How to make an ecosystem

I visited Scotland vicariously last week (meaning that I did not actually cross the border but a little bit of Scotland made its way south to me).   In this case, my wife had been reconnoitring potential sites for a field course along the Fife coast and had visited the sand dunes at Tentsmuir National Nature Reserve to see if the plant succession there would make a suitable exercise for her students.  Behind the sand dunes there was a low lying area of saltmarsh and, within that, large areas of algal mats.  I’m guessing that, having brought me a bottle of Highland Park whisky as a reward for not killing her houseplants during her previous trip to Scotland, she thought that my liver deserved a break.

Tentsmuir is a dynamic ecosystem, with sand dunes on the coastal side and, in places, a complete succession from colonising grasses on the seaward side to mature forest on the land.   However, there are also slacks behind the dunes which are periodically inundated by seawater, leading to the development of saltmarshes.   The periodic wetting and drying of saltmarshes is ideal for filamentous algae and these, in turn, create a mesh of interlocking filaments that binds the sand grains and traps organic matter.   Over the course of many tidal cycles, conditions become suitable for higher plants such as glasswort and sea asters.   I have a soft spot for saltmarshes and sand dunes as these are the habitats where I made some of my first forays as an ecologist (see “How to be an ecologist #4”); however, I have never looked in detail at the algal mats before.   So, I poured myself a glass of Highland Park, turned on my microscope and teased out a few of the filaments from my present.

Algal mats from saltmarsh at Tentsmuir National Nature Reserve.  The left hand picture shows a plant of Salicornia europaea agg. (Common Glasswort, or “samphire”) surrounded by algal mats (photo: Heather Kelly).  The right hand picture demonstrates how the mat retains its integrity after being removed from the saltmarsh.

The mat, in this case, seemed to be made up predominately of two types of alga: the yellow-green alga Vaucheria and the Cyanobacterium Microcoleus chtonoplastes.   I often see Vaucheria in freshwaters so it was the Microcoleus that attracted my attention.   It belongs to the same family as the Phormidium that we met in Mallerstang (see “The stresses of summertime …”) and we can see several of the same features: rows of almost identical cells and, in particular, no “heterocysts”, specialised cells that are responsible for nitrogen fixation.   Technically, the chain of cyanobacterial cells is referred to as a “trichome” and these are enclosed in a “sheath” (seen most clearly in genera such as Scytonema: see “Tales from the splash zone …”).  In Phormidium there is a single trichome per sheath but each sheath of Microcoleus contains several, often twisted around each other to form rope-like bundles.

Microcoleus cf chthonoplastes from the saltmarsh at Tentsmuir National Nature Reserve, August 2017.  Scale bar: 10 micrometres (= 100^th of a millimetre).

Although I mentioned that Microcoleus lacked heterocysts, this does not mean that it is not capable of nitrogen fixation.   The reason that cyanobacterial cells need heterocysts is that the nitrogenase enzyme only works in anerobic conditions.  The oxygen that is produced as a result of photosynthesis is, therefore, a toxin that needs to be kept away from nitrogenase. Heterocysts have thick cell walls and less chlorophyll as means of keeping the nitrogenase in an oxygen-free environment.  However, some non-heterocystous cyanobacteria, including Microcoleus, are able to fix nitrogen at night (when the photosynthetic apparatus is not pumping out oxygen) .   As there seems to be no protection for the enzyme inside the cells, it is possible that the daily destruction of enzyme is offset by renewed synthesis when light levels fall and there is no more oxygen being produced internally.   Nitrogen-fixation is already an expensive process for cells, requiring a large amount of energy, and this will increase the cost further.  However, in the case of the saltmarsh at Tentsmuir, there is a large amount of habitat available and few other organisms capable of exploiting it, so perhaps this is an investment worth making?

The benefits of that investment then “trickle down” (or up, depending on your point of view) through the ecosystem.   The cyanobacteria “fix” carbon and nitrogen and, in effect, create the soil within which other organisms thrive.  Janet Sprent, of the University of Dundee, calculated that, assuming nitrogen to be the limiting nutrient, then the fixation by Microcoleus and other cyanobacteria in such habitats could probably support the biomass of higher plants that is usually observed.  They are, in other words, a self-perpetuating “green manure” that creates a habitat within which other organisms can thrive.  In turn, by binding sand, they help to stabilise coastal features and, in turn, protect other coastal habitats and the communities that live amongst these.

References

Malin, G. & Pearson, H.W. (1988).  Aerobic nitrogen fixation in aggregate-forming cultures of the nonheterocystous Cyanobacterium Microcoleus chthonoplustes. Journal of General Microbiology 134: 1755-1763.

Omoregie, E.O., Crumbliss, L.L., Bebout, B.M. & Zehr, J.P. (2004).  Determination of nitrogen-fixing phylotypes in Lyngbya sp. and Microcoleus chthonoplastes cyanobacterial mats from Guerrero Negro, Baja California, Mexico.  Applied and Environmental Microbiology 70: 2119-2128.

Sprent, J.I. (1993).  The role of nitrogen fixation in primary succession on land.  pp. 209-219.  In: Primary Succession on Land (edited by J. Miles & D.W.H. Walton), Blackwell Scientific Publications, Oxford.

Sroga, G.E. (1997).  Regulation of nitrogen fixation by different nitrogen sources in the filamentous non-heterocystous cyanobacterium Microcoleus sp.  FEMS Microbiology Letters 153: 11-15.

How to win the Hilda Canter-Lund competition (4)

Daniella Schatz’ image of the coccolithophore Emiliania huxleyi is one of a relatively small number of electron micrographs to have made it to the shortlist of the Hilda Canter-Lund prize and, though not an outright winner, it offers some useful lessons to anyone considering submitting an image in next year’s competition.

The first point to note is that Daniella has not submitted a single image, but a montage of two separate images. The competition rules state that “basic image enhancement (i.e. cropping, adjustment of contrast, colour balance etc) is permitted, along with focus stacking and stitching. However, excessive image manipulation is not acceptable.”   “Excessive image manipulation” is not easy to define; however, Daniella’s montage worked for the judges because the two elements together tell a story about the life of this alga.  The left- and right-hand images are the “before” and “after” cases of a major factor controlling the ecology of Emiliania huxleyi.  Daniella wanted to tell the story of the decline and fall of E. huxleyi blooms in the oceans; in the process she also evoked a long tradition of memento mori – artworks that remind viewers of their own mortality, and of the fragility of all life on earth. Another montage, this time by Alizée Mauffey, made it to the short list in 2017; again, the images were not selected and placed for aesthetic reasons, but to illustrate the range of functional traits within intertidal macroalgae.

Daniella piles on a little more “image manipulation” by using false colour to highlight the tiny EhV201 virus cells that are scattered across the right hand cell and which are responsible for its sorry state.  A couple of SEMs that have been enhanced by false colour are submitted each year but the artificiality of the medium rarely results in a major improvement to the image.  The stark monochrome of SEMs places them in a long and noble tradition of black and white photography that should not need this type of enhancement.   She, however, challenges this by using false colour very sparingly and to draw attention to an important element of her story.

And so to the “story”: we now ask all entries to the competition to be accompanied by a legend of about 100 words explaining a little more about the picture.   Most experienced phycologists will recognise the left hand image as a coccolithophore but many viewers will see these as abstract geometric shapes. The legend is important to help the viewer decode these shapes and place them into a broader context; in this case, by emphasising their role in global carbon cycling.  Having said that, most of the shortlisting takes place without reference to the legend with initial screening based primarily on the quality of the images.  I do remember, however, that Daniella’s image was one where we did need the legend in order to understand what she was trying to say.

A detail from Daniella Schatz’ Scanning Electron Micrograph (SEM) of the coccolithophore Emiliania huxleyi showing the large dsDNA Emiliania huxleyi virus (EhV201, coloured orange). EhV is a large dsDNA virus that is responsible for the demise of vast oceanic blooms of E. huxleyi. During viral infection the cells undergo programmed cell death and shed their coccoliths, important components of the carbon cycle.  The individual viruses are each about 100 nanometres (1/10000^th of a millimetre) in diameter.

We also encourage photographers, particularly those submitting microscopic images, to include a measure of scale in the legend, particularly for microscopic images.  This is important, as lay audiences will have little idea about the size of the objects that are being portrayed.   When images are used as illustrations, then a scale bar is appropriate (see “The stresses of summertime …” for a recent example); however, a scale bar is likely to be an unwelcome intrusion in an otherwise balanced composition so a sentence in the legend is usually more appropriate.   Remember that the term “micrometre” might not be easily understood by many viewers, and it is a good idea to explain dimensions in millimetres as well.

When the votes were counted in 2015, Daniella’s image lost out to Günter Forsterra’s stunning view of the Beagle Channel off the coast of Chile.  However, it stands as a fine example of conceptual approach to the Hilda Canter-Lund competition – with several different elements combining to convey an idea that is more than the sum of its parts.   The photographer of the microscopic world rarely has the luxury of the “decisive moment” and, instead, the quality of the final image often lies as much in post-production as it does in image capture.

Rolling stones gather no moss …

Back in early July I mused on how rivers changed over time (see “Where’s the Wear’s weir?”) and reflected on how this shapes our expectations about the plants and animals that we find.  In that post, I compared a view of the River Tees today with the same view as captured by J.R.W Turner at the end of the 18^th century.   The photograph above is taken about 40 kilometres further upstream from Egglestone Abbey and shows the River Tees as it tumbles along in a narrow valley between Falcon Clints and Cronkley Scar.   I’ve written about this stretch of river before (see “The intricate ecology of green slime” and “More from Upper Teesdale”) and it is an idyllic stretch.   It all looks, to the uninitiated, very natural, almost untouched by the hand of man.

However, a couple of kilometres beyond this point we turn a corner and are confronted by a high waterfall, Cauldron Snout, formed where the river cascades over the hard Whin Sill.   Scrambling up the blocky dolerite is not difficult so long as you have a head for heights but, on reaching the top, a wall of concrete comes into view.  This is the dam of Cow Green Reservoir, constructed between 1967 and 1971 and highly controversial at the time.  The purpose of the reservoir was to regulate the flow in the River Tees, in particular ensuring that there was sufficient flow in the summer to ensure a steady supply for the industries of Teeside (most of which have, subsequently, closed).  My first visit to Cauldron Snout was in the early 1980s on a Northern Naturalist Union field excursion led by David Bellamy.  As we scrambled down Cauldron Snout, Tom Dunn, an elderly stalwart of the NNU, told me how much more impressive Cauldron Snout had been before the dam was closed.

Now look back at the picture at the top of this post.   The dark patches on the tops of the boulders emerging from the water are growths of the moss Schistidium rivulare, which thrives on the tops of stable boulders that are occasionally submerged.    The old adage “a rolling stone gathers no moss” is, actually, true, leaving me wondering how much less of this moss an walker beside this river in the mid-1960s might have seen.   How many more powerful surges of storm-fuelled water would have there been to overturn the larger boulders on which Schistidium rivulare depends?   Bear in mind, too, that two major tributaries, the Rivers Balder and Lune, also have flow regimes modified by reservoirs and the potential for subtle alteration of the view that Turner saw at Egglestone increases.   I wrote recently about how differences in hydrological regime can affect the types and quantities of algae that are found (see “A tale of two diatoms …”).   I may have stood at exactly the same place where Turner had sat when he drew the scene at Egglestone, but I was looking at a very different river.

The dam of Cow Green Reservoir looming above the top of Cauldron Snout in Upper Teesdale National Nature Reserve, Co. Durham, July 2017.  The picture at the top of this post shows the Tees a couple of kilometres downstream from Cauldron Snout.

Trevor Crisp from the Freshwater Biological Association showed that the consequences of Cow Green Reservoir on the River Tees extend beyond alterations to the flow.  Impounding a huge quantity of water in one of the coolest parts of the country also affects the temperature of the river, due to water’s high specific heat capacity.  This means that there is not just a narrower range of flows, but also a narrower range of temperature recorded.   The difference between coolest and warmest temperatures in the Tees below Cow Green dropped by 1 – 2 °C, which may not seem a lot, but one consequence is to delay the warming of the river water in Spring by about a month, which delays the development of young trout.  However, Crisp and colleagues went on to show that any reduction in growth rate due to lower temperatures was actually offset by other side-effects of the dam (such as a less harsh flow regime) to result in an increase in the total density of fish downstream.   Others have shown significant shifts in the types of invertebrate that he found in the Tees below Cow Green, with a decrease in taxa that are adapted to a harsh hydrological regime, as might be expected.   Maize Beck, a tributary which joins just below Cauldron Snout, and which has a natural flow regime, shows many fewer changes.

One conclusion that we can draw from all this is that healthy ecosystems such as the upper Tees are fairly resilient and can generally adapt to a certain amount of change, as Trevor Crisp’s work on the fish shows us. The big caveat on this is that the upper Tees is relatively unusual in having no natural salmon populations, as the waterfall at High Force presents a natural obstacle to migration.  Had this not been present, then all potential spawning grounds upstream of the reservoir would have been lost.   A second caveat is that there is still a lot that we do not know.   The studies of the river that followed the closure of the dam focussed on lists of the animal and plant species found; a modern ecologist might have put more effort into understanding the consequences for ecological processes, the “verbs” in ecosystems, rather than in the “nouns”.  Who knows how different energy pathways are now, compared to the days before regulation, and what the long-term consequences of such changes might be?  Schistidium rivulare is a good example of the limitations of our knowledge: its presence offers insights into the hydrology of the river, but we know relatively little about the roles that these semi-aquatic mosses play in the river ecosystem.   Knowing that there is much that we do not know should, at least, keep us humble as we struggle to find the balance between preserving natural landscapes and their sustainable use in the future.

Note

Twenty years ago, I would have recognised Schistidium rivulare, if not in the field, then at least after a quick check under the microscope.  Now, however, my moss identification skills are rusty and I had to turn to Pauline Lang to get this moss named.   I mentioned in “The Stresses of Summertime …” how the ecologist’s niche becomes the office not the field.  One danger is that we remain familiar with names (as I am with S. rivulare and other aquatic mosses) but, through lack of practice, lose the craft that connects those names to the living organisms.

References

Armitage, P.D. (2006).   Long-term faunal changes in a regulated and an unregulated stream – Cow Green thirty years on.  River Research and Applications 22: 957-966.

Crisp, D.T. (1973).  Some physical and chemical effects of the Cow Green (upper Teesdale) impoundment.  Freshwater Biology 7: 109-120.

Crisp, D.T., Mann, R.H.K. & Cubby, P.R. (1983).  Effects of regulation on the River Tees upon fish populations below Cow Green Reservoir.  Journal of Applied Ecology 20: 371-386.

Lang, P.D. & Murphy, K.J. (2012).  Environmental drivers, life strategies and bioindicator capacity of bryophyte communities in high-latitude headwater streams.  Hydrobiologia 612: 1-17.

A hidden world in a salty puddle …

An exchange of emails amongst a group of us preparing an obituary for Hilary Belcher led me to a short paper written by herself and Erica Swale on diatoms from a salty puddle close to a bridge under the M11 motorway in Cambridgeshire.  They had noticed some brown patches that looked like diatoms on the bottom of this puddle in 1979 and took a sample home to examine under the microscope. What they saw was an assemblage of diatoms that was more suggestive of a brackish habitat than freshwaters, leading them to conclude that the road salt that was spread on the M11 in winter was draining off the road and creating these mini salt lakes.  These were not one-off observations: they returned several times to find similar assemblages of diatoms in the same puddles.   Of these, only Surirella brebissonii is common in freshwaters.  Entomoneis and Cylindrotheca are two genera that I have written about before, both from marine or brackish habitats (see “A typical Geordie alga …” and “Back to Druridge Bay”).

Some diatoms associated with a puddle close to the M11 in Cambridgeshire: A: Entomoneis paludosa var. salinarum; B: Surirella brebissonii; C: Tryblionella hungarica; D: Nitzschia sigma; E: Nitzschia vitrea; F: Cylindrotheca closterium; G: C. gracilis.  From Belcher and Swale (1993).

I do occasionally find diatoms from marine habitats in rivers, and often suspect road salt to be the culprit.  One of the most extreme cases I encountered was a sample from the Ingrebourne, a small stream close to my childhood home where Bacillaria paxillifer constituted a third of all the diatoms present.  Bacillaria paxillifer is an intriguing diatom (see “The paradox that is Bacillaria” and links) but one that is very definitely a species that prefers saline rather than fresh water.  The Ingrebourne passes under the M25 motorway within about a kilometre of its source and crosses the busy A12 trunk road just upstream of the sampling location, so periodic pulses of salt are a possibility.

The ephemeral nature of these events, however, make them hard to prove and we are left with scattered notes such as this one in a small natural history journal.   These journals are, in many cases, struggling to survive in the modern age and I guess blogs such as this are taking over from them as records of botanical observations that are not structured in a way that makes publication in a mainstream scientific journal a possibility.  Hilary Belcher and Erica Swale made a number of substantial contributions to algal research over the course of their careers, but they were also consummate observers and recorders of their local environment – the wellspring from which an understanding of the natural world ultimately flows.

I am thankful to Hilary in one other way: she and her partner Erica Swale wrote a small (47 page) booklet with clear line drawings of the most common freshwater algae that was a required purchase for all undergraduates (and demonstrators) attending Brian Whitton’s algae practicals at Durham and it was through this book that I started to learn how to identify algae.  There are, I notice, just 17 genera of diatoms illustrated in this book but there was enough here to start putting names onto the shapes that floated – or flitted – through my field of view as I struggled to learn the rudiments of the craft.

Left: Hilary Belcher on a sampling trip to the Thames in the early 1990s (photo: Alison Love) and, right: the cover of her introductory guide to freshwater algae, co-authored with Erica Swale.

Reference

Belcher, H. & Swale, E. (1993).  Some diatoms of a small saline habitat near Cambridge.  Nature Cambridgeshire 35: 75-77.

A full appreciation of the life and work of Hilary Belcher, compiled by Jenny Bryant, will appear in the next edition of The Phycologist.

The stresses of summertime …

One reaches a stage in an ecological career when your “niche” becomes the office not the field and you are expected to focus your hard-earned experience on data that others have collected.  That means that I spend more time than I wish – even in the summer – staring at computer screens and writing reports – and far too little time engaging directly with nature.   Today’s post is the result of a Saturday’s excursion around some of the more enigmatic parts of the Yorkshire Dales National Park (the enigma being, basically, that we spent most of our time in Cumbria, not Yorkshire).

The photograph above shows a steam locomotive hauling a train along the Settle to Carlisle railway as it makes its way through Mallerstang, the upper part of the Eden Valley.   It is a beautiful little valley, hidden away from the main tourist drags and the sight of a steam train imparted a sense that we were somehow detached, albeit briefly, from the modern world.   The river channel itself lies amidst the ribbon of woodland in the valley bottom.

The River Eden in Mallerstang (SD 778 985) with (right) a large pebble with a Cyanobacterial film.

Curious to see what kind of life thrives in such a heavily shaded stream, I hopped over a fence, pushed through some bankside vegetation, crouched down and lent out as far as possible to grab a few of the stones from the streambed.   As I would have expected in a stream in such a location, the slippery film on the stone surface was thin (this is the time of year when the algae and other microbes can barely grow fast enough to keep up with the voracious appetites of the invertebrates that inhabit the crevices among the rocks) but, when I held it up to the light, there was a distinct greenish tinge that piqued my curiosity.

Under the microscope, this green tinge revealed itself to be due to numerous filaments of a thin, non-heterocystous cyanobacterium (blue-green alga), similar to that which I see in the River Ehen (see “’Signal’ or ‘noise’?”).  There, Phormidium autumnale forms tough leathery mats whereas here there was no obvious arrangement of the filaments.   In fact, the filaments seemed to be randomly organised within a mass of organic matter that made photography difficult and the photograph below is of one that had glided into a clear space on the coverslip.   I was surprised that there were relatively few diatoms present but, amidst the clumps of cyanobacteria and organic matter, I could see cells of Gomphonema pumilum, though it was very definitely sub-dominant to the Phormidium.  That was not very easy to photograph either, and my images have been built-up using Helicon Focus stacking software.

Some of the algae living on stones in the upper River Eden, August 2017: a. Phormidium cf autumnale; b. and c.: Gomphonema cf pumilum.  Scale bar: 10 micrometres (= 100^th of a centimetre). 

I have seen other streams where non-heterocystous cyanobacteria thrive during the summer months and suspect that their unpalatability relative to other algae may play a part in this.  This is partially induced by the proximity of grazers – a recent study suggested that filaments of Phormidium did not need to come into contact with the grazer itself, only to detect chemicals associated with the grazer in the ambient water.  This, in turn, can promote production of a tougher sheath, making the filaments less palatable.   I’m always a little surprised that aquatic invertebrates find diatoms, with their silica cell walls, palatable, but I see enough midge larvae greedily hoovering-up diatoms to recognise that they know something that I do not.

My brief visit to the upper River Eden reminds me that summer can be a tough time for stream algae.   Not only is this the time that the invertebrate larvae are scouring rock surfaces for algae to serve as the fuel that will catapult them into their brief adult phases, but also the trees are in full leaf, limiting the amount of energy that the algae can capture in order to power their own growth.   Not surprising, then, that so many algae – diatoms and other groups alike – are more prolific in the winter, when the invertebrates are not so active and there is less shade from marginal trees (see “Not so bleak midwinter?” and “A winter wonderland in the River Ehen”).   I’ll probably be sitting indoors staring at spreadsheets and writing reports this winter too, but I’ll still be looking for excuses to get out and explore nature’s hidden diversity.

Pendragon Castle, guarding the entrance to Mallerstang in the upper Eden Valley. 

Reference

Fiałkowska, E.  & Pajdak-Stós, A. (2014).  Chemical and mechanical signals inducing Phormidium (Cyanobacteria) defence against their grazers.   FEMS Microbiology Ecology 89: 659-669.

Freshwater Benthic Diatoms of Central Europe

I mentioned last year that I was working on an English translation of Diatomeen im Süßwasser-Benthos … (see “Tales of Hofmann …”) and I am pleased to say that it has just been published by Koeltz Books.   The original German edition was written by Gabi Hofmann, Horst Lange-Bertalot and Marcus Werum and included over 700  of the most commonly-encountered benthic diatoms.   The new edition has added Marco Cantonati as an additional author and myself as an editor and has also been expanded so that there are now over 800 species represented.  Marco also undertook the primary task of translating the German into English after which I stepped into to give the text a final polish.

We’ve also taken the opportunity to update the taxonomy.  One frustration for many was the conservative approach that the first edition took to Fragilaria and relatives.  There has been a vigorous debate about this group for the last thirty years, with unanimity on the limits of the various genera still not achieved to everyone’s satisfaction.  There are, however, few who would regard lumping all into Fragilaria to be an acceptable solution.  The new edition unpicks the Fragilaria mega-genus in greater detail than in the first, adding Ctenophora, Pseudostaurosira, Staurosira, Staurosirella and Ulnaria to the list of genera.   Similarly, Tryblionella has now been split off from Nitzschia. Several other new genera also make their debuts in this edition (including Gilwiczia, Humidophila, Khursevichia, Paraplaconeis and Prestauroneis) whilst Eolimna has disappeared, the extant species subsumed into Sellaphora.   Finally, some former Diatoma species are now found in Odontidium (see “A tale of two diatoms …”).    Fragilaria pectinalis (see “And another one …”) is another species that has been included in this volume.

We have also put in some time improving the keys.   The original edition had a worrying tendency to include ecological information in the couplets, which means that any inferences drawn from the diatom assemblage about the habitat is compromised as the name itself depends partly upon that habitat (see “Identification by association?”).  I have tried to remove such circularity from the identification process in this version.

I’m a big believer in all analysts who work within a program using the same identification literature (ideally we should be using the same identification literature as was used by the developers of the metrics that are being used).  This brings a measure of consistency to the outputs, and also provides an indication of the level of detail that is required, which can limit the amount of time spent tracking down the correct name for a few valves of a rare diatom.   The original version of this book served that purpose well, I thought, and I hope that the new edition will continue that trend.

If 158 euros for 2.7 kg of dense scientific prose is not your thing, my cousin Pippa Kelly has an alternative offering that I can recommend.  Her first novel, Invisible Ink, differs from Freshwater Benthic Diatoms in just three respects:

1. it is cheaper (£8.99 for the paperback, £3.99 for the e-book);
2. it is lighter (344 grams); and,
3. it is a book you might actually want to read from cover to cover.

Tough choice.