The bivalves

Mussels and cockles are the most familiar examples of the Bivalvia and together they display all the major morphological changes undergone by this group of molluscs through their evolutionary history (Fig. 18(a), (b)). Bivalves have adopted a sedentary existence; the mantle forms two broad lateral flaps that completely enclose the body of the animal and secrete a two-piece shell hinged and articulated along its upper, dorsal side. Both head and foot have been drastically reduced: the former is represented simply by elongated lips, or palps, surrounding the mouth, eyes and tentacles being quite absent, while the latter, instead of the solid, flat-soled ancestral shape, is usually round or oval in section, tapered and highly flexible. The triangular shape of the bivalve foot is alluded to in the other Latin name for the class, Pelycypoda, or hatchet-foot. The viscera of a bivalve, its heart, gut and other organs, lie in the dorsal portion of the cavity formed by the enfolding mantle, but the greatest amount of space is occupied by its gills. These are flat sheets of linked rods, folded once or twice, with blood vessels passing along the axes of the folds, and with surfaces thickly covered with cilia. The only other conspicuous structures seen between the two valves of a cockle or mussel are the thick, transverse muscles that hold the shells tightly closed, and whose points of attachment are visible in dead shells as distinct adductor muscle scars (Fig. 18(b)). The hinge area of the shell consists of an elastic ligament, stretched when the valves are closed and serving to open the valves when the adductor muscles relax. Bivalves are predominantly sedentary animals that make a living through filter feeding, and all of their basic morphology can be seen as an adaptation to this simple mode of life. Sensory functions are carried out by fringes of pallial tentacles around the mantle edge and cephalic tentacles are no longer required. Bivalves utilise cilia and mucus to obtain food: no special buccal apparatus is required; water drawn into the mantle cavity filters through the gills and potential food particles are gathered into mucus strings and driven towards the mouth by ciliary currents where they are drawn in by the labial palps. A mechanism probably originating as a system for cleaning the delicate surfaces of the gills is employed in highly efficient feeding among the bivalves.

Their secondarily simplified morphology has not been an evolutionary disadvantage to the bivalves, which have radiated into an impressively varied range of habitats. This adaptive radiation is recorded in corresponding modifications in the form of the shell, which in all bivalve species is the clearest indicator of the mode of living of the animal. Accompanying modifications can also be seen in the soft body parts, especially the mantle edge and the flexible foot. Although molluscs are coelomate animals, in all of them the coelom is very reduced, consisting of just a small fluid-filled cavity surrounding the heart. Blood is pumped from the heart through several short, open-ended arteries and then circulates through channels termed sinuses. These channels, and the muscle sheets surrounding them, constitute the hydrostatic skeleton of the mollusc, and in many bivalves this is coupled with the rigid shell valves and their adductor muscles to form a digging and burrowing mechanism. The earliest bivalve probably evolved for life on or in soft, unconsolidated sea floors and the majority of living species still occupy these habitats, sometimes within the surface layers of sediments, but more often within the substratum as members of the infauna. The dog cockle, Glycymeris glycymeris, is an offshore species, the boldly patterned shells of which are commonly washed up on sandy shores (Fig. 19(a)). Glycymeris is a rather primitive bivalve that can be viewed as the template with which the adaptive radiation of the bivalves began. Its shell consists of identical right and left valves, each with an almost perfectly circular outline, hinged dorsally by two rows of small, interlocking teeth. These simple, taxodont teeth are arranged in each valve in an anterior and a posterior series on either side of the midline of the shell, which is marked by the juvenile shell, developed as a projecting umbo. Each valve is lined by its fold of mantle, and in respiring and feeding both valves and mantle are parted, allowing a flow of water over the gills.

Glycymeris has a rather small foot and moves little, lying on one side among the gravelly sands in which it lives. Cockles live within the intertidal sands they favour, with the anterior margin of the shell downwards and the posterior more or less flush with the surface; incurrent and excurrent water currents pass through a narrow posterior gape and they are kept separate by partial fusion of the posterior mantle edge which defines a pair of short, tubular siphons. The incurrent siphon is closest to the hinge line, thus dorsal to the excurrent one. The distinctive orange foot of the cockle is used in digging, both in a slow probing action which digs the animal deeper into the substratum, and in rapid reflex actions which result in the animal actually jumping from the sand.

The cockle’s way of life can be clearly read from the form of its shell. Compared with those of Glycymeris, its two identical shell valves are quite asymmetrical. The animal lives head down; the anterior margin is shorter than the posterior and the umbones have moved anterior to the midline of the shell valves. The longer posterior margins are slightly incurved, so that the cockle displays an almost flat, heart-shaped profile at the sand surface, with its short, fringed mantle siphons just projecting above it. Its valves are deeply concave, and the animal has a bulbous form, which, together with the bold radiating ribs of each valve, contributes to the stability of the shell, resisting overturn in the swash of the tide. The hinge teeth are also more complex than those of the dog cockle: beneath the umbo in each valve is a group of three differently shaped cardinal teeth (Fig. 19(b)) which interlock with their counterparts in the opposite valve, while anterior and posterior of the umbo the inner face of the shell margins carries long, narrow lateral teeth. This closely interlocking series of teeth is much more efficient than the simple taxodont dentition of Glycymeris in counteracting lateral slippage of the hinge area.

Fig. 19 (a) Glycymeris glycymeris, interior view of the right shell valve. (b) Cerastoderma edule, interior view of the right shell valve. (c) Spisula solida, exterior view of the right shell valve and detail of the left valve hinge teeth. (d) Lutraria lutraria, internal view of right shell valve. (e) Mya arenaria, interior view of left shell valve.

In most species of bivalve the lifestyle of the animal can be, to a considerable extent, inferred from its shell morphology. Trough shells, Spisula species (Fig. 19(c)), and venus shells, such as Chamelea gallina (Plate 6(d)), also live in the top few centimetres of medium to coarse sands, feeding in a similar manner to the cockle. They show the same reduction of the anterior portion of the shell, and the same consequent asymmetry, and the valves are thick, quite concave and often with characteristic ridges and ribs. The hinge area of each valve has an equally complex and tightly interlocking dentition. Tellins, such as the largely intertidal Angulus tenuis (Plate 6(e)), are thin-shelled clams generally associated with fine, muddy sands, and live within the top layers of the sediment, lying on one side. Their valves are less asymmetrical than those of most venus shells, but are often slightly dissimilar: the animals are said to be inequivalve. One valve may have a different outer sculpture from the other, or part of the posterior margin may be twisted or curved to one side. The two mantle siphons are separate, very long and extremely flexible and may be completely retracted into the shell. In feeding, the exhalant siphon is held directly upwards while the inhalant siphon may be directed horizontally into the flow of bottom water, or may wander over the surface of the sand sucking in material deposited on the sediment. Scrobicularia plana, the absurdly named ‘peppery furrow shell’, lives in muddy estuarine or brackish water habitats burrowed headfirst some 10 centimetres or so into the sediment. Dead shells are easily found where they accumulate in drainage channels, but the live animal is only discovered through the star-shaped pattern in the mud surface centred on its respiratory channel (Plate 7(b)), showing where its long, slender inhalant siphon has repeatedly contracted following a period of deposit-feeding.

Razor shells can be found on almost any fully marine sandy beach, and when fresh are beautifully glossy (Plate 7(c)). As they dry and age this outer patina disappears as the organic layer responsible for it, the periostracum, cracks and peels to uncover a rather dull shell. This silky periostracum aids the astonishingly rapid movement of the razor shells in their burrows. They are very active animals living in deep vertical tubes in the sand, moving to the top to protrude two short, fused siphons for suspension feeding, but rocketing the half-metre or so to the bottom of the tube when disturbed. Apart from their smooth, low friction exteriors, razor shells are enabled to move so swiftly through special adaptations of their soft body parts. In most bivalves the two opposing mantle flaps are fused to some degree, at the very least forming short fused siphons as seen in cockles. In razor shells the mantle flaps are almost completely fused together; the short anterior end is elaborated to form the siphons and the equally short posterior edge has a small gap for the protrusion of the animal’s powerfully muscular foot. Abrupt muscular contraction closing the shell valves ejects the water held in the mantle cavity and effectively jet-propels the animal downwards. Otter shells, Lutraria (Fig. 19(d)), and gaper clams, Mya (Fig. 19(e)), also live deeply buried in sediment, but these large, heavy-shelled animals move very little; instead, they possess long, very muscular, extensile siphons which reach the length of the burrow to just protrude at the surface. Fully contracted, they form a thick, wrinkled mass almost as large as the rest of the animal, and cannot be withdrawn into the shell valves.

Mussels are sedentary for much of their lives, attaching to solid surfaces, or to other mussels, with strong elastic byssal threads. In these bivalves the anterior end has been so reduced that the umbones lie at or close to the pointed anterior shell margin, and beyond the dorsal hinge the shell margin consists of a continuous posterior and ventral edge. Despite their apparently sessile habit mussels are surprisingly mobile. Juveniles actively migrate, casting off from their attachment and drifting from a parachute of byssal threads, while adults detached from their base are quite able to re-attach if the opportunity offers. Oysters, saddle oysters and some small scallop species attach permanently to their chosen substratum, cementing themselves firmly as they grow, while other scallop species have taken to a roving existence, swimming just above the sea bottom by shell-clapping. In oysters and scallops, shells are usually inequivalve, but each valve is often more or less equilateral; the mantle edges are unfused and there are no siphons.

The range of morphological adaptation displayed by bivalve molluscs is extraordinary for such apparently simple animals. Apart from the major types noted above, there are rock-boring species such as Hiatella arctica (Fig. 20(a)), the pink-rimmed siphons of which are conspicuous on shaded limestone surfaces on the lower shore. Fragile, white, delicately ridged shells of the clay-boring piddock, Pholas dactylus (Fig. 20(b)), are common on sheltered, muddy shores, and timber bored by shipworms, Teredinidae, can be found through the year on most British coasts. A moderately rich intertidal sandy habitat might yield perhaps 20 species of infaunal bivalve, including a number of tiny commensal species living in association with sea urchins, sea cucumbers and burrowing prawns. Bivalves are not quite so evident on rocky shores, but are nonetheless equally diverse, including several small species of mussel, apart from the almost ubiquitous Mytilus edulis, and several crevice-dwelling species including the tiny reddish Lasaea adansoni, which can occur in dense populations among high-shore seaweeds.

Reproduction is a fairly simple business among bivalves. In most species sexes are separate, but distinguished with difficulty only by the colour or texture of the gonads; the great scallop, Pecten maximus, queen scallop, Aequipecten opercularis, and the common saddle oyster, Anomia ephippium, are among the minority of hermaphroditic species. There are no specialised sexual organs. Eggs and sperm are simply shed into the mantle cavity, and in most species are carried out with exhalant currents, with fertilisation occurring in the sea around the parents, and the eggs developing into planktonic larvae. This potentially wasteful process is regulated to a certain degree. Spawning in most species is initiated by a temperature trigger and is usually synchronous within populations. The common oyster, Ostrea edulis, is one of an interesting minority of bivalves that further reduces reproductive loss by brooding its eggs within the mantle cavity. Sperm shed by the males are gathered by the inhalant currents of the females and fertilise their eggs within their mantle cavities. The females eventually shed their offspring as advanced veliger larvae that spend some weeks in the plankton before settlement. Brooding also occurs in Tellimya ferruginosa, which lives as a commensal in the burrows of heart urchins; presumably, swimming veliger larvae are at less risk of loss than freely broadcast gametes. In two specialised rocky shore species, Lasaea adansoni and Turtonia minuta, the larval stage is completely suppressed. Both species live high on the shore, in crevices and among barnacles and Lichina, and among Corallina and Mytilus lower down, and avoid over-dispersal by retaining developing embryos on the gill lamellae and releasing fully formed juveniles. In Turtonia minuta sexes are separate, but Lasaea adansoni is a self-fertilising hermaphrodite that seems to reproduce parthenogenetically; sperm serve merely to activate development of the egg, and there is no fusion of male and female gametes. On a shore in North Wales, L. adansoni was found to exist as three separate and genetically unrelated clonal populations at three different tidal levels. There is one curious aspect of bivalve reproduction, a tendency for sex reversal, which is seen commonly throughout the class. Most frequently young animals mature first as males, changing within just two or three seasons to females, which may continue to grow and breed for many more years. It is possible to see a benefit in larger, more productive animals producing eggs while the smaller produce energetically less expensive sperm. However, among some scallop species, and in oysters, sex reversal continues annually and each individual is alternately male and female through much of its life, and the advantage in this is less obvious.

Fig. 20 (a) Hiatella arctica, interior view of right shell valve (above) and exterior view of left shell valve (below). (b) Pholas dactylus, interior view of left shell valve (above) and exterior view of right shell valve (below). Scale bars = 10 mm.

Newly settled from the plankton, the juveniles of most bivalve species are just a few tenths of a millimetre in length. Initial attachment and stabilisation is achieved using sticky byssal threads secreted by the foot, but the first site of settlement need not be the final. Cockles and other soft substratum infaunal species may disperse following settlement, secreting loose byssal threads that drift the young animals across the surface of the sea bed, and even normally sedentary animals, like the mussels, may cast off their first byssus and creep on the sole of the foot to new sites before finally securing themselves.

Ever-evolving spirals: the gastropods

The Gastropoda is the largest class of molluscs with more than 50,000 species known worldwide and at least 200 present on British and north European coasts. They are far less conservative animals than the bivalves, with shells that display an amazing variety of size, shape and colour. Gastropod shells are among the most intricate and beautiful objects found on the seashore. While bivalves are pre-eminently sedentary, and largely infaunal in habit, gastropods are principally active, epifaunal animals. A satisfying diversity of species can be found on soft shores of sand or mud, but the greatest variety is seen on rocky shores. The earliest mollusc was probably a type of gastropod, perhaps resembling a modern limpet, with a broad-soled foot and a low conical shell. The evolutionary success of the group may be attributed to two major morphological features especially characteristic of the gastropods. First of these is the feeding apparatus, the radula (Fig. 21(a)). The number of radular teeth, and their structure, varies between different gastropod types. Each transverse row consists of a single large central tooth, the rachidian, flanked on each side by slightly smaller lateral teeth, and usually larger marginal teeth. Six major types of radula are recognised, characterised by the number of each type of tooth in a transverse row; they are helpful in the classification of the Gastropoda, but more interesting when related to the mode of feeding of different kinds of gastropods. The second major morphological feature of the Gastropoda is less obvious, but important in describing and understanding the adaptive radiation of the class; it is the phenomenon referred to as torsion. All gastropod larvae undergo torsion at an early stage in their development: the visceral hump of the larval snail rotates through 180° to bring the primitively, and embry-ologically, posterior mantle cavity into an anterior position immediately above the head of the animal (Fig. 21(b)). The evolutionary advantages of torsion are still argued over; one consequence is that in withdrawing into its shell, the vulnerable head of the animal precedes the more robust foot, which now seals the opening of the shell. An equally important consequence is that the gills, and chemosensory organs called osphradia, contained within the mantle cavity, now benefit from a stronger inflow of water as the animal moves forward. Whatever its initial advantages, torsion and its consequences have had a profound influence on the subsequent evolution of the gastropods.

Fig. 21 (a) A single transverse row of radular teeth in the limpet, Patella vulgata (left) and the periwinkle, Littorina littorea (right): R = rachidian tooth; L = lateral teeth; M = marginal teeth. (b) Position of the mantle cavity (MC) in a hypothetical ancestral gastropod (left) and a modern prosobranch (right).

There are three major divisions of the Gastropoda. The Pulmonata are essentially terrestrial or freshwater animals and include the slugs, garden snails and pond snails. They may be shelled or not, but in all the gills have been lost and the mantle cavity serves as a lung. Several pulmonate species have returned to the seashore, but being air-breathing are limited to its upper reaches and cannot withstand prolonged immersion. On Cornish coasts the warty green sea slug Onchidella celtica (Plate 7(d)) is often seen as the tide recedes emerging from damp crevices high on rocky shores and browsing the recently uncovered surfaces. Onchidella is a representative of a successful and widespread group of pulmonate sea slugs, but in extreme southwest Britain the group reaches its northern limit in the east Atlantic, perhaps restricted by an inability to tolerate winter freezing. More common are the opisthobranch sea slugs, the second subclass of the Gastropoda. These attractive, mostly shell-less animals are entirely marine in distribution. However, the largest subclass is the Prosobranchia, the marine snails that abound on all rocky coasts, and this will be considered at some length. Prosobranchs are undoubtedly the most successful molluscan group; they occur in every marine habitat, including the pelagic realm, have invaded fresh waters, and include species that live essentially terrestrial lives at the furthest edge of the sea’s spray.

The simplest prosobranchs are the Order Archaeogastropoda, or diotocardian snails, and among these one finds animals that are perhaps not too different in form from their earliest ancestors. Top shells, limpets, slit limpets, keyhole limpets and ormers all belong to this prosobranch order, and they include some of the most abundant gastropod species on British seashores. The common limpet, Patella vulgata (Plate 7(e)), abounds on all rocky shores, from the most exposed to weedy shores in extreme shelter. Like almost all archaeogastropods it is a strictly intertidal species, ranging scarcely at all below the lowest level of the tide. The china limpet, P. ulyssiponensis, is externally similar to the common limpet, but is distinguished by the sole of its foot, which is a rich apricot colour. On moderately exposed shores, where encrusting coralline algae manage to secure living space the much smaller tortoiseshell limpets, Tectura virginea and T. tessulata, may be common low on the shore, though never achieving populations as dense as those of the common limpet, and the delicate blue-rayed limpet, Helcion pellucidum (Plate 7(f)), can be found wherever its principal algal habitats, Laminaria digitata and L. hyperborea, occur. The limpet shell form, a low, broad-based cone, is probably a very primitive prosobranch feature, but the earliest limpets were perhaps more similar to the slit limpets, such as Emarginula (Fig. 22(b)), which has a long fissure at the front of the shell, or the keyhole limpets, such as Diodora (Fig. 22(a)), with a hole at the shell’s apex. In these little limpets the mantle cavity bears paired gills and osphradia, and respiratory currents entering to the right and left of the snail’s head exit either through an anterior slit in Emarginula, or through the apical hole in Diodora. In both cases this perhaps resolves one awkward problem, namely that of sanitation. While the mantle cavity contains the most sensitive of the limpet’s external organs, it also houses the anus and the openings of the kidneys, and directed currents obviously carry waste material away from the delicate gill surfaces. However, a holed shell poses problems; water loss cannot be easily prevented, and predators find a site of entry. Patellid limpets have solved the problem without weakening the integrity of their shells; they have dispensed with, and lost, the mantle cavity gills and instead respire by means of secondary pallial gills present beneath the mantle skirt along the edges of the foot.

Fig. 22 (a) The keyhole limpet, Diodora graeca. Scale bar = 15 mm. (b) The slit limpet, Emarginula fissa. Scale bar = 5 mm.

The other major archaeogastropod group found on the shore is the top shells, Family Trochidae, especially exemplified by the common species, the grey top shell, Gibbula cineraria (Plate 8(b)), the flat top shell, G. umbilicalis (Plate 8(c)), and the exquisitely coloured painted top shell, Calliostoma zizyphinum (Plate 8(a)). Top shells have lost the right gill and osphradium, perhaps as a consequence of their coiled shell, and respiratory currents passing into the left side of the mantle cavity first bathe the remaining gill before flowing out of the right side, over the anus and kidney openings. However, like all other diotocardians, top shells retain the paired kidneys and renal openings of primitive gastropods.

Archaeogastropods are a successful group of intertidal snails. In the most primitive types, the slit limpets and top shells, the radula is of a kind termed rhipidoglossan: each tooth row consists of a central rachidian, flanked on each side by seven lateral teeth and very large numbers of long, slender marginal teeth. The radular teeth are scarcely mineralised and function simply to sweep detrital particles into the animal’s mouth. Patellid limpets have lost their marginal teeth, and often the rachidian as well, and the short rows of hard lateral teeth, termed docoglossan, are employed in scraping or, in conjunction with a hardened pad on the roof of the mouth, in cutting algal shoots. Sexes are separate in all archaeogastropods, but reproduction is a simple business. Eggs and sperm are shed in synchrony, fertilisation and development occur in the sea, and the larva spends some weeks in the plankton before settling on a suitable surface. To achieve successful breeding, species are constrained to live in dense populations and to attune their reproductive cycles to environmental cues; they are especially adapted to intertidal life, but are found rarely beyond the influence of the tides.

The Order Mesogastropoda includes all the most familiar sea snails, and is taxonomically the most diverse of the three prosobranch orders. Together with the Neogastropoda, they are sometimes termed the monotocardian prosobranchs, in which the right gill, osphradium and kidney have disappeared. Mantle sanitation is effectively achieved, with the respiratory current entering on the left and the effluent stream exiting on the right, and the remnant of the right kidney contributes to a reproductive system much more complex than that of the archaeogastropods. Throughout the monotocardian prosobranchs there has been a strong evolutionary trend towards reproduction that involves copulation, and the production of egg cases and capsules, the internal brooding of embryos, and even ovoviviparity. The flexibility and adaptability of monotocardian reproductive systems, together with an extraordinary radiation of feeding modes, has resulted in an equally extraordinary array of species. The most abundant and conspicuous mesogastropod snails on rocky shores are grazers and browsers, and together with the patellid limpets they are the most significant factor structuring intertidal seaweed communities. Predominant among these are the periwinkles, small, robustly shelled snails constituting the Family Littorinidae. On moderately sheltered shores with a good covering of brown seaweeds, populations of the common periwinkle, Littorina littorea (Plate 8(d)), may number hundreds per square metre of rock. The radula of L. littorea is of the type termed taenioglossan, in this case with one lateral tooth and two marginals on each side of the rather broad rachidian. The teeth are all stout, with cusped tips suited to cutting fine textured green algae and young sporelings of fucoid algae. The delicate green sea lettuce, Ulva lactuca, owes its ephemeral existence to the voracity of limpets and winkles. Large plants persist in deep pools not emptied by the tide, from which molluscan grazers are excluded by predatory crabs and fish, but on intertidal rock surfaces the spring flush of Ulva is swiftly removed by grazing. In extreme shelter, Ascophyllum nodosum may come to dominate the middle regions of the shore. Large, old Ascophyllum plants are too tough a prospect even for the common periwinkle, but the flat periwinkle, Littorina obtusata, flourishes among them, perhaps feeding partly on the delicate growing tips of the plants, but probably principally on the microalgae and diatoms that teem on the surfaces of all large seaweeds. Among dense blankets of eggwrack, yellow, green and brown-chequered flat periwinkles may occur in hundreds per square metre. Downshore, where the Ascophyllum thins out, there is usually a band of the serrated wrack, Fucus serratus, which supports populations of another flat periwinkle, Littorina fabalis, thinner shelled and rather smaller than L. obtusata, but otherwise very similar in appearance. Littorina is an extremely diverse genus. On barnacled areas of the upper shore the rough periwinkle, L. saxatilis (Plate 8(e)), can be found, grazing microalgae on damp rock surfaces. It achieves peak abundance on moderately exposed rocky shores, and as wave exposure increases towards headlands it is joined by several smaller species, most frequent of which is the tiny, dull black Melaraphe neritoides (Fig. 23(a)), which lives high in the splash zone among cthamalid barnacles.

The Mesogastropoda are rather more sophisticated snails than the Archaeogastropoda, especially in the matter of sexual reproduction. Rather than shedding eggs and sperm directly into the sea, mesogastropods conserve their reproductive products, ensuring fertilisation by copulation and enclosing their eggs in gelatinous capsules. Littorina littorea and Melaraphe neritoides display what is probably the primitive condition, releasing pelagic egg capsules from which hatch planktonic veliger larvae. This is still a hazardous undertaking, but has the advantage of dispersing eggs and larvae widely, and both of these species of periwinkle can be found in suitable habitats around the whole of the northwest European coast, from Brittany to the North Cape of Norway. Other species of winkle either attach their egg capsules to a firm surface, or brood them within the mantle cavity of the female until they hatch as crawling juvenile snails. These different reproductive strategies have interesting consequences for the population genetics of Littorina species. The widely dispersing eggs and larvae of L. littorea and Melaraphe neritoides ensure that there is continual outbreeding and genetic mixing, and populations of both species show little genotypic or phenotypic difference across much of their geographical range. Conversely, populations of rough periwinkles are often reproductively isolated and reduced gene flow leads to adaptation to local conditions; L. saxatilis shows an extraordinary range of colours and forms, many apparently characteristic of particular, quite narrowly defined habitats.

While the littorinid snails are among the most ubiquitous and conspicuous of the intertidal mesogastropods, an enormous number of smaller, less obvious, species abound on seaweed-covered shores, some of them in numbers equal to those of the winkles. Delicate, hemispherical or ring-shaped, gelatinous egg cases glued to fronds of Fucus belong to the two chink shells, Lacuna vincta (Fig. 23(b)) and L. pallidula (Fig. 23(c)): neither grows larger than 10 millimetres, but both may exist in populations of thousands per square metre on suitable shores. The ring-shaped egg capsule of L. vincta may contain as many as 1,000 eggs; these hatch as free-swimming larvae that may spend two or three months in the plankton before settling on their favoured food plant. The eggs of L. pallidula complete larval development within the egg capsule, and juvenile snails emerge ready to begin feeding on the Fucus serratus plants the population is usually restricted to. As fucoid algae are replaced by shrubby red algae in more exposed habitats, a new community of tiny snails appears. Many of these are just a few millimetres in length and not easily seen in the field; however, a tuft of an alga such as Ceramium rubrum, Lomentaria articulata or Plumaria elegans, gently rinsed in a bowl of seaweed, will shed sometimes hundreds of minute snails, particularly the red banded Barleeia unifasciata (Fig. 23(d)), and species of Rissoa, Alvania and Cingula, all of which require a good hand lens and considerable patience to identify. Most of these minute mesogastropods feed on silt, diatoms and other microorganisms trapped by or growing on their host plants, but a few, such as Cerithiopsis, are specialists, feeding on sponges growing around the bases of the seaweeds.

Fig. 23 (a) Melaraphe neritoides. (b) Lacuna vincta. (c) Lacuna pallidula. (d) Barleeia unifasciata. (e) Trivia monacha. Scale bars = 2.5 mm (a–c), 0.5 mm (d), 5 mm (e).

While diet and feeding mode vary widely among the mesogastropods, few coastal species have adopted carnivory. However, these few include several interesting species. The two cowrie species common on northwest European shores, Trivia arctica and T. monacha (Fig. 23(e)), feed exclusively on encrusting colonial sea squirts, especially the brightly coloured Botryllus schlosseri and Botrylloides leachi. Neither is found very far from its prey organism, and during summer months female cowries tuck their egg capsules into cavities chewed in the sea squirt colony. Necklace shells, species of Polinices, are usually the only mesogastropods commonly found on sandy shores; their glossy globular shells are especially beautiful. Necklace shells are hunting carnivores; the snail has a large, muscular foot and ploughs through the top few centimetres of sediment in search of shallow burrowing bivalves. Tellins, wedge shells and trough shells are particularly favoured by Polinices, and encountering one the necklace shell envelops and immobilises it with its foot preparatory to commencing feeding. To do this, it must first penetrate the bivalve’s shell. In common with most predatory prosobranchs, the mouth of Polinices is borne on the end of a flexible proboscis and opens to reveal a radula with short rows of relatively large teeth. These are effective at scraping through the mineralised layers of shell, but their effect is enhanced by acid secretions from a glandular pad on the underside of the proboscis, close to its tip. At intervals the snail lifts the tip of the proboscis and presses the gland into the developing hole, softening the shell. Alternating radular rasping with acid solution the snail eventually drills a neat, circular hole with regularly chamfered edge, usually through the broad dorsal region of the bivalve, close to the umbo. The tip of the proboscis is then inserted and the radula begins cutting and tearing the flesh of the prey. Polinices catenus and P. polianus (Fig. 24(a)) are the two most common necklace shells on Britain’s beaches; the animals themselves are quite conspicuous, if sparsely distributed, remaining only partly buried as the tide recedes, but their presence is equally often attested to by accumulations of bivalve shells with the telltale chamfered hole drilled close to the umbo. The egg masses of necklace shells are perhaps even more conspicuous than the snails. Eggs are deposited in small round capsules, and hundreds of capsules are glued together with mucus and sand grains in broad strap shapes, 2 centimetres or more wide, formed into spiralled or collar shapes 5 centimetres or so in diameter. Not all of the thousands of eggs laid by a female necklace shell will hatch, most instead providing food for the few which do develop into juvenile snails.

Fig. 24 (a) Polinices polianus. (b) Thin-shelled specimen of Nucella lapillus. (c) Thick-shelled specimen of Nucella lapillus. (d) Ocenebra erinacea. (e) Urosalpinx cinerea. (f) Buccinum undatum. Scale bars = 5 mm (a), 10 mm (b–e).

The most advanced prosobranchs constitute the third order, Neogastropoda, sometimes called the Stenoglossa. There are relatively few neogastropod species that achieve abundance between the tides, but they include the dog whelk, Nucella lapillus (Fig. 24 (b), (c)), which may be extremely common on barnacled shores. The dog whelk is particularly interesting in being largely limited to the British Isles, and in being entirely intertidal in distribution. It has also raised concern through its susceptibility to organotin compounds formerly prevalent in marine paints, and has proved to be a sensitive indicator of environmental contamination. Neogastropods are typically whelk-shaped; the tapered, spired shell has a relatively large body whorl; the aperture is usually bounded by flared, often thickened lips, and at its distal tip is drawn out into a channelled or enrolled canal, supporting or enclosing a very long, very flexible and retractile siphon. Neogastropods are adapted for carnivory or carrion feeding and the siphon is important in locating food, and drawing water into the mantle cavity and across chemosensitive organs. Nucella and its allies, the oyster drills Ocenebra erinacea (Fig. 24(d)) and Urosalpinx cinerea (Fig. 24(e)), like necklace shells, use a combination of radula and acid glands to break through the defences of the barnacles and bivalves on which they feed, but in their case the acid secretory gland, the accessory boring organ, is situated on the sole of the foot. At low tide dog whelks are usually found in groups on shaded, vertical surfaces, but solitary individuals clamped over isolated mussels or barnacle patches have suspended feeding activities during the tide’s recess, and peeling one off will reveal the developing hole in its selected prey.

The neogastropod radula typically bears three stout teeth in each row, suited to ripping and tearing its food. Whelks and oyster drills are selective carnivores, but the common whelk, Buccinum undatum (Fig. 24(f)), which, curiously, is esteemed as seafood by some portions of humanity, is a thorough-going scavenger, feeding on any animal carcass it encounters. Buccinum is predominantly subtidal in distribution, but juveniles up to 1 centimetre in length can be common on some seashores, and lacking the thickened apertural lip of the adult are often frustratingly difficult to recognise. More frequent are the smaller whelks, Hinia reticulata (Fig. 25(a)) and H. incrassata (Fig. 25(b)), also efficient scavengers and often common on moderately sheltered rocky shores. Neogastropods have sophisticated reproductive modes. All species encapsulate their eggs, which in most northern, cold temperate species hatch as well-developed juveniles. In many species as little as ten per cent of the eggs undergo embryonic development, the rest serving as food for the few. Egg cases of neogastropod snails are conspicuous, and often resistant to decay, lasting long after the juveniles have hatched. Those of Nucella are slender-stalked and urn-shaped, bright yellow when fresh, and plastered in tight sheets on damp, shady surfaces by groups of spawning females. Species of Hinia produce flat, oval, translucent cases, attached by very short stalks and aligned in neat rows. Those of the common whelk are familiar on all strandlines; the female produces a series of small, lens-shaped capsules each containing up to ten eggs, and linked one to another to form a spongy, fist-sized ball. Females often spawn in groups, and the rounded egg masses of each may also be glued together, developing enormous accumulations.

Fig. 25 (a) Hinia reticulata. (b) Hinia incrassata. Scale bars = 5 mm.

Unwinding again: the opisthobranchs

The last, and most remarkable, group of gastropods to be considered is the Opisthobranchia, or sea slugs (Fig. 18 (e)). This amazingly diverse group of molluscs includes the bulky sea hares, the delicate, planktonic sea butterflies, a myriad, tiny ectoparasites with tapered, spired shells, and the colourful and occasionally bizarre nudibranchs. A combination of morphological characteristics unites this suite of animals, and distinguishes it from all other gastropod groups. Firstly, opisthobranch evolution has largely reversed the effects of larval torsion. The anterior mantle cavity typical of prosobranchs has migrated posteriorly, along the right side of the body, decreasing in size and significance, and in most living sea slugs is quite absent. In consequence, the ciliated gill seen in prosobranchs is also lost, and opisthobranchs have instead a variety of branching, fleshy structures developed as outgrowths of the body wall, and varying in position from one family to another. A second, allied, evolutionary trend has been a reduction and eventual loss of the shell. One obvious result of these two changes is that the sea slug body is clearly bilaterally symmetrical, and usually bears a conspicuous and well-developed head. However, the sea slugs have retained and refined one feature of their prosobranch ancestry, and that is the radula. In some families the radula is not very different from that of the mesogastropods, with numerous transverse rows of teeth; in others the number and width of the tooth rows have both decreased as the animals adapted to increasingly specialised feeding modes and diets. A minority of opisthobranchs is entirely herbivorous; the majority consists of carnivores, often highly specialised predators with radular teeth modified for seizing and cutting prey. Probably very few species of sea slug can be regarded as generalist feeders; most are instead adapted for feeding on a very narrow range of food items, with interesting consequences for their ecology.

Relinquishing the hard protective shell that contributed to the evolutionary success of the molluscs might seem a damagingly retrograde step. It is not easy to understand how this dangerous evolutionary gamble was achieved, or how it stimulated an extraordinary new adaptive radiation. Primitive sea slugs with small shells, too small to completely enclose the body of the animal, are often good swimmers, a fact possibly of great importance in their evolution. Bulky sea hares with very small, internal shells, of unknown significance, appear to taste noxious, and also have the ability to eject clouds of distasteful or camouflaging substances when attacked, while numerous small carnivorous sea slugs are decidedly poisonous, and advertise the fact by their bright coloration. Colour plays a camouflaging role for some slow-moving grazing species, while others have tough dorsal surfaces stiffened with calcareous spicules and frequently equipped with groups of glandular cells that secrete acidic substances. In the most unusual species, those feeding on hydroids, sea anemones and other cnidarians, the stinging nematocysts of its prey are retained by the sea slug and used in its own defence. While sea slugs may have surrendered a secure retreat in shedding the mollusc shell, they have evolved a variety of defensive strategies that render them invulnerable to all but the most specialised predators.

A final distinction between the opisthobranchs and other gastropods is that all of them are hermaphroditic, a fact which correlates with their equally distinctive life cycles. Most sea slugs have a life span of less than a year and most are semelparous, breeding just once towards the end of their life cycle. Populations of many species thus seem to be ephemeral; through much of the year they just cannot be found, but aggregations of mature adults appear quite suddenly, usually on preferred prey species, feeding voraciously, spawning and often disappearing again equally suddenly. Such sudden plagues were formerly thought to result from migration, with adults aggregating to breed. Actually, juveniles of most species are almost certainly present in their favoured habitats through spring and summer, but are simply not apparent because of their small size.

One interesting exception to the above general rule is the primitive shelled opisthobranch Acteon tornatilis (Plate 8(f)), a rather rare species sporadically distributed on sandy coasts of western Britain. Acteon is rather long-lived for a sea slug, achieving a life span of five years or more. It possesses a robust, pink and white-banded shell, with a short pointed spire and a bulbous body whorl. It is a specialist predator, feeding on the tubicolous polychaetes Owenia fusiformis and Lanice conchilega, and at low tide is easily seen trundling at an impressive pace through the silty top layer of sand, leaving a deep, grooved trail behind. Acteon has a substantial shell into which the entire body of the animal can be withdrawn, but in most other shelled species, while the animal is able to retract head, foot and mantle margin into a rounded, compact mass, the shell is far too small to accommodate it and usually only encloses the visceral mass. Akera bullata (Fig. 26(a)) is a good example: this rather striking sea slug has a glossy, globular shell up to 4 centimetres long, but the rest of the body adds another 6 centimetres to the animal’s length. Akera is a rather elegant creature. The edges of its elongate body are drawn out into wing-like flaps, termed parapodia, which it uses in graceful swimming. Like Acteon, Akera can be found in silty bays, particularly among seagrasses. It is not very common, but sometimes appears in astonishing swarms. Pleurobranchus membranaceus and Berthella plumula are representative of slightly more advanced sea slugs. Both possess a small internal shell and a single posteriorly situated gill on the right side, just below the edge of the mantle skirt. These two species are found on rocky shores where they prey on compound sea squirts, especially Botryllus schlosseri. Pleurobranchus is another swimmer, employing extravagant flapping movements of the ample mantle skirt.

Fig. 26 (a) Akera bullata (scale bar = 5 mm). (b) Limapontia senestra (scale bar = 1 mm). (c) Acanthodoris pilosa (scale bar = 10 mm). (d) Diaphorodoris luteocincta (scale bar = 5 mm).

While carnivory is the usual rule among opisthobranchs, several families are entirely herbivorous in habit. Aplysia punctata (Plate 9(a)), the sea hare, browses a wide range of red, brown and green algae. It is an impressively large animal up to 30 centimetres in length with a fleshy body variably marbled with green, brown, red or deep purple pigment. Sea hares can be found as juveniles in low-shore rock pools, but they are most often observed as adults on sheltered sandy shores, and among seagrasses. When undisturbed they are quite unmistakeable, and the source of their common name is obvious. The plump body, flanked by flared parapodial wings, is tapered anteriorly and carries at the very front a pair of oral tentacles, with lobed edges and resembling the ears of a hare. Behind these is a pair of shorter, tubular processes, the rhinophores, common to most sea slugs and of primary importance in chemo-sensation. Sea hares are among the largest opisthobranchs with some tropical species exceeding 1 kilogram in weight. They also display complex behaviour: the parapodia flap rather laboriously, but enable the animals to swim determinedly. They are able to orientate and to navigate, and are probably the only sea slugs to migrate actively, gathering together and linking in chains to copulate and spawn. They will discharge clouds of dense purplish ink to mask themselves when threatened, and also opaque streams of a noxious substance, opaline, which is very effective in deterring predators.

Elysia viridis (Plate 9(b)) and the three tiny species of Limapontia (Fig. 26(b)) are the best examples of several families of rather specialised herbivorous sea slugs. Limapontia capitata and L. depressa are often common in mid-shore rock pools, where they feed on small, filamentous green algae, but they are rather difficult to find, neither being much more than 5 to 6 millimetres long. The easiest way to find them is to collect tufts of Cladophora, Enteromorpha, Chaetomorpha or other fine-fronded green algae and tease them apart in bowls of clean seawater. These little slugs are rather dull coloured, in shades of brown or black, but move swiftly and are readily seen once crawling. The bulky green alga Codium tomentosum is the preferred food plant of the strikingly coloured Elysia viridis and large plants in deep sheltered pools may support substantial numbers. Elysia grows to 40 millimetres in length and as its name suggests is usually bright emerald green, and flecked with almost iridescent spots of blue, red and pale green. Limapontia, Elysia and their relatives belong to an order of Opisthobranchs termed the Sacoglossa. They are all specialist feeders, and all have a radula with a single series of knife-like teeth used to slit algal cell walls, enabling the slug to suck out the cell sap.

One further group of opisthobranch specialists deserves mention, namely the Pyramidellidae. There are perhaps more species of pyramidellids in European waters than all other opisthobranchs together, but they are minute, most around 3 to 5 millimetres in length, and notoriously difficult to identify. All of these tiny animals have spired shells and might be mistaken for mesogastropods except for the fact that the larval shell, or protoconch, visible in live or freshly dead animals at the tip of the adult shell, is sinistral, or coiled to the left, while the dextral adult whorls, viewed from the aperture, rise to the right. Also, unlike prosobranchs, the head of a pyramidellid has an additional lip, the mentum, between the lower side of the head and the front edge of the foot. Little is known about the biology or ecology of these small, shelled opisthobranchs; malacologists still argue over their systematic affinities and they have been successively and regularly reclassified as either opisthobranchs or prosobranchs. Many seem to be ectoparasitic in habit, living in association with bivalves or large polychaete worms and feeding on the live tissues of their hosts.

The Order Nudibranchia comprises the majority of opisthobranch species, excluding the pyramidellids; about 50 species occur commonly on Britain’s coasts (Thompson, 1988). They can be ordered into a number of systematic groups, each of several families, with fundamentally similar morphologies and usually with similar lifestyles and feeding preferences. The dendronotacean slugs include the largest north European nudibranch, Tritonia hombergi, and in the genus Doto some of the smallest species. In all dendronotaceans the dorsal surface of the body carries a paired series of branching or knobbly structures along the entire length of the animal. There is a pair of distinctive rhinophores at the head end, with cupped or trumpet-shaped sheaths. Tritonia hombergi feeds exclusively on the soft coral, Alcyonium digitatum, as an adult and is rarely found on the seashore. It is broadly oval in shape, growing to 20 centimetres in length and coloured yellow to brownish-orange on a white background. At the front end the mantle edge is lobed and frilled, overhanging and hiding the head, but the pimply dorsal surface bears a prominent row of branching feathery structures on each side, usually about six pairs of large ones, with numerous smaller ones between. The rhinophores, protruding from deep cups at the head end, are also branched and feathery. In Tritonia these branching processes function as gills; they are soft and retractile, and increase in number as the animal grows, presumably in response to an increasing demand for oxygen. Dendronotus frondosus is similar to Tritonia but smaller, reaching about 10 centimetres in length, and with fewer, more regular series of gills, usually no more than nine pairs. Dendronotus feeds on hydroids, adults especially on Tubularia, and can be found on the lower shore, although it demands careful searching. Like so many other small marine animals, species of Doto (Plate 9(d)), despite an often bright coloration, are difficult to spot on the seashore, and best looked for by placing clumps of hydroids in bowls of seawater and waiting patiently until the slugs reveal themselves. At least a dozen species of Doto occur around the British Isles; none is larger than 3 centimetres, and most are much smaller than this. All have slender bodies with rather square heads and a pair of long, thin rhinophores set in trumpet-shaped basal sheaths. However, the most characteristic feature of the genus is the paired series of knobbly, club-shaped structures running dorsally along the length of the animal, brightly coloured in most species and held stiffly erect as the slug moves about its business. These are termed cerata; they are especially capacious outgrowths of the body containing lobes of the digestive gland in which the animal’s food is broken down and absorbed. A Doto species might have from five to ten pairs of cerata, each roughly cylindrical, with a narrow stalk, and with rings of large, rounded tubercles giving it a warty appearance. The smallest sea slugs absorb oxygen over the whole of their body surface and thus do not need gills, but several species of Doto have finely branched feathery gills at the base of each ceras. All species of the genus are associated with hydroids, on which they feed, lay their spawn, and probably first settle and metamorphose from their larval form. The radula of Doto is adapted to the particular feeding mode: each row consists of just a single, broad, multicusped tooth used to cut into the hollow stem of the hydroid, so allowing the slug to suck out fluid and soft tissue. In effect these minute carnivores might perhaps be regarded as ectoparasites; it is doubtful that they ever kill their host and hydroids are able continually to regenerate colony parts. Doto coronata is one of the smallest species, at just 12 millimetres long, and is apparently the most widespread as well. It has up to eight pairs of cerata; the body is white to pale yellow, with spots and flecks of red, purple or brown, and with a deep maroon spot on each tubercle of the cerata. It has been found on a number of small hydroids, an unusually wide selection of hosts, given that most Doto species appear limited to just a single hydroid species. However, some recent research has shown that this pretty yellow and red sea slug consists of a group of very similar, but genetically distinct species, each with perhaps just a single hydroid host species, and it is certain that other small, widespread sea slugs, with an apparently catholic taste in food organisms, will prove to be species complexes, each of two or more distinct species which taxonomists have yet to recognise.

The doridacean slugs include a number of distinctive families, among which are some of the most frequently encountered British sea slugs. They fall naturally into several major morphological types, but all the slugs in this suborder have thick, club-shaped rhinophores, with transversely ridged tips, and in all the branching, pinnate gills are situated posteriorly in a ring or circle around the dorsal anus. The Family Onchidorididae includes a number of dull-coloured, white or yellow slugs with domed, elongate oval bodies. In almost all onchidorids the mantle overhangs and hides the head and foot, and only the chunky rhinophores and feathery gill circlet are visible to show when the slug is active. The mantle is thick and warty, and stiffened with spicules of calcium carbonate; many species, perhaps all, produce acid secretions from scattered clusters of glandular cells as an added deterrence to predation. The onchidorid radula usually has two large, hooked lateral teeth, each bordered by up to a dozen smaller marginal teeth; the median, rachidian, tooth is small or lacking. The two lateral teeth are of most importance and are effective in stripping their food organisms, namely the flat, encrusting colonies of sea mats, or bryozoans. Each species has a fairly narrow range of preferred prey species. Acanthodoris pilosa (Fig. 26(c)), a large slug growing to 7 centimetres in length and coloured off-white to dirty grey, feeds principally on the uncalcified bryozoan Flustrellidra hispida, and species of Alcyonidium, which live largely on fucoid algae. The smaller, prettier Diaphorodoris luteocincta (Fig. 26(d)) can be found on lower surfaces of rocks, grazing colonies of calcified bryozoans. The sea lemon, Archidoris pseudoargus (Plate 9(c)) (Family Archidorididae) is the largest British doridacean, growing to 12 centimetres long, and can be found without difficulty on most moderately sheltered rocky shores through much of the year. Its rough blotchy mantle is an effective camouflage on the low-shore rocks it clings to. Archidoris is another specialist, feeding on siliceous sponges such as Halichondria panicea.

The Aeolidiacea is probably the most speciose order of sea slugs in northern cold waters, and around the British Isles the group includes some extraordinarily beautiful animals. They all have slender, posteriorly tapered bodies; the head is usually large and conspicuous, with long, graceful tentacles, and equally long rhinophores. Many are brilliantly coloured, and the colour is often concentrated in bands and spots on the long, slender, sausage-shaped or fingerlike cerata that are characteristic of all aeolid slugs. Aeolids feed on cnidarians: commonly on hydroids, frequently on sea anemones, while some species even specialise on scyphozoan jellyfish. Their apparent disregard for the vulnerability of their delicate bodies is attributable to a unique and effective defensive strategy. Examine the tip of a ceras of any aeolid and it will show an opaque white body, the cnidosac, in which the slug sequesters undischarged nematocysts derived from its cnidarian prey. There is no doubt of the effectiveness of the cnidosacs; few marine animals will interfere with live aeolid slugs. Pycnogonids have been known to pluck individual cerata from small aeolids, but many pycnogonids feed also on cnidarians and perhaps have either an immunity to the cnidocytes of their prey, or the same ability as aeolids for neutralising them. However, the most severe threat some aeolid species face is actually from their potential prey, especially when this is a large and powerfully armed sea anemone. Aeolidia papillosa (Plate 9(e)) is a large, purplish-grey sea slug, which in spring can appear suddenly in considerable numbers on some coasts. Aeolidia feeds on several species of seashore anemone, especially Actinia equina and Urticina felina. It can grow to a length of 12 centimetres, although most specimens found on the seashore will be no longer than 3 to 5 centimetres. Its cerata are packed in a dense mat along its back, each with a distinct, opaque white cnidosac at its tip. Aeolidia uses its oral tentacles and rhinophores to sense and locate its prey and bites chunks of tissue from the column of the anemone. In response the sea anemone will contract abruptly; for Urticina this is probably sufficient to escape further attack, its gravel-encrusted column effectively foiling the attention of the predator. Other sea anemone species will balloon, filling their coelenteron with water, and then release their grip on the substratum and drift away. However, Actinia, and perhaps others, will retaliate by stinging the attacker. The degree of damage it can inflict probably varies according to the size and species of sea anemone, but it may be considerable; large Aeolidia appear able to withstand the counterattack, but there have been reports of juveniles being killed by their intended prey.

Species of Eubranchus, Facelina, Favorinus and Cuthona constitute the majority of aeolid sea slugs on Britain’s seashores. Most of these are 2 to 5 centimetres in length, with fewer cerata than Aeolidia, usually arranged in orderly series, and in many species banded or spotted with brilliant colours (Thompson & Brown, 1984). Most of these small sea slugs appear to be specialists, perhaps being limited to one or two species of hydroid on which they feed, lay their eggs and settle as metamorphosing larvae. None occurs as frequently on the seashore as Aeolidia, and they are always an exciting find.

The last molluscan class, the Cephalopoda, features only sporadically in seashore biology. The bleached cuttlebone of the common cuttlefish, Sepia officinalis, is a common enough find; Sepia is always present just below the limit of the tide, but is rarely seen on the seashore. However, the little cuttle, Sepiola atlantica, is not uncommon during the summer in deeper low-shore rock pools, and can even be caught over sand with a prawn net. They are wonderful to watch, but they are delicate animals that do not survive jam jar transport, and are best left on the seashore. The curled octopus, Eledone cirrhosa, is also found sometimes low on the shore in early spring, as a participant in the inshore movement of breeding animals. Again, they do not take to captivity and will not be confined in any container; they are best photographed, at most, and left alone.

Life in between: lophophorates

In passing to the final few groups of marine seashore animals one crosses a major divide in systematic zoology, from the protostomian invertebrates to the deuterostomes, a group of animal phyla sharing a similar body plan, similar embryological development, and perhaps a common, though remote, ancestry from which the vertebrate animals also arose. Firstly, however, it is worthwhile considering briefly three animal phyla that occupy a position perhaps transitional between these two great divisions of the animal kingdom. These are the Brachiopoda, Phoronida and Bryozoa, often collectively termed the lophophorates and occasionally formally united as a single Phylum Lophophorata. The body plan in all three phyla appears to be deuterostome in character, their embryology appears to be a mix of protostome and deuterostome features, but what unites them is the lophophore, a ring, whorl or circlet of hollow, ciliated tentacles surrounding the mouth. Lophophorates are profoundly sedentary, feeding by filtering water through the tentacle crown, and capturing and transporting suspended particles by ciliary action. Whether shared morphological features actually indicate a common ancestry, or are just parallel adaptations to a sedentary, suspension-feeding life is still argued over, and is actually of less interest than the evolutionary history and modern ecology of these three groups of animals.

The brachiopods, or lamp shells (Fig. 27(a)), dominated shallow seas through much of the Mesozoic era, but suffered massive extinction 100 million years ago and today exist as a small phylum of essentially sublittoral, hard ground animals. They are rare and unfamiliar on the seashore, although their curious shells might be found on northern coasts. The brachiopod body largely consists of a spiralled lophophore of hundreds of tentacles, and is completely enclosed by a thin and rather brittle shell of two dissimilar valves. Unlike the laterally bivalved shells of clams, the two valves of a brachiopod shell are dorsal and ventral, the former being the larger, with a narrowed posterior end bearing an open hole, resembling the classical oil lamp for which the animals are named. Phoronids are worm-shaped animals with a terminal mouth and lophophore; some species build tubes in sand, others bore in limestones or shell. Like the brachiopods, the few species known, possibly 20 worldwide, are primarily subtidal in habit. However, they may be extraordinarily abundant where they occur. Phoronis hippocrepia (Fig. 27(b)), which grows to about 4 centimetres long but no more than 1 millimetre in width, bores into oyster shells and crusts of calcareous algae, and is a major factor in the degradation of limestones. At just a metre or so below ELWS on limestone coasts it may achieve densities of hundreds per square metre of exposed limestone. It is almost impossible to see on the seashore, but occasionally patient watching by a low-shore pool will reveal the tiny, horseshoe-shaped lophophore of Phoronis emerging from crusts of Lithothamnion.

While neither brachiopods nor Phoronids are at all obvious to the seashore naturalist, bryozoans are quite impossible to miss on weedy shores. Furry, purplish sheets investing the fronds of Fucus serratus, or developed as thick cylinders around the lower parts of Mastocarpus and Chondrus, are the bryozoan Flustrellidra hispida (Plate 9(f)); smoother, rubbery patches intermingled with Flustrellidra are various species of Alcyonidium. At the tide’s edge the blades of Laminaria, in summer, carry lacy sheets of another bryozoan, Membranipora membranacea (Plate 10(a), (b)), commonly termed the sea mat. Turning boulders will reveal orange, pink or greyish patches of another half-dozen or so species of Bryozoa. A hand lens is now indispensable. Bryozoans are colonial, or rather, modular animals; their colonies may impress by their overwhelming abundance on some seashores, but appear rather dull. Most of the modules, or zooids, which comprise the colony are around a half-millimetre in length and their often extraordinary form can only be appreciated through a hand lens. Flustrellidra is quite an obliging animal; a small colony placed in a bowl of seawater, and shaded from the sun, will appear to flower as each zooid extends its delicate tentacle crown. The bryozoan zooid is a box- or bottle-shaped structure; each is functionally independent, with a feeding unit, the polypide, consisting of the lophophore and a looped gut, contained in a peritoneum-lined coelom, and with its own nerve net and reproductive organs. However, each zooid is linked to those adjacent to it, metabolic products pass between zooids via specialised communication pores, and the colony as a whole is the individual animal. The colony is founded by a single larva which settles and metamorphoses as the founding zooid and then proceeds to grow by budding, essentially expanding its outer body wall at determined points to form new coelomic space, which is then compartmentalised to form new zooids. This is easy to see in the kelp-encrusting Membranipora membranacea, which grows rapidly through spring and summer. The white lace structure of Membranipora is imparted by the calcified vertical walls of its regular, rectangular zooids, which can be seen quite clearly with the unaided eye. Around the edges of the growing colony is a broad, pale band in which the lacework is incomplete. This is the growing zone of the colony, a common coelomic space formed by the continually expanding body wall of the bryozoan, and longitudinal walls of developing zooid compartments can be faintly seen radiating into the growth zone from the most recently formed zooids. In Membranipora all the zooids of a colony are identical; they are termed autozooids, each capable of performing all physical and metabolic functions. In many other bryozoans heteromorphic zooids have evolved to carry out specific functions, such as reproduction or colony defence; these are usually non-feeding and are supported by energy supplied through the colony-wide communication system from feeding autozooids. The array of heteromorphic zooids present in some bryozoan species can be bewildering.

Fig. 27 (a) The brachiopod, or lamp shell, Terebratulina retusa (scale bar = 5 mm). (b) The lophophore of a phoronid, or horseshoe worm, Phoronis hippocrepia. (c) Growing tip of a colony of the ctenostome bryozoan, Bowerbankia imbricata (scale bar = 0.5 mm). (d) Three autozooids of the cheilostome bryozoan, Electra pilosa (scale bar = 0.5 mm).

The British bryozoan fauna includes around 300 species, and 30 or so can be found between the tides on a moderately sheltered weedy shore. In terms of abundance and biomass the seaweed epiphytes Flustrellidra and Alcyonidium outstrip all other species. They belong to the Order Ctenostomata (Hayward, 1985), all of which are uncalcified, with rubbery, gelatinous or bristly colonies built of identical autozooids. Few ctenostomates display any degree of zooid heteromorphy, although one large group, the stoloniferan ctenostomates, is characterised by a curious and elegant colony form based on a marked colony dimorphism. Towards the top of the Fucus serratus zone some plants will carry small clumps of Bowerbankia imbricata (Fig. 27(c)), a common intertidal stoloniferan. These clumps, usually just 3 to 4 square centimetres, consist of groups of cylindrical autozooids, each less than 1 millimetre long, attached to a slender, creeping stolon firmly attached to the seaweed frond. Under a microscope, the stolon is seen to consist of a series of short cylinders separated by transparent vertical walls; each is in fact a zooid polymorph, budded in the same way as an autozooid, but contributing to a common colony structure. Bowerbankia is rather inconspicuous, although several of the species found on the shore can develop substantial tufts, 2 to 3 centimetres in length, hanging below rock shelves. Together with these one can find erect species of calcified bryozoans, belonging to the largest order, the Cheilostomata (Hayward & Ryland, 1998, 1999), but developing diffuse, tree-like forms rather than flat sheets. Bugula flabellata, one of ten species of the genus to occur in the British sea area, is common low on the seashore, developing stiff orange clumps easily distinguished from hydroids and seaweeds. However, once again a microscope is necessary to appreciate the most extraordinary characteristic of this genus. Viewed under water, the edges of the branches can be seen to carry minute bird’s-head structures, a globular cranium with a sharply hooked beak, borne on a short stalk; these nod almost continuously, at intervals snapping shut the lower mandible of the beak, and then opening it again much more slowly. These are avicularia, highly modified heteromorphic zooids which act to discourage settlement of other invertebrate larvae, and equally effectively to deter the mites, and particularly small polychaete worms which seem to be the principal predators of many bryozoans. Although it is easy to find bryozoans on the seashore, only a very few species can be confidently identified in the field. Flustrellidra hispida and several species of Alcyonidium are easily recognised, as are Membranipora membranacea, and the star-shaped patches of Electra pilosa (Fig. 27(d)) on Fucus serratus, but the rest require a microscope, and many are only found by searching through clumps of Bugula, or well-encrusted small seaweeds.

Across the great divide: deuterostomes

Starfish, sea urchins and brittlestars all belong to one of the most interesting and thoroughly marine phyla of invertebrates, the Echinodermata. Apart from fish, they are probably the one group of seashore animals immediately recognised by every person visiting the coast. Echinoderms share a number of key features that together make them truly unique in the animal kingdom. Firstly, there is the curious symmetry of their bodies: examination of a starfish reveals no obvious right and left side, no apparent front and back end, and comparison to a sea urchin leads to considerable doubt as to the homology of upper and lower surfaces. The echinoderm body has a five-rayed, or pentameral symmetry; certain starfish, it is true, have many more than five arms, but the arrangement of other body structures always conforms to the five-rayed plan. The often brightly coloured body of a starfish may be stiff and relatively inflexible, or softer and rather flaccid; the shell or test of sea urchins is usually quite rigid. Whatever the skeletal type, in all echinoderms it is fundamentally the same, and represents another singular feature of the phylum. The echinoderm skeleton is internal, formed from a series of larger or smaller plates, or ossicles, each developed from a single calcite crystal formed by a single cell. In sea cucumbers (Class Holothurioidea) these ossicles are dispersed throughout the body wall of the animal, frequently with regular arrangements, but not closely juxtaposed. In starfish, different types of ossicle are packed together to make a fairly firm skeletal structure, with large plate-like elements forming the mouth and flanking the sides and undersurfaces of the arms, and smaller, often spiny plates forming the upper surface of the animal. In sea urchins, the plates interlock in regular series and have only a thin outer covering of tissue, so that the test appears as an external shell. Orientation is always a problem in radially organised animals. Primitive echinoderms had mouth and anus on a defined upper surface, and a lower surface indicated by a basal attachment. The typical modern echinoderm has its mouth on the lower surface, which is consequently termed the oral surface; the anus may be on the upper surface, laterally situated, close to the mouth or may be lacking altogether. Conventionally, and logically, the upper surface of an echinoderm is termed aboral; this mostly avoids confusion, although sea cucumbers may still defy easy orientation.

The problem with orientation reflects another unique characteristic of the echinoderms, namely their unusual evolutionary history. They are an extremely ancient group of animals that very early in their evolution adopted a sedentary, suspension-feeding lifestyle. Suspension feeding obviates the need for a head and tends to favour the development of radial symmetry. The earliest echinoderms resembled modern-day sea lilies, with cup-shaped bodies attached to the sea floor by long stalks, and bearing on the upper surface a ring of arms held stiffly above the mouth and collecting food from the water column. What is extraordinary is that having adopted such a specialised and limiting morphology, echinoderms then abruptly changed adaptive tack, abandoned their sedentary existence and took to a free-ranging benthic existence. This was achieved through adaptations of the final unique feature of this phylum, namely their internal water vascular system, derived from part of the tripartite coelomic cavity characteristic of deuterostome animals. Overturn one of the orange coloured common starfish, Asterias rubens (Plate 10(c)), which can always be found on rocky shores, and it will endeavour to right itself, using rows of flexible, extensile tube feet which run the length of the underside of each arm. In Asterias the tube feet are suckered, enabling the animal to cling firmly to a rock, but are used also in stepping locomotion. They are hydraulically powered. Each tube foot issues through a pore in the ambulacral ossicle, in the centre of the arm. Internally it is connected to a small water reservoir, or ampulla, and the double row of tube feet beneath each arm is linked by a single water vascular canal. Within the central body of the starfish a ring canal links together those of each arm and is connected via an especially thickened tube, the stone canal, to a finely perforated, sieve-like ossicle on the upper surface of the starfish, termed the madreporite.

In the earliest echinoderms tube feet were probably employed in feeding, capturing food particles and passing them down the inner surface of the arms towards the mouth. Various kinds of echinoderm still use tube feet for feeding, but for the majority, they serve in often agile and sometimes surprisingly rapid locomotion, and were probably the single most important feature of primitive echinoderms, which allowed them to return to a motile existence. Tube feet are highly muscular and richly supplied with nerves; they react immediately to external stimuli with rapid extension or contraction, and hydraulic pressure is maintained by their inner reservoirs. The madreporite and its associated stone canal was thought to function to top up the water system, but it seems instead that water simply diffuses from the main body coelom through the walls of the coelomic water vascular system. The function of the madreporite is still a puzzle, but it appears to be sensitive to external water pressure and perhaps acts as a combined monitor and safety valve. While this elegant hydraulic system has stimulated a significant adaptive radiation in modern echinoderms it has imposed one major restriction on them. Their internal fluids have the same salt composition as sea water and venturing into freshening water results in osmotic flooding and death. Consequently, few echinoderms can tolerate any reduction in seawater salinity and the group has been unable to penetrate freshwater habitats.

Reproduction is an uncomplicated business among echinoderms; almost all are separately sexed, but there is no external dimorphism and it is not possible to distinguish male from female. Spawning is usually synchronised; eggs and sperm are shed in streams through special pore plates and fertilisation occurs in the surrounding water where zygotes develop into rather long-lived planktonic larvae. There are some exceptions; the females of some starfish and brittlestar species retain their eggs and brood them, eventually releasing well-grown juveniles.

The four classes of living shallow water echinoderm all include species found on north European seashores. One or two common species can be found easily on almost any coastline, and a few can be amazingly abundant. The feather star, Antedon bifida, ranges from Shetland down the western coasts of Britain to Portugal, and into the western English Channel. It is primarily a subtidal animal, but on occasion can be found commonly among kelps on the lower seashore. It belongs to an order of sea lilies (Class Crinoidea) that has abandoned the firmly attached basal stalk and instead clings to the substratum with a group of curled, prehensile cirri radiating from the base of its cup-shaped body. Much of the bulk of a feather star consists of its ten long, curling arms, with delicate branches, pinnules, in alternating series along their sides. Antedon spreads its arms widely, using its tube feet to trap suspended food particles, but despite an apparently sedentary habit it is a very active animal. It will move position frequently, and if disturbed will detach and swim with long strokes of its arms.

Sea urchins, Class Echinoidea, are especially convenient models of echinoderm symmetry and its modifications. They are divided into a number of orders, but are best considered as two major types, the regular and irregular urchins. The common sea urchin, Echinus esculentus (Plate 10(e)), is a good example of the former. The globular test of Echinus is often used in tasteless seaside souvenirs, but at least its symmetry is easily appreciated once dried and devoid of spines. At the apex of the test is a pattern of five large and five small plates surrounding the periproct, a disc of tiny irregular plates with the anus at its centre (Fig. 28(a)). Each of the five large plates has a conspicuous pore, marking the five openings of the genital ducts, and is thus termed a genital plate; one of these is speckled with numerous tiny pores and is the madreporite. The genital plates alternate with five smaller ocular plates, each also with a pore, but for the exsertion of a tube foot; the ocular plates are the points of origin of the five ambulacral rays while the genital plates are the apices of broader interambulacral areas. The alternating ambulacra and interambulacra each consist of a double row of interlocking, plate-like ossicles, which increase in area towards the widest part of the test. The narrow plates of the ambulacra are pierced by pairs of small pores, where tube feet emerge, and all the plates of the test have regular series of large and small tubercles on which, in life, the spines of the urchin articulate.

Echinus is a strictly subtidal species, but it can be found in deep, calm pools with a good growth of Laminaria. It is a far more attractive object in life than dead and dried. The test is thickly and evenly covered with short, sharp, violet-tipped spines, and the five ambulacral rays are clearly marked by five radiating bands of translucent white tube feet. On the lower half of the animal the tube feet appear short and thick, and their suckered tips are usually clamped firmly to the seaweed or rock on which the urchin sits; on its upper half they often extend to perhaps twice the diameter of the test, waving freely in the water column. They are practically the only unplated portion of the animal in contact with the surrounding water and are important in gas exchange, excretion and sensory perception, as well as locomotion. The lower, oral surface of Echinus has at its centre a disc of tough, flexible membrane partly covered with small, irregular plates and with the tips of five white, pointed teeth protruding from the central mouth (Fig. 28(c)). These are the tips of the urchin’s jaws; within the test they are part of a curious basket-like structure, called Aristotle’s lantern (Fig. 28(b)), on which the muscles of the jaw apparatus are inserted. Thus equipped, Echinus is an effective omnivorous grazer, crunching kelp fronds and holdfasts, and their burden of epiphytic plants and animals. It is far from sedentary in its habits; in fact, the food consumption of large, regular sea urchins is such that they soon exhaust immediate resources, and all species continuously, and steadily, move as they graze.

Among the spines of Echinus it is just possible to see with the unaided eye shorter structures bearing tweezer-like jaws on flexible stalks. These are pedicellariae, found on many starfish and most urchins; they are employed in ridding the surface of the test of debris, and perhaps also deter prospecting larvae of other invertebrates, and small predators. One type of pedicellaria seen in Echinus is associated with venom-secreting cells, although these are not known to cause even minor irritation to persons handling the animal. Echinus is the most spectacular of the regular echinoids found around the British Isles, but between the tides on rocky shores the common species is the small, greenish Psammechinus miliaris (Plate 10(d)). It is usually found in gravelly areas beneath rocks, clamped tightly to its surroundings by its tube feet. Psammechinus is another omnivore, grazing both seaweeds and sessile animals. The common urchin of sandy shores is the heart urchin, Echinocardium cordatum (Plate 11(e)), a classic example of the other echinoid morphotype, the irregular urchins. The thin brownish test of Echinocardium is often found among strandline debris after autumn gales, its shape and colour recalling its other common name, the sea potato (Fig. 29(a)). Like all echinoderms, it is much more attractive when alive, covered with a crisp pelt of fine yellowish spines, with tufts of stiffer, yellowish-white spines at one end. The five-fold symmetry of echinoderms is still evident, but the external form of all irregular urchins has been so modified that all show a superficial bilateral symmetry. Firstly, the ambulacral rays are now confined to the upper, aboral surface, arranged in five short petal shapes; in Echinocardium one runs to the edge of the test in a deep furrow and is defined as anterior. The apical plate system is unclear; it is just possible to recognise the madreporite in a dried test, close to the centre of the petaloid ambulacra, but the periproct has shifted to the flat, posterior end of the animal. Turning it over reveals that the mouth also is no longer central but has moved towards the anterior, has no protruding jaws and is partly shielded by a projecting lip. Echinocardium lives low on the shore, buried from 5 to 15 centimetres deep in medium to fine silty sand. It digs deeper as it grows, and moves horizontally, using especially thickened, slightly spoon-shaped spines on the oral side. This can be nicely demonstrated by disinterring a specimen close to the water’s edge and placing it on the surface of saturated sand; as it digs steadily a slow-moving wave of sand rises around the animal and gradually covers it. Heart urchins must find their food in their immediate surroundings, and use tube feet to pick up and guide particles towards the mouth. On the central portion of the aboral surface modified spines and particularly long tube feet maintain a respiratory channel towards the sand surface, while others around the anus form drainage channels to carry waste material away from the animal. Several other species of Echinocardium occur offshore, and on southwestern coasts, and around the Channel Isles it is sometimes possible to find the beautiful purple heart urchin, Spatangus purpureus, which may grow to 10 centimetres or more in length. Spatangus burrows so shallowly that often it is not completely covered and if present on a shore cannot be missed. However, perhaps the most interesting of these irregular urchins is the tiny Echinocyamus pusillus (Fig. 29(b)), which is usually less than 1 centimetre long. Echinocyamus is rather common around Britain, but because of its small size is difficult to locate easily. Most often, it is only the test that is found, among material held by a sieve.

Fig. 28 Echinoderm symmetry. (a) The apical plates of the regular urchin, Echinus esculentus: five genital plates, including the distinctively patterned madreporite, and five smaller ocular plates, surrounding the periproct and anus. The five ambulacral rays each originate from an ocular plate, the five interambulacral rays from the genital plates. (b) Echinus esculentus: the Aristotle’s lantern in lateral view. (c) Echinus esculentus: oral view of Aristotle’s lantern. (d) The disc and arm bases of the brittlestar, Ophiura ophiura. (e) Detail showing one of the five jaws of O. ophiura.

Fig. 29 (a) Test of the irregular urchin, Echinocardium cordatum, in aboral (left) and oral (right) view. (b) Test of Echinocyamus pusillus in aboral (left) and oral (right) view. (c) The holothurian Pawsonia saxicola: the branching, filamentous tentacles surrounding the mouth are shown here partially contracted (scale bar = 5 mm).

In starfish (Class Asteroidea) the five ambulacral rays are completely confined to the oral surface of the animal, while the upper surface is covered with close packed ossicles, often bearing tubercles or with a continuous dense sheet of spines. The anus is still apical, but usually quite indistinct, and only the madreporite is obvious, displaced to a position in the angle of two of the starfish’s arms. The centrally situated mouth is large, and from it the five series of tube feet run in a deep groove along the midline of each arm. The skeleton of a starfish is built from series of recognisably distinct types of ossicle. The upper surface of the common starfish, Asterias rubens, is covered with a thick skin within which ossicles are linked together to form a stiffening, net-like skeleton. In the gaps between the network are soft areas with patches of thin skin which balloon outwards and function as gills; these balloons, or papulae, are often surrounded by clumps of large pedicellariae. Some of the ossicles are formed into short, blunt spines and these are usually plastered with small pedicellariae. The ambulacral grooves on the undersides of the arms in Asterias consist of large, regular ossicles, closely packed together, and the sides of the grooves are formed by additional series of large plates and flanked by lines of long spines. Asterias is not rendered completely rigid by its skeleton; indeed it is often found draped rather limply over mussel-covered rocks, its network of interlocking ossicles allowing it considerable flexibility. However, the common starfish of sandy shores, Astropecten irregularis (Plate 11(a)), is as stiff as a biscuit, its flat profile resisting overturn by swell. In Astropecten the ossicles are tightly interlocked; the upper surface of each is packed with tiny branched spines, called paxillae, so that most of the aboral surface of the starfish has a uniform, slightly rough surface, resembling an extremely fine, short-toothed brush. Astropecten is a very elegant starfish; each arm is edged by a single line of large, smooth marginal plates, while the sides and lower surfaces are formed from linear series of large adambulacral and ambulacral ossicles. Additionally, the margins of the arms and the edges of the ambulacra are bordered by symmetrical lines of large spines.

Asterias rubens is the most abundant starfish in northern European seas and can be found on almost any kind of seashore, at almost any time of the year. In some years, on shallow, sheltered coasts, Asterias appears in slow-moving swarms of millions of individuals. They move steadily along the coast, feeding on bivalve molluscs, and must continue to move as each prey population is exhausted. Foraging parties may venture into the intertidal, feeding mostly on mussels, but these swarms of Asterias rarely persist between the tides; they may fall foul of rough weather, become stranded by especially low tides, or simply move on as they outstrip their food sources. Asterias will swallow small bivalves whole, but it uses its suckered tube feet to pull apart the shell valves of larger prey, such as mussels, everting its stomach to kill and partially digest them. Astropecten is never as abundant as Asterias, but is reasonably common on most medium to fine sandy beaches during spring and summer. It also feeds on bivalves, but taking smaller species and individuals than Asterias, and perhaps engulfs other small invertebrates, and detrital matter, as well. On good low tides it is sometimes possible to find a much larger starfish, the bluish-green Marthasterias glacialis, immediately recognised by the large spiny tubercles projecting from the larger ossicles on its upper surface. Marthasterias is catholic in its choice of food but, like most large starfish species, it is especially partial to its smaller relatives, including Asterias and Astropecten.

The cushion star, Asterina gibbosa (Plate 11(b)), is a short-armed, rather small starfish, rarely more than 4 centimetres across. Along the west coasts of Britain it is quite common on rocky shores, in pools, or clamped to the undersides of large rocks. It was only recently realised that especially small individuals, less than 2 centimetres across and with a dark star pattern on the centre of the disc, were not juvenile common cushion stars, but another species, now named Asterina phylactica. This little cushion star is found on the southwestern coasts of England and Wales, and is particularly adapted to wave-exposed shores. The two species of cushion star have quite different life cycles; A. gibbosa sheds its eggs to develop into planktonic larvae, but A. phylactica broods fewer eggs and releases fully developed juvenile starfish.

The fourth echinoderm class to be found on the seashore, at least as frequently as starfish and sea urchins, is the Ophiuroidea, or brittlestars. These are the most agile of the echinoderms. The brittlestar body consists of a small round disc covered with a thick skin, and usually plated with flat ossicles, and five very long and flexible arms (Fig. 28(d)). Two or three species of brittlestar can be found on most rocky shores, and another two or three on all but the most exposed sandy shores. Most species move swiftly when disturbed, the arms looping ahead of the disc, usually with one leading. The extreme mobility of these rightly named brittle echinoderms is attributable to the structure of their arms, each of which appears to consist of a series of segments, narrowing towards their tapered tips, and each segment with a fan of stiff spines on each side. In section, each ‘segment’ consists of a ring of six large ossicles with a pair of tube feet on its under surface. All of the ossicle rings within an arm are bound together by connective tissue and muscles; the latter allow both horizontal and vertical movement, and the rapid movement of brittlestars results from muscular flexure of the arms, rather than use of the tube feet. The mouth is large and obvious in all brittlestars and is clearly pentagonal. Five triangular jaws alternate with the arm bases (Fig. 28(e)), the apex of each carrying tubercles or plate-shaped ossicles that function as jaws. There is no anus, undigested material being voided through the mouth; the madreporite is hidden close to the angle of one jaw, and there is no other evidence of the apical plate system of sea urchins.

Starfish are well known for their ability to regenerate damaged arms. Some tropical species have adapted this ability to allow asexual replication, shedding entire single arms that will then regrow into a completely new starfish. Brittlestars are masters of regeneration. It can be disquieting to see how readily they lose arms, but this is an effective method of defence, shedding portions of one’s body to preoccupy a would-be predator and escaping, regrowing missing limbs afterwards. Some brittlestar species appear literally to fall apart when interfered with, shedding the top portion of the disc, the gonads and much of the arms, yet are still able to regenerate as one or more individual animals.

Like many other echinoderms, brittlestars seem to be rather unselective feeders, and varied in their mode of feeding. Tube feet towards the bases of the arms will pick up small particles of detritus, or small invertebrates, packing them directly into the mouth. Those towards the tips of the arms pass food along a conveyor towards the mouth, and in some cases the entire arm will loop around a food item and carry it to the jaws. Many species will feed by more than one method, and feeding modes employed will vary according to the size of the individual and conditions in its immediate environment.

About ten species of ophiuroid occur commonly in the inshore waters of the British Isles. Of these, Ophiocomina nigra and Ophiothrix fragilis (Plate 11(c)) are the most common; the first is readily recognised by its black disc and the second by its spiky arm spines. The two species often occur together and in water of 10- to 20-metre depth aggregate in dense patches that may number several thousand animals for every square metre of sea floor. Between the tides they can be found on weedy shores beneath rocks, often together and in small groups. There are two common species on intertidal sandy shores. The largest, Ophiura ophiura (Plate 11(d)), is unusual for a brittlestar in having a stiff, rather inflexible body. Ophiura lives on the sand surface and, like Astropecten, its flat, rigid body resists overturn. Amphiura brachiata, conversely, is infaunal in habit and not always immediately evident; usually only the tips of its thin curling arms project above the sand surface. The rest of the animal is not far below; the tiny disc, about 1 centimetre diameter, is buried just a few millimetres deep and the arms, about fifteen times longer than the disc diameter, are spread evenly around it.

Finally, the sea cucumbers, Class Holothurioidea, constitute the most unusual group of living echinoderms. These odd animals are basically pentameral in symmetry, but enormously elongated along the aboral-oral axis so that the five ambulacral rays run the length of a long, sausage-shaped body, from terminal mouth bordered by a ring of retractile, branching tentacles, to a terminal anus. In most, the five rays have shifted somewhat, so that three lie close together defining a functional ventral surface while the other two run along an opposite dorsal surface. The outer body layer of a sea cucumber is typically a thick knobbly skin; it is stiffened with numerous small and large ossicles, but these are layered within the skin and not externally visible. Sea cucumbers are especially associated with tropical seas; tropical species may grow to a metre or more in length, and some may be extremely abundant. They are not a prominent part of the benthos in northern seas, but a dozen or so species occur around Britain and a few can be found occasionally on the seashore. They are rather somnolent animals, leading sedentary lives in cracks and crevices, within kelp holdfasts, or shallowly buried in silty sands, and using their finely branched tentacles to collect food. On Scottish coasts the dark brown Cucumaria frondosa lives on rocky shores, especially among and within Laminaria holdfasts, while the milk-white Pawsonia saxicola (Fig. 29(c)) is present in similar habitats on the southwest coasts of England and Wales, and western Ireland. All holothurians inconveniently contract to rigid cylindrical objects when disturbed, and are consequently rather difficult to tell apart. However, Pawsonia can be confidently identified, if observed relaxed and feeding, by its long, dark brown to black tentacles. The sand-dwelling Leptosynapta inhaerans is also easily recognised. It is a soft, flesh-pink animal resembling a plump polychaete, but with no sign of segmentation, no head and no bristles.

Two other groups of deuterostome invertebrates present on the seashore are particularly interesting for the light they may shed on possible evolutionary pathways to the vertebrate animals. One, the Phylum Hemichordata, is rather rare, and examples are found infrequently by digging muddy sand flats. They are worm-like animals with an extremely delicate, three-part body consisting of a long or short anterior proboscis arising from a short, flared collar, and a long soft trunk which forms the majority of the animal. Glossobalanus sarniensis (Fig. 30(a)) is found around the Channel Isles and the Isles of Scilly, and sporadically on sheltered coasts of South Devon and South Cornwall. It has a short, ovoid proboscis cupped in an equally short collar, the two resembling an acorn and providing the common name for the group, acorn worms. The fragile trunk of Glossobalanus may be up to half a metre in length. Saccoglossus ruber, which can be found on the coasts of Wales, Ireland and western Scotland, may grow as long as Glossobalanus, but the proboscis is large and finger-like. Acorn worms use mucus and cilia on the outer surface of the proboscis to collect fine particles of food from among the silty sand in which they live. They are uninspiring, apparently rather simple animals; their interest lies in their larval form, which resembles those of echinoderms, and in the structure of the front part of the gut, the pharynx, which suggests an ancient link with chordate animals. The anterior portion of the acorn worm’s trunk has a series of small pores passing through the body wall and linking with larger slits in the wall of the pharynx, reminiscent of the pharyngeal gill slits seen in primitive chordates, such as the sea squirts, or ascidians, the other group of deuterostome invertebrates to be considered.

Together with two classes of equally curious planktonic animals, the Thaliacea and the Larvacea, the Ascidiacea constitute the Urochordata, regarded by some authorities as a phylum, by others as a subphylum of the Chordata, which includes all the vertebrate animals. Their chordate credentials are evident in their larval stages: the long tail of the tadpole larva common to all ascidians is stiffened by a rigid skeletal rod, the notochord, lying beneath a dorsal, hollow nerve cord. Sea squirts soon lose their chordate identity. They are sessile animals, and as the larva attaches itself permanently to its chosen home site a profound metamorphosis overcomes it and the tail, notochord and nerve cord are entirely lost. Sea squirts are suspension feeders, filtering fine food particles from ciliary currents drawn through a fine-meshed branchial sieve. They may be unitary, though often living in dense clumps, or they may form colonies analogous to those of cnidarians and bryozoans, the metamorphosed larvae proceeding to grow by non-sexual budding and developing a colony of morphologically and genetically identical modular units, usually termed zooids. Some species are adapted for life in soft substrata, but the overwhelming majority, including all those found between the tides, attach themselves to permanent substrata. The rather simple body plan of ascidians is best appreciated by reference to Ciona intestinalis (Fig. 30(c)), a soft-bodied cylindrical animal, yellowish-green and growing to 15 centimetres or so in length. Ciona occurs in clumps on almost any hard substratum, but is most abundant in estuaries and on well-sheltered coasts. At its free end Ciona has a lobed oral siphon through which it draws its incurrent water flow; just below this, on its conventional dorsal side, is the excurrent atrial siphon. Much of the volume of Ciona is bounded by a greatly enlarged pharynx pierced by thousands of fine slits in regular longitudinal rows. This fine-meshed structure is alternatively termed the branchial sac; at its base is the animal’s stomach, from which a long intestine ascends one side of the branchial sac to the anus, which is located just below the atrial siphon. Within the loop of intestine beneath the stomach lie the reproductive organs. This simple body is enclosed by a delicate body wall, or mantle, which is itself enveloped by a thick outer test, or tunic, the structure that provides the other common name for these animals, tunicates. Strictly, the test is not a tissue, merely a mixture of protein, cellulose and mucropolysaccharide secreted by the mantle, but in all tunicates it contains some free cells originating from the mantle as well as extensions of the animal’s blood vessels.

Fig. 30 (a) The hemichordate, Glossobalanus sarniensis (scale bar = 2 cm). (b) Styela clava (scale bar = 2 cm). (c) Ciona intestinalis (scale bar = 5 cm). (d) Ascidiella aspersa (scale bar = 2 cm).

The branchial sac is richly ciliated and maintains a constant current of water, flowing in from the oral siphon and out through the pharyngeal slits into the body cavity, or atrium, and thence exiting through the atrial siphon. Tentacles at the mouth of the pharynx prevent coarse material passing inwards, and the finest particles are trapped in a mucous net secreted by the endostyle, a glandular rod lying along one side of the branchial sac. At intervals the net and its catch of food particles are gathered into a pellet and carried along ciliary tracts to the mouth. All ascidians are hermaphroditic. Eggs and sperm are shed into the atrium; in some species fertilisation and development are entirely external, in others eggs are fertilised internally by sperm drawn into the branchial sac and develop internally, the sea squirt then shedding fully formed larvae.

The anatomy of Ciona is easily studied; a single specimen allowed to relax in a tank of sea water will obligingly expand and commence feeding, and the internal structure is clearly visible through the translucent test. In most other species of ascidians, however, the test is so thickened that no internal morphology can be seen at all, and only the paired siphons show the animal to be an ascidian. While Ciona is most frequently found on sheltered, estuarine coasts, species of Ascidia and Ascidiella are the common solitary ascidians on fully marine rocky shores. These sea squirts are attached by one side of the test, rather than at its base; the oral siphon is still terminal in position, but the atrial siphon has been displaced further towards the other end, and its position relative to the oral siphon is often the only guide one has in distinguishing the four or five species found on the seashore. Ascidia mentula is the most striking; a large sea squirt, often up to 20 centimetres in length, it is mostly subtidal in distribution, but small specimens can be found on the lower shore and are recognised by their translucent, pinkish-red coloration and widely spaced siphons. Ascidiella aspersa (Fig. 30(d)) is probably the most frequently encountered species, and often lives in dense groups. Its dirty grey, rough-surfaced test is sometimes partly overgrown by other encrusting plants and animals, but the two siphons, one-third of the body length apart, are always visible. Styela clava (Fig. 30(b)) is an exotic species, thought to have originated in the western Pacific and now spread widely around the world, including north European coasts. Its distinctive, stalked and club-shaped body, with both siphons at the broad end, render it immediately recognisable.

The few solitary ascidian species discussed so far are quite conspicuous animals, but most of the more abundant species on the seashore are colonial, or compound, ascidians, and while they are usually quite obvious it is not always equally obvious what kind of animal they are. In these sea squirts the zooids are typically rather small, usually less than a millimetre or two in length, and clustered together in a common, colonial test. They are often brightly coloured; a combination of colour and patterns in the distribution of zooids can be used to recognise a few species, but identification of most can only be achieved by dissection and microscope examination of individual zooids. The star ascidian Botryllus schlosseri (Plate 12(a)) cannot be mistaken. It forms smooth gelatinous sheets investing fucoid seaweeds, kelp holdfasts, rock surfaces and large hydroids. It is mostly blue, purple or shades of red, with the zooids arranged in star-shaped groups, each with its own oral siphon, but all in a group sharing a common, central atrial siphon. The zooids of Botryllus are differently coloured than the test, often gold or deep yellow, and this striking animal could only be confused with the equally brilliant Botrylloides leachii (Plate 12(b)), in which the zooids are arranged in winding double chains rather than stars. Both Botryllus and Botrylloides are common on weedy shores, often occurring together on the same substratum, and can be found all around the British Isles. Kelp holdfasts also support reddish, knobbly sheets built of closely packed ovoid zooids, each with its own pair of siphons. These may be either the solitary species, Dendrodoa grossularia, which often lives in densely packed aggregations, or the compound Distomus variolosus, in which each zooid is fused basally to its neighbours, contributing to a common, colonial test. Mushroom-shaped or lobate colonies, often 2 or 3 centimetres long or wide, attached to kelp holdfasts, or hanging beneath large rocks may belong to one of four or five genera, totalling ten or more species. Aplidium, Polyclinum or Sidnyum are the most widely distributed of these, but all are confusingly similar in gross features, and all are pink, yellow or orange; none can be confidently assigned to a species without examination of the zooids.

While seaweeds and invertebrates can be completely absorbing, finding fish on the seashore always adds interest to a field trip. A surprising number of species live within the littoral fringe but, apart from the indomitable shanny, none is able to risk even the briefest period of emersion and all must retreat downshore or into the deeper pools as the tide recedes. Intertidal fish need to be looked for. The shanny, Lipophrys pholis, is ubiquitous on rocky shores and can stick out the low tide period in the smallest pool, under damp seaweed, or even jammed into a cool, shady crevice. The rock goby, Gobius paganellus, is almost as tough, and smaller individuals can withstand the rigours of some of the highest rock pools. Low on the shore, the worm pipefish, Nerophis ophidion, is the commonest of several pipefish species that can be discovered beneath large rocks, often in company with the butterfish, Pholis gunnellus. Rocky shore fish faunas are especially interesting in being a mixture of essentially resident species, which simply retreat downshore, and often to below low-water mark, during the winter, and visitors that may move inshore for longer or shorter periods during the spring and summer. Fish are less conspicuous on sandy shores, but they are nonetheless there, as an excursion with a shrimp net will show. Fish biology and ecology are very broad topics, and seashore fish are considered in detail in Chapter 7.