilliarity and provide a substratum amongst which the sundew’s rootlets can gain a foothold.

Zygogonium ericetorum from the peat “stalactite” in the Newlands Valley.  Scale bar: 20 micrometres (= 1/50^th of a millimetre).  

As well as the Zygogonium ericetorum, there were plenty of cyanobacteria too.  Prominent amongst these was a species of Stigonema (possibly S. minutum) – a close relative of the cyanobacterium from the River Liza that I’ve written about previously (see “Fieldwork notes, August 2021” and links therein) but I also saw Tolypothrix tenuis and also some filaments of Scytonema.   All three of these are interesting because they are nitrogen-fixers.   They are faced with the same problem of scarce nutrients as the sundews but have adopted a different solution.  

Stigonema minutum from the peat “stalactite” in the Newlands Valley.  Scale bar: 20 micrometres (= 1/50^th of a millimetre).  

Alongside the green algae and cyanobacteria, there were also several diatoms present, most prominently chains of Tabellaria flocculosa and individual cells of Frustulia crassinervia.   There were also several desmids, but I didn’t have enough time to work out what these all were.   If I had worked through the sample in more detail, I’m sure that I could have made a list of twenty or more species from this one inauspicious strand of peat.

This is one more manifestation of a theme that I’ve returned to several times over the year: the role of algae and cyanobacteria as ecosystem engineers (most recently in the Burren: see “Landscape architects …”).   This is another good example of how algae can add both structure and nutrients to a habitat, allowing other organisms to gain a toehold.   Our eyes were drawn to this particular habitat by the colourful sundews, but the same patterns will be repeated across much of the damp peatland that surrounded us.   Algae are the plant world’s fifth columnists, a clandestine faction of organisms that mobilize to prepare the ground for the more overt botanical forces that follow.   

Tolypothrix tenuis from the peat “stalactite” in the Newlands Valley.  Note the heterocyst just above the branch.  Scale bar: 20 micrometres (= 1/50^th of a millimetre).  

Some other highlights from this week: 

Wrote this whilst listening to:   J.S. Bach Cantata 77: Du solist Gott, deinen Herren, lieben (Thou shalt love God, thy Lord). 

Currently reading:  Robert Harris’ Imperium.  First part of his trilogy about the life of Cicero.

Cultural highlight:  The Great North Run.  

Culinary highlight:  Linguine picante at La Piazza in Richmond, North Yorkshire, serving the double purpose of loading on the carbs before the Great North Run and getting me in the mood for our trip to Italy.

The view north from the ridge leading towards High Spy, with Catbells in the foreground, Derwent Water, Skiddaw and Blencathra beyond and Bassenthwaite just visible on the left hand side of the image.

More from the splash zone …

It was unfortunate, but the long spell of hot weather came to an end the day before we were due to head out for our regular fieldwork in the Lake District.  The day started with rain which petered out by mid-morning. Clouds had started to lift by the time we reached Wastwater, although had still not cleared the peaks of Great Gable and Scafell Pike.   The scene in the photograph above may look idyllic, but the water was choppy, with white horses visible on the lake and waves adding an extra complication to my sampling efforts.  

One recurring feature of Wastwater is persistent growths of algae on the rocks in the lake littoral zone.   I’ve never quite been able to explain why this is the case.   We do see visible growths of green algae in other lakes nearby, but these are usually transitory phenomena whereas Wastwater’s margins nearly always have growths that are obvious with the naked eye.  Wastwater is probably the lake with the lowest level of human influence in the region, so the usual kneejerk association between algae and nutrients doesn’t really hold.   It is a conundrum still awaiting an explanation.  

As well as these green growths, however, there are also very dark crusts growing on larger boulders around the air-water interface.  I’ve written about these before (see “Notes from Wastwater …” and “Close to the edge in Wastwater …”) and Allan Pentecost has also made a study of them (see reference below).  Today, with the water levels going up and down as the waves came in, I held my camera underwater and managed to photograph these two communities in situ, revealing their clear zonation.   Spirogyra dominates in the fully-submerged zone whilst the cyanobacterial crusts are in the zone that is often exposed.

Algal zonation on an emergent boulder in Wastwater, August 2022.   The green algae in the lower part of the image is Spirogyra and the black patches in the upper part are cyanobacteria.  The picture frame is about a metre across.

Scraping the crusts off the rocks for later examination was not easy in the choppy conditions.   I just got enough to confirm that the predominate cyanobacterium was a Calothrix species, but not enough to photograph.   The Spirogyra was easier to collect: it was a broad filamentous form with two chloroplasts which is very common in the Lake District.  I’ve never seen it conjugating so cannot put a species name on it.  

This type of zonation is well known in marine environments, where tides exacerbate the effects.   In natural lakes, water levels do not fluctuate to the same extent so the potential for zonation is more limited.  There is some evidence of zonation in deep Alpine lakes (see “Depths of imagination …” and “Life in the deep zone …”) and these studies are useful reminders that our understanding of benthic algal zonation in freshwaters is limited by our capability (I wear chest waders when sampling, the Alpine studies used SCUBA).  The study in the Bodensee I discuss in an earlier post found this zonation most clearly expressed on submerged vertical rock faces which, to the best of our knowledge, do not exist in Wastwater.   Deepwater benthic algae will not be able to establish in depositional environments.  But, from my shore bound perspective, deepwater benthic algae are a subject on which I can speculate but not explore for myself.

Spirogyra filaments from the submerged zone of a boulder in the littoral of Wastwater, August 2022.  Scale bar: 20 micrometres (= 1/50^th of a millimetre).

Wastwater empties into the River Irt, to which we travelled straight after our sojourn on the lake shore.  Both of these also had extensive coverage of filamentous algae.  Once again, algae are almost always visible at these sites despite a lack of obvious human drivers.   Quantities were greater today than we usually find at this time of year, most likely because of the long period of warm, dry weather, and this was the case at almost all the sites I’ve looked at recently.   Of note, however, was the absence of obvious growths of Torularia atrum, which was abundant when I visited in June (see “All change …”).   For every constant on this regular tour of Lake District habitats, there seems to be an inexplicable variable too.  The algae change and I learn.   

Reference

Pentecost, A. (2014). Distribution and ecology of cyanobacteria in the rocky littoral of an English lake district water body, Devoke Water. Life, 4: 1026-1037.

Other highlights from this week: 

Wrote this whilst listening to: Rocket, 2017 album by Americana/Indie artist Alex G.

Currently reading: The Country of Others by Leïla Slimani, about the last days of French colonialism in Morocco.

Cultural highlight:  Hit the Road, a film described as an Iranian Little Miss Sunshine.  

Culinary highlight:  Tasting menu at Peace and Loaf in Newcastle