And the Oscar for best alga in a supporting role goes to …

Low_Force_022006

I know that the focus of this blog can meander, depending on what takes my fancy week-to-week.  My core business is, however, writing about the hidden world of algae so, having written about Sam Mendes’ use of the River Tees Upper in his film 1917 in my previous post, I thought that I ought to take a trip up Teesdale to take a closer look at what is growing in the river at this time of year.   With Storm Ciara looming ominously on the forecast, I knew that if I did not sacrifice my Saturday morning it might be a while before I had another opportunity (there’s a graph at the end of this post which confirms this hunch).  And so I found myself buffeted by the wind with clouds scudding across the sky and the peaty water of the Tees thundering across the sequence of cascades that make up Low Force.

The main river was, even after a period without much rain, too deep and fast-flowing for me to venture far in so my activities were confined to the margins.   The rapid current, however, means that there were few of the small and medium-sized stones that I would normally remove and inspect.  Most had been picked up and transported further downstream leaving wide expanses of the Whin Sill bedrock.   In the shallow areas towards the edges that were not exposed to the full force of the current, there were dark green patches that I picked at with a pair of forceps.   When I was able to look at these under my microscope, I saw that they were Ulothrix zonata, a common inhabitant of northern British streams during the winter, and an alga that I have written about previously (see “The intricate ecology of green slime …” and “Bollihope Bhavacakra” amongst others).

Ulothrix_zonata_Tees_200208

Ulothrix zonata growing on Whin Sill in the River Tees at Low Force, Teesdale in February 2020.   The upper and central pictures on the left hand side show vegetative filaments and the lower picture shows empty cell walls after zoospores had been released, to which a germling is attached.  Scale bar: 20 micrometres (= 1/50thof a millimetre).   

The rocks were very slippery, even when not covered by green patches of Ulothrix zonata.   My usual approach to collecting specimens is to remove the whole stone and scrub the top surface with a toothbrush.  That, however, was impossible here so I had to resort to brushing the surface of the Whin Sill and hoping that enough of the slippery film remained attached to my toothbrush, which I then agitated in a bottle containing some stream water to shake the gunk off before repeating the process.  The small amount of material that I did manage to transfer from the rocks imparted a chocolate-brown hue to the water that signifies that diatoms were present.

Sure enough, when I did get a drop of the suspension under my microscope, there were diatoms aplenty, mostly wedge-shaped cells of Gomphonema growing at the end of long, branched mucilaginous stalks.  These, like Ulothrix zonata, are very common in northern British streams at this time of year.  I described similar assemblages from the River Wear at Wolsingham although, in that case, the Gomphonema shared their habitat with motile Navicula species as well (see “The River Wear in January”).   The Gomphonema in the River Tees is most likely G. olivaceum or a relative but I will need a closer look to be sure.  If I used an old Flora such as Hustedt’s 1930 Süsswasser-flora Mitteleuropas, I would have been able to be more assertive in naming this “Gomphonema olivaceum” but we now know that diatom systematics are more complicated than was thought to be the case in Hustedt’s days.

Gomphonema_Tees_200208

Gomphonema olivaceum-type colonies growing on Whin Sill in the River Tees at Low Force, Teesdale, February 2020.  Scale bar: 20 micrometres (= 1/50th of a millimetre).   

The sequences of 2017 were filmed in June not January so George Mackay would not have found the bedrock of the Tees to be quite as slippery as it was on my visit.   As the water warms up, grazers become more active and, as a result, the biofilms in the summer are much thinner than those in January.  That means that fewer slippery, slimy polysaccharides are produced, making it easier to keep your balance when walking at the edges of the river.

As I mentioned in my previous post, the sequence in 1917 involves George Mackay falling into a river in Picardy but crawling out of a river in Upper Teesdale.   I know less about the rivers of Picardy than I do about those in northern England, but a combination of low relief, extensive canalisation and the presence of heavy industry and coal mining in the area will mean that the algae found there will be very different to those in the Tees.   However, if 1917 can get 10 Oscar nominations (including for best sound editing) despite having the call of a Great Northern Diver echoing over No-man’s Land, then we can be fairly sure that the Wrong Sort of Algae is a level of detail that Sam Mendes and Roger Deakins thought they could safely ignore.

References

You can find some information about the diatoms of Picardy rivers in this paper:

Prygiel, J. & Coste, M. (1993).  The assessment of water quality in the Artois-Picardie water basin (France) by the use of diatom indices.  Hydrobiologia 269: 343-349.

This week’s other highlights:

Wrote this whilst listening to:  Michael Kiwanuka and other acts who will be playing at the Green Man festival in August.   I’ll be there too, talking about slimy algae, at Einstein’s Garden, the on-site science festival, along with (I hope) a gang of volunteers from the British Phycological Society.

Cultural highlight:   Two picks this week.  The first was Monteverdi’s Vespers performed at Durham Cathedral.  The cavernous interior of the cathedral joins the choir and orchestra as part of the experience, providing resonances that raise the experience beyond anything that a CD can offer.   The second is Bong Joon-ho’s film Parasite, a strong contender, along with 1917, at this evening’s Oscar Awards Ceremony.

Currently reading:  John le Carré’s Mission Song

Culinary highlight: a Napoli pizza cooked with locally-grown flour (www.gilchesters.com), part of a push this year to source more of our ingredients locally.  There’s obviously more to a Napoli pizza than can be grown in the UK but it is a start.

Tees_Middleton_levels_200208

River levels at the Tees at Middleton-in-Teesdale (x km downstream from Low Force) in the week from 3 to 9 February 2020. The arrow shows the time of my visit; note the steep rise in level a few hours later, coinciding with Storm Ciara moving through the region.  Graph from the excellent https://riverlevels.uk website.

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.

Kelly_PLECVO_2019_fig3

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.

Reflections from Castle Eden Burn

As 2019 draws to a close, I have looked back at all the data I have collected from Castle Eden Burn over the past twelve months.   I chose this location precisely because it was different to my usual haunts and, despite having visited this Dene and others along the Durham coast for over thirty years, I realised that I had never had a look at the algae.  Dry river beds are not the most obvious hunting grounds for aquatic biologists, after all.   This year, I put that right over the course of a number of visits between January and November and in this post I am summarising what I found.

I found a total of 77 different diatoms in the six samples that I collected, not to mention green and yellow-green algae (see “When the going gets tough …”) and mosses (see “A thousand little mosses …”).   Of these diatoms, 48 were rare and infrequent, only found in one or two samples, and never forming more than one percent of the total number of diatoms present.   Of the remainder, only two were found in every sample (Humidophila contenta-type and Achnanthidium minutissimum) whilst another eight formed at least ten percent of the total on one occasion.  Numbers of each species waxed and waned over the year: Humidophila contenta-type was abundant in the sample from my first visit in January 2019 but relatively scarce thereafter.  In comparison, Luticola frequentissima was very abundant on two occasions (more than 80% of individuals), quite abundant on three other occasions but absent from the sample from my final visit in November.

Some of these differences are due to the variable flow regime: the stream was dry on three occasions, ponded on one and flowing on just two occasions.  Those occasions when there was no running water were those when the proportions of diatoms that are tolerant to desiccation (see “Life out of water …”) were most abundant, forming from 20 to 97 percent of all individuals.  When there was running water, it was motile Nitzschia  species that dominated.    In fact, there was a strong negative correlation between proportions of desiccation-tolerant and motile taxa in the samples, indicating that the diatoms responded rapidly to the changing pressures experienced in the stream.  There was also a relationship between the proportions of desiccation-tolerant diatoms and the number of taxa recorded – the latter is a good measure of the level of physiological stress experienced in a stream.

What of the diatoms themselves?  Humidophila contenta-type was one of the two ever-presents.  It is, however, very small (few of those in our samples were more than a 100th of a millimetre long), making it difficult to photograph and, indeed, to discern many of the features of the valve.   This species sometimes forms short chains though I did not see any in the Castle Eden Burn samples.  It is strange to think that, when I first started to identify diatoms, this was considered to be part of the genus Navicula.   Since then, it has moved into the genus Diadesmis before finally being transferred to the new genus Humidophila by Rex Lowe and colleagues in 2014.    Some recently-described Humidophila species cannot be differentiated from H. contenta without a scanning electron microscope, so I have referred to this as “Humidophila contenta-type”. Humidophila_contenta

Humidophila contenta ag. from Castle Eden Burn, Co. Durham, January 2019.  Scale bar: 10 micrometres.   Photograph: Lydia King. 

The most abundant diatom in samples collected during the dry periods was Luticola frequentissima.  I started the year referring to this as “Luticola mutica” but was gently corrected by colleagues more au fait with recent literature than me.   Luticola mutica is larger (length: 11-28 µm; breadth: 6-9.5 µm) and has more widely-spaced striae (16-18 / 10 µm) than L. frequentissima (length: 7 – 13.8 µm breadth: 4.8 – 6.8 µm; striae: 20 -24 / 10 µm).  The specimens in the plate below all fit the description for L. frequentissima.  Some of the large specimens have size ranges that overlap with L. mutica (though even the largest specimen as a striae density consistent with L. frequentissima).   L. mutica is associated with more brackish habitats whilst L. frequentissima prefers freshwaters.

Luticola_frequentissima

Luticola frequentissima from Castle Eden Burn, Co. Durham, January 2019. Scale bar: 10 micrometres (= 1/100th of a. millimetre).  Photographs: Lydia King.

Simonsenia delognei is another characteristic species of habitats that dry out periodically.   This species, which is in the same family as Nitzschia, is quite small and only lightly silicified so easily overlooked.  It was common early in the year, but rare thereafter.  Whether this is a real characteristic of the species or an artefact of the conditions in Castle Eden Burn this year is difficult to tell as it is not a particularly common species so there are few other records against which this trend can be compared.

Simonsenia_delognei_CEB

Simonsenia delognei from Castle Eden Burn, Co. Durham, January 2019.  Scale bar: 10 micrometres (= 1/100thof a millimetre). Photographs: Lydia King.

Two other species of Nitzschia were common: I illustrated N. clausii in “Out of my depth …” and have included photographs of N. sigma here.   I’m intrigued that two of the most conspicuous Nitzschia in this sample are sigmoid in outline.  I’ve visited the question of sigmoid diatoms before, and still don’t have any good explanation why a few diatoms have this outline (see “Nitzschia and a friend …”).  Note, too, that Nitzschia species can be sigmoid in valve view (i.e. looking down from above) or girdle view (i.e. looking from the side), although the great majority of species are straight in both planes.

Nitzschia_sigma

Nitzschia sigma from Castle Eden Burn, Co. Durham, January 2019.  Scale bar: 10 micrometres (= 1/100th of a millimetre).   Photographs: Lydia King.

Finally, one more relative of Nitzschia that was found in a couple of samples, but never in large numbers, was Tryblionella debilis.  The genus Tryblionella was treated as part of Nitzschia for much of the 20th century.   As it appears to form a natural group with some distinctive characteristics, it is now generally treated as a distinct genus, although the molecular evidence indicates a complicated evolutionary history.   The principle characteristic of the genus is a longitudinal undulation on the valve face that is most clearly manifest on those species in the genus which have visible striae.   T. debilis is a small species with striae that are not resolvable with the light microscope; however, the undulations are just apparent as faint longitudinal lines running along the valve face.

Tryblionella_debilis

Tryblionella debilis from Castle Eden Burn, Co. Durham, January 2019.  Scale bar: 10 micrometres (= 1/100th of a. millimetre).  Photographs: Lydia King.

That’s a lot of diatoms from a stream that is not always a stream.   I am sure that someone with interests in other groups of algae could probably make similarly long lists for some of those, and a more thorough exploration of habitats within the stream could add to the number of diatoms.  That’s before suggesting a molecular study, which might well reveal cryptic diversity (i.e. significant taxonomic variation that is impossible to discern with a light microscope) within the species I have already described.   The greater our capacity to unravel the mysteries of the microscopic world, the more, it seems, we discover we don’t know.

Reference

Lowe, R.L., Kociolek, P., Johansen, J.R., Van de Vijver, B., Lange-Bertalot, H. & Kopalová, K. (2014).  Humidophilagen. nov., a new genus for a group of diatoms (Bacillariophyta) formerly within the genus Diadesmis: species from Hawai’i, including one new species.  Diatom Research 29: 351-360.

Castle Eden Dene in November

Castle_Eden_Burn_Nov19

For the first time this year, I heard Castle Eden Burn before I saw it.  Walking down from the car park, the distant roar of water was apparent almost as soon as the canopy of largely leafless branches closed over me.  A few trees still held their leaves – spectacularly golden on beech and birch, in particular, and the Dene’s famous yews were still green, of course – but the forest was dressed for winter now, much as it was on my first visit this year, back in January (see “Castle Eden Dene in January”).  Then, I was surprised that there was no water in the Burn.  On this trip, however, I wore my chest waders.  Back in August, I had compared Castle Eden Burn to a wadi (see “The presence of absence in Castle Eden Dene”) so the heavy rain of the previous few weeks had led me to suspect that today would be different.

The water surging through the Dene was very turbid, so collecting stones to examine involved feeling around on the river bed with my hand until I located one that was not sufficiently bedded into the substratum to remove.   That’s not ideal, but needs must and I got the five cobbles I needed, each with a distinct biofilm, slimy to the touch.  This is the first time, after eleven months, that Castle Eden Burn’s substratum has looked and felt remotely like the substratum from most of the other rivers I know in this part of the world.

Under the microscope, I see lots of particulate matter but also plenty of algae.   Apart from a few filaments of the cyanobacterium Phormidium, these were mostly diatoms.   The green algae I described in “When the going gets tough …” back in May were not obvious.  The diatoms were mostly largely motile cells of Navicula, with a few sigmoid cells of Nitzschia clausii and some smaller cells whose identity I will need to confirm once I have cleaned the sample and prepared a permanent slide.  The Navicula species, in particular, are typical inhabitants of local rivers during winter and early spring, all tolerant to a wide range of conditions.   I suspect that the rainfall has washed a lot of fine particulate debris from the industrial estates in the upper catchment into the river, and these diatoms will have the resilience to cope with such types of pollution.  A large storm sewer overflow also empties into the burn about a kilometre upstream of where I was standing and this, I suspect, has been flowing over the past month or two.

I also saw a few cells of Achnanthidium minutissimum, which I generally associate with cleaner conditions.  I suspect, however, that numbers will be relatively low compared to its more pollution-tolerant brethren.   Again, I can give a more authoritative answer once I have cleaned the sample and performed a full analysis.

CEB_diatoms_Nov19

Diatoms from Castle Eden Burn, November 2019.  a., b.: Navicula trpunctata; c. – e.: Navicula lanceolata; f., g.: Rhoicosphenia abbreviata; h., i.: Nitzschia clausii; j., k.: Navicula gregaria; l. Achnanthidium minutissimum.   Scale bar: 10 micrometres (= 1/100thof a millimetre).   The photograph at the top of the post shows Castle Eden Burn just downstream from the point I sampled.

I originally set out to visit Castle Eden Burn six times during 2019 and this was the last of those. I’ve written about most of these visits already but not about my September visit.  There was, on that occasion, little new information to justify a separate post but I will include the sample I collected in my final overview of the algae of Castle Eden Burn, just as soon as I get this final sample cleaned and analysed.   Before then, I have one more post to write about the diatoms, based on some more detailed observations of a few of the species, and then it will be time to think about where to focus my observations during 2020.

Messy bedrooms …

Sand_Loch_May19

When I was tramping around the Shetland Islands earlier this year (see “Hyperepiphytes in the Shetland Islands“), looking at the algae that live in the freshwater lochs, I noticed some meandering hieroglyphs made from fine sediment on the tops of some of the stones in the littoral zone.   I see these occasionally at other places too, and know that they are the “galleries” of caseless caddis flies.  Caddis flies are close relatives of the butterflies and are best known because many of their larvae use “found materials” (in contemporary art jargon) to construct cases to protect themselves.  Some species use fine gravel, silt and sand, some use fragments of plants, some have cases that are very neat, some have a more haphazard approach to construction.  However, a few families of caddis flies eschew cases and, instead, build these galleries.

Many caddis fly larvae, whether cased or not, are grazers, scraping the algae off the rocks on the bed of the stream or lake.   There is evidence that the cases offer some protection against predators such as trout which, by increasing survival rate, means that it is worthwhile for the caddis larvae to divert some of their hard-earned energy into building these.   Presumably, their caseless cousins gain the same advantage to building their galleries but recent research has suggested that these galleries offer a further benefit.

Think of caddis larvae as adolescent caddis flies.  Now imagine that the caddis gallery is the equivalent of an adolescent’s bedroom.   Horribly messy, in other words.   Let’s leave that image of a teenager behind (as most human teenagers know their way to the bathroom) and consider what happens to all that waste material that emerges from the far end of a caddis larva’s digestive system.   This nutrient-rich “ manure” encourages algae, meaning that our caseless caddis flies are, in fact, gardeners and are able to tap into this extra energy resource within their galleries in order to grow.   That brings us back to the analogy with teenagers, as these also frequently graze in their bedrooms (the diatom Campylodiscus is even the same shape as a Pringle, whose empty containers litter the bedroom floor of my own progeny).   I guess it is a good thing that caddis larvae don’t wear socks as, with six legs and two prolegs, the mess inside the gallery would be indescribable.

Psychomiiddae_Sand_Loch_May19

Galleries of caseless caddis flies (possibly Psychomiidae) on the top surface of a cobble from Sand Loch, Shetland Islands with (right) a close-up of a single gallery. The photograph at the top of the post shows Sand Loch in May 2019.

A recent study in the Lake District has shown that this “gardening” means that the algae which grow in the fine sediment from which the galleries are constructed are different to those found elsewhere on the rock surface, with a greater proportion of diatoms, which are considered to be more palatable to invertebrates than other types of algae.  Some caddis flies are thought to go even further, and can selectively remove and discard the algae that are least palatable (some Cyanobacteira, for example).

It is possible that up to 40% of the larva’s energy needs are met from the gallery itself.   The tube is, in fact, not a static construction: the larva pokes its head out in order to graze the algae immediately in front of the gallery, and extends the gallery as the food supply within easy (and safe) reach is exhausted.   At the same time, it is consuming the alga-rich rear part of the gallery (reminiscent of Hansel and Gretel eating the gingerbread house?).   A gallery only has a life-span of 10 days in the laboratory; whether this is the same under field conditions is not clear but that gives us some idea of the transience of these structures.   This rapid turnover means that the caddis larva is always feeding on succulent early-succession species, rather than the tougher and less digestible algae that might appear in more mature biofilms.

I also see similar galleries on the bed of the River Ehen from time to time but have been told that these are formed by non-biting midge (chironomid) larvae, rather than by caddis.  I presume that the same processes are happening in these although I have not been able to find much written in the literature.

Organisms that can significantly alter the habitat in which they live, and affect the conditions experienced by other species in the habitat are termed “ecosystem engineers”.  Beavers are good examples, as their dams can have significant effects on organisms extending for hectares.  Yet, in their own small way, caseless caddis larvae are also ecosystem engineers.  As are adolescent boys.   Which makes me wonder, having only talked until now about the algae in their galleries, whether caseless caddis larvae also have patches of mould extending up their walls.

Chironomid_galleries_Ehen_March19

Galleries made by chironomid larvae on a boulder in the River Ehen, March 2019.

References

Hart, D. D. (1985). Grazing insects mediate algal interactions in a stream benthic community. Oikos 44: 40-46. https://doi.org/10.2307/3544041

Johansson, A. (1991). Caddis larvae cases (Trichoptera, Limnephilidae) as anti-predatory devices against brown trout and sculpin. Hydrobiologia 211: 185-194. https://doi.org/10.1007/BF00008534

Ings, N. L., Hildrew, A. G., & Grey, J. (2010). Gardening by the psychomyiid caddisfly Tinodes waeneri: Evidence from stable isotopes. Oecologia 163: 127-139. https://doi.org/10.1007/s00442-009-1558-8

Ings, N. L., Grey, J., King, L., McGowan, S., & Hildrew, A. G. (2017). Modification of littoral algal assemblages by gardening caddisfly larvae. Freshwater Biology 62: 507-518. https://doi.org/10.1111/fwb.12881

Otto, C., & Johansson, A. (1995). Why do some caddis larvae in running waters construct heavy, bulky cases? Animal Behaviour 49: 473-478. https://doi.org/10.1006/anbe.1995.0061

Spheres of influence

Back to Moss Dub for this post because Chris Carter has sent me some stunning images of the filamentous desmid Desmidium grevillei that I talked about in my earlier post.   I mentioned that it is surrounded by a mucilaginous sheath, which was just apparent in my brightfield image.   Chris has added Indian ink to the wet mount.  The ink forms a dense suspension in the water but is repelled by the mucilage around the desmid cells, resulting in a much better impression of the extent of the sheath around the cell than is otherwise possible.

Desmidium-grevillei_CCarter_#1_Sept19

Desmidium grevillei from Moss Dub, photographed by Chris Carter using Indian ink to highlight the mucilage sheath around the cells. 

Indian ink is a negative stain, which means that it is the background, rather than the specimen itself, which takes up the colour.   This, in turn, alters the passage of light through the sample and appears to improve the contrast of the final image.   Chris’ images of the apical view show this well, and also illustrates the complicated three-dimensional arrangement of the chloroplasts within each semi-cell.   His photographs also show the pores through which the mucilage is secreted.

The curious thing about this negative stain is that, whilst it appears to emphasis a halo of nothingness around the Desmidium filament, it is actually drawing our attention to something important.   In his presidential address to the British Phycological Society in 1981 A.D. Boney referred to mucilage as “the ubiquitous algal attribute” and goes on to list the many functions that the slimes produced by a wide range of algal groups may perform.  Not all will apply to our Desmidium but Boney does use desmids as examples of some of the roles slime may play: it can be, for example, a buoyancy aid, keeping the desmids in the well-lit regions of a lake or pond and it can protect cells against desiccation if a pond or lake dries out.  It may also play a role in helping desmids adhere to their substrates and there is also evidence that mucilage layers may help to protect algae from toxins.

Desmidium-grevillei_apical_view_CCarter_Sept19

Apical view (at four different focal planes) of Desmidium grevillei from Moss Dub, photographed by Chris Carter, September 2019.

But that’s only part of the story.   There is two-way traffic across the membranes of algal cells, with essential nutrients moving into the cell but, in some cases, enzymes moving in the opposite direction.  If nutrients are in short supply then these enzymes can help the cell by breaking down organic molecules in order to release nutrients that can then be absorbed. Those enzymes take energy to manufacture, and the sheath of gunk around the filament means that there is a lower chance of them diffusing away before doing their job (see “Life in the colonies …”).   The same principle applies to sexual reproduction too, with mucilage serving, in some cases, as “sperm traps” or simply as the phycological equivalent of KY Jelly.

It is not just the algae that benefit from this mucilage: the outer layers, especially, can be colonised by bacteria which will also be hoovering up any spare organic molecules for their own benefit with, no doubt, some collateral benefits for the organisms around them.  The connection is probably too tenuous to count as a symbiosis with the desmids but we could think in terms of mutual benefits.

So that “nothing” really is a “something”, and that is before we consider the role of these extracellular compounds in the wider ecosystem.  I mentioned the role of similar compounds in consolidating the fine sediments on coastal mudflats in “In the shadow of the Venerable Bede” to give a flavour of this.   The least prepossessing aspect of the least prepossessing plants can, given time, change landscapes.  That should give us all pause for thought.

Desmidium-grev_apical_pore_CCarater

Close-up of Desmidium grevillei filament with focus on the left-hand cell adjusted to show the apical pores.   Photographed by Chris Carter from material from Moss Dub collected in September 2019.

Reference

Boney, A.D. (1981). Mucilage: the ubiquitous algal attribute.  British Phycological Journal 16: 115-132.

Domozych, D. S., & Domozych, C. R. (2008). Desmids and biofilms of freshwater wetlands: Development and microarchitecture. Microbial Ecology https://doi.org/10.1007/s00248-007-9253-y

Sorentino, C. (1985). Copper resistance in Hormidium fluitans (Gay) Heering (Ulotrichaceae, Chlorophyceae). Phycologia 24: 366-388. https://doi.org/10.2216/i0031-8884-24-3-366.1

 

The little tarn of horrors …

In addition to desmids, we found several other algae in the samples collected from Cogra Moss.  One of these consisted of colonies of cells in mucilaginous masses attached to floating mats of vegetation (which looked like terrestrial grasses).  We decided that these were probably Chrysocapsa epiphytica, the second representative of the Chrysophyta I’ve described in this blog this year (see also “Fade to grey …”).  As is the case for Chromulina, much of what we know about Chrysocapsa epiphytica is down to the patient work of John Lund who first described this species back in 1949.

Chrysocapsa_epiphytica

Colonies of Chrysocapsa epiphytica growing on submerged vegetation at Cogra Moss, Cumbria, September 2019.  Cells are 7.5 – 15 micrometres long and 7.5 – 12 micrometres wide. 

He described the various mucilaginous lobes as “reminiscent of the …. human brain”.  The spherical, oval or ovoid cells form a layer, two to four cells deep, at the surface of the colony.   The cells have the typical yellow-brown colour of chrysophytes and, though it is hard to see the chloroplasts in this photograph, John Lund says that there are usually two, sometimes four, in mature cells.

Its presence in a soft-water lake probably means that it is a species that relies on dissolved carbon dioxide rather than bicarbonate as its raw material for phytosynthesis (see “Concentrating on carbon …” for some background on this).   We know, from laboratory studies, that most chrysophytes rely exclusively on carbon dioxide, and lack the capacity to use bicarbonate.  This confines them to water where the pH is low enough to ensure a supply of carbon dioxide (the chemistry behind this is explained in “Buffers for duffers”. It may also explain why Chromulina lives in surface films rather than submerged in the pond (the locations where we’ve it found are unlikely to have sufficiently low pH).

One extra twist to the story is that many chrysophytes are “mixotrophic”, meaning that they can switch between using photosynthesis as a means of getting the carbon they need to grow from inorganic sources, and “feeding” on other organisms.  Our Chrysocapsa epiphytica, in other words,  has parked itself beside a convenient supermarket of pre-packaged carbon in the form of decaying vegetation and associated bacteria which it then ingests by a process known as “phagotrophy”.

Phagotrophy is, in fact, a very ancient characteristic, insofar as the very first eukaryotic cells were the result of Cyanobacteria-type cells being ingested by larger heterotrophic cells and being retained as on-board “energy farms” rather than digested and treated as one-off vegetarian dinners.   However, the shift to a permanent role for chloroplasts within a eukaryotic cell involved a lot of rewiring of intercellular machinery, and effectively “switching off” the intercellular mechanisms involved in phagotrophy.   Retaining the ability to “feed” on bacteria alongside a capacity for photosynthesis is the cellular equivalent of a hybrid car: there is a lot more to cram under the bonnet.  Flexibility, in other words, comes at a cost.

On the other hand, phagotrophy does not just result in extra carbon for the Chrysocapsa cells in Cogra Moss.   In an oligotrophic tarn such as this, the extra nutrients that are obtained when the bacteria are absorbed will also be a useful boost.   Once again, though, you can see that, in environments where nutrients are more plentiful, the cost to the cell of maintaining the equipment required for phagotrophy outweighs the benefits.

I’m sure that a close inspection of the land around Cogra Moss would have revealed insectivorous plants such as Drosera(sundew) and we also recorded Utricularia minor, an aquatic insectivorous plant, in another tarn we visited whilst desmid-hunting (see “Lessons from School Knott Tarn”).  Chrysocapsa is, in many senses, a microscopic equivalent of these carnivorous plants.   OK, so it has a taste for bacteria rather than flesh but, somewhere out there, there must be a sub-editor in search of a headline …

References

Lund, J.W.G. (1949). New or rare British Chrysophyceae. 1.  New Phytologist48: 453-460.

Maberly, S. C., Ball, L. A., Raven, J. A., & Sültemeyer, D. (2009). Inorganic carbon acquisition by chrysophytes. Journal of Phycology 45: 1052-1061. https://doi.org/10.1111/j.1529-8817.2009.00734.x

Raven, J. A. (1997). Phagotrophy in phototrophs. Limnology and Oceanography 42: 198-205. https://doi.org/10.4319/lo.1997.42.1.0198

Saxby-Rouen, K. J., Leadbeater, B. S. C., & Reynolds, C. S. (1997). The growth response of Synura petersenii(Synurophyceae) to photon flux density, temperature, and pH. Phycologia 26: 233-243. https://doi.org/10.2216/i0031-8884-36-3-233.1

Saxby-Rouen, K. J., Leadbeater, B. S. C., & Reynolds, C. S. (1998). The relationship between the growth of Synura petersenii (Synurophyceae) and components of the dissolved inorganic carbon system. Phycologia 37: 467-477.  https://doi.org/10.2216/i0031-8884-37-6-467.1

Terrado, R., Pasulka, A. L., Lie, A. A. Y., Orphan, V. J., Heidelberg, K. B., & Caron, D. A. (2017). Autotrophic and heterotrophic acquisition of carbon and nitrogen by a mixotrophic chrysophyte established through stable isotope analysis. ISME Journal. https://doi.org/10.1038/ismej.2017.68