Marine stonemasons

If I mention the word “worms”, most people think of earthworms and many view them with distaste. There are several species, all looking rather similar, and we don’t find them attractive because they are slimy and often live in decomposing organic matter. However, it is not unknown for infants to try eating them, so our dislike is something we learned from adults or older children.

We are less familiar with marine worms, and there are many different forms. The white calcareous tubes you see on rocks, or the small spiral tubes found on seaweeds like wracks, are secreted by worms and there is every likelihood that the worm is still resident when you see their ”home” at low tide. Marine worms of many species live in tubes and, in addition to those made from secreted calcium salts, these may be poorly consolidated – as with the lugworms beloved of sea anglers – or constructed of grains cemented together to prevent abrasion by moving sand grains. However, these tubes offer little protection against predation by wading birds in shallow water.

The mason worm (Lanice) is widely distributed and extends from the inter-tidal down to 1900 m [1] and may occur in very high densities (up to 20,000 individuals per square metre [2]). Lanice makes tubes that extend above the surface of the sandy mud in which the worms live and each tube has extensions at its tip. Where present as dense reefs, Lanice tubes promote sedimentation of fine mineral and organic particles and these sediments increase biodiversity [3]; the worms being referred to as “ecosystem engineers”. Close examination shows the tube and extensions to be made of sand grains and shell fragments cemented together by a secretion of the worm - thus the term mason worm (see above in a wonderful image captured by Jim Greenfield).

Lanice is in the group of worms known as terebellids and they feed when the worm and its tube are covered by water, so feeding can best be observed when worms are transplanted to an aquarium tank. The tentacles at the front of the body (see above) are extensible and very mobile and, if we  look at them under a microscope, we see many hundreds of thousands of beating hairs (cilia) over their surface and also a covering of mucus, produced from cells within the tissues of the tentacles [4]. Algae and detritus become attached to the tentacles when they are spread on to the substratum and the cilia then carry the mucus-bound “packages” to the mouth where they are ingested. Waste products are removed by the currents of water that the worm generates by moving its body within the tube.

Lanice also feeds by spreading the tentacles over the “fan” of extensions constructed at the top of its tube, collecting particles from the currents that result from wave action. We know that the particles carried in suspension contain micro-aggregates formed by bubbles created when waves break [5] and these, too, form part of the food for the worms, together with anything else that becomes swept up.

How do the worms locate their habitat? The answer is that it is largely a matter of chance. After reproduction (there are separate male and female worms [6]), larvae become planktonic and are carried around in the water column by currents and by their own swimming by means of the ciliated bands on their body (a second use of cilia for larvae as they also use these organelles to gather food). The large majority of planktonic larvae are eaten, or fail to reach a suitable substratum, but, when they do, each larva swims down and begins to transform into a small worm and begin their work as “masons”.

Far from feeling distaste at the sight of these worms, I marvel at their biology and how they evolved their form and habits. The sense of wonder is one of the pleasures of Natural History and the never-ending fascination of looking at living creatures.

[1] R. M. S. Alves, C. Van Colen, M. Vincx, J. Vanaverbeke, B. De Smet, J.-M. Guarini, M. Rabaut and T.J. Bouma (2017) A case study on the growth of Lanice conchilega (Pallas, 1766) aggregations and their ecosystem engineering impact on sedimentary processes. Journal of Experimental Marine Biology and Ecology 489: 15-23.

[2] A. Nicolaidou (2003) Observations on the re-establishment and tube construction by adults of the polychaete Lanice conchilega. Journal of the Marine Biological Association of the United Kingdom 83: 1223-1224.

[3] B. De Smet, A.-S. D’Hondt, P. Verhelst, J. Fournier, L. Godet, N. Desroy, M. Rabaut, M. Vincx and J. Vanaverbeke (2015) Biogenic reefs affect multiple components of intertidal soft-bottom benthic assemblages: the Lanice conchilega case study. Estuarine, Coastal and Shelf Science 152: 44-55.

[4] R. P. Dales (1955) Feeding and digestion in terebellid polychaetes. Journal of the Marine Biological Association of the United Kingdom 34: 55-79.

[5] R. S. Wotton (1996) Colloids, bubbles and aggregates: a perspective on their role in suspension feeding. Journal of the North American Benthological Society 15: 127-135.

[6] https://www.marlin.ac.uk/species/detail/1642

Rotifers, Henry Gosse and me

This image by Charles Krebs of Floscularia ringens was posted yesterday on the “Walking with Gosse” Facebook page by Dr Susan England of Clio Publishing. It is of a rotifer that lives in fresh water and builds a tube that acts as protection, support and a means of attachment. Looking closely at the image we can see the groups of cilia which it uses to produce a feeding current. The tube is composed of balls largely of detritus, which are stuck together and the balls maintain their integrity for weeks, Floscularia extending the tube to take it further out into the water as the individual rotifer grows. The whole is approximately 1 mm in length and we see only a small portion here.

Henry Gosse, the great Natural Historian and illustrator, was fascinated by rotifers and assisted C.T.Hudson in a two-volume monograph on the animals. Despite Hudson’s protests, Gosse insisted on his attribution as assistant and this was typical of the man. The two enthusiasts were really co-authors and Gosse contributed much of his own detailed research to the volumes. In looking at rotifers, as with other living creatures, Henry Gosse saw evidence of the power of God and His Creation and it filled him with a sense of wonder.

As an evolutionist, I have several points to consider:

Why are the cilia used for feeding arranged in bundles?

Rotifers have many cells but had single-celled ancestors which used cilia for locomotion and feeding. Through evolution, cilia of some organisms became more complex and the bundles seen in Floscularia may promote increased feeding efficiency. The pattern of bundles seems very similar in form across the corona (the transparent lobes), so what caused their development in the first place? Did all the bundles appear simultaneously?

Building the tube

Several groups of rotifers build tubes and the tube of Floscularia is unusual in being made up of balls, primarily of detritus. The photograph shows the location of the “ball-forming device” in the cuticle of the rotifer and its constituent tiny particles will be collected readily from the water by the feeding current. We often ignore the presence of organic particles in water, yet they are found in vast numbers and have many important roles in the functioning of aquatic systems. Once a ball is formed, and compressed to a certain size, the rotifer can then locate it on the tube and having a tube with a wall of spherical balls is a very efficient use of materials. How did the “ball-forming device” and tube-building evolve?

Why do the balls in the tube maintain their shape and how do the balls stick together?

As mentioned, rotifers collect small particles of detritus and other organic matter. Detritus results from the breakdown of the bodies of living things and also consists of material that passes from living things as waste products or exudates. There will also be many different kinds of microorganisms (bacteria, etc.) that are attached to the fragments of detritus and are important in breaking them down into smaller and smaller pieces. To attach, microorganisms exude polymers and these are “Nature’s glue”, often becoming free from the microbes which produce them. It is these polymers which keep the balls intact as they are difficult to decompose and there are many "sticky" contact points when the ball is compressed. The exudates are in the form of minute fibrils and the rotifer could not make balls without the previous evolution of exudates by bacteria.

Amazing, isn’t it? 

Do I have any idea how Floscularia developed all these modifications? – No. Do I believe that they evolved by changes in genes occurring over huge numbers of generations? – Yes. Is a God responsible? – I don’t know, but do not think so. Evolution generates such a sense of wonder. I’m right with Henry Gosse in having that feeling when looking at living organisms, but we would not agree on the reasons why we felt that way.