LECTURE 4 BIODIVERSITY OF ANIMALS ON THE ROCKY SHORE

NB It is possible to preface this lecture with an introduction to zonation. Please select COMBINATION OPTION 2 (118 slides) NB If you wish to present a complete lecture on zonation, plants and animals please select COMBINATION OPTION 3 (197 slides)

Slide no. 1 Title Slide. 2 Introductory. Illustrated: common periwinkle Littorina littorea ; shore crab Carcinus maenas ; beadlet anemone Actinia equina ; encrusting red algae such as Lithophyllum spp. all in a small rock pool near Plockton in NW Scotland. The colours are real! 3 Rocky shore study in progress. 4-5 An invitation to examine the undersides of stones etc. with the important message: PLEASE TURN THE BOULDERS BACK to preserve the organisms being being studied. 6 Animals of the upper shore. 7 Sea slater Ligia oceanica , a large woodlouse which can be found beneath stones during daylight, but scuttles about the surface in large numbers as it feeds at night.

8-15 Sand hoppers Orchestia gamarellus (NB often mis-spelled 'Orchestria') and Talitrus saltator . I think this is Orchestia although the tell-tale large 'claw' on the second leg (uropod) cannot be seen in any of the pictures. Yonge (1949) wrote: "These animals may fairly be grouped with the sea-slater and the rough periwinkle [slide 36 et seq. ] as creatures which have very nearly crossed the threshold of the shore on to dry land". He quotes from Paley's Natural Theology wherein is described a scene I doubt we might witness in these days of anthropogenic reduction in diversity and numbers of wildlife: "Walking by the sea- side, in a calm evening, upon a sandy shore, with an ebbing tide, I have frequently remarked the appearance of a dark cloud, or rather very thick mist, hanging over the edge of the water, to a height perhaps of half a yard, and a breadth of two or three yards, stretching along thew coast as far as the eye could reach, and always retiring with the water. When this cloud came to be examined, it proved to be nothing else than so much space filled with young Shrimps , [Yonge presumes sandhoppers] in the act of bounding into the air from the shallow margin of the water, or from the wet sand". 16 Animals of the middle shore. 17 A second invitation to examine the undersides of stones etc. with the message: PLEASE TURN THE BOULDER BACK to preserve the organisms being being studied. 18 The centipede Strigamia maritima is not well known, but in some areas is very common. It doesn't look much like garden centipedes, whereas the non- Ligia woodlice with which it frequently shares this habitat seem very familiar. 19-21 Where there is a modicum of sea water Gammarus spp. can be found. They lurk in huge numbers under suitable stones and can be found beneath seaweed and in rock pools: just about everywhere. Sorting them our to species is a job for the specialist or the meticulous enthusiast. 22-23 Acorn barnacles can inhabit rock surfaces in unbelievable numbers. There are only two main species to trouble us on the seashore, but others may be found below low water or in specialist situations, such as piggy-backing on periwinkles (Balanus hameri ?). Look closely and you will discover that such barnacles are different from the commmon species such as Semibalanus balanoides which also grows on molluscs, but those that don't move e.g. mussels. As adults, these are static crustaceans. The larva (cypris) attaches itself to rocks etc. by its head and develops a shell with an aperture through which it spreads its paddling legs when under water to collect suspended food material. Surprisingly, fertilisation does not occur at random in the sea, but the male finds females with its enormously long penis and fertilises them in situ . 24 Not far below high water on exposed shores there is a relatively narrow band of barnacles that, on very close inspection (a hand lens is essential, and prolonged stooping and painful, barnacle-pitted knees are inevitable), can be identified as Chthamalus montagui . (Careful of spelling and pronunciation; this is not 'Chthalamus'). It has a relatively well-constructed shell, not easily damaged with a finger nail, which is much more robust than that of the neighbouring barnacle species. 25 Two main features characterise C. montagui . The aperture is shaped like an old- fashioned kite (diamond-shaped, but longer below and shorter above the mid line) and the rostral plate underlaps those on either side (compare with description and illustration of S. balanoides , slide 27). 26 The most numerous barnacle on British shores is Semibalanus balanoides which forms a wide zone lower down the shore than C. montagui . It is absent from exposed shores and can be incredibly numerous on sheltered shores. It is poorly constructed, and breaks up fatally when picked at by a curious biologist. This fragility enables populations to compete for space, and vigorous individuals can exclude others, weaker than themselves, gaining more room in which to grow. Sometimes these barnacles do not evict one another, instead growing to great height (in barnacle terms) side-by-side. 27 Two main features characterise S. balanoides . The aperture is a regular, equilateral diamond shape and the rostral plate overlaps those on either side (compare with description and illustration of C. stellatus , slide 25). 28 The common limpet Patella vulgata is a gastropod with an uncoiled body, much like early molluscs, though this is very much a 21st century animal. It tends to inhabit a specific place on its rock, crawling away to graze when covered by the tide, but returning for the intertidal period of exposure. 29 Lower shore limpets tend to get covered in barnacles or seaweeds which may help disguise them from gulls which certainly feed on them. 30 For various reasons, perhaps poor camouflage, bad weather or the attentions of a large fish, some never make it back to base after a feeding trip. 31-32 The common, edible, mussel Mytilus edulis can be found in large colonies on solid rock and large boulders, particularly near fresh water or where organic pollution makes suspended food available to this filter feeder. It can also be found on particulate shores where it exists as lone individualsor small groups, often atttched by its byssus to stones, vacated shells or other sedentary molluscs such as cockles. The byssus is a feature shared by a number of other bivalves and is a tuft of exceptionally strong proteinaceous fibres which rapidly cement themselves to anything within reach. Small mussels of this and other species can be found densely packed along cracks in rock where few can attain maturity. 33 Periwinkles come in variety, tend to occupy overlappping, but definable zones and can be difficult to identify with certainty. However, if one eliminates all but the commonest four species, identification is possible and ecological data may be successfully gathered. 34-35 Common periwinkles Littorina littorea may be found from the middle of the shore downward. In counting them, care should be taken to look under stones and seaweed otherwise significantnumbers will be overlooked. (For identificationguide see slides 42-43). 36-37 Rough periwinkles L. saxatilis occupy the upper regions of the shore, being so tolerant of conditions above the tide that they are almost terrestrial animals (see notes to sldes 8-15). (For identification guide see slides 42-43). 38-41/44 Until relatively recently, flat periwinkles were considered to be a single species L. littoralis . However, these days there are two common species which, if you look closely, are not difficultto tell apart: L. obtusata and L. mariae . (For identification guide see slides 42-43). They can usually be found grazing on the fronds of the wrack seaweeds from mid-shore downwards where some colour morphs successfully mimic bladders, perhaps escaping the attention of fish that certainly feed on winkles. 42-43 Identifying four of the commonest periwinkles (hopefully, self explanatory). 45-56 Unlike the periwinkles that graze, dog whelks Nucella lapillus are predatory carnivores. They can be found wherever their favourite food, mussels and barnacles are and, if you lift them off their prey, you can often see what they have been up to, particularly on a live mussel (see slides 51-56). At first sight they may be mistaken for common periwinkles (slide 47), but the the shell is rougher and more 'spired', and the opening has a distinct channel where the occupant's respiration tube (siphon) emerges. Dog whelks have a radula for boring through the shells of prey and produce hydrochloric acid (dissolves the calcium carbonate of which shell is mostly constructed) to assist in this process. 57-59 The collembolan Anurida maritima (formerly known as Lipura maritima )isa minute primitive insect, fossilised ancestors of which have been discovered associtated with some of the first land plants in Devonian rocks (rhynie chert) which are some 450 millionyears old. Truly marine insects are very unusual and Anurida is no exception, for it never really comes into contact with sea water, being coated in wax and totally unsinkable. It never uses the sea as other real marine animals do for respiration, bodily mositure and reproductive processes, and might as well be considered a terrestrial insect did it not live exlusively on the sea shore.

60 Pomotoceros triquetur is just one of several sea shore worms that build a protective, calcareous tube to live in, but it is featured here because it is probably the commonest and most wide-spread. It is used in the laboratory to demonstrate animal fertilisation and embryology, for if evicted from their tubes and set aside, both male anf female worms release their gametes into the water, as they do from within in the wild. If the worms have been segregated by sex, the student may mix eggs and spermatozoa and observe fertilisation over the following few hours and further development, later, daily. 61 Animals of the lower shore. 62-63 Sponges abound on and under rocks of the lower shore. Just two are illustrated. Interesting experiments may be performed with Halichondria (which comes in a selection of colours from almost white to greens and browns). Its components can be disaggregated by careful mashing through a sieve and then, if left alone a while in a container of coll sea water, they will reassemble to create a new, somewhat amorphous, but more or less functional sponge. 64-66 Only the beadlet Actinia equina among several common sea anemones is illustrated for it is found all over shores where there is rock for attachment (see also snakelocks Anemonia viridis and dahlia Urticina felina anemones at low tide). It comes in several colour forms, but deep red is by far the most frequently encountered. Like Pomotoceros and Halichondria , Actinia is an excellent experimental animal, for it displays territorial aggression bahaviour, dominant individualscausing others to submit to a battering with tentacles and blue coloured organs called acro ragae then float away. This activity can all be easily observed in the laboratory. 67 Lineus longissimus is (or can be) the longest animal in the world, specimens having been measured that were even longer than the biggest blue whale! It is very commonly found under boulders where it lives as a knotted tangle when not out being, somewhat incredibly, a predatory carnivore. With care the head end can be detected, but it still seems to live a life with no apparent purpose or organisation, and one wonders how it knows where various parts of its body might be. Other, shorter, nemerteans of assorted colours may also be found. 68-69 There are many more purposeful seeming worms than Lineus and the ragworms, which are also voracious predators, frequently achieve significant size. One as big a the specimen of Nereis diversicolor in the picture should be handled with a little respect because its extrusible tooth-bearing pharynx, used to catch and devour crustceans etc., can give a finger an alarming, if harmless, nip. The parapodia bear spiny chaetae and no leaf-like paddles. 70-71 Like Nereis , Phyllodoce species can be found in sand, but they are usually smaller individuals or smaller species (e.g. P. maculata see lecture 5, slide 68). Instead of three spots per segment as in P. maculata , this worm has brown patches on its paddles and a brightly coloured iridescent sheen on the dorsal surface. The parapodia bear spiny chaetae plus leaf-like paddles which make it a competent swimmer when under water. 72-73 There are several common species of scale worm (polychates like the preceding two worms), but this author has yet to study them well enough to tell them apart by name. Harmothoë might be the correct generic name for this one, but I am not confident of my identification. 74 Spirorbis species abound on rocks and seaweeds low on the shore. They are small and live in a spiral calcareous tube, and this worm Spirorbis spirorbis, lives exclusively attached to fronds of Fucus serratus . Like its cousin Pomotoceros, Spirorbis is an excellent tool for simple embryology experiments and, with care, young spirals can be generated, attached to F. serratus fragments in a lab. receptacle within a few days. A WORK OF POETIC GENIUS BY STEVE MEES student and proud 'father' of a wriggly horde at Millport, 1979 Originally published inScallopel (special maritime edition of Scalpel , the house magazine of the Biology Department, University of York) 1. The hour is late, the beer is waiting, But hold it, hush, Spirorbis mating. Yikeroos! by a process magic It's given birth to things pelagic. 2. Orange zizzlies zooming round Fairly soon to be frond-bound. With algal thrutch, more thrusts to come, It eventually ends, held fast by bum. 3. And then, behold, watch the Fucus , The baby is secreting mucus. Round and round, but without haste Hooray, Spirorbis perpetuates! 75 Chitons are unique among molluscs in that they have an articulated shell, rather like that of a woodlouse or armadillo. However, they do not move much, having the standard single, sucker-like molluscan foot. 76 Flat top shells Gibbula umbilicalis begin life as fairly flat, but they hunch up with age and become very worn and rounded. 77 Whelks Buccinum undatum can be found wandering about the sea floor at low springs or under rocks higher up the shore. The shell closure (operculum) is carried on the end of the foot when not in use and the siphon held out to pick up oxygen- rich water. 78 Whelk eggs are laid in clusters and, when hatching is over, they become a familiar feature of the strandline. 79 Close-up includes a sea squirt, centre (see slides 87-90) and Pomotoceros triquetur (slide 60). 80-81 Commonest of the crabs is the shore crab Carcinus maenas which feeds on mussels etc., cracking them with powerful claws (chaelae) by exerting continuous pressure until the fabric of the shell gives way making the contents available. They are also carrion feeders. Other crabs that might be found occasionally are the edible crab Cancer pagurus and, sometimes, spider crabs. 82 Small, young shore crabs are often patterned giving them the ability to hide by camouflage in various substrata. 83 Included in the diet of the common starfish are bivalve molluscs, particularly scallops which it recognises by their 'flavour'. Scallops, for their part, can taste starfish and escape by clapping their shells, vigorously expelling water and jetting away like snapping dentures. If it succeeds in grabbing its prey, the starfish surrounds it with its arms, clamped in place by powerful tube feet, pulls the shells apart and inserts its stomach, digesting the unfortunate scallop in situ . 84 Small urchins Psammechinus miliaris live, often in small groups, under stones low on the shore. They adorn themselves with stones, and fragments of shell and seaweed, held in place by tube feet which let this disguise fall off if the urchin is disturbed, a rather temporary camouflage. 85 The large edible sea urchin Echinus esculentus is only found exposed during low spring tides. It has a large grazing organ around the mouth known as 'Aristotle's lantern', which has five highly specialised teeth. E. esculentus live on kelp and under rocky overhangs, always submerged, but they are a favourite food of gulls which are able to catch them, bring them inland and smash them on the rocks to eat. People, especially the French, like to eat the male gonads. 86 There are three common brittle stars which live in the protective cover of boulders and Laminaria holdfasts when young. Out to sea, the floor is often entirely covered by untold numbers of brittle stars. Ophiocomina nigra is illustrated. Ophiothrix fragilis and Ophiura ophiura may also be found. 87-90 Sea squirts are almost chordates, because the larva has a rudimentary notochord. The adults lack this feature and are all sedentary, feeding and respiring via short in and out siphons. They may be solitary, paired, grouped or collonial 91 Whenever you turn a rock on the lower shore there is a good chance of finding a fish awaiting the tide. There are many possiblities, but the butter fish Pholis gunellus (a blenny) is almost a certainty. Try to catch it with your hand! 92 One other likely fish find is the shannyLipophrys pholis . 93-94 Sea mats - bryozoa - colonies are found on the fronds of wracks and kelps on the lower shore. Structure is not easily understood with the naked eye, but place a frond fragment in a dish of sea water and examine bryzoa with the dissecting microscope (top-lit) and, when the animals emerge to feed . . . fascination! 95 Seaweed surfaces are home to a wide variety of organisms: encrusting, colonial and microscopic. Examine back at the lab. with a top-lit dissecting microscope, patience and good field guides. 96 Limaria (formerly Lima ) hyans , the file shell, is unable to close its shell from which scarlet tentacle-like mantle projections protrude. This mollusc has a very powerful shell closing adductor muscle. When in open water, i.e. when not lurking safely within the holdfast of Laminaria saccharina , it swims quite efficiently by snapping the shell valves together.