Eating a Lake. How insect larvae transform lake mud to their needs.#

# This title was inspired by Olive Morton (2007), 'Eating the sun'.

One of Charles Darwin’s greatest contributions to our understanding of the world was his appreciation of the huge changes wrought on the environment by tiny inconspicuous animals (Darwin, 1881). I refer to the burrowing activities of the humble earth worm, each individual making a miniscule contribution to a dramatic overall effect on their soil habitat. The loosening of the soil sometimes leads to human buildings sinking slowly into the ground over the years. Tiny changes with large cumulative effects are not confined to earthworms. Other well known examples are termites and moles.

I wish to consider the role, not of soil dwellers, but of inhabitants of the mud of lakes. I will attempt to show that mud dwellers slowly consume the bottom of a lake and by so doing profoundly change the nature of their habitat. In the words of Lawton and Jones (1995), these organisms are ecosystem engineers. These aquatic ‘earthworms’ are typically dominated by insect larvae rather than annelids, particularly larvae of the chironomid midge (Armitage, Cranston, and Pinder, 1995; McLachlan and McLachlan, 1976). But it is not easy to demonstrate their effect. This is because most lakes are thousands or millions of years old and we arrive to collect samples at an unknown point in the lake’s history. What is needed is a situation which permits access to a lake before mud dwelling animals can start to reshape it. Just such an opportunity is provided regularly by a common type of giant swanp lake, such as Lake Chilwa in Malawi (Africa) (Fig. 1.). Such lakes typically occupy thousands of km² when full but dry up completely and refills every few years.

Fig. 1. Map of Chilwa showing open water with depth contours and surrounding swamp (k). After (McLachlan, 1974).

With great good fortune I was appointed to a lectureship at Chancellor College (University of Malawi) for the period 1965 to 1970. Chancellor College is conveniently close to Chilwa and when I arrived was nearly completely dry but refilled too during my tenure. What an excellent opportunity to study the whole process of drying and recolonization and the accompanying ecosystem changes. At that time none of us knew what to expect during a refilling of such a large lake, but Professor Margaret Kalk, head of the zoology department, set up the Lake Chilwa Coordinated Research Project at just the right time. The appearance of Chilwa during a typical dry and refilling cycle are shown in Figs. 2 and 3.

Fig. 2.   Chilwa full after 6 weeks with fishing in full swing and with Typha swamp in the background (photograph by G. Lenton).

Fig. 3. Chilwa drying with Brian Moss inspecting the dry lake scattered with the shells of the snail Lanistes ovum (see also Fig 9.3 in (McLachlan, 1979) 

Lake Chilwa covers some 2000 km², half of which is impenetrable Typha swamp. It is the open water habitat which concerns me here. To start at the point of drying – at this time the dry mud surface was scattered with the shells of the mollusc Lanistes ovum (Fig. 3). The presence of these shells infers that before drying the mud supported a thriving population of this snail. For various reasons which I will not go into here, I believe these molluscs inhabited the mud of the open lake rather than being migrants from the Typha swamp. In any case, their presence on the mud surface in Fig.3. is sufficient to suggest that the mud before drying was firm enough to support these large snails.

During refilling the dry lake bottom is stirred and eroded by wave action leading to a fine precipitate of mud several cm deep. Informal trials in the laboratory showed that this loose material was incapable of supporting even the larvae of the common midges measuring a up to nearly 2 cm in length and presumable thousands of times lighter than the golf ball sized Lanistes. Mature larvae of the chironomid Chironomus transvaalensis introduced to a beaker of water with precipitated mud from the newly flooded lake, simply sank through the mud surface and kept going to the bottom of the beaker.  Associated characteristics of the fine material were described by me in 1974 (McLachlan, 1974). It can reasonable be concluded that the same effect explains the complete absence of both chironomid larvae and Lanistes from the open lake mud just after refilling. However, larvae of chironomids but not Lanistes were abundant wherever there was any solid substrate such as that provided by the submerged leaves of typha and other aquatic vegetation at the edge of open water - but there only (Fig. 4.).

Fig. 4.  Distribution of animals just after refilling in February 1969. The area of each circle is proportional to the biomass of the faun. Hatched area – C. transvaalensis. Unshaded part of the circles - other fauna. Shading of the open water can be ignored for the present purposes. After (McLachlan, 1974). The swamp is not shown.

So, at some point between refilling and drying there appears to have been a change in the physical structure of the mud surface which then became able to support a dense fauna of chironomid larvae but still no Lanistes. This leads me to the hypothesis that it is the activity of the larvae of chironomids that converts the original almost liquid mud to a structurally firm one. I propose that it is specifically the feeding activities of chironomid larvae that are responsible. Feeding results in the production of hard faecal pellets, each larva producing a substantial 0.2mg of pellets day^-1 (McLachlan and McLachlan, 1976). The larvae of chironomids are thus an extraordinary lake-bed processing engine. So it is probably the accumulation of pellets in the mud that is ultimately responsible for the changes in the mud habitat. I imagine the process starting at the swamp margin and progressing to the lake centre. When the centre is reached the process is complete - provided the process is not interrupted by a dry phase. 

I got close to this realisation in the late seventies. “As pointed out by us (McLachlan and McLachlan, 1976), chironomid larvae have the ability to change the prevailing particle size in their environment. This is done by converting the fine material taken in the search for food into aggregates many time greater in diameter, by the formation of faecal pellets, these pellets are ideally suited to tube building operations and, being bound together with silk, persist for a considerable time, perhaps years, before eventually disintegrating. Given time, a larval populations can eventually process a sediment such as that on the Lake Chilwa bed, to create a habitat more acceptable to themselves”, (McLachlan, 1979) - and it should be added, to other animals such as Lanistes as well. To be clear, I have simplified the situation on Lake Chilwa by putting aside the important role of water chemistry and the role of the silk chironomid larvae use in construction the tubes they inhabit. Such details can be found in the publications listed below.

To summarise, I suggest that, by consuming the young lake bottom chironomid larvae provide the proximate explanation for the mud becoming habitable to other animals. Faecal pellets provide the ultimate cause. In brief chironomid larvae, by consuming the lake bottom, turn it into faecal pellets.

I am not suggesting that the consequences of chironomid feeding are some kind of community level adaptation. Explicitly not so. These effects are by-product effects which may benefit other speies but are clearly not an adaptation evolved to help others (Williams, 1966, p247)(McLachlan, 2011, p545).

The time has come to test my hypothesis. Passing soil through screens of various mesh sizes is a standard method for characterising the physical nature of soil in terms of particle size composition. The same method is applicable to the mud of lakes of course. By screening mud through an appropriate series of sieves, at regular time intervals immediately after filling starts and for as many years as necessary thereafter, the particle size distribution of the mud habitat can be recorded. Specifically, the role of faecal pellets can be determined because as trials showed, mud passes through a 105µ mesh sieve leaving virtually nothing but faecal pellets behind (McLachlan and McLachlan, 1976). The sieve method thus gives neat and clear results. I predict an increase in the proportion of pellets over the years leading eventual to a stable mud substrate. The character of faecal pellets found in the field will benefit from a separate programme to confirm their resistance under various conditions, see also (Joyce, Warren, and Wotton, 2007).

Processing the lake bed by consuming it is a vivid example on a grand scale of what has become known as niche construction (Odling-Smee, Laland, and Feldman, 2003), i.e. the restructuring of habitats by the activities of the inhabitants. In an historical context, lakes such as Chilwa provide a wonderful opportunity for the prepared mind. By resetting the ecological clock such lakes can reveal how the ecosystem gets started as well as the full course of succession following from this - something hidden in most lakes. It seems to me that it is this opportunity that lead my colleague and friend Brian Moss from his studies of Chilwa in the 1960s, to a novel and compelling view of the nature of the lake ecosystem, a concept set to succeed and replace the traditional view (Moss, 2015).

Re-reading this post in January 2021 suggested an alternative introduction to me. I offer it below:

I am interested here in animal engineering reviewed by Hansell (Hansell, M. H. 1984). His concern is with the building activities of animals leading to the construction of termitaria, the dwelling tubes of caddis fly nymphs. earthworms in the soil and many, many others. Hansell's could have included, in his  fascination review, the tube building activities of the larvae of the chironomid midges which, in terms of the variety of structures produced, far outstrip that of  the cadddis flies (Imada, Y. In press).

 

references

Armitage, P., Cranston, P. S., and Pinder, L. C. V. (1995). The Chironomidae. The biology and ecology of non -biting midges. . London: Chapman & Hall.

Darwin, C. (1881). The Formation of Vegetable Mould, through the Action of Worms, with Observations on Their Habits. . London: Murray.

Joyce, P., Warren, L. L., and Wotton, R. (2007). Faecal pellets in streams: their binding, breakdown and utilization. Freshwater Biology.

Hansell, M. H. (1984). Animal Architecture and Building Behaviour. Longman, London and New. 

Imada, Y. (In Press). Diversity of Underwater chironomid tube structures. Zookeys, 47834.
Lawton, J. H. & Jones, C. G. (1995).Linking species and ecosystems: organisms as ecosystem engineers. In: Jones CG, Lawton JH (eds). Linking species and ecosystems. Chapman & Hall, London.

McLachlan, A. J. (1974). Recovery of the Mud Substrate and its Associated Fauna Following a Dry Phase in a Tropical Lake. . Limnology and Oceanography, 10, 74 - 83.

McLachlan, A. J. (1979). Decline and Recovery of the Benthic Invertebrate communities. In M. Kalk, A. J. McLachlan and C. Howard-Williams (Eds.), Lake Chilwa. Studies of change in a Tropical Ecosystem. London: W. Junk. Publishers.
McLachlan, A. J., and McLachlan, S. M. (1976). Development of the mud habitat during the filling of two new lakes. Freshwater Biology, 6, 59 - 67.
McLachlan, A. J. and Ladle, R. J. (2011). Barriers to adaptive reasoning in community ecology. Biologival Reviews. 86, 543 - 548.
Morton, O. (2007). Eating the Sun. How Plants Power the Planet. Fourth Estate. London.

Moss, B. (2015). Mammals, freshwater reference states and the mitigation of climate change. Freshwater Biology, 60, 1964 - 1976.

Odling-Smee, F. J., Laland, K. N., and Feldman, M. W. (2003). Niche Construction. The Neglected Process in Evolution. Princeton: Princeton University Press.
Williams, G. (1966). Adaptation and Natural Selection. Princepton Univerity Prtess. Princeton, New Jersey.