Blaxter Lough

Fig. 1. View of Blaxter Lough, the humic lake habitat studied here.

I want to return to an extraordinary situation discovered by me on the high moors of Northumberland. My intention is to re-examine this purely ecological story but this time in the light of evolution theory. This opens the door to some interesting and testable questions previously hidden. The story concerns the interrelationships among three organisms which allows them to flourish in the nutritionally impoverished environment of a humic lake. Relationship hinges on the faecal pellets produced by larvae of a chironomid midge, Chironomus lugubris, feeding on particles of peat introduced to the lake by wave action. Particles in suspension are rapidly colonised  by decomposer micro-organisms which evidently make otherwise refractory peat nourishing as food for the midge larvae. Faecal pellets are yet more heavily colonised by micro-organisms and  should therefore be attractive to the larvae as food. However, perhaps because they are too hard for their mandibles, the larvae appear not to make use of this seemingly valuable resource.

Fig. 2. Sectional diagram of a tube dwelling Chironomus larva with a swarm of Chydoris  swimming precisely over the faecal end of the tube. 

But now comes the interesting part. Midge pellets, although ignored by the insect larvae, appear to be grazed by a second arthropod, the Cladoceran Chydoris sphericus. These hold a pellet between their valves and rotate it while grazing its surface. In the lab, a cloud of Chydoris can be seen swimming precisely over the pile of faecal pellets produced by larvae, at only one end of the tube (Fig 2). Of course the crustacea also produce faecal pellets. Passing through the fug of a chironomid larva boosts  micro-organism populations so passing through the gut of a chydorid  would be predicted to harbour yet higher loads of micro-organism. Unlike their own pellets, those of Chydoris are of a size which should be easily consumed by larvae. Here there are two gaps in our data which call for formal investigation. First, what is the nutritional actual value of Chydoris pellets and are they actually consumed by Chironomus larvae? Second,  in artificial pools in the laboratory, unless chironomid larvae are added to the culture, Chydoris does not make an appearance. In the wild Chydoris adults appear in large numbers in the summer, supposedly spending the winter as diapausing eggs (ephippia), in the mud. Something, largely unknown, is required to break this diapause (Barnes, Calow, and Olive, 1988; Bronmark and Hansson, 2005). Thus there is a hint here of  some fundamental relationship between chironomids and chydorids beyond that of  food.

This whole interaction between these two arthropods is discussed by Mike Begon and colleagues (Begon, Townsend, and Harper, 2006), pp 340-341, and by Brian Moss (Moss, 2010), p 315. Research details can be found in (McLachlan, 1976, 1978; McLachlan and Dickinson, 1977; McLachlan and McLachlan, 19975; McLachlan, Pearce, and Smith, 1979).

Fig. 3.  Diagram summarising relationships between players, an insect larva, a crustacean and micro-organisms, in a putative mutualism centred on faecal pellets. a, chironomid faecal pellets. b, chydorid faecal pellets. The consumption of 'b' by the chironomid awaits testing.

I turn now to look at this story from an evolutionary perspective. As far as I know this has not been attempted before. The central question is whether the observed relationship between three organism; insect, crustacean and micro-organism, is an economy in the sense of Richard Dawkins (Dawkins, 2004), p 266, or an adaptation in the sense of George Williams (Williams, 1966). Only if it is an adaptation can it be referred to as a mutualism (Boucher, 1992). This is not an easy question to answer because economy and adaptation merge into each other and an economy may be moving, under selective pressure, toward an adaptation. The application of Pittendrigh's principal of teleonomy (discussed by George Williams (Williams, 1966), is useful here. What is required is the identification of a function. For example, in one case of well established mutualism, that of bees and flowers, the question 'what is the function of a flower?', is readily answered - it is to attract bees. Hence the bee/flower relationship is a true mutualism. Turning to the feeding relationships shown in Fig.3., feeding relationships based on faeces are by-product relationships (Dawkins, 2004). Faecal pellets are not organisms and hence cannot respond to natural selection. But they are colonised by bacteria and fungi which can respond. So we may be dealing with a mutualism after all. For a discussion of the relationship between mutualism and reciprocal altruism see (Boucher, 1992).

Turning from feeding to diapause; recall the finding that the presence of Chironomus larvae appear necessary for the appearance of Chydoris. What is implied is that the chironomid larvae somehow break the diapause of  Chydoris. In other words, there  appears to be some kind of intimate  relationship here not based on by-products. A formal, but straight forward experiment is required to explore this idea. A survey of humic lakes and perhaps of other representative kinds of lakes as well, could strengthen an assumption of mutualism if all three players are invariably found together. Thus diapause could be an adaptation if it answers to the principle of teleonomy because a function is readily identified - the function of Chironomus is to break diapause of Chydoris.

To summarise - what I have attempted is to re-examine an old piece of work in the light of evolution theory. This shows up a new set of questions. Key questions are; first that we are dealing with a true mutualism based on faeces and second that Chironomus larvae must be present for Chydoris also to be present. The first question can be tested by determining how consistently the three players are found together. An obligate association supports an hypothesis of mutualism. The second, the diapause breaking,  is readily tested by a simple experiment in the laboratory with replicate aquaria containing winter lake mud with chironomid larvae and a control set of replicate aquaria but without insect larvae. Thus both question are testable. Perhaps some one will pick it up. It could be rewarding.

references

Barnes, R. S. K., Calow, P., and Olive, P. J. W. (1988). The Invertebrates, A new synthesis. Oxford: Oxford University Press.

Begon, M., Townsend, C. R., and Harper, L. (2006). Ecology. From Individuals to Ecosystems. (4 ed.): Blackwell Publishing 

Boucher, D. H. (1992). Mutualism and Cooperation. In E. F. Keller & E. A. Lloyd (Eds.), Keywords in Evolutionary Biology. (pp. 208-211). London: Harvard University Press.

Bronmark, C., and Hansson, L.-A. (2005). The Biology of Lakes and Ponds. (Second ed.). Oxford: Oxford University Press.

Dawkins, R. (2004). A devil's chaplain. London: Phoenix.

McLachlan, A. J. (1976). Factors Restricting the Range of Glyptotendipes paripes EDWARDS (Diptera: Chironomidae) in a Bog Lake. Journal of Animal Ecology, 45, 105-113.

McLachlan, A. J. (1978). Interactions between Freshwater Animals and Microorganisms. Annals of applied Biology, 89, 162-165.

McLachlan, A. J., and Dickinson, C. H. (1977). Micro-organisms as a foctor in the distribution of Chironomus lugubris ZETTERSTEDT in a Bog Lake. . Archiv fur Hydrobiology, 80, 133 - 146.

McLachlan, A. J., and McLachlan, S. M. (19975). The Physical Environment and Bottom Fauna of a Bog Lake. Archiv fur Hydrobiology, 76, 198 - 217.

McLachlan, A. J., Pearce, L. J., and Smith, J. A. (1979). Feeding Interactions and Cycling of Peat in a Bog Lake. Journal of Animal Ecology, 48, 851-861.

Moss, B. (2010). Ecology of Fresh Waters. A view for the Twenty-First Century. (4 ed.). Chichester, UK: Wiley -Blackwell.

Williams, G. C. (1966). Adaptation and Natural Selection. Princeton: Princeton University Press.

Freshwater Biology - How I would teach it

Figure 1. The  beauty of amphibians, here an unnamed frog.

 

As a young man in Africa and later in the UK, I taught freshwater biology at both second and final year levels. My 1966 PhD and postdoc work were undertaken over a period of some eight years at such wonderful places as Lake Kariba ( 4 years) and lake Chilwa (4 years), in tropical Africa and I remained active in freshwater research and publication until the mid 1980s. I was thus presumably qualified to carry out teaching responsibilities in freshwater biology. My aim here is to produce an outline plan for a hypothetical course in freshwater biology which I would teach today, given the chance. From the perspective of nearly 40 years I have been looking back on those early years and wondering why freshwater biology seemed such an intellectually unrewarding subject and how it might be improved. A large part of this failing, I believe, is the absence of a unifying theme in undergraduate courses. This applies as much to my own earlier teaching as to the efforts of others. It  applies to freshwater biology specifically and not so much to ecology in general. Furthermore, freshwater biology, as it its taught today, has tended to be about the nature of the habitat rather than about the biota. It is this emphasis on habitat that may be responsible for the absence of a strong theme. A greater role for freshwater fauna could readily lead to a unifying theme. The theory of evolution custom made for the role. We freshwater biologists should continuously reminded ourselves of Theodore Dobzhansky's famous maxim . ... "Nothing in biology makes sense except in the light of evolution" (Dobzhansky 1973).

With this in mind I thought a way forward  might be to create a list of key literature sources. Under the umbrella of evolution I would emphasise three things. First, weight would be placed on  the waters of Africa. Africa has an exceptional diversity of freshwater habitats and faunas and was the cradle of mankind and, to quote Richard Dawkins, p265, ..." this alone makes African ecosystems an object of singular fascination" (Dawkins 2004). For that reason field courses in Africa would be desirable and a realistic possibility, at least in the financial climate prevailing before I retired in 2004. Second, in contrast to most courses I know of, I  would make vertebrates the principal study organism. This melds well with an emphasis on Africa with its wonderful world of fish and amphibians (Fig. 1). The study of amphibians leads naturally to the adaptive laboratories of ephemeral waters such as rain pools. Amphibians illustrate beautifully two things; phenotypic plasticity, that is the facultative response of which an organism is capable in the face of environmental challenges. An example of phenotypic plasticity is the development of  calluses on the hands of gardeners. Most amphibians have a larval stage dependent on standing water. It is these immature stages that show an astonishing range of adaptations to typically ephemeral and unpredictable water on which they depend. The larval stages are amenable to experimental manipulation, for example, the addition of iodine to the water, to alter developmental rate (Spaul 1928). Such manipulation opens the possibility of exploring mechanisms of plasticity and developmental adaptation. I can think of no finer laboratory to engage the interests of students.

Turning to fish (and I expressly do not meant commercial fisheries): fish tend to dominate permanent waters to the virtual exclusion of amphibians. The fish faun of the great lakes of Africa; Malawi, Tanganyika, and Victoria,  have captured the interest of biologists for many years. Here there is an outstanding demonstration of the wonders of adaptive speciation. I refer to the  indigenous cichlid flocks inhabiting these waters (Kocker 2004).

I give little attention to rivers and streams only because I am here attempting a  hypothetical exercise with myself as sole teacher and my research experience does no fit me for advanced teaching in those habitats. 

Core literature sources appear below:

  1). Two books to provide the ecological background. Begon et al (Begon, Townsend et al. 2006)/Corze and Reader (Croze and J. 2000).

Townsend et al. are here intended to provide access to the general principles of ecology. They provide the ecological setting for freshwater biology and set ecology within the evolutionary landscape. Croze and Reader offer a good general ecology text set in Africa and hence an appropriate accompaniment for Beadle (below).  Croze and Reader provide a fine introduction to the rich mammalian ecology of Africa. *

2).  The inland waters of tropical Africa.  Leonard  Beadle (Beadle 1974).

Leonard has the knack of exciting in his reader a sense of adventure and wonder at the wilderness and the adaptive challenges encountered by freshwater dwelling animals in  the  waters of Africa. This is just the text, I believe, to attract students to a research career in the subject.  Here both an introduction to both phenotypic plasticity (traditionally called 'adaptation' by physiologists), and changes in gene frequency within a population. i.e. evolution, can be found.

3). The Biology of Lakes and Ponds. Brönmark and Hanson (Bronmark and Hansson 2005).

To broaden an African emphasis and to introduce small and ephemeral water bodies, I would  include this excellent book. Research effort in Europe and America has favoured large lakes. By contrast these authors emphasise biotic adaptations in smaller waters. These, after all must be many orders of magnitude more abundant than larger lakes and because they are small tend to be ephemeral - drying out or freezing in unpredictable patterns which raise fascinating questions about adaptation.

4) The evolutionary ecology of rain pools

To build on the biology of temporary waters there are the ubiquitous rain pool. These are the ultimate in small bodies of water. They are the  most ephemeral and numerous waters, sometimes holding only a few ml of water. They lend themselves well to experimental manipulation. In view of their abundance rain pools may be where adaptive changes in the evolution of freshwater faunas principally take place - and even where life on earth may have originated, see Charles Darwin famous,  'Warm Little Pond' (Darwin 1Feb 1871). Some fine work on the biogeography of rain pool dwelling crustacea is being undertaken  by Brian Tims, Vanshoenwinkel  and colleagues in Africa and Australia (Pinceel, Brendonck et al. 2013). My own research in Africa focused on the extraordinary insects breeding exclusively in rain pools on rock surfaces (McLachlan and Ladle 2001). A recent explosion of research on rain pool faunas include some interesting adaptations among amphibians and even fish. 

References

Strother, P.K., Battison, L., Brasier, M. D. and Wellman, C. H. (2011). Earth's earliest non-marine eukaryotes. Nature 473, 505-509.

Beadle, L. C. (1974). The Inland Waters of Tropical Africa. London, Longman.

           

Begon, M., C. R. Townsend, et al. (2006). Ecology. From Individuals to Ecosystems., Blackwell Publishing 

           

Bronmark, C. and L.-A. Hansson (2005). The Biology of Lakes and Ponds. Oxford, Oxford University Press.

           

Croze, H. and R. J. (2000). Pyramids of Life. London, Harvill Press.

           

Darwin, C. (1Feb 1871). Warm Little Pond.

           

Dawkins, R. (2004). A devil's chaplain. London, Phoenix.

           

Dobzhansky, T. G. (1973). "Nothing in Biology makes sense except in the Light of Evolution." The American Biology Teacher 35: 125-129.

           

Kocker, T. D. (2004). "Adaptive Evolution and Explosive Spciation: The Cichlid Fish Model." Nature Reviews Genetics 5: 288-298.

           

McLachlan, A. J. and R. Ladle (2001). "Life in the puddle: behavioural and life-cycle adaptations in the Diptera of tropical rain pools." Biological Reviews 76: 377-388.

           

Pinceel, T., L. Brendonck, et al. (2013). "Environnmental change as a driver of diversification in temporary aquatic habitats: does the genetic structure of extant fairy shrimp populations reflect historic aridification?" Freshwater Biology 58: 1556-1572.

           

Spaul, E. A. (1928). "Comparative Studies of Accelarated Amphibian Metamorphosis. ." Journal of Experimental Biology 5: 212-232.

* On reflection, and with an eye to the evolutionary theme, I cannot avoid adding the highly effective text book by Scott Freeman and Jon Herron (1988). I wish this fine book had been available when I was an undergraduate.

Freeman , S. and Herron, J. (1998). Evolutionary analysis. Prentis Hall, New Jersey.