Bollihope Bhavacakra*

Bollihope_ulothrix_160528

My explorations of the biology of Ulothrix zonata have taken me from Bollihope Burn in Weardale (see “Bollihope Burn in close-up”) to upper Teesdale (see “The intricate ecology of green slime”) and one of the outcomes is this representation based on the diatom-smothered filaments that I observed in Bollihope Burn, close to the sink hole.   The picture illustrates the suggestion that I made in the post about Bollihope Burn – that the switch from “vegetative” to “reproductive” mode leads to less energy being available for the alga to manufacture the slime that it needs to stop epiphytes gaining a foothold.   By intercepting the limited light that penetrates into the water, these algae can shade the host plant to such an extent that it cannot gain the energy it needs to grow.   The mucilage is the equivalent of the “anti-fouling paint” that mariners use to stop barnacles encrusting their hulls.

My image shows a single healthy filament of Ulothrix zonata at the bottom right of the image and, on the left, two filaments of cells that are producing flagellated gametes that will eventually be released.  I write “gametes” with mild trepidation, as they may also be nascent zoospores associated with the asexual phase (see below).   A third filament, in the background, is composed mostly of empty cells that have already released their gametes.   There are no “male” or “female” gametes; any two can combine to form a zygote, so long as they come from different filaments.   This zygote then attaches to the substratum and does little more over the summer.

In my image, the Ulothrix filaments have been colonised by needle-like cells of Fragilaria gracilis, Achnanthidium minutissimum cells on short stalks, and a couple of cells of Gomphonema pumilum.   There are also a couple of cells of Ulnaria ulna and some zig-zag colonies of Diatoma tenuis.   The effect of these cells on the appearance of the Ulothrix zonata is marked, smothering the filaments entirely so that, with the naked eye, the assemblage appears brown rather than green.

The diagram below summarises the life cycle of Ulothrix zonata and emphasises the point that the green filaments that most people associate with this alga are only a small part of the story.  The cell contents divide in one of two ways.  The first produces zoospores, each with four flagellae, which are released, settle and grow directly into a new vegetative filament.  The second, however, produces a number of cells which are smaller but otherwise look similar to the zoospores except that each has two rather than four flagellae.  These gametes then fuse with gametes produced by another filament to produce a “zygote” which, in turn, germinates to produce several (typically eight) zoospores, each with four flagellae, from which new vegetative filaments grow (see illustration of putative “germlings” in “The intricate ecology of green slime”).

Ulothrix_zonata_lifecycle

The life-cycle of Ulothrix zonata, following Lokhorst and Vroman (1974).   “2n” refers to diploid stages; “n” refers to haploid phases (note that the vegetative filament is also haploid).

The asexual phase can be produced at any time, but is stimulated by high temperatures; the sexual phase, however, is more strictly regulated.   The formation of gametes only occurs under “long day” conditions, which means that it will happen as daylight hours extend in the spring.   By contrast, the division of the zygote requires short day conditions and low temperature, meaning that the zygote is relatively inactive over the summer months, only dividing to produce zoospores, and ultimately, new filaments, in late autumn and winter.   This creates a useful niche for the organism during a period of the year when nutrients are relatively plentiful in upland rivers (as they are washed off the land following rainfall) and grazers are relatively inactive.   It also means that this apparently simple green filament actually has some sophisticated controls that regulates how and when it divides.

I’ve talked about algal life cycles in the past, commenting that the concepts behind these are not always easy to grasp (see “Reflections from the trailing edge of science …”).   The problem is that undergraduates of my generation were taught this as part of a broader overview of plant evolution and the variations between patterns in different groups tended to befuddle rather than enlighten students already struggling to grasp the big picture.   The interesting twist to my explorations of Ulothrix zonata is that it has shown how the idiosyncrasies of an organism’s life-cycle can have a practical significance that helps the organism survive in a particular habitat.   Knowing about the life cycle can, in turn, inform our understanding of processes occurring within a stream or river.  The problem is that these topics have largely fallen off the agenda both for teaching and research, so we are generally limited to interpreting descriptions from old journals, and often forget completely the role that these factors may play in creating the mosaic of algae in a stream.

Reference

Lokhorst, G.M. & Vroman, M. (1974).  Taxonomic studies on the genus Ulothrix (Ulotrichales, Chlorophyceae) III.  Acta Botanica Neerlandica 23: 561-602.

* “Bhavacakra” is a symbolic representation of the cyclical nature of existence used in Tibetan Buddhism.  The title of this post is also an affectionate tribute to Brian Moss, who died a few days ago.

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Bollihope Burn in close-up

Bollihope Burn does not disappear dramatically down a single swallow hole in the way that Gaping Gill swallows up Fell Beck on the slopes of Ingleborough.  Rather, there is a gradual diminishment of flow, as the river percolates through the joints in the limestone, before the remnants of the stream swirl down a final sinkhole (see “Co. Durham’s secret Karst landscape”).   I was intrigued to see how the organisms that inhabited Bollihope Burn reacted to these stresses so got down on my knees close to this final sinkhole to get a closer look.

My waterproof Olympus TG2 (see “Getting close to pearl mussels with my underwater camera”) set to super-macro mode is equivalent to putting my head under the surface of the water and then peering at the rock through a magnifying glass … but gets fewer odd looks from passers-by.   Fortunately, this is an isolated corner of Weardale and passers-by were limited to a few rabbits, because sticking a camera into a stream to take a photograph of a stone is, itself, odd enough to attract stares from most people.

These close-up views of freshwater algae in their natural habitat continue to surprise me.  It is only in the last few years that waterproof digital cameras with macro facilities have fallen to an affordable price.  Before this, underwater photography required special kit that few freshwater biologists could afford.  Yet, removing a stone to photograph the algal growths meant that the algae were never photographed in their natural habitat, and were deprived of the buoyancy that the water afforded them.   I have plenty of photographs of green or brown gunk composed of different algae but, with the algae removed from their context, these photographs offer few insights into the biology of the stream bed.  The photograph below, however, shows a community with a distinct structure – a “turf” of near-vertical filaments waving in the gentle eddies of the stream as it swirls around before disappearing down the swallow hole.

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A cobble in Bollihope Burn, close to the swallow hole, covered by a short “turf” of algae, April 2016.   Scale bar: approximately two centimetres.

Under the microscope, the structure of this “turf” starts to reveal itself.   The filaments appear to be aggregations of diatoms around dying filaments of the green alga Ulothrix zonata.   This is an alga that is common in Pennine streams in the winter and early Spring but which disappears as the weather starts to warm up. It often forms very conspicuous green patches on the river bed for a short period of time, as in the following picture, which I took a few kilometres away from my current location, in the River Wear at Wolsingham.   The difference in appearance between the alga in the two photographs is mostly due to the Bollihope population being smothered with diatoms whilst the Wolsingham population was virtually a pure growth of Ulothrix.   This may be partly due to the Bollihope picture being taken taken two months later than the Wolsingham image.   Ulothrix zonata produces copious quantities of mucilage and the Wolsingham population was slimy to the touch.  I rarely see epiphytes on this or any other slime-producing algae in their healthy state.   However, Ulothrix is a species that thrives in cold water.   Indeed, a study has shown that when the water starts to warm up and the day length increases, the Ulothrix filaments switch into their dispersal and reproductive modes and that is what may be happening here.   As the rate of photosynthesis declines, so there is less carbohydrate from which the slime molecules can be made and, as a result, less of a deterrence to any diatom looking for a perch.   From now until next winter, Ulothrix zonata will not be very obvious in the streams that I visit.  This is because the zygotes which are produced by sexual reproduction lie dormant until day length decreases and temperature drops.   At this point, they germinate and divide to produce zoospores which, in turn, grow into new Ulothrix zonata filaments.

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Growths of Ulothrix zonata on cobbles in the River Wear at Wolsingham, February 2009. 

The photographs taken under the microscope illustrate this well.  On the left hand side there is one of the few healthy looking Ulothrix filaments that I found, with a chloroplast wrapped around the inside of the cell wall   On the right hand side you can see that the chloroplasts have gone, replaced by dark green blobs which are (I think) bundles of gametes awaiting release.   More significantly, you can also see several diatoms around the Ulothrix filament, taking advantage of it to lift themselves up above the rock surface.

The paradox is that these algae are entering their senescent phase just as most of the plant life in Weardale is flourishing.   This is probably not a coincidence: life in cold water means fewer grazing invertebrates and less shade to intercept the precious winter sunlight.   I suspect that algae, once masters of the planet, have gradually adapted and evolved to live a subordinate life, flourishing in those periods of the year when most of us are content to stay indoors.

Ulothriz_zonata_Bollihope_B

Ulothrix zonata from Bollihope Burn, April 2016.  The left hand image shows a healthy vegetative filament; the right hand image shows zoospore production and colonisation by diatom epiphytes. 

References

Graham, J.M., Graham, L.E. & Kranzfelder, J.A. (1985).  Light, temperature and photoperiod as factors controlling reproduction in Ulothrix zonata (Ulvophyceae).  Journal of Phycology 21: 235-239.

van den Hoek, C., Mann, D.G. & Jahns, H.M. (1995).  Algae: an Introduction to Phycology.  Cambridge University Press, Cambridge.

Bollihope Common

I spent part of last weekend wandering in the vicinity of a small reservoir on Bollihope Common in Weardale.   It is one of many small manmade water bodies in this part of the northern Pennines constructed to power the mills that served the lead mines in the region.

Rocks on the northern shore of the reservoir had tufts of a dark green, almost black, moss inhabiting the splash zone.   Under the microscope, I saw the characteristic wavy-edged cells which indicated that this was a Racomitrium.   This is Racomitrium aciculare, a semi-aquatic cousin of the species we encountered on rocks in Teesdale last year (see “Upper Teesdale in March”).   The southern shore of the lake, by contrast, was not fringed with rocks, but with rushes and Sphagnum moss, along with some Polytrichum.   This side of the reservoir receives the drainage from the fells above and, I suspect, the constant supply of sediment has led to the gradual infilling of the original shoreline.   There were at least a couple of species of Sphagnum present here, but I was most interested in the submerged moss, S. cuspidatum.

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Looking north towards the unnamed reservoir on Bollihope Common (NY 989 348).   The road on the left hand side of the image leads to Stanhope.

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Aquatic mosses from the unnamed reservoir on Bollihope Common.  The left hand image shows Racomitrium aciculare on the tops of boulders and the right hand image shows Sphagnum cuspidatum from the boggy areas on the southern shore.

I shook portions of both mosses vigorously in a small amount of water from the reservoir to dislodge the attached algae.   The clear water quickly turned brown and I sucked up a few drops of each with a pipette and dropped them onto a microscope slides.  First up was the sample from the Racomitrum.  This was dominated by the small diatom Achnanthidium minutissimum (a – e in the figure below).  When I had looked at the Racomitrium leaves under the microscope, I had seen many of these attached to the leaves by short stalks.   These comprised just over half of all the diatom cells that I counted.  Long needle-like cells of Fragilaria rumpens (or something similar) which attached to the leaf by their base formed another 27% and another genus, Gomphonema (one or more forms in the G. parvulum complex), formed about 16%.  Most interesting to me were a few gracefully-curved cells of Hannaea arcus, as these are good indicators of a relatively pristine habitat.

Next up was the sample I had obtained from the Sphagnum.   Sphagnum usually favours acid habitats so I was intrigued to see what diatoms would be associated with it, having seen that the diatoms associated with Racomitrium, a hundred metres or so away, mostly suggested neutral or slightly alkaline conditions.

Once again, it was Achnanthidium, Fragilaria and Gomphonema that comprised the majority of the diatom cells (54, 19 and 16% respectively) but this time, about 8% of the total belonged to at least three species of a different genus, Eunotia, which is often associated with acid habitats, and the curved cells of Hannaea were conspicuous by their absence.   Interestingly, Sphagnum does not only favour acid conditions, peculiar features of its cell wall chemistry also helps to create those acid conditions and the diatoms living in the microhabitats around the submerged Sphagnum were clearly indicating a slight change in conditions, compared to those I found on the Racomitrium.

Bollihope_diatoms

Diatoms growing on and around mosses in the unnamed reservoir at Bollihope Common; a – e: Achnanthidium minutissimum complex; f,g: Gomphonema parvulum complex; h. Eunotia spp (probably E. implicata); i. Navicula (probably N. cryptocephala); j. Fragilaria (probably F. gracilis); k. Hannaea arcus.  Scale bar: 10 micrometres (1/100th of a millimetre).   Note, particularly for h and k, healthier specimens were present in the samples but none presented in a manner amenable to photography.

There was much more Sphagnum underfoot as I walked over Bollihope Common.  Given time – a couple more centuries, maybe – and the gradual invasion of Sphagnum from the moorland around the reservoir might continue and, we can hypothesise, the acid-loving diatom species might become more abundant.  Indeed, we could even argue that this would simply be nature re-establishing its influence, the reservoir being an unnatural and – in the grand scheme of things – temporary intrusion into the landscape.