Little pond of horrors …

One of the highlights of the British Phycological Society’s recent meeting in Plymouth was a talk by Sebastian Hess from the University of Cologne about amoebae which preyed upon microscopic algae.  His presentation included several video clips, one of which featured the aptly-named Vampyrella attaching itself to the outside of an alga cell and slowly sucking out its contents.   The clip drew audible gasps from the audience, none of whom had walked into a dryly-named session on “Algal interactions across the tree of life” expecting the tropes of a horror movie to be displayed before their eyes.

The link to the YouTube video below gives you some idea of the predatory nature of these organisms.   They are not technically parasites but “protoplast feeders”, penetrating the cell wall of the victim and consuming the cell contents by a process known as “phagocytosis”.   Although these organisms have been known for a long time (they were first described in 1865), it is only in recent years that the diversity of these organisms has become apparent.  That’s because, like many unicellular organisms, it is difficult to fully appreciate the differences just by peering at them through a microscope.  It has only with the advent of environmental DNA analyses that this has been understood.   We now know, for example, that the species found in freshwater, soil and marine environments are all different and that each vampyrellid is fairly specific to a particular group of algae (more about Sebastian Hess’ work can be found here.

The vampyrellid amoeba Arachnomyxa cryptophaga feeding on the green alga Eudorina elegans, from the German YouTube channel “Nicht interessant”

Those of us who are interested in algae tend to go on about their importance in trapping the sun’s energy via photosynthesis but rather less time thinking about how that energy then passes from the algae through to higher trophic levels.   I often see chironomid larvae feeding on algae when examining samples (see, for example, “More about very hungry chironomids”) but these tend to use the larger filamentous algae as supports while they graze on the smaller epiphytes (mostly diatoms in the streams I look at) which grow on the surface of the filaments.   The vampyrellids, by contrast, have powerful enzymes that can punch holes in the though cell walls of filamentous algae so that they can suck out the contents.   At the simplest level that creates a tasty meal for the vampyrellid but, from a broader ecological perspective, these amoebae are turning large unpalatable chunks of carbon that an insect larva cannot manipulate into its mouth into smaller nuggets that could, in theory, be consumed by small beasts.  These small beasts, in turn, fuel the slightly larger bugs which may be prey for a fish.   The vampyrellids, in other words, help keep carbon pumping through the aquatic ecosystem.

It is not just predatory amoebae that perform this function.  Another talk at the Plymouth meeting by Davis Laundon of the Marine Biological Association showed that microscopic fungi may play a similar role.   Again, I’ve mentioned these organisms before (see “Little bugs have littler bugs upon their backs to bite ‘em …”) but not really reflected on what role they play in an aquatic ecosystem.  Davis worked in marine rather than freshwater ecosystems but the same principle seems to be at play: large chain-forming diatoms such as Chaetoceros are too big for many zooplankton grazers to feed upon but thraustochytrid fungi inadvertently convert these big indigestible hunks of carbon into bite-sized portions which then fuels the ecosystem in Plymouth Sound.

Coincidentally, my own interest in the microscopic world started when I read about amoebae in school textbooks, and my earliest natural history explorations involved trying to find amoebae in local ponds, usually without success (when I was in Nigeria, protozoans returned the favour … but that’s another story).   Even now, I do not regard amoebae as particularly easy organisms to observe and have not tried to identify them.  However, once your eyes (and mind) are tuned to noticing particular phenomena in nature, there is a positive feedback loop and you start to notice these phenomena more and more.  I suspect I have been suffering from “amoeba blindness” for some time.  Last year I wrote an essay about what we see and don’t see when peering down a microscopeand Marian Yallop, one of my co-authors, included some photographs of amoebae, reminding me of my earlier fascination with these unicellular organisms.  I’ll be watching out for these as I examine samples, and trying to learn a little more about them during 2020.

A plate from showing interactions between algae and other protists from Kelly et al. (2019).  A. A ciliate has consumed a variety of live pennate and centric diatoms and cyanobacterial filaments. B. Algae autofluorescing red and cyanobacterial filaments yellow within the ciliate. C. Other protists e.g. Vorticella select relatively smaller soft-bodied green algae. D. This amoeboid protist had previously consumed two relatively large diatoms E. Some reorganising of the cell contents is required to shuffle these engulfed cells to the periphery. F. Exocytosis takes place to release the partially digested cells, and the amoeba rapidly moves away. This sequence of events lasted a few minutes. Images (A-B, D-F) were taken from biofilm material from Winford Brook, North Somerset, UK by Marian Yallop; Image C was taken from the Danube at Zimmern, Baden-Württemberg, Germany by Lydia King.

References

Hess, S., Sausen, N. & Melkonian, M. (2012).   Shedding light on vampires: the phylogeny of vampyrellid amoebae revisited.  PLoS One 7: e31165. 

Hess, S.& Melkonian, M. (2013).   The Mystery of Clade X: Orciraptor gen. nov. and Viridiraptor gen. nov. are Highly Specialised, Algivorous Amoeboflagellates (Glissomonadida, Cercozoa).  Protist 164: 706-747.

Kelly, M.G., King, L.. & Yallop, M.L. (2019).  As trees walking: the pros and cons of partial sight in the analysis of stream biofilms.  Plant Ecology and Evolution 152: 120-130.  

 

This week’s other highlights:

Wrote this whilst listening to: PJ Harvey

Cultural highlight: Tutankhamun: Treasures of the Golden Pharaoh at the Saatchi Gallery in London.   Was looking forward to seeing Girl From The North Country, a musical based around Bob Dylan’s songs, on the same trip to London but it was cancelled 40 minutes before the start due to cast illness.

Currently reading: Nine Lives: In Search of the Sacred in Modern India by William Dalrymple

Culinary highlight: Mildreds, a vegetarian restaurant in London’s Soho.   You can’t book ahead, so we had to wait for a table.   We spent this time at the closest pub, which just happened to be the John Snow, featured in “A drink of water with John Snow”, a post from 2013.  Mildreds was worth the wait, particularly for the desserts.  I was diagnosed as lactose-intolerant last year and normally gaze miserably at dessert menus packed with dairy-rich offerings.  Mildreds, however, is fully vegan throughout January, so the entire dessert menu was there for the choosing.

Quantifying our ignorance …

I am fairly sure that I am not a popular person after my latest choice of slide for the “ring test”, the regular calibration exercise that UK and Irish diatomists perform.   I had noticed a few taxa that we had not seen in previous ring tests in a sample I collected during my visit to the Shetland Islands back in May 2019 (see “Hyperepiphytes in the Shetland Islands”) but, on closer examination, the sample proved to be both highly diverse and very challenging.  The seven experienced analysts who provide the benchmark analyses for the ring test found, between them, over 150 different species: some we could name with confidence, but others we could match to no published description.  Amongst those was the species of Achnanthidium photographed below.   It might be Achnanthidium digitatum or possibly A. ertzii but, then again, it does not quite match the characteristics of either of these so, once again, we have left it unnamed (you can find the original descriptions of both these species in the reference list).

According to Algaebase there are 116 species of Achnanthidium that are currently accepted but descriptions of these are scattered through the literature so it is really hard to be confident that you have found a new species during a routine survey.  This is particularly the case when we only have light microscopical analyses with which to work, as the small size of Achnanthidium species means that you really need a scanning electron microscope to see the fine details clearly.  This, however, assumes that the pool of unnamed Achnanthidium species is finite and that the 116 species on Algaebase is a significant proportion of the total number of Achnanthidium species.  A recent study by Eveline Pinseel and colleagues based on samples from Arctic regions offers hints that there is still plenty of diversity within the genus that cannot be linked to named species

This may, however, be a naïve assumption.   My colleague Maria Kahlert, who works in Sweden, comments that she is quite happy looking at samples that I send her from polluted sites in the UK as she can name most of the species (Achnanthidium and otherwise) from her own experience.   It is the samples from pristine habitats that fox her because so many of the forms are different to anything she has encountered in Sweden.  We have, in other words, a neat reversal of the opening line of Anna Karenina (“All happy families are alike, each unhappy family is unhappy in its own way”), with very high beta and gamma diversity of diatoms (probably other microalgae too) as a characteristic of regions with low population density (see “Baffled by the benthos (2)”).  We often miss this in our enthusiasm to fit all that we see down the microscope to published descriptions, but when we take time to look hard, that diversity – and those differences between sites – start to mount up.

The unknown Achnanthidium species from Petta Water, Mainland, Shetland Islands (pictured at the top of the post).  Scale bar: 10 micrometres (= 1/100^th of a millimetre).   Photographs: Lydia King

Let’s think of this as an ecological experiment to understand the diversity of Achnanthidium, following the capture-mark-capture approach.   Capture-mark-recapture is a technique used by ecologists to assess the size of a population.   As it is rarely possible to count all individuals, a portion of the population is collected, marked (a dab of paint on a snail’s back, for example) and released.   Some time later, the population is sampled again, and the proportion of those that bear the mark in this second sample is used as an indicator of the proportion of the population captured by the original sample.   Though devised for population biology, some have used the same principles to understand diversity in other contexts too so might it work as a means of understanding the yet-to-be discovered diversity of diatoms?

What we have in the scattered taxonomic literature is a record of all the Achnanthidium species that have been “captured” (i.e. observed) and “marked” (i.e. described) by taxonomists.   Suppose we now go some locations not previously visited by taxonomists, take some new samples and see 1) how many different forms of Achanthidium we can see and b) how many of these are “recaptured” (i.e. forms that align with previously described species).   Or, thinking about the problem in a different way, the number of named species could be compared with the number of distinct “operational taxonomic units” (“OTUs”) detected by metabarcoding.   More relevantly, how many extra OTUs are added when more lakes and streams are added to the dataset?   There are well-established methods for deriving “rarefaction curves” that might be useful in understanding regional diversity of diatoms, and modifications of “capture-mark-recapture” have been used to understand taxonomic diversity in palaeobiolgoical contexts, so why not in contemporary ecology too?

The Shetland Islands would make an ideal test ground for such a study as they are geologically-diverse habitats providing the types of conditions where Achnanthidium species thrive (low population density and agricultural intensity.   The diatoms of the region were studied about 40 years ago by my late mentor John Carter and although one of his samples yielded the type material for Achnanthidium caledonicum there have been so many developments in Achnanthidum taxonomy subsequently that this archipelago represents a tabula rasa for a modern taxonomist.   Its many remote lochs and streams offer the setting for a natural experiment which sets out, to put it bluntly, to quantify our ignorance.

Achnanthidium caledonicum from Loch Osgaig, Highland Region, Scotland.   Originally described as Achnanthes microcephala f. scotica Carter & Bailey-Watts 1981 (Scale bar: 10 micrometres (= 100^th of a millimetre).  Photographs: Lydia King.

References

Carter J. R., Bailey-Watts A. E. (1981). A taxonomic study of diatoms from standing freshwaters in Shetland. Nova Hedwigia. 33: 513-630.

Pinseel, E., Vanormelingen, P., Hamilton, P. B., Vyverman, W., Van de Vijver, B., & Kopalova, K. (2017). Molecular and morphological characterization of the Achnanthidium minutissimum complex (Bacillariophyta) in Petuniabukta (Spitsbergen, High Arctic) including the description of A. digitatum sp. nov. European Journal of Phycology 52: 264-280. https://doi.org/10.1080/09670262.2017.1283540

Van der Vijver, B., Jarlman, A., Lange-Bertalot, H., Mertens, A., de Haan, M. & Ector, L. (2011).  Four new European Achnanthidium species (Bacillariophyceae).  Algological Studies 136/137: 193-210.

Liow, L.H. & Nichols, J.D. (2010). Estimating Rates and Probabilities of Origination and Extinction Using Taxonomic Occurrence Data: Capture-Mark-Recapture (CMR) Approaches.  The Paleontological Society Papers 16: 81-94).

This week’s other highlights:

Wrote this whilst listening to: Sheku Kanneh-Mason’s recording of Elgar’s Cello Concerto.   Taking me back to his performance at the proms on a warm evening last summer.

Cultural highlight: Sam Mendes’ film 1917 which, coincidentally, uses the River Tees (as featured sporadically in this blog) as one of its locations

Currently reading: I have just finished Good Economics for Hard Times by Abhijit V. Banerjee and Esther Duflo, which I mentioned a couple of weeks ago.  It left me with the feeling that, had both Boris Johnson and Jerermy Corbyn read it and taken on its messages, the election campaign and the UK political landscape might have been very different.

Culinary highlight: OK Diner on the southbound side of the A1 near Grantham.  Felt like we were walking into the opening scene from Pulp Fiction (the one where Tim Roth jumps up onto a table and attempts to rob all the customers).   Escaped with wallet intact.

 

Hooray for hippo dung …

I’ve only seen hippopotami in the wild once in my life, and then only at a distance in the Yankari game reserve in northern Nigeria.   I took some photos, but these were taken with only a moderately-powerful telephoto lens and crocodiles basking a few metres from where our Land Rover was parked were a more pressing concern.  In any case, the prints from that holiday (years before digital cameras) are now lost.   The photo at the top of this post is, in fact, a pygmy hippopotamus – a different genus to the common hippopotamus (Hexaprotodon liberiensis rather than Hippopotamous amphibious) – taken at smaller wildlife park (a glorified zoo, really) near Jos but it will do for my purposes. 

A couple of years ago, I wrote about the role that bears may play in the transfer of essential nutrients from the ocean to the forests of north-western North America (see “Ecology’s bear necessities”).  I recently came across a paper that described a situation where hippos were responsible for a significant movement of nutrients in the opposite direction: from land to water.   We think of hippopotami as beasts that wallow in muddy water, but that is because they are filmed and photographed when there is enough light.   Hippos are actually nocturnal animals, coming out of the water to feed on the savannah grasslands when it is dark, and resting in pools during the day.    As they rest in their pools, the grass that they eat during the day is slowly digested (hippos are “pseudoruminants”) and, eventually, passes out of their colons as faeces.   That is an important source of carbon, nitrogen and phosphorus for the river, but also of silicon, an essential nutrient for diatoms.   Diatoms form the base of the food chain in Lake Victoria so, consequently, depend upon a constant supply of silica from the surrounding catchment, and the hippos are inadvertent vectors for this.

There is plenty of silicon in the natural environment (it is the second most abundant element on earth, after oxygen) but most is tightly-bound in particles and so is not in a form that is accessible to other organisms.   Some plants, especially grasses, however, use silicon as a means of strengthening and supporting their cells.  In the process, they also provide a measure of protection (as anyone who has been cut by the sharp edge of a grass leaf will know).  The silicon is taken up by the plant’s roots, but is then laid down in the cells as structures called “phytoliths”.  When these phytoliths are released back into the environment via a tortuous path through the hippo’s digestive system, the silicon they contain is in a much more accessible form than when it was trapped into minerals in the savannah soil.

The phytoliths released by the hippos form about three quarters of all the biologically-available silicon in the hippo pools and, when these have made their way down the stream, may also have an effect on the ecology of Lake Victoria.  At this point, the paper gets rather speculative, but noting that there has already been a significant decline in hippo numbers in recent decades, the authors suggest that this may have had an impact on the ability of diatoms to compete with other algae, contributing to the greater dominance of cyanobacteria that has been observed in recent years.

Even allowing for a little academic hyperbole, this is a useful reminder that trying to keep ecology neatly compartmentalised is never a good idea.  Everything is connected to everything else: lakes, rivers, terrestrial systems.  We sort of know this instinctively but, at the same time, scientists spend so much time absorbed by their specialisms that they often forget this too.   The hippopotamus seems to be an unlikely benefactor of tiny diatoms, but maybe that is the fault of our imagination rather than of nature.

Reference

Schoelynck, J., Subalusky, A. L., Struyf, E., Dutton, C. L., Unzué-Belmonte, D., Van De Vijver, B., Post, D.M., Rosi, E.J., Meire, P. & Frings, P. (2019). Hippos (Hippopotamus amphibius): The animal silicon pump. Science Advances 5: https://doi.org/10.1126/sciadv.aav0395

A baboon, photographed at Yankari game reserve in 1990.  The photograph at the end of the post shows a waterbuck, photographed on the same visit.

And, once again, some notes on what else I have been up to this week:

Wrote this whilst listening to: Keith Jarrett’s Köln Concert

Cultural highlight: Keith Jarrett’s Köln Concert is so good that I am prepared to enter it under two headings.  Worth listening to Tim Harford’s Cautionary Tales Podcast (Episode 7: Bowie, jazz and the unplayable piano) to learn more about this remarkable piece of music.

Currently reading: Raynor Winn’s The Salt Path.  I’m in south-west England so a book about walking the South West Coast Path seems appropriate.

Culinary highlight: yet to happen.  I’m at a conference at the University of Plymouth, subsisting on breakfast from a chain hotel and lunch from a university catering service that offers few options for those who are lactose-intolerant.

 

 

Fit for purpose?

 

It is sobering to think that the Water Framework Directive (WFD) will be twenty years old this year (23 October, to be precise).  The 70 pages of legalese that comprise this directive have, to a large extent, determined the course of my career over the past two decades (it is a few sentences in Annex V, to be precise, but unravelling and interpreting these has been enough).  Just before this anniversary arrives, however, the European Commission has published a “fitness check”, giving the Directive a thorough once-over before reaching a mixed verdict on its performance.

The report’s conclusion is that the WFD has provided a governance framework for water management but, overall, the condition of Europe’s water bodies has shown little significant improvement since the WFD passed into law.   The original objective – grossly optimistic in hindsight – was for all Europe’s water bodies to be at least at good status by 2015.  Instead, we are still in the situation where less than half are at good status.  There is no doubt that there have been local improvements, and the rate of deterioration may have decreased but this is not the same as a general trend towards better ecological quality in our water bodies.   I’ll offer three possible reasons for the shortcomings, based on my own experience of WFD implementation, in the hope that lessons learned from turning a well-intentioned policy instrument from theory into practice will have some broader lessons as we tackle the climate emergency.

The first lesson is that complex problems, by necessity, spawn complicated legislation.  The Water Framework Directive arose from an attempt, in the early 1990s, to produce a directive addressing the Ecological Quality of Waters.  As debates about this progressed, people realised that you cannot consider the state of the aquatic environment in isolation, without also considering broader economic issues such as water pricing and, indeed, all aspects of catchment management that respects the rights of other legitimate users.  Each of these issues requires a small army of bureaucrats to unpack and apply within the 28 Member States.   In some countries and for some aspects of the legislation, there were procedures in place that simply needed tweaking to be fit-for-purpose.  Some other aspects were, however, completely new for almost everyone.

The whole idea of using the health of an aquatic ecosystem (“ecological status”) as a measure of the long-term sustainability, for example, was something never attempted on such a scale before.  It had been advocated in the academic literature, and there were a few localised attempts to apply the system (RIVPACS in the UK, for example) but, as the sun rose on 23 October 2000, the task of working out how the fine words of Article 4 had to be translated to a practical reality that was both faithful to the intentions of the WFD and that worked within public sector budgets had to start.

A second big issue that was relatively under-acknowledged in the fitness check is that solving environmental problems cannot be achieved without engaging other sectors as well.   A recent review, to which I contributed, highlighted this, emphasising the need, first, to integrate water policy with other sectors (such as agriculture) whilst, at the same time, emphasising the need to demonstrate tangible benefits that extend beyond the subtleties of shifts in ecological parameters.  Bring agriculture on board to achieve more sympathetic management of catchments, in other words, recognise the contributions that farmers make (“public money for public goods”) but also back this up with substantial demonstrations of reduced flood risk for urban areas downstream.   That calls for a level of joined-up thinking across sectors that has not yet been achieved in Europe and which is, perhaps, an opportunity that the UK, shortly to be freed from the leviathan that is the Common Agricultural Policy, may be in a better position to address.  We live in hope.

The third reason may be that the ambition of the WFD may be higher than many politicians and civil servants are happy with.   Article 1 sets out the objective of promoting “sustainable water use based on a long-term protection of available water resources”.  A phrase such as that could have appeared in any of the party manifestos for our recent election but when the scientists unpack this and explain that this will mean that every river in the country needs to have average phosphorus concentrations of well under 0.1 milligrams per litre, and the water planners put a price on this, alone, that runs into hundreds of millions (if not billions) of euros, then that ambition falters.   More particularly, the noisy nature of much ecological and environmental data gives ample opportunity for bureaucrats to prevaricate rather than take steps that are unlikely to play well with the media (the WFD enshrines the “polluter pays” principle and, as we all contribute to urban wastewater loading, this translates to “voter pays”).

As its 20^th anniversary approaches, the WFD will have spanned four electoral cycles (assuming national parliaments have five-year terms), at each of which policy wonks will have been thinking less about long term sustainability of water resources and more about short-term swings in voting preferences.   Moreover, since 2008, much of Europe has felt the consequences of the banking crises, with public sector finances often badly affected.  Again, the scientific challenges that the WFD creates provides easy excuses for cash-strapped regulators to kick the can down the road rather than make potentially unpopular decisions.

Governance may be in place, in other words, but a willingness to push this governance to deliver may be lacking.  That, in turn, reflects a perceived unwillingness on the part of the electorate to accept the costs.  Imperfect democracies will always deliver imperfect solutions, particularly when the underlying problems are complex and the opportunity costs are high.

Pictures in this post are from a New Year’s Day walk around the riverbanks in Durham.  New feature for 2020 is a few notes on what else I’ve been up to during the week in which this post gestated:

Wrote this whilst listening to:  Bob Dylan’s John Wesley Harding; Bruce Springsteen’s Nebraska

Cultural highlight: Greta Gerwig’s Little Women.

Currently reading: Good Economics for Hard Times by Abhijit V. Banerjee and Esther Duflo – two Nobel Prize winners setting global problems into a broader economic framework.  Not an easy read but very stimulating.   A good follow-up to Kate Raworth’s Doughnut Economics, which I mentioned in a couple of posts last year.

Culinary highlight: followed a recipe in The Guardian which involved cramming all the leftovers from our Christmas dinner (turkey, stuffing, roast potatoes, parsnips, brussel sprouts) into a loaf tin along with some breadcrumbs and two eggs to bind.  This created a meatloaf which I froze and then produced on New Year’s Day to provide a final reminder of the festive season before the realities of 2020 intruded.  Doubly enjoyable as West Ham had their first win of the Festive Season as it was being demolished.

Reference

Carvalho, L., Mackay, E. B., Cardoso, A. C., Baattrup-Pedersen, A., Birk, S., Blackstock, K. L., Borics, G., Borja, A., Feld, C.K., Ferreira, M.T., Globevnik, L., Grizzetti, B., Hendry, S., Hering, D., Kelly, M., Langaas, S., Meissner, K., Panagopoulos, Y., Penning, E., Rouillard, J., Sabater, S., Schmedtje, U., Spears, B.M., Venohr, M., van de Bund, W. & Solheim, A. L. (2019). Protecting and restoring Europe’s waters: An analysis of the future development needs of the Water Framework Directive. Science of the Total Environment 658 1228-1238. https://doi.org/10.1016/j.scitotenv.2018.12.255