Thursday, 24 September 2015

The evolution of a fascinating mutualism

How did mutualisms between individuals of different species develop? These associations take many forms, but some symbioses evolve so that dependence results; the best known examples being lichens, where fungi and algae live together to mutual advantage.

A symbiosis is found between a species of hermit crab, Pagurus prideaux and a sea anemone Adamsia palliata (pictured below, the Adamsia having pink spots), although it is not essential for the survival of each [1]. There are many species of hermit crabs, but all are characterised by having a soft abdomen that is held within a snail shell left behind after the gastropod has died. This is a remarkable association between a living animal and the remains of another and, as an individual crab grows, it leaves one shell and searches for another that is more suitable for its increasing size. The aperture of shells occupied by P. prideaux usually has an individual of A. palliata attached to it, located the entrance in a position where it doesn't have a marked effect on the centre of gravity of the shell.

The advantages of symbiosis between sea anemones and hermit crabs have been reviewed by Gusmão and Daly [2], with the sea anemones benefitting from an increase both in dispersal and in the chance of encountering food; and the hermit crabs being protected against predators by the stinging cells of the sea anemone. So how does the sedentary sea anemone move to the snail shell occupied by the crab? The locating behaviour was described by Philip Henry Gosse, the great nineteenth-century Natural Historian. Here is his observation [3]:

Carefully taking up the shell with the aquarium-tongs, and bringing it close to the surface, but not out of water, I gently dislodged the Adamsia with my fingers, and allowed it to fall prone upon the bottom. I then released the shell with its tenant, and drove the latter towards the spot where the zoophyte lay.

No sooner did the Crab touch the Adamsia than he [sic] took hold of it with his claws, first with one, then with both, and I saw in an instant what he was going to do. In the most orderly and expert manner he proceeded to apply the Adamsia to the shell. He found it lying base upward, and therefore the first thing was to turn it quite round. With the alternate grasps of the two pincer-claws, nipping up the flesh of the Adamsia rudely enough, as it seemed, he got hold of it so that he could press the base against the proper part of the shell, the inner lip. Then he remained quite still, holding it firmly pressed, for about ten minutes; at the end of which time he cautiously drew away first one claw, and then the other; and, beginning to walk away, I had the pleasure to see that the Adamsia was once more fairly adhering..

Long-term attachment is aided by the secretion of chitin, this being a feature of several sea anemones and not just Adamsia. However, the chitin produced by Adamsia forms an extension of the snail shell and, in the following description of the process [4], the reference to chitine and a horny membrane come from the observations of Henry Gosse:

..sea anemones of the genus Adamsia living on gastropod shells inhabited by hermit crabs may extend the shell's lip by secreting what is variously called a cuticle, "chitine", a horny membrane, or solidified mucus.

This is what Gosse wrote in Actinologia Britannica [5]

Very frequently, there is found intervening between the Adamsia and the shell to which it is affixed, a film of membrane, of a horny texture, somewhat brittle, of a translucent dark greenish-brown colour. After death this film is found adherent to the surface of the shell, from which, however, it easily peels when dry.. ..From several specimens.. .. I have been able to learn the nature and object of this membrane.. appears to me manifest that the membrane is a provision for the support of the growing Adamsia.. .. it is composed mainly of chitine, having no calcareous element.. .. The membrane is not invariably present.

Gosse goes on to say [5]:

Pagurus Prideauxii seems to be as dependent on the Adamsia, as the latter is on it.. ..Why one species of Soldier-crab must needs seek the companionship of this Anemone, while other Soldier-crabs are able to live alone; and why this species of Anemone must needs associate with the Soldier-crab, while others kinds of Anemone are solitary, I can by no means answer.

As described above, we now have information of the mutualism and how it benefits both partners. For Henry Gosse (whose beautiful illustration is shown below), the association of the hermit crab and gastropod shells and the mutualism between Pagurus prideaux and Adamsia palliata were yet more wonderful examples of the complexity of God's Creation.

For those of us that believe in evolution, it is fascinating to speculate on the various steps that must have taken place to allow the association between the crab and the shell, and then the crab and the sea anemone. The secretion of chitin by the sea anemone was a pre-adaptation and may have originally been a means of ensuring that broken, or friable, substrata could be colonised. It now results in the secure attachment to snail shells and gives the hermit crab the advantage of changing shells less frequently. How did the crab learn to transplant a sea anemone on to a new shell; and why this one species?

Evolution fills one with a sense of wonder, doesn't it?

[1] R. M. L. Ates (1995) Pagurus prideaux and Adamsia palliata are not obligate symbionts. Crustaceana 68: 522-524.

[2] Luciano C. Gusmão and Marymegan Daly (2010) Evolution of sea anemones (Cnidaria: Actinaria: Hormathiidae) symbiotic with hermit crabs. Molecular Phylogenetics and Evolution 56: 868-877.

[3] Philip Henry Gosse (1865) A year at the shore. London, Alexander Strahan.

[4] Daphne Fautin Dunn and Martin H. Liberman (1983) Chitin in sea anemone shells. Science 221: 157-159.

[5] Philip Henry Gosse (1860) Actinologia Britannica: a history of the British sea-anemones and madrepores. London, Van Voorst.

Wednesday, 16 September 2015

Sea silk – the Natural History of an unusual textile

Anyone preparing mussels for moules marinières [1] is familiar with the beards that need to be pulled free of the closed shell. These beards are more properly termed byssus threads and they are the means by which mussels attach to substrata, allowing them to withstand the effects of waves and water currents. Unlike snails, bivalves do not use their foot for gliding locomotion and, instead, it provides an effective burrowing organ or, in mussels and their relatives, a means of secreting threads and then holding them in tension. The threads are produced from a gland on the foot and pass along a groove, being attached to the substratum and the foot then withdrawn, each proteinaceous thread hardening very rapidly and thus ensuring secure attachment. The bivalve shells are opened by the elastic hinge when the muscles that hold the valves tightly together are relaxed and the mussels then feed on the good supply of suspended food particles brought by tidal flows.

Pinna nobilis, commonly called the pen shell, is a large bivalve that can grow to 1 metre in length and it requires strong attachment by byssus to avoid being moved by currents and to hold the animal upright to allow efficient feeding (an example of a pen shell is shown in the video clip above). Pen shells are found on soft bottoms but are most commonly associated with beds of seagrasses, underwater flowering plants that are anchored into sediments by means of rhizomes [2]. In a study in the Ebro Delta in Spain, Prado et al [3] concluded that:

Seagrass beds have been considered to be the most suitable substrate for P. nobilis, since their rhizomes allow a complex connection between byssus filaments and the sediments. In fact, although individuals were detected in both vegetated and unvegetated areas, higher abundances (by ca. 40%) were observed in areas with 80%-100% cover, thus suggesting that dense meadows may favour the highest abundances of individuals.

In addition to providing ideal locations for attachment, seagrass beds are also highly productive marine habitats and it is likely that these provide an abundance of food for the growing bivalves. The large number of shells also provides good conditions for the colonisation by plants and animals; shells from dead bivalves transplanted experimentally into areas of bare soft sediment readily became colonised by a diverse community of marine creatures [4].  

The natural community of Pinna nobilis, and its associated plants and animals, could not develop if it were not for byssus, recognised increasingly as an important biomaterial [5]. Byssus consists mainly of collagen, a fibrous protein that shares many characteristics with fibroin, the main constituent of insect silk. The most well known insect silk is that produced by silkworms to form a cocoon in which to pupate. The pupae and cocoons are harvested and it is important that these are placed into boiling water to kill the pupae before the adult insects emerge to cut through the threads. The long fibres are unwound and, as they are produced by being exuded through an aperture, they are uniform in both diameter and consistency. Byssus threads, on the other hand, vary in diameter and they are usually elliptical in cross section, a result of their method of production from the byssal gland and byssal groove on the bivalve foot.

It may come as a surprise to know that the byssus of Pinna nobilis is collected, carded and spun to produce a thread used in weaving, knitting and embroidery. Recently, this use was highlighted in an article on the BBC web site [6] that included a portrait of Chiara Vigo, a Sardinian collector, weaver and embroiderer and the strong feeling and respect that she has for byssus. The same attitude is shown by Felicitas Maeder who has a wonderful web site that is packed with historical and scientific information, as well as having an illustrated inventory of many items made from sea silk. If you are interested in the Natural History of this unusual material, an historian of textiles, or an enthusiast for weaving, knitting and embroidery please visit It is a fascinating site and makes one wonder about the evolution of byssus and the ingenuity of humans who saw it as a useful fibre, both for clothing and ornament.


[3] Patricia Prado, Nuno Caiola and Carles Ibáñez (2014) Habitat use by a large population of Pinna nobilis in shallow waters. Scientia Marina 78:555-565

[4] Lotfi Rabaoui, Walid Belgacem, Dorsaf Ben Ismail, Lamjed Mansour and Sabiha Tlig-Zouari (2015) Engineering effects of Pinna nobilis shells on benthic communities. Oceanologia 57:271-279.

[5] J. Herbert Waite and Christopher C. Broomell (2012) Changing environments and structure-property relationships in marine biomaterials. The Journal of Experimental Biology 215:873-883.