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

We can't exist without slime

What is your reaction to slime? Most people find the substance, and even the thought of it, distasteful and yet we would not be alive if it was not for slime in one form or another.

Slime consists of chemical polymers that expand on contact with water, producing a clear, sticky substance that is ubiquitous and which we recognise from its slipperiness and its ability to stick to surfaces. The compounds that make up slime are referred to as exopolymers, or EPS, by those that study them and they consist principally of carbohydrates and proteins, although many other chemicals may also be found in the EPS produced by different organisms. They are truly ubiquitous: bacteria using them to attach to substrates; single-celled algae release them when producing an excess of carbohydrate during photosynthesis; and multicellular organisms use them for protection, locomotion, to aid in feeding, to aid buoyancy, and as a means of attachment [1].

During evolution, some cells in multicellular organisms became adapted to have the sole function of producing the EPS that result in slime. These goblet cells (see above) discharge their contents to become hydrated and we are familiar with the resulting sliminess of animals like worms, slugs and fish. 

I talked about EPS to an audience of trout fishers and this was recorded by the Wild Trout Trust [2] and one of the illustrations is shown below, together with the link to the video. I could only give a very few examples, but you get the drift of my talk: EPS are everywhere and yet they are largely ignored, even by scientists who should know better. Of course, there are prejudices to be overcome and at one conference dinner I was given a special prize for "the most revolting talk" given during the sessions. An award made in good humour, of course, but indicating that the subject was one that most find unpleasant. This is a pity, because EPS are one of the most important families of chemicals known.

It is fair to say that humans would not exist if it was not for slime. This argument has two components: one that develops ideas on the evolution of humans and the other on the very important role slime plays in allowing our survival. Our most distant ancestors lived in water and left this medium when fish transitioned into the amphibians (and then into reptiles and mammals). Reptiles and mammals have body coverings that reduce the loss of moisture, something that is a threat to amphibians and also the first fish making visits to land. Anyone handling a fish is aware that they have a slippery covering and this protects the animal from attack by parasites and may aid locomotion: it is a feature that is retained by amphibians and serves to reduce water loss from their bodies when they are exposed to the air for long periods. It is also a common feature among soft-bodied terrestrial invertebrates such as worms and slugs, while others, like the arthropods, have an impervious exoskeleton that much reduces the threat of desiccation.

Fish slime protects the gills from abrasion and also provides a barrier against osmotic stress, a feature that is very important to salmon as they migrate from the sea to fresh waters. Yet gas exchange occurs from the water to the mucus and then to the tissue of the gill surface and this is a feature retained through the evolution of respiratory organs of amphibians, reptiles and mammals. Human lungs and nasal passages have a coating of mucus, moved by cilia that are a throwback to our very ancient protozoan ancestors, and it can be so plentiful that it has to be removed by blowing, coughing, or swallowing, the latter normally being a continuous and unconscious process. In addition to allowing gas exchange, this mucus acts as a trap for particles, both living and dead, and it is a convention that we blow an excess of the slime into handkerchiefs, often noting the extent of hydration once the mucus becomes dried, demonstrating admirably the extent to which the EPS had undergone considerable expansion when in contact with water. Larger quantities of slime than usual are produced when this first defence mechanism is triggered by infection.

It is not only nasal, and bronchial, tissue that produce mucus in humans, and other mammals, as slime is also found in the digestive tract and in the reproductive system. The slippery quality of mucus acts as a protection for the oesophagus and slime is produced elsewhere in the gut to allow smooth passage of the contents while protecting the wall of the digestive tract. The mucus is not broken down by enzymes and, when aqueous solutions of food chemicals are removed, characteristic compacted faeces result. These are bound with slime produced originally by the gut wall and also by EPS released by the many micro-organisms that are resident within the digestive tract; the microbes protecting themselves against digestion by secreting EPS that then become a binding material for the faeces.

The final use of slime in humans is in reproduction and, especially, in allowing the migration of sperm deposited within the female genital tract. Each sperm swims within seminal fluid that contains EPS and then traverses the cervical mucus and onwards into the uterus, where one sperm fertilises a waiting egg, if one is present. It should also be pointed out that mucus provides a lubricant to facilitate copulation. 

Vital rôles indeed and it is fair to say that we would not exist without slime in one form or another, nor would very many other organisms

Having read this far in the blog post, what are your reactions? Perhaps you agree that I deserve to be thought revolting in writing, and talking, about such things, even though I respect proper taboos in polite company? Yet I am only highlighting the remarkable diversity of uses for slime and EPS and this deserves to be much better known, rather than being given the "Ugh! response" that seems to be most people's reaction to the subject. Why do we feel that way?

[1] Roger S. Wotton (2005) The Essential Role of Exopolymers (EPS) in Aquatic Systems. Oceanography and Marine Biology: An Annual Review 42: 57-94.

[2] https://www.youtube.com/watch?v=XNN-NeSwQj0

Eating slugs – and a fascinating defence mechanism

Mention slugs to people and you are likely to get "Ugh!" as a response - and from gardeners a more hostile reaction. This is because slugs are slimy and they also eat plants, often in competition with humans when we are growing plants for food or decoration.

To a Natural Historian, slugs are fascinating, as they are gastropod molluscs that have lost their shell during evolution. Adult gastropods, with few exceptions, move using muscular contractions and expansions of the foot, sliding over a film of secreted slimy mucus. Production of mucus is also important in providing a body covering to prevent desiccation and as a deterrent to predators. Nevertheless, many slugs are predated and gardeners are encouraged to provide areas for hedgehogs or predatory birds. One solution to the pest problem that is rarely mentioned is the collection of slugs for food, just as we gather some types of snails (Roman snails, winkles, whelks, etc.). Here is a recipe adapted from one posted on the "eattheweeds" website [1]:

Allow slugs to feed on salad leaves and then kill them in a vinegar-water mixture before boiling them in water, repeating this three times. The prepared slugs can now be used to make patties.

Beat 3 eggs with 3 tablespoons of double cream and add the mixture to 3 tablespoons of flour, the same quantity of cornmeal, and 10 slugs (chopped into bite-sized pieces). Whisk, form into patties, and then fry in butter. Serve with bread and salad.

Some of you may find this low on your list of recipes to try, but slugs are attracting the interest of at least one celebrity chef [2] and they are a source of protein that is readily available. Hugh Fearnley-Whittingstall recommends slugs cooked in a tomato sauce [2].

Less familiar to us than terrestrial slugs are those that live in the sea and these are not easily gathered in quantity, so are unlikely to be utilised widely as food. There are reports of sea slugs being eaten by humans, but these accounts arise from confusion with sea cucumbers (holothurian echinoderms) that are eaten in many parts of the World. Holothurians formed part of the famous dinner of the Acclimatization Society in 1862 where views on flavour and consistency were mixed [3]. However, true sea slugs are now finding their way on to speciality restaurant menus [4] – and note that the article refers to them as "trash from the sea". It is an unfortunate term for remarkable and beautiful animals.

It was a sea slug, Marionia sp, that I "adopted" at the UCL Grant Museum of Zoology [5]. It is mounted with the foot facing the viewer and this was done to allow students, and other observers, to see the dimensions of the foot and thus the area in contact with the substratum (see above left).  Unfortunately, preservation in spirit removes pigment and the living specimen would have been light orange in colour, providing camouflage (see above right). Reference to the Sea Slug Forum [6] shows the range of sea slugs and some of their extraordinary adaptations and beautiful colours. These colours are not for our appreciation, of course, although a Creationist might disagree, but to provide warning or camouflage. Warning of what? I'll come to that question, but first we need to know a bit more about the body plan of sea slugs and how they are different to snails.

During evolution, some of the internal organs of gastropods underwent torsion, with the gut opening forward into the mantle cavity at the shell entrance. Slugs, including sea slugs, have undergone de-torsion, with the anus being towards the rear, nearer to their ancestral positions. The anterior end of the gut of snails and slugs features a rasping tongue, or radula, and this is used to remove food from the surface of stones or vegetation, or for scraping away the tissue of living plants and animals. Marionia feeds on corals [7] and the Grant Museum specimen, labelled Marionaria quadrilatera (but actually Marionaria blainvillea) would have fed on these colonial animals while living in the Mediterranean Sea.

A characteristic of corals is the ability of individual polyps to retract and to use stinging cells as a means of catching food, just like their relatives the jellyfish (many corals also generate their own food by harbouring algal cells within their tissues). The stinging cells, or nematocysts (see below), have a trigger that releases a thread through which toxins are injected to immobilise prey, a series of small barbs holding the thread into the tissue. They also serve in defence and a grazing sea slug will be at risk of being attacked by these stinging threads as they eat the coral tissue, even when polyps are retracted. The evolution of stinging cells in coelenterates is an amazing adaptation, but there are some sea slugs that eat coral tissue without the nematocysts discharging. Not only that, intact cells can be moved to extensions of the body, called cerata, on the back of the sea slug through branches of the gut that extend into the projections. Any animals attacking these sea slugs now receive stings from coral nematocysts and the bright colour of the molluscs probably acts as a warning.

Slugs may not appeal to everyone, but we should all be amazed at some of their adaptations. How these evolved can only be speculated upon, but there are few examples in nature as extraordinary as the evolution of nematocysts by coelenterates, followed by their hijacking by some sea slugs. It's worth thinking about if you feel tempted to eat some.

[1] http://www.eattheweeds.com/are-slugs-edible-what-about-snails-2/

[2] http://www.telegraph.co.uk/foodanddrink/foodanddrinknews/5556313/Eat-slugs-in-tomato-sauce-says-television-chef-Hugh-Fearnley-Whittingstall.html

[3] G.H.O.Burgess (1967) The Eccentric Ark: The Curious World Of Frank Buckland. New York, The Horizon Press.

[4] http://www.dailymail.co.uk/femail/article-2349140/Sea-slugs-tuna-spines-make-way-restaurant-menus-chefs-ditch-expensive-fish-cheap-trash-sea.html

[5] http://www.rwotton.blogspot.co.uk/2015/07/two-wonderful-museums-and-mention-of.html

[6] http://www.seaslugforum.net/

[7] http://www.seaslugforum.net/showall/mariblai

The UCL Grant Museum of Zoology gave permission for me  to use the photograph of the preserved Marionaria specimen.

Shells, floats and an interesting association

I grew up by the sea and always enjoyed walking on local beaches looking for shells washed up by the tide. There were many shell fragments, especially of cockles that must have grown in their millions just offshore, but also a wide variety of whole shells, especially those of snails. I continued to enjoy beachcombing and, while on a family holiday in Jersey, found an excellent beach, dominated by shells of the flat periwinkles Littorina obtusata and L. mariae. [1] Some were bright yellow, others orange, white, or of a reddish hue. We collected as many of the shells as we could and, more than twenty years later, they are still exhibited in a glass jar in our bathroom.

Occasionally, violet shells from the snail Janthina are washed up on beaches, especially after long periods of strong winds. They are similar in form to those I had collected in Jersey, but they have less strengthening than the Littorina shells, which need to be strong to withstand the erosive action of the water, and suspended mineral particles, over the shores on which the snails live. Can we assume, therefore, that Janthina exists in a less erosive habitat? Indeed it does - the snails live at the surface of oceans, attached to a float of bubbles.

 

In July and August 1954, there were sustained, strong westerly winds in Great Britain and Ireland and several people reported finding large numbers of Janthina shells on exposed beaches This prompted Dr Douglas P. Wilson of the Marine Biological Association to write a letter to The Times to ask readers for more information about sightings. Reports came in from many locations and, among all the shells, there were a few living specimens. These offered the scope for investigations of the formation of the float, adding to the information acquired by earlier investigators. 

Among the first to make observations was Reynell Coates, who, in 1825, published a description of the float. Coates qualified as a medical doctor in Philadelphia and then set sail as a ship’s surgeon on a voyage to the East Indies. He was very interested in Natural History and took samples of organisms from the surrounding water (presumably when becalmed, or unable to continue the passage - the journey terminated at Kolkata after the outbreak of the Burmese War [2]). This is what he wrote about some specimens of Janthina:

Individuals being placed in a tumbler of brine, and a portion of the float being removed by the scissors, the animal very soon commenced supplying the deficiency in the following manner: the foot was advanced upon the remaining vesicles, until about two-thirds of the member rose above the surface of the water; it was then expanded to the uttermost, and thrown back upon the water.. ..it was contracted at the edges, and formed into the shape of a hood, enclosing a globule of air, which was slowly applied to the extremity of the float. A vibratory movement could now be perceived throughout the foot, and when it was again thrown back to renew the process, the globule was found in its newly constructed envelope. [3]

Wilson’s  description of float formation in Janthina included these observations:

Sometimes the new bubble fails to be attached and floats away as a tiny glassy sphere.. ..The completed float is firm between the fingers, springy and dry - it is not in any sense sticky. [4]

Although the bubbles are surrounded by mucus secreted from glands in the snail’s foot, there are clearly components of this secretion (proteins?) that, after dehydration of the mucus mass, form a solid coating for the trapped bubbles. This ensures that the float is near-permanent, although older pieces break off and need to be replaced. [4] To say that the float is important for the snail is an understatement as, specimens of Janthina that sink into the water column cannot regain the surface. [4]

Janthina is a predator and feeds on other members of the floating community at the air-water interface. It is especially associated with Velella (the “by-the-wind sailor”) [3], and both are blown ashore in masses. Velella is a colonial relative of jellyfish, with polyps attached to a secreted, flattened float that has a sail rising from it (see below), allowing the colony to be transported by wind. The polyps use stinging cells to capture small creatures from within the water column, such as invertebrates and small fish. Wilson quotes Mr Peter David in describing the manner in which Velella is preyed upon by Janthina, the snail cutting out semicircular pieces of the float and attached polyps “in much the same way as a caterpillar does on the edge of a leaf.” [4]

Gastropod snails, like Littorina and Janthina, have very similar body plans and it is relatively easy to see how the latter evolved from a shore-dwelling ancestor, but how did it develop an ocean-going existence? Observation of pond snails shows that some individuals move across the underside of the water surface while the foot is held in the surface film and, to these snails, the interface is like a solid surface. [5] They move here as they do over the substratum, using muscular contractions of the foot, and feed as they go. A characteristic of pond snails is their relatively thin shell, as strengthening calcium salts are not as available in fresh waters as they are in the sea. It is likely that the ancestral Janthina did not strengthen the shell in the way that Littorina does and that it moved under surface films as well as over the substratum, just like some pond snails. In time, the mucus used for lubrication and attachment during crawling was used to coat bubbles formed by the foot and this resulted in the development of the float. They then lost the power of locomotion, or it was highly reduced, and their feeding changed from scraping materials from surfaces to the removal of sections of prey such as Velella, into which they had drifted, or which had been blown towards them.

How Velella evolved its current form is a mystery. There are various theories on how gastropod molluscs evolved from their ancestral molluscan form, but how did the colony of polyps develop, complete with a float to which they were attached? Velella has many sedentary colonial relatives (members of the Cnidaria), but how did life at the ocean surface begin - and what were the origins of the sail?

[1] Gray A. Williams (1990) The comparative ecology of the flat periwinkles, Littorina obtusata (L.) and L. mariae Sacchi et Rastelli. Field Studies 7: 469-482.

[2] W.J.Snape (1968) Reynell Coates (1802-1886): politician, poet, editor, naturalist, lecturer and physician. Transactions and Studies of the College of Physicians of Philadelphia 35: 112-118.

[3] Reynell Coates (1825) Remarks on the floating apparatus, and other peculiarities, of the genus JANTHINA. Journal of the Academy of Natural Sciences of Philadelphia 4: 356-360.

[4] Douglas P. Wilson and M. Alison Wilson (1956) A contribution to the biology of Ianthina janthina (L.). Journal of the Marine Biological Association of the United Kingdom 35: 291-305.

[5] Roger S. Wotton and Terence M. Preston (2005) Surface films: areas of water bodies that are often overlooked. BioScience 55: 137-145.

Impressive sea foams

Ten years ago, I had a holiday in Denmark with my wife and daughter and we spent a few days in the wonderful city of Copenhagen. As we wandered along the waterfront, I noticed that there were large amounts of foam accumulated at one end of a dock and I started explaining (how typical of an academic) that this was the result of natural processes and not pollution. We were surprised to then turn round and find a TV crew just behind us. The reporter had been sent to cover the appearance of the foam and she had overheard my comments and asked me to talk about the origins of the foam to camera. I explained that, although the accumulations look unpleasant, they disperse and do not usually create a bad odour.

In contrast to this small accumulation in Copenhagen, sea foams can be of much larger dimension, creating banks of foam over a metre deep on shore, with winds carrying the flocs inland. One genus of algae is well-known as the origin of foams - Phaeocystis. These algae are found as single cells or, commonly, in large groups embedded in a globe of transparent mucus (see below). When nutrients are plentiful, and when day length increases, the excellent conditions for algal growth result in blooms. Excess carbohydrate, resulting from photosynthesis, is exuded from the cells to form a field of exopolymers ¹ around each cell and, in Phaeocystis, the exudates from cells combine and a globe of mucus results, in which individual algae become embedded. The globe protects individual cells from capture by herbivores and acts as a means of retaining nutrients close to each cell. As the mucus consists largely of water bound within a matrix of carbohydrate to give structure, it is energetically cheap to produce. ¹

So, how does Phaeocystis contribute to masses of sea foam? Let’s begin with an analogy. When we make meringue, we whip transparent egg whites (mainly protein in water) to include air, and the masses of tiny bubbles that we create are trapped within the developing meringue, each coated by some of the protein. The trapped bubbles then give the whole its white appearance. Now back to Phaeocystis. When huge numbers of globes at, or near, the surface of the sea are whipped up by waves, the mucilaginous colonies are broken up and their organic matter covers bubbles, so the whole becomes whisked into foam. The more algae, the more foam, and it is easy to see how this light, floating mass can then be blown ashore. Like all foams, it consists largely of gas and is white because of all the bubbles that are included, although green or brown colouration sometimes occurs. This is because algae or brown organic compounds are also bound into the mass, or become stuck to its surface.

All surf creates foams because bubbles are covered with the organic matter that accumulates at the water surface and this means bubbles do not collapse instantly, like those produced by shaking tap water vigorously, for example. We’ve all seen the white masses of coated bubbles that form when waves break, but the huge accumulations that can occur after Phaeocystis blooms are in a different league.

¹ Roger S Wotton (2005) The essential role of exopolymers (EPS) in aquatic systems. Oceanography and Marine Biology: An Annual Review 42: 57-94.