Springtime surprises …

My last few trips to the Lake District have been plagued by indifferent, if not inclement, weather.  High flows are the ultimate curse of anyone working on rivers, and recent trips have all been uncertain until almost the last moment as I watched the fluctuations of weather forecasts and hydrographs.  Even once we had arrived, clouds were low and we never seemed to be out on one of those crisp winter days that offers views of distant, snow-capped peaks.   Finally, last week, the sun was able to break through the clouds, at least occasionally, daffodils, primroses and cowslips were in flower and the woodlands were heady with the scent of wild garlic.   

Life under water, however, follows a different trajectory to life on land.   At this time of year, stream beds in West Cumbria tend to look less, not more, verdant.   The algae that are so prolific during the winter were still there, but nowhere near as prolific now.   That was the case at several of the sites we examined but one – the River Cocker just below Crummock Water – bucked this trend in quite a dramatic way.  Peering through my bathyscope, I saw bright pink-red growths, particularly on fronds of the moss Fontinalis antipyretica.   These turned out to be filaments of the red alga Audouinella hermainii, which also smothered many of the stones.

Audouinella hermainii epiphytic on the moss Fontinalis antipyretica in the River Cocker, just downstream from Crummock Water, April 2014.  The photo at the top of the post shows the site where this photograph was taken.

The growths on the stones looked different to those on the mosses, with longer filaments and a brownish, rather than red, colour.  The colour difference may simply be due to the balance between reflected and transmitted light in the two locations; however, the difference in growth form between the two habitats is harder to explain.  In the River Ehen the same alga (so far as I can tell) has the habit shown in the top photo, but here growing on rocks rather than on mosses (see “Not so bleak midwinter?”)

The other complication is that, in the River Ehen, Audouinella hermainii is extremely abundant in the winter and early spring but is not visible between about May and August, after which it starts to become obvious again.   The growths I saw last week were not the first records from this site, but they are both the most abundant records and the only time it has been so prolific this late in spring.   I also found one record from the River Crake, just below Coniston Water, where A. hermainii was prolific in June.  What’s more, neither the Freshwater Algal Flora of the British Isles nor West and Fritsch’s Treatise on the British Freshwater Algaemakes reference to this species having a particular predilection for winter and spring.   The former says it is “… most common as an epiphyte on … bryophytes” whilst the latter says “… usually attached to rocks and stones in rapid rivers”.   Both agree, however, that it is more likely to be encountered in streams and rivers than in lakes.  It is the Ehen that seems to be the outlier, but it is also the river where I find it most often, hence my inference about its seasonality.   

Audouinella hermainii on stones in the same stretch of the River Cocker as the epiphytic growths in the previous photograph.   

Another reason for treading cautiously is that the red algae present us with some particular challenges when it comes to identification (see “Something else we forgot to remember” and “Reflections from the trailing edge of science”).   Although the view through a microscope shows similarities amongst these populations, these differences in habit and seasonality make me question whether I am looking at the same organism across all these locations. 

I’m conscious that my understanding of this species is drawn from records from a limited geographical area.  On the other hand, the “big picture” for other people may encompass different sites to mine but, I suspect, will include fewer records from the depths of winter.   Then again, mid-winter and early spring in rivers flowing out of lakes will have quite different thermal and hydrological characteristics to the same seasons in unregulated streams flowing off the Alps, for example.   Is anyone’s “big picture” ever big enough to make generalisations?

Vegetative filaments of the red alga Audouinella hermainii from the River Cocker, just downstream from Crummock Water.   Scale bar: 20 micrometres (= 1/50^th of a millimetre).  

There are certain other algae that I also associate with late winter and early spring (Ulothrix zonata, Draparnaldia glomerata, for example).  However, most of these turned out to show similar patterns to Audouinella hermainii when I collated my data, with just enough outliers to confound my expectations.  The likelihood is that these plants do not have circannual rhythms hard-wired into their physiology, but are opportunistic, reacting to circumstances.  Their optimal conditions may be more likely to occur at particular times of the year, but there are also exceptions, giving rise to my observations last week.   

That unpredictability is what keeps me wanting to head out into the field, even when the weather is not ideal.  It is also a reason to want to keep going back to the same sites, so that I can watch patterns unfold, and also a reason to want to visit different sites, so that I can fit my observations drawn from a limited area into a broader perspective.  Beware the ecologist who speaks with too much confidence.  The chances are that they are not spending enough time getting cold and wet in the field.   

Records of Audouinella hermainii from West Cumbrian rivers and streams, 2020 – 2022.  The y axis shows the cover of the alga using the 9-point scale adopted for macrophyte assessments in the UK.   Vertical lines indicate the twelve months of the year.  

Some other highlights from this week:

Wrote this whilst listening to:  Easter music: Stanier’s Crucifiction and Bach’s St Matthew’s Passion.

Currently reading:   Still Colm Tóibín’s The Magician.

Cultural highlight: The Raphael exhibition at the National Gallery.   

Culinary highlight: Grilled mackerel on Asian salad, prepped and made at the Cordon Bleu cookery school in London during a short course on knife skills.

Something else we forgot to remember …

The story of the mysterious red alga that I wrote about a couple of weeks ago (see “More than just an insignificant dot?”) has taken another intriguing turn.   Having decided that the alga was probably Audouinella pygmaea, I was shown a paper from 2011 by Orlando Necchi and Marianna Oliveira in which they consider the affinities of Audouinella species and came to the conclusion that Audouinella pygmaea only really exists in the imaginations of people who write identification guides. I’ve written before about the complicated life history of red algae (see “The schizophrenic life of red algae …”) and commented that it can be hard to differentiate between simple red algae such as Audouinella and stages in the life history of more complicated red algae.

Audouinella hermanii, the red alga that I was writing about in those earlier posts, does not present us with any serious problems, as it is possible to see all the reproductive structures, which enables us to distinguish between the (haploid) gametophyte filaments and the (diploid) sporophytes. However, reproductive organs have not been observed on populations of A. pygmaea, which presents us with some problems. Is this really an independent species of Audouinella or just a “chantransia” (gametophyte) stage of another red alga? Necchi and Oliveria took a number of populations of A. pygmaea and another species, A. macrospora (which has not been recorded from Britain or Ireland) and compared their genetic composition with other freshwater algae. What they found was that these chantransia stages were more closely related to known species from other red algal genera than they were to each other.   Their conclusion: “Audouinella pygmaea” does not exist in any meaningful sense. Rather, the populations we describe as A. pygmaea represent life history stages of other red algae. These life history stages are impossible to tell apart from one another using morphological criteria.   However, there is a good chance that a thorough search of the Anghidi Fawr stream upstream of where the sonde was placed will reveal another red alga – most likely Batrachospermum or Thorea – that was releasing the carpospores that produced the filaments that we named Audouinella pygmaea.

Curiously, this brings us back close to the situation almost 100 years ago as, reading my trusty old copy of West and Fritsch I read that the freshwater species we now call Audouinella were then placed in the genus Chantransia and that “C. pygmaea is probably a stage in the life-history of Batrachospermum moniliforme Roth.”   Another case, perhaps, of things we forgot to remember?

Reference

Neechi, O. Jr. & Oliveira, M.C. (2011). Phylogenetic affinities of “chantransia” stages in members of the Batrachospermales and Thoreales (Rhodophyta). Journal of Phycology 47: 680-686.

West, G.S. & Fritsch F.E. (1927). A Treatise on the British Freshwater Algae.   Cambridge University Press, Cambridge.

Reflections from the trailing edge of science

All this talk of algae life-cycles alternating between diploid and haploid stages takes me back to winter afternoons in undergraduate botany practical classes when the basics of plant life cycles were driven into us.   Roughly speaking, the principles of biology can be split into those that are common sense and those that need to be explained over and over again to overcome our natural preconceptions.   “Common sense”, in this instance, means that the principle in question roughly aligns to our own anthropogenic outlook.  And one thing that humans – along with all other animals – don’t have is alternating generations.

A step backwards: “diploid” means a cell with a full complement of chromosomes and “haploid” is a cell with half a set of chromosomes (see note).   In the human, the “haploid” phase is the short period of the life cycle between production of sperm and egg cells (collectively termed “gametes”) and the successful fertilisation of an egg by a sperm cell.   So the human life-cycle consists solely of the alteration between a multicellular diploid phase (that’s you) and a unicellular haploid phase.  In the case of all but the very simplest algae, there is a multicellular haploid phase (the “gametophyte”) which produces the gametes.  These then fuse to produce a multicellular diploid phase (the “sporophyte”), some cells of which undergo meiosis to produce haploid spores.  These spores germinate to form the next generation of gametophytes.

Got that?  Probably not.  It is not an easy concept to grasp partly because it does not accord with the human experience.  Moreover, in flowering plants, the sporophyte is dominant and the gametophyte stages are reduced to “parts” of the flower (the entire male gametophyte, for example, is contained within the pollen grain).   It does not help the cause that the most conspicuous group of plants have their alternation of generations largely hidden from view.   When I was an undergraduate, knowing about alternation of generations was regarded as necessary if we were to understand the evolution of plants.   Unfortunately, the experience of having plant life cycles drilled into them probably turned many undergraduates off botany forever.   I am fairly sure that few UK university departments teach these principles in anything like the detail that my generation had to endure.

Alternation of generations isn’t something that the average biologist needs to know in great detail and, to be honest, I forgot a lot of the details.  I had to refresh myself when I taught courses on algae and the lower plants to undergraduates in Nigeria and, once again, when I started boning up for the post about Audouinella.   As Bill Farnham pointed out, I may not have got all the details right.   No excuses for my own failings but this is yet another manifestation of a problem that I have mentioned before: that science has a “trailing edge” of knowledge as well as a “leading edge” (see “An inordinate fondness for … algae”).  There is an enormous amount of information on algal life cycles in the literature but it is not always easy to find, especially when accessing the literature via internet search engines.   We might not need the information very often but it is as easy to lose familiarity with the terminology as it is for an athlete to fall out of condition through lack of exercise.

Note: another way of looking at it is to say that the haploid phase has a full set of chromosomes whilst the diploid phase has two full sets.  I was being deliberately anthropocentric in describing the haploid phase in this way.  And, if we are going to be pedantic, every “multicellular diploid phase” necessarily starts out, albeit briefly, as a single celled diploid phase.

The schizophrenic life of red algae …

Back in October, I showed a photograph of red algae growing in the River Ehen, naming this as Audouinella (“At last .. a red alga that is really red ...”).  A friend commented in an email that I was brave to have made this identification if there were no spores or reproductive organs and that, in Germany, these filaments would simply be referred to as “chantransia stage”.   Although I had seen reproductive organs earlier in the year, I worried afterwards, that maybe I had been rash, and was mightily relieved when, a couple of months later, filaments with reproductive organs re-appeared.

What you can see in the picture below is the vegetative filaments from which short branches bearing carposporangia (female reproductive organs) arise.   There are over 300 species of Audouinella, mostly found on sea coasts with just a few freshwater representatives.   The life cycle seems to vary considerably from species to species so it is hard to generalise but, like many algae, there are two distinct phases, a diploid phase, following fertilisation of the carpospores by a male sexual cell, and a haploid phase, which occurs after these diploid cells have undergone meiosis.   In this image, you can see filaments in the haploid phase with bundles of carpogosporangia on short side branches.   In Audouinella, the diploid phase looks very similar but – and here’s the problem – they also look similar to the diploid phases of many other species of red algae.   Indeed, for a long time, these diploid phases were regarded as distinct species.   My 1927 flora, by West and Fritsch, for example, includes these filamentous stages as a distinct genus, Chantransia, and it was only later that people realised that they were one part of a more complicated life cycle.

Filaments of Audouinella hermanii from the River Ehen, January 2014, with the carposporangia indicated by arrows.   Scale bar: 10 micrometres (= 1/100^th of a millimetre).

At this particular site on the River Ehen I have also found another red alga, Lemanea (see “The River Ehen in April”).  Lemanea also has a chantransia stage, so it pays to be careful with my identifications.   Lemanea, in my experience, tends to be found in the fastest-flowing stretches of streams attached to stable boulders, whereas Audouinella is generally more widespread across the river bed.

At last … a red alga that really is red …

The bed of some parts of the River Ehen on my last visit had a distinctly pinkish-red hue, which is a sure sign that we are moving towards autumn and winter.   This is Audouinella hermanii, which we have already met in earlier posts.   Having written recently about a green alga that is actually red, and also described Lemanea, a red alga that is typically olive-green in colour, it was reassuring to finally encounter a red alga that is unequivocally red in colour.

A rock from the River Ehen, near Ennerdale Bridge, with a thick coating of Audouinella hermanii. Photographed in October 2013.

The red colour in Audouinella and other red algae is due to a pigment called phycoerythrin.  This is a protein-based pigment which is also found in blue-green algae.  By contrast, the carotenoids which gave Haematococcus its bright colour are lipid-based.     The astaxanthin of Haematococcus is, as we saw on 6 October, a natural sunscreen but phycoerythrin and many carotenoids have a different role inside the algae.

Phycoerythrin appears red to us because it is reflecting red light whilst at the same time absorbing other wavelengths.   Beccause blue light penetrates water to a greater depth than light of longer wavelengths, phycoerythrin allows red algae to absorb this and use the energy for photosynthesis.  We can think of the phycoerythrin (and, indeed, many carotenoids) as “turbochargers” for the photosynthetic apparatus, allowing the algae that contain them to live in a wider range of habitats.

This argument works in coastal areas, where red algae can live at great depths where relatively little light penetrates but why should Audouinella be so common in the River Ehen?    The same reasoning applies: the stretch of river where I found Audouinella was heavily shaded and this species is most common in autumn and winter when the sun’s rays are much weaker.  Again, the phycoerythrin gives the normal photosynthetic apparatus a boost to help it make the most of the light that is available.

Cells of Gomphonema truncatum growing within the Audouinella colonies in the River Ehen near Ennerdale Bridge, 9 October 2013.   The two left hand images are in “valve view” whilst those on the right are in “girdle view”.   Scale bar: 10 micrometres (= 100^th of a millimetre).

Whilst examining the Audouinella under my microscope, I noticed some clumps of diatom cells that looked like inverted Coke bottles.   These are a species known as Gomphonema truncatum which grows on long mucilaginous stalks which branch to form bush-like colonies.   Unlike Coke bottles, Gomphonema cells are not round, so the characteristic shape is only seen when peering down onto the flat surface of the cell.   When viewed from the side, the cell is wedge-shaped.  Diatomists refer to these two different views as “valve view” and “girdle view” respectively.   Note, too, the characteristic yellow-brown appearance of the chloroplasts.  This is due to the carotenoid fucoxanthin which, like Audouinella’s pigments, gives a boost to the photosynthetic machinery when natural light is in short supply.