A load of balls …

Lough_Cullin_BKennedy

This post is still mostly about the ecology of Lough Down, though it draws heavily upon photographs taken at Lough Cullin, in County Mayo, Ireland.   Lough Down shares some characteristics with Lough Cullin, but more with Lake Wobegon.   I suspect that the summers in Lough Down are not quite as long or as hot as those experienced around Lake Wobegon but, also, that a walker passing around the edge of Lake Wobegon would not see the round balls of algae that are a common sight along the shoreline of Lough Down.   Maybe I’m wrong: if anyone in Minnesota knows differently, please do let me know.

From a distance, these look like an unsightly mass of algae cast up on the foreshore; it is only when you get close that you see that this mass is, in fact, composed of a large number of discrete spherical growths.   You can see, in the photograph below, where Bryan Kennedy, my erstwhile Lough Down correspondent, has built a few of these into an Andy Goldsworthy-esque sculpture.   These are “Cladophora balls”, a phenomenon encountered in lakes around the northern hemisphere.  In Japan, they’ve even made their way onto postage stamps.

Aegagropila_Lough_Cullin

Aegagropila linnaei washed up on the shore of Lough Cullin, Co. Mayo, Ireland.  The photograph at the top of the post also shows Lough Cullin (photographs: Bryan Kennedy).

Until relatively recently, as their name suggests, the alga from which these balls are formed, belonged to the genus Cladophora, a frequent subject on this blog (see “The pros and cons of cell walls” for a recent example).   Like Cladophora, these are branched filaments composed of relatively large, multinucleate cells with a reticulate chloroplast.  This was, however, recognised as a different species to Cladophora glomerata, the common species of enriched lowland rivers: Cladophora aegagropila.  However, recent molecular studies have shown that it is not so closely related to Cladophora glomerata as its outward appearance suggests, leading to the resurrection of a very old name, Aegagropila linnaei.

In rivers, Aegagropila linnaei forms carpet-like growths of short filaments, not growing into the long wefts that we associate with Cladophora glomerata.  However, C. glomerata can sometimes be profusely branched as well, so telling these two species apart both in the field and under the microscope can be tricky.   One of the most useful characteristics is that the branches of Aegagropila are sub-terminal, meaning that they arise just below the end of the parent cell, rather than at the end, as is the case in Cladophora (see diagram below).   It is strange that two such similar species in appearance are, in fact, not particularly closely-related.  This is, however, an important distinction asA. linnaei prefers, as far as we can tell, less enriched conditions than C. glomerata.

Aegagropila

Left: a section through a ‘Cladophora’ ball from Lough Cullin and, right, profusely-branched filaments of Aegagropila linnaei.  Photographs: Bryan Kennedy.

Why does it form these distinctive spherical growths in lakes?   I have not managed to find a paper that gives an authoritative explanation so here are a few possibilities, none mutually exclusive.  First, filamentous algae that display apical growth and copious branching tend to form hemispherical growths if attached and spherical ones if not.  We’ve seen that for Cyanobacteria such as Rivularia (see “More about Rivularia”) and Gloeotrichia (see “Rewriting history at Talkin Tarn”).  Second, the constant ebb and flow in the lake littoral zone will create a physical stress on attached carpets of Aegagropila leading, eventually, to parts becoming detached.  Third, the profuse branching that is characteristic of Aegagropila will mean that adjacent filaments will become entangled around another, creating a Velcro-type effect.   Finally, the apices of the filaments will continue to grow towards the light, meaning that the free-floating balls gradually expand in size.

Aegagropila’s dislike of nutrient-rich conditions mean that the number of places where it is found has been decreasing over recent decades.   It was, for example, recorded from several locations in the Netherlands in the past but not since 1967.  There are records from in the UK, but mostly from the more remote regions.   There are also a number of records from loughs in Ireland, as is the case here  The river form is, in my opinion, hard to differentiate unequivocally from Cladophora glomerata without very careful examination and this raises the spectre of “identification by association”, particularly when it is recorded by macrophyte surveyors who often do not have time to check material under the microscope.   Christian Boedeker, who has done much of the recent work on Aegagropila, thinks that a limited dispersal capability will mean that it will be slow to re-colonise habitats once it has been lost.

So that’s another day over here at Lough Down, a quiet lake that no-one has visited but everyone has got to know very well.   It’s one of those places, I like to think, where naturalists notice all of nature, not just the pretty, cuddly and exciting things.  Everyone leaves a little wiser, even if only because they have noticed that something everyone else overlooks is, actually, a thing of great intrinsic beauty.  As Garrison Keillor himself once said: “Thank you, God, for this good life and forgive us if we do not love it enough”.

Aegagropila_v_Cladophora

Diagrams of branching patterns in Aegagropila linnaei (a.) and Cladophora glomerata (b.).   Note how the branches of A. linnaei arise just below the end of the cell (“sub-terminal”, indicated by arrows) whereas the branches of C. glomerata arise at the ends.

References

Boedeker, C., & Immers, A. (2009). No more lake balls (Aegagropila linnaei Kützing, Cladophorophyceae, Chlorophyta) in The Netherlands? Aquatic Ecology. https://doi.org/10.1007/s10452-009-9231-1

Boedeker, C., Eggert, A., Immers, A., & Wakana, I. (2010). Biogeography of Aegagropila linnaei (Cladophorophyceae, Chlorophyta): A widespread freshwater alga with low effective dispersal potential shows a glacial imprint in its distribution. Journal of Biogeography. https://doi.org/10.1111/j.1365-2699.2010.02309.x

Boedeker, C., Kelly, C. J., Star, W., & Leliaert, F. (2012). Molecular phylogeny and taxonomy of the Aegagropila clade (Cladophorales, Ulvophyceae), including the description of Aegagropilopsis gen. nov. and Pseudocladophora gen. nov. Journal of Phycology. https://doi.org/10.1111/j.1529-8817.2012.01145.x

 

Some other highlights from this week:

Wrote this whilst listening to: This post has been a long time in gestation, so ’ve listened to a lot.  These included Bob Dylan’s Shot of Love, Infidels and Real Live, as well as Courtney Barnett’s A Sea of Split Peas and Arvo Pärt’s Tabula Rasa.

Cultural highlights:  The National Theatre At Home’s Streetcar Named Desire, starring Gillian Anderson.

Currently reading:   JK Rowling’s Harry Potter and the Philosopher’s Stone.  Comfort reading.

Culinary highlight:   I have to admit that fish, chips and mushy peas from Bells in Gilesgate was hard to beat.

Baffling biodiversity …

Few of the participants in the UK / Ireland diatom ring-test that I described in my previous post felt any need to thank me for my choice of slide for our 50th test.  The slide came from a spring in County Mayo, Ireland, which is part of the Agricultural Catchments Programme, a large study into the effect of farming on water quality. The sample itself came from the stems and leaves of the submerged water cress (Nasturtium officinale*) plants which fill the entire channel.  It was a real stinker, with a mess of Gomphonema forms, several of which did not neatly fit any species description that we could find.   A conservative reckoning is that there were at least eight different Gomphonema “species” and that raises a further question about what it was about this habitat that led to so much diversity within a single genus within a single sample.

First, a quick tour around some of the Gomphonema forms that we found.   There was general agreement that the most common type was close to G. micropus Kützing 1844 but not a perfect match to published descriptions (the stria density, in particular, was too low).   The situation was further complicated because the status of G. micropus was questioned at times, with it being treated as a variety of G. parvulum and placed in the G. angustatum complex by different authorities during the 20th century.  Then there were a number of valves with more rounded ends and a higher striae density than G. micropus but which, if you look closely, are not symmetrical around the long axis.   We thought that these were close to G. cymbelliclinum Reichardt & Lange-Bertalot 1999.   Unfortunately, there were also quite a lot of valves that had intermediate properties, making it hard, in many cases, to say whether it was one species or the other.

Gomphonema cf micropus from Cregduff spring, Co. Mayo, Ireland, September 2017.  Photographs: Bryan Kennedy.  Scale bar: 10 micrometres ( = 100th of a millimetre).  The image at the top of the post shows Cregduff spring (photo by Lauren Williams)

Gomphonema cf cymbelliclinum from Cregduff spring, Co. Mayo, Ireland, September 2017.  Photographs: Bryan Kennedy.  Scale bar: 10 micrometres ( = 100th of a millimetre).

We also found some valves that were close to descriptions of Gomphonema utae Lange-Bertalot & Reichardt 1999 and some that were close to G. parallelistriatum Lange-Bertalot & Reichardt 1991.  We also found representatives of the G. parvulum complex, G. tergestinum and G. subclavatum (more about this one in the next post).

Gomphonema cf utae from Cregduff spring, Co. Mayo, Ireland, September 2017.  Photographs: Bryan Kennedy.  Scale bar: 10 micrometres ( = 100th of a millimetre).

Gomphonema cf parallelistriatum from Cregduff spring, Co. Mayo, Ireland, September 2017.  Photographs: Bryan Kennedy.  Scale bar: 10 micrometres ( = 100th of a millimetre).

So what is going on here?   There are, I suspect, two key elements to the story that we need to explain.  The first is the limits of species within Gomphonema.  I’ve touched on this before (see “Diatoms and dinosaurs”) and some recent studies that combine morphological and molecular biological evidence also cast doubt on our ability to differentiate within this genus using classical approaches.   Whilst I was struggling to disentangle the species in this sample, I had a conversation with an eminent taxonomist and she hinted darkly that Gomphonema was “over-described”.  There is a readiness to “split” established taxa and describe new species that, in her opinion, runs ahead of the evidence.

The limitations of taxonomy cannot explain all of the variation that we observed in this sample, so the second question to ask is what it is about the conditions here that allow so many representatives of one genus to thrive.   I’ve touched on this subject before (see “Baffled by the benthos (1)” and “Baffled by the benthos(2)”).  In these posts I introduced G. Evelyn Hutchinson’s “paradox of the plankton” in which he suggested that environments that look uniform, to mortals six orders of magnitude larger than algae are, in fact, considerably more heterogeneous  and, so offer more opportunities for “variations on a theme” to thrive.   In the second post I went on to suggest that this type of diversity imparts resilience to an ecosystem and so should be looked upon as a positive feature of the ecosystem when doing ecological status assessments.

There is, however, one final possibility that, to my knowledge, has not yet been explored.  The presence of transitional forms in the diatom assemblage at Cregduff may be an artefact of our inability to differentiate biological species based on a limited range of morphological criteria on offer. However, it is also possible that we are looking at a situation where the Linnaean species are not reproductively isolated from one another, allowing hybridisation.   The concept of a “hybrid swarm” is well known in some other groups (e.g. orchids) but has never been formally demonstrated in diatoms.  However, the wide morphological diversity within a single genus in one sample alongo with, in some cases, apparent continua of variation, does raise questions about speciation within thi genus.

The final twist to this story is that, from the point of view of current ecological status assessments, all this diversity has little effect.  Though everyone grumbled about the difficulties in naming the Gomphonema species, the results, as the box-and-whisker plot in the previous post show – were less variable than in many of our other ring tests.  What I suspect happened is that the underlying taxonomic confusion means that many of these taxa have “mid-range” scores for the TDI (and other indices), so the final calculation cancels out the identification issues.  Bear in mind that this may not always be the case!

* I understand that this is the correct name now, rather than Rorippa nasturtium-aquaticum.  See Al-Shehbaz, A. & Price, R.A. (1998).  Delimitation of the genus Nasturtium (Brassicaceae).  Novon 8: 124-126.

References

The two papers that deal with variation within Gomphonema to which I refer are:

Abarca, N., Jahn, R., Zimmermann, J. & Enke, N. (2014).  Does the cosmopolitan diatom Gomphonema parvulum (Kützing) Kützing have a biogeography? PLOS One 9: 1-18.

Kermarrec, L., Bouchez, A., Rimet, F. & Humbert, J.-F. (2013).  First evidence of the existence of semi-cryptic species and of a phylogeographic structure in the Gomphonema parvulum (Kützing) Kützing complex (Bacillariophyta).  Protist 164: 686-705.

More about Rivularia

My post on Rivularia from softwater habitats (‘“Looking’ is not the same as seeing”’) prompted an email from Bryan Kennedy in Ireland with some pictures of Rivularia from a moorland stream in Co. Mayo in the west of Ireland, once again from a catchment completely lacking limestone.   Bryan estimates the calcium concentration in the water to be between 5 and 10 milligrams per litre, which means that the water here is very soft.  He also comments that it was recorded in the 1970s from the Caragh catchment in south-west Ireland (average calcium concentration: 2.15 milligrams per litre: see Heuff & Horkan, 1984).

Yellow_river_trib

A tributary of the Yellow River, Co. Mayo, Ireland (left) with dark brown / black colonies of Rivularia beccariana on a submerged stone (right).  Photos: Bryan Kennedy.

The photomicrographs show the colony structure very well with filaments radiating out from the centre.   The major difference between these and the Rivularia biasolettiana I photographed in Upper Teesdale (“Blue skies and blue flowers in Upper Teesdale”) is that colonies of the latter contain calcite crystals, though these were not visible in my images.  The right hand image shows the structure of Rivularia filaments very clearly; the tapering blue-green filament gradually narrowing to a colourless hair.   Note the colourless cell at the base of the filament.  This is the “heterocyst”, and is the location where nitrogen fixation takes place.  This is a very useful adaptation in the nutrient-poor habitats where Rivularia is found, as it means that, like peas and beans, it can capture nitrogen directly from the atmosphere, rather than relying upon dissolved minerals.

Nitrogen-fixation, however, needs a lot of energy and organisms do not fix nitrogen if there is a ready supply available from other sources.   Once nitrogen is abundant, species such as Riviularia are at a competitive disadvantage and it is no surprise that Rivularia and it’s close relatives are found only in remote parts of the country, given the extent to which nitrate fertiliser washes off the land and into streams and rivers.   Even in upland areas, there are often nitrogen compounds in rain water, much of it originating in the exhaust emissions from our cars.   One wonders if Rivularia might have been much more widespread a hundred years ago than is the case now.

Rivularia_beccariana_tribYe

A close-up of a Rivularia beccarina colony from the tributary of the Yellow River, Co. Mayo, Ireland.  Photos: Bryan Kennedy.  

Reference

Heuff, H. & Horkan, K. (1984).  Caragh.  Pp. 363-384.  In: Ecology of European Rivers (edited by B.A. Whitton).   Blackwell Scientific Publications, Oxford.