Benthic Living: The Seashore - Elements of Marine Ecology PDF

CHAPTER 6 Benthic living: the seashore Every country in the world with a coastline has seashores. These vary from classic san- dy beaches used by holiday makers to vertical cliff faces. Whatever their form, sea- shores encompass the fringe of land between the lowest of low tides and the highest of...

CHAPTER 6 Benthic living: the seashore Every country in the world with a coastline has seashores. These vary from classic san- dy beaches used by holiday makers to vertical cliff faces. Whatever their form, sea- shores encompass the fringe of land between the lowest of low tides and the highest of high tides for that particular area. Also called the intertidal or littoral zone, the sea- shore forms part of the ocean seabed, albeit one that is only covered by water when the tide comes in. The causes and effects of tides are described in Section 2.9. Organisms that live on or in the seabed, anywhere from the seashore down to abyssal depths, are termed the benthos. In this chapter the ecological way of life of benthic seashore organisms is described, whilst Chapter 7 covers the equivalent ecol- ogy of sublittoral (subtidal) organisms. 6.1 Problems and solutions for intertidal living Living on the seashore poses a number of special difficulties for marine organisms. This is a harsh environment, where the physical conditions change hour by hour as the tide ebbs and rises. When the tide is out, there is little protection from rain and snow, from scouring ice in polar regions, from hot sun and drying winds and from crashing, storm-generated waves. Organisms living on seashores where low tide falls in the middle of the day will experience the greatest fluctuations in some of these condi- tions. However, the first and most obvious problem is how to cope with continuous alternate submergence by water and exposure to air. Even when the tide is in, the physical and chemical conditions in the shallow water along the coast are less stable than in deep water. In particular, there are wider and more rapid changes of temperature and fluctuations of salinity associated with evaporation, or freshwater dilution. Often the inshore water is also very turbid, because quantities of suspended matter are churned up from the bottom by waves, or carried into the sea by rivers. On most shores the ecological conditions are dominated by the tides and the waves. The detrimental effects of exposure to air restrict much of the intertidal population to sheltered parts of the shore, which are not left completely uncovered at low tide. Many algae, anemones, hydroids, bryozoans, shrimps, prawns and fish occur only in rock pools, where they are safe from drying and relatively protected from wide tem- perature fluctuations. Shelter can also be found between the fronds and holdfasts of Elements of Marine Ecology r 2023 Elsevier Ltd. DOI: https://doi.org/10.1016/B978-0-08-102826-1.00001-6 All rights reserved. 257 258 Elements of Marine Ecology the shore seaweeds, under stones and boulders or in rock crevices. Some of the most numerous shore animals have a flattened shape well suited for hiding in narrow spaces, for example the crab Porcellana platycheles, the leptostracan crustacean Nebalia, amphi- pods, isopods and chitons. Others burrow into the shore deposits for protection and these comprise virtually the entire population of sandy and muddy shores. Environments with fluctuating conditions favour the evolution of species that exhibit wide variations, both physiological and anatomical. Where an unstable habitat also includes environmental gradients, different forms of a species are likely to occupy different zones. On the seashore it is obvious that some species are highly variable, with differences which can be correlated with environmental variables and sometimes with differences of zonation. For example the Bladder Wrack (Fucus vesiculosus) nor- mally has distinctive pairs of air bladders, but when growing on wave-exposed rocks, these are often lacking. The periwinkle Littorina saxatilis exhibits differences in shell size and shape, colour and surface texture, but this species is easily confused with sev- eral very similar species (see Section 6.3.3). The Dogwhelk Nucella lapillus and the mussel Mytilus edulis can also be polymorphic, with some evidence of different forms in different localities around Great Britain (Kitching, 1977). 6.1.1 Drying out The majority of seashore inhabitants are essentially fully marine aquatic organisms that have evolved adaptations for survival in a partially aquatic environment. When left exposed to the air, they start to lose water by evaporation and would eventually die from dehydration if not resubmerged within a certain time. Organisms which live in exposed positions on the surface of the shore must therefore have some means of retarding the rate of water loss sufficiently to survive during the periods when they are left uncovered during the tidal cycle. The danger of desiccation is most severe where exposure to air also involves exposure to sun or wind. Water loss can be fatal in several ways. Death may be due to disturbances of metabolism resulting from the increasing concentration of internal fluids. In many cases the immediate hazard is asphyxia some organisms require a continuous cur- rent of water over the gills for adequate gaseous exchange. Others can survive for a time in air, but all must preserve at least a film of water over their respiratory surfaces (Box 6.1). In a fish out of water, the weight of the gill lamellae, when unsupported by water, causes them to collapse against each other and adhere by surface tension. Only a small area of gill surface is then left exposed for respiratory exchange and the fish asphyxiates, despite the high oxygen content of the air. Intertidal organisms have solved the problem of water loss in a variety of ways and some are better at it than others. This is one (but only one) of the drivers behind shore zonation as, in simple terms, those organisms that are better at preventing water loss,  Benthic living: the seashore 259 BOX 6.1 Intertidal fishes. Most of the many different species of intertidal fishes follow the tide down the shore or retreat into rock pools as the tide ebbs. However, some species have physical and physiolog- ical adaptations that allow them to survive out of water for many hours. The Shanny (Lipophrys pholis) (Fig. 6.1), found on seashores in the NE Atlantic Ocean, is an expert in this field. Although it often lives in rock pools, it can survive under damp seaweed or rocks for many hours and can cross between one pool and another when the tide is out. It has a sli- my, scaleless skin through which it can absorb oxygen as long as it remains damp. It has also been shown to exhibit homing behaviour, allowing it to navigate back to a safe and familiar pool (Jorge et al., 2012). can live higher on the shore (see Section 6.2.1). The most obvious solution is to have a protective covering to prevent excessive drying. In this respect animals such as mol- luscs and crustaceans that have a hard, impermeable shell, are at an advantage. Gastropod molluscs (Gastropoda) are abundant on many rocky shores and most can withdraw into their shell and close the opening with a sturdy operculum. This helps protect them from predators, but in intertidal species, ‘shutting the door’ also helps prevent water loss. Periwinkles (Littorinacea), top shells (Trochoidea), dog whelks (Muricacea) and serpulid worms (Sabellida) are all common intertidal inhabitants and close the shell aperture in this way. This is particularly important for species such as Rough Periwinkles (L. saxatilis agg.) that live high up on the shore. However, closing the shell with an operculum makes it more difficult to cling onto rocks and stay in the same, safe place whilst the tide is out. So rough periwinkles can secrete a mucus that glues them temporarily to the rock. This can lead to the slightly strange sight of a peri- winkle apparently defying gravity stuck on a rock on its side, rather than in the normal position when clinging on with the foot. In barnacles (Crustacea, Cirripedia), the movable plates of the shell, the terga and scuta, are kept shut most of the time when the animals are uncovered, occasionally opening momentarily to allow gaseous exchange within the shell. Some barnacles such as Semibalanus and Chthamalus (see Section 6.3.2) which can live high on the shore do not open the shell, but instead have a tiny hole called a micropyle through which gaseous exchange can take place with minimal water loss. The legendary ability of limpets (Patelloidea) to clamp down onto rocks allows them to retain water under their shell. Some, such as Patella species, return to the same spot each time the tide recedes and eventually wear a groove in the rock into which the edges of the shell fit exactly. Limpets lift the edge of the shell slightly to allow oxygen and carbon dioxide to diffuse in and out without allowing much evaporation. Some seaweeds such as the brown wracks (Fucus spp.) that dominate many shores on both sides of the North Atlantic, exude mucilage which reduces evaporation and 260 Elements of Marine Ecology Figure 6.1 Intertidal organisms employ a variety of methods to survive whilst the tide is out. (A) The limpet Patella vulgata clamped tightly to rocks (right shows underside of foot); (B) the Common Periwinkle Littorina littorea closes its shell with a watertight operculum; (C) the strong holdfast and slippery fronds of Bull kelp Durvillaea potatorum; (D) the Shanny Blennius pholis absorbs oxygen through its slimy skin. when the tide is in, allows the fronds to slide easily over each other with wave action. Most anemones are too soft-bodied to survive on exposed rocks, but the Beadlet Anemone (Actinia equina), common on shores in the NE Atlantic, can withdraw all its tentacles and also has a slimy, protective coating.  Benthic living: the seashore 261 To some extent animals adapt to the drying conditions at different shore levels by metabolic adjustments. For instance, specimens of the limpet Patella vulgata living at high shore levels have lower respiratory rates, lower rates of water loss and can tolerate greater percentage water losses than those low on the shore during summer (Davies, 1966 1970). In addition to losses by evaporation, animals also lose water by excretion. The majority of marine animals excrete ammonia as their chief nitrogenous waste product. This is a highly toxic substance which has to be eliminated in a very dilute urine, involving the passage out of the body of a copious amount of water. On the seashore, this must present a difficulty to animals already in danger of desiccation and some of the littoral gastropods reduce their excretory water loss by excreting appreciable amounts of uric acid, a less soluble and less toxic substance than ammonia and which can be excreted as a semisolid sludge, thereby conserving water. Species of periwinkles living higher up on temperate seashores have the ability to excrete more of their waste products in the form of uric acid than those living lower on the shore. Excreting uric acid instead of ammonia is a trade-off between saving water and saving energy, as pro- ducing uric acid requires more energy than producing ammonia. 6.1.2 Temperature fluctuations During low tide, wide and rapid changes of temperature can be encountered on the shore. Strong sunshine can produce high temperatures on exposed shore surfaces, and the temperature of any water standing on the shore when the tide recedes, may be raised well above the normal limits. Shallow pools on English coasts sometimes reach a temperature of 25 C 30 C on hot summer days. In the tropics, temperatures of 50 C or higher have been recorded in shore water. Intertidal organisms may also be exposed to severe frosts. When shore water freezes, they face the additional dangers of moving ice, which may scrape them off the rocks or crush them within their hiding places. In high latitudes the shore may be kept virtually barren by the effects of moving ice. Most marine invertebrates are poikilothermic, with body temperatures that match that of their surroundings. Some are physiologically better able to withstand temper- ature variations than others and this is described in more detail in Section 4.2.4 (Effects of water temperature on physiology). However, many intertidal animals use behavioural responses to avoid temperature extremes and reduce water loss. Rock crevices, holes and fissures on rocky shores are often crammed with gastropod mol- luscs that move into such shady, damp spots as the tide recedes. Sessile, soft-bodied animals such as sponges can often be found relatively high up the shore on the shaded roofs and sides of extensive crevices and on the cool underside of rocks and boulders. 262 Elements of Marine Ecology Intertidal species not only have to contend with daily and seasonal changes in tem- perature (especially in temperate zones) but also with longer-term fluctuations. This can lead to modifications in the distribution of species, especially at the edges of their normal northward or southward limits. The prolonged and severe cold weather expe- rienced around Great Britain in the winter of 1962 63 produced noticeable reduc- tions in the northward and eastward distribution of southern shore species, such as the Toothed Topshell (Osilinus lineatus), in spite of its tolerance of a wide range of tem- peratures. Now, possibly as a result of ocean warming, this species is extending its range northwards and reproducing over a longer period of the year. 6.1.3 Waves and surf Enormous forces are transmitted to the shore by breaking waves. The destructive impact of a great weight of water, together with stones and other suspended matter hurled by the waves, presents a major hazard to surface-living shore inhabitants. Beneath the surface, burrowing forms are safer, but still face the danger of being crushed when waves churn beach deposits. When masses of stones, sand, or organic debris are washed up and stranded by the waves, the shore population is in danger of becoming smothered. Continuous rapid movement of the water presents difficulties for the settlement and attachment of spores and larvae and in very wave-exposed places, may prevent colonization of the shore except in crevices and sheltered parts. There is also the danger of dislodgement by waves, which may carry mobile ani- mals up or down the shore to levels unsuitable for their survival, as well as potentially damaging them. Shells are again the chief form of protection from physical damage. The heavy wear sometimes visible on the shells of shore molluscs indicates the severity of the abrasion to which they are subjected. Many rocky shore organisms have adaptations that allow them to clamp firmly to the substratum and resist dislodgment and some have exceptional powers of adhesion. Sublittoral fringe kelps, whose extensive fronds mean they are subjected to consider- able drag, have particularly strong holdfasts (Fig. 6.1C). Barnacles and serpulid worms have shells firmly cemented to the rock. Mussels (Mytiloida) attach to rocks and stones by strong byssus threads (Box 6.2). The remarkable adhesion of the foot of Patella has given rise to the expression ‘sticking like a limpet’. These limpets have a large and muscular foot, but suction is not the only mechanism behind their sticking ability. Specialised mucus on the foot acts as a lubricant when the animal is moving but can change state under the influence of enzymes, to become a strong adhesive. Many other marine gastropod molluscs can also alternate between a glued down state and actively moving around (Smith, 2002). Some genera of coastal and intertidal fishes have the pelvic fins specialized to form a ventral sucker by which they can cling to a firm surface. This makes them  Benthic living: the seashore 263 BOX 6.2 Mussel byssus. The strong attachment system used by mussels is so efficient that it has inspired many stud- ies with a view to improving man-made adhesives and protective coatings, especially for underwater use. The byssus of an individual mussel consists of a system of acellular, secreted threads tipped by adhesive plaques. The threads are deposited radially around the mussel in order to spread the load. Each thread originates from within the shell and this proximal por- tion or holdfast can be jettisoned allowing the mussel to change orientation and position and reattach. Cohen et al. (2019) describe the structure of the byssus and the multiscale mechanics of the whole system, which is mechanically and chemically complex. The tiny adhesive plaques are filled with a foamy, protein matrix and various fluids and can conform to microscale irregularities in the rock surface. Collagen fibres from within the threads stretch into the plaque material. Thread and plaque are covered by a hard cuticle. particularly well-adapted to shore life. In European waters, gobies (Gobiidae) and clingfish (Gobiesocidae) which have such suckers are common shore fishes. The European Lumpsucker (Cyclopterus lumpus) has an especially strong sucker because the eggs are laid and attached to rocks close to shore, often within the zone of breaking waves. The male then remains to guard them for several weeks. 6.1.4 Salinity fluctuations Shore organisms often encounter water of much reduced salinity due to dilution of the shore water by rain or freshwater flowing off the land. On the other hand, evapo- ration may raise the salinity of shore water above that of normal seawater. Increased salinity and raised temperature usually occur together. Organisms living in estuaries may experience similar daily salinity fluctuations. Most marine organisms cannot tolerate sudden changes from normal salinity, for any length of time. However, some species can either tolerate changes to their osmotic equilibrium or control such changes, as described in Section 2.2.1 in the subsection on Physiological effects of changing salinity osmotic regulation. Species in either of these cate- gories can do particularly well in intertidal habitats, with reduced competition from similar species that lack such adaptation. Examples include lugworms (Arenicola spp.) and the Shore crab (Carcinus maenas), which is abundant on shores in the NE Atlantic. 6.1.5 Sunlight The illumination of the shore varies widely with the rise and fall of the tide. When the tide recedes during daylight hours, the shore is directly exposed to sunlight. When the shore is covered, the illumination is much reduced, especially where the water is very turbid. However, when the tide is out and without the support of the water, 264 Elements of Marine Ecology seaweeds and algae lie in collapsed heaps and so cannot anyway photosynthesize well. In any case very high intensities of light can be detrimental to many algae. Strong sun- light is detrimental to many organisms due to the combined effects of radiation, heat- ing and drying, but it is difficult to dissociate their separate influences. 6.1.6 Gaseous fluctuations and respiration Whilst shore pools can and do provide a refuge for fish and other mobile animals, where they can remain submerged and continue normal respiration when the tide recedes, nevertheless the levels of oxygen and carbon dioxide in small shore pools can fluctuate significantly. In larger pools such changes are likely to be moderate. During periods of emersion when the tide is out, photosynthesis and respiration alter the relative amounts of oxygen and carbon dioxide in shore pools, with consequent effects on pH. In bright light, photosynthesis by dense algal vegetation produces oxygen and can raise levels appreciably, whilst carbon dioxide produced by the vegetation and animal respiration is used up. This leads to higher pH levels (more alkaline). In similar pools exposed by the receding tide at night, oxygen levels can fall dramatically and carbon dioxide levels can rise as a result of seaweed and animal respiration, leading to lower (more acid) pH levels. This will obviously affect fish and other animals living in such pools. Diminished oxygen, increased carbon dioxide and reduced pH may also result from rapid bacterial decomposition in stranded detritus, both within pools and outside them. The majority of shore-dwelling animals respire using gills of varying design, which can absorb the oxygen dissolved in seawater. Any such animals living outside of shore pools may face long periods of reduced respiration. Intermittent submergence presents problems in connection with respiration because no respiratory organs function equally well in both air and water. For animals living high up the shore, especially within the littoral fringe, the infrequency of immersion calls for the ability to breathe air. Some of the inhabitants of this fringe zone are essentially marine forms which have become adapted for aerial respiration and they face the problem of drowning if sub- merged for too long. Air-breathing shore animals have either evolved from landforms, which have spread to the seashore, or have evolved directly from marine forms, their respiratory organs having become adapted to absorb atmospheric oxygen. In the for- mer category are some insects and gastropod molluscs. Insects are essentially land ani- mals restricted to air breathing (though many freshwater insects have aquatic larval phases, as do a very few marine ones), but a variety of insect groups have adapted to live along the fringes of the shore and along the strandline feeding on detritus. Some show adaptations for storing air and can survive short periods of submergence. The collembolan insect, Anurida maritima, widespread among rocks above mid-tide level, carries a layer of air among its surface bristles, whilst the intertidal beetle, Aepus  Benthic living: the seashore 265 marinus, has internal air sacs for air storage. The Marine Bristletail Petrobius maritimus avoids submergence, feeding mainly on lichens on maritime cliffs and rocks. Land- dwelling gastropod molluscs (snails) breathe using a pallial lung developed from the mantle cavity and some marine upper-shore gastropods, such as Otina and Leucophytia, have evolved from land-dwelling forms and do the same. All air-breathing gastropods make up an informal group known as pulmonate gastropods. A variety of crustaceans have evolved from marine forms, to live high up on the shore. They have modified gills and particular behaviour patterns that allow them to survive in air for prolonged or indefinite periods. The NE Atlantic amphi- pods Talitrus saltator and Orchestia gammarellus have gills and can live fully sub- merged but are usually found scavenging amongst damp piles of strandline material. Their gills can function as long as the air around them remains moist. The sea slater Ligia survives in a similar way and can extend its range well above the highest tides. The giant-sized, tropical Coconut Crab (Birgus latro) and the Christmas Island Red Crab (Geocarcoidea natalis) live entirely terrestrial lives, but like all crustaceans remain dependent on reaching the sea (or freshwater in some cases) to release their aquatic eggs. Birgus has modified gills in the form of a bran- chiostegal lung (Farrelly and Greenaway, 2005) and will drown if submerged for more than an hour or so. Various species of marine littorinid gastropods such as the Black Periwinkle (Melarhaphe neritoides) and the Rough Periwinkle (L. saxatilis agg.) have also evolved to the stage where they cannot survive permanently sub- merged. The gill (ctenidium) is reduced and the mantle cavity is modified to func- tion as a lung. Melaraphe lives high up in the splash zone mostly above high water and like the Coconut Crab is only really tied to the shore by its aquatic planktonic larva. 6.1.7 Reproductive adaptations The difficulties of survival on the shore affect all phases of life, including reproductive processes and larval and juvenile stages. The majority of benthic organisms start life as planktonic floating or swimming forms and may become widely dispersed in the water before they settle on the sea bottom. Shore animals risk great losses of pelagic eggs and larvae during this phase, if they drift far from the shore and settle outside the zone in which their survival is possible. For some inhabitants of the shore, the chances of suc- cessful settlement in suitable areas are enhanced by certain aspects of the behaviour of their larvae. Some produce larvae which are at first strongly attracted by light and pre- sumably rise close to the sea surface during the day. Wind direction is often landward during the daytime, driving the surface water towards the coast and so it is likely that positive phototaxis improves the chances of pelagic larvae returning to the shore. At night, offshore winds tend to predominate and surface water is moved away from the 266 Elements of Marine Ecology shore with replacement water coming in shoreward along the bottom. Under these circumstances, descent of larvae to deeper levels away from the surface must then have a similar effect of keeping them concentrated along the shoreline. The larvae of many benthic species can discriminate between substrata and can for a time delay settlement until favourable conditions are encountered (Rainbow, 1984) (see Section 7.1.2). Some tend to settle gregariously, often in response to the presence of successfully metamorphosed members of the species. Examples include many barna- cles, the reef-building worm Sabellaria alveolata, many serpulid worms, mussels and some bryozoans. Settlement in shallow water may also be favoured by larval response to wave action, for example, cyprids of Semibalanus balanoides are reported to settle more readily under fluctuating water pressure. When settlement occurs in the sublitto- ral, or at lower levels of the shore than are usually occupied by the adults, the responses of the juveniles to various environmental stimuli may cause migration up the shore towards the appropriate zone. When the planktonic larvae of Black Periwinkle (M. neritoides) metamorphose, they tend to settle within the barnacle zone on rocky shores. The young then move further up into the splash zone responding to light and gravity. In many shore animals the planktonic phase is abbreviated or omitted, and this simplifies the problem of finding the correct shore level. For instance, the lugworm Arenicola marina, which is one of the most successful intertidal worms burrowing in muddy sand in the North Atlantic, has only a brief pelagic period. In late autumn or early winter the gametes are shed from the burrow onto the surface of the sand during low spring tides and here fertilization occurs. The fertilized eggs may be dispersed up the shore to a limited extent by the rising tide, but being heavier than water and slightly sticky, they tend to adhere to the surface of the sand. They hatch after about 4 5 days and the larvae, although capable of swimming, seem from the outset to bur- row into the deposit wherever the substratum is suitable. Direct development Other shore animals completely eliminate pelagic stages by developing directly from egg to miniature adult form. These eggs are well charged with yolk to enable the young to hatch in an advanced state. The Flat Periwinkles Littorina obtusata and L. faba- lis deposit eggs in gelatinous masses on the surface of seaweed. The young occasionally emerge as advanced veliger larvae but probably more often do not hatch until after the velum has been resorbed and then appear as tiny crawling winkles. The Dogwhelk (N. lapillus) lays vase-shaped egg capsules which often occur in large numbers stuck to the underside of stones or sheltered rock surfaces. Each capsule contains several hun- dred eggs, but eventually only a dozen or so whelks crawl out of each capsule, the rest of the eggs serving as food for the first few to hatch.  Benthic living: the seashore 267 Parental protection Eggs laid on the seashore are exposed to all the vicissitudes of this environment and some shore animals provide a degree of parental protection. For example, several species of inshore fish guard their eggs, such as the Butterfish (Pholis gunnellus) and the Shanny (Lipophrys pholis). Females lay sticky masses of large eggs from which advanced young are born and one of the parent fish, usually the male, remains close to the eggs until they hatch, courageously protecting them against marauders. Female pipefish lay their eggs in a pouch on the male’s belly. Here they remain until they hatch as miniature adults. Amphipods and isopods, often very numerous on the shore, also retain their eggs within a brood pouch from which fully formed young emerge. In the gastropod mollusc L. saxatilis, the eggs remain in a brood pouch in the mantle cavity until they hatch as minute winkles. The tiny bivalve Lasaea rubra, often abundant in rock crevices and empty barnacle shells, incubates its eggs and young within the gills until they are suffi- ciently developed to crawl out and maintain themselves near the parent. The Viviparous Blenny (Zoarces viviparus) gives birth to well-developed young about 4 cm in length. Some sublittoral fish species such as the California Grunion (Leuresthes tenuis) deposit their eggs onshore, where predators are fewer in number. The synchronous spawning of this species also means that any predators there, such as seabirds, are overwhelmed by the sheer number of eggs laid. 6.1.8 Food and predation Despite its dangers, the shore is often densely populated by a variety of organisms excellently adapted to the difficult conditions. So great are the numbers on some shores that every available surface is colonized and there is severe competition for liv- ing space. A numerous population indicates an abundant supply of food and this is derived from several sources. On rocky coasts, especially in temperate areas, there is often a thick cover of seaweed. The rapid growth of these autotrophs is favoured by the excellent lighting conditions (when the tide is in) and by a good supply of nutri- ents. The nutrients are continually released and replenished by wave disturbance of sediments, weathering of the coastline and input from freshwater flowing off the land and are well distributed by water movements. Some animals browse directly on sea- weeds. Many more obtain food from the masses of organic debris formed by the break-up and stranding of pieces of seaweed. Even where there are no large seaweeds, the surface of the beach may be covered by a film of microscopic algae (see Biofilms in Section 7.3.2). In addition to primary production on the shore, large quantities of food are brought in on each rising tide. Inshore water is often rich in plankton on which innu- merable shore organisms feed, whilst they are covered in water. Also, pieces of plant material torn from the seabed below low tide level become deposited on the shore. 268 Elements of Marine Ecology The land, too, makes a contribution, various organic substances of terrestrial origin, from detritus to dead domestic animals, finding their way onto the beach. On the down side, few shore animals can feed adequately when the tide is out, especially filter-feeders. Thus feeding activities have to be concentrated into the times when the animals are covered by water. As the tide rises, some normally sublittoral animals, particularly fish, swim up onto the shore to take advantage of rich shore pickings. Other less mobile species ride in on waves. South African Plough Snails (Bullia spp.) have a large, fleshy foot which helps them surf up sediment beaches on an incoming tide in search of carrion. These scavengers have an excellent sense of smell which guides them to their food. The inhabitants of the seashore are exposed to a double set of predators. During submergence they are preyed upon by other marine creatures. When uncovered they encounter enemies from the land and air. On some parts of the British coast, seabirds exact a very heavy toll on shore populations during low tide. For example, oyster- catchers (Haematopus ostralegus) eat huge numbers of cockles from the large, intertidal beds in South Wales. Studies in the Burry estuary indicate that as many as 500 cockles per bird per day can be taken. Oystercatchers prefer 2-year-old cockles and in some circumstances, have been blamed for consuming up to 70% of the stock of this age group. However, local declines in numbers of oystercatchers have also been linked to exploitation of cockle beds by fishermen. In other areas more bivalves are taken by flatfish when the tide is in, than by waders when it is out. The Common Dab (Limanda limanda) found around NE Atlantic coasts is renowned for biting off the siphons of buried bivalves and may venture onto the shore when the tide is in. 6.1.9 Changes in behaviour and activity Whilst many shore organisms have physical and physiological adaptations to help them sur- vive whilst the tide is out, behavioural adaptations are also important. Shore animals must be capable of making appropriate adjustments of behaviour to meet the profoundly different conditions of submergence and exposure to air. The most obvious of these is a reduction or cessation of activity. When we visit a shore at low tide we see the animals in a quiescent state, which can perhaps be compared to seeing nocturnal animals during the daytime. Movement, feeding or reproduction is only possible for many intertidal species during the periods when they are covered by water. When uncovered, the heart rate slows (in those animals that have one) and they become much less active. In this quies- cent state their respiratory needs are reduced, water is conserved and by keeping still, there is less danger of attracting the attention of seabirds and terrestrial predators. Animals that live among algal fronds are also usually coloured to match their sur- roundings and some, such as the Sea Scorpion (Taurulus bubalis) have considerable powers of colour change to match different backgrounds.  Benthic living: the seashore 269 Restriction of movement as the shore dries during low tide may also help to con- fine mobile species to their appropriate zones. Some regulate their activity according to wind conditions, only moving about over the shore surface in calm or light winds and sheltering in crevices or under stones in strong, drying winds, for example, the top shell Phorcus lineatus (Courtney, 1972). In temperate areas many mobile animals show seasonal changes of level, usually moving slightly down the shore during the coldest part of the winter and ascending in spring. Wave splash as the tide returns is often the signal for mobile animals to start mov- ing about again (see also Box 6.3). The limpet (Patella), if wetted with freshwater, pulls its shell hard down and remains still, but if repeatedly splashed with seawater it begins to wander about. Lugworms (Arenicola spp.), the faecal casts of which are so common on northern European sediment shores, perform intermittent irrigation cycles, which replace the water in its burrow. However, before doing so, the worm moves back- wards up the rear end of its burrow and appears to test the quality of the surface water with its tail, modifying the subsequent sequence of irrigation activity accordingly. Endogenous rhythms Circadian and diurnal rhythms are common in animals, regulating physiology and behaviour to synchronise with a 24-hour cycle or a day and night cycle. However, for shore animals, day and night may not be as important as the ebb and flow of the tides and many show endogenous (built in) tidal rhythms. Many shore animals display cycli- cal changes of activity that have a tidal frequency, even when removed from the shore. This includes both invertebrates and fish, for example the Shore Crab Carcinus maenas, the polychaete Eurydice pulchra, the Shanny B. pholis (a small fish) and the prawn Palaemon elegans, all apparently controlled by endogenous rhythms. There are many early studies (1950s 1980s) on species such as these. However, a complex BOX 6.3 Travelling with the tide. The tiny estuarine mud snail Peringia ulvae, is very common on the surface of mudflats in the NE Atlantic, mainly above mid-tide level. When the snails are first uncovered by the tide, the majority are found crawling on the surface of the mud. In areas where the mud surface remains wet, the animals continue their active browsing on the surface throughout the tidal cycle, but where the surface dries, the majority of the population then burrow just below the surface, remaining buried until they are covered by the returning tide. Newell (1962) describes a cycle of behaviour related to feeding. As the tide ebbs, the snails follow the water down, feeding as they go. When the tide starts to flow back in, they float to the sur- face and are carried back to their starting level and at high water, numbers of floating Peringia can sometimes be skimmed from the sea surface. However, this observed behaviour may not be a universal or regular cycle of activity (Graham, 1988). 270 Elements of Marine Ecology interrelationship between tidal and circadian rhythms may well control activity in some intertidal animals. Chandrashekaran and Sharma (2010) review much early work on tidal rhythms and the relationship between tidal and circadian rhythms in intertidal animals. Mobile shore animals are in some danger that their own movements may carry them out of their proper zones into levels too high or too low on the shore or into positions too exposed to wave, wind or sun. Endogenous rhythms may help mobile animals find and keep within suitable parts of the shore. For example, in various small crustaceans which burrow in intertidal sand (such as Corophium volutator, Synchelidium, E. pulchra) an endogenous rhythm evokes emergence from the sand for swimming mainly during the ebb tide. This pattern of activity avoids the danger of stranding too high up the shore but promotes swimming at the stage of the tide when food and oxygen have just been replenished. Homing and responses to physical factors The ability to return to the same place on the shore after feeding excursions is obvi- ously advantageous in terms of safety, allowing animals to avoid desiccation when the tide is out and to remain at an optimal shore level. Some shore animals including fish and gastropod molluscs show ‘homing’ behaviour. Patient observational, marking and experimental work on rocky shores in the UK has shown that adult P. vulgata limpets clearly demonstrate such behaviour. When the tide recedes, the limpets usually return from their feeding forays to a particular site or ‘home’ on the rock, often from a dis- tance of 1 2 m. Patella feeds chiefly by scraping the surface with its long, toothed rad- ula, rasping off the microscopic film of algae which forms a slimy coating on the rocks. The limpets remain on their home spot until the tide returns, although some crawl around while uncovered on damp nights. Homing behaviour is most strongly developed in individuals living high on the shore. On returning home, Patella settles in the same position and orientation and the margin of the shell grows to fit the rock surface very accurately. On soft rocks the home is often marked by a ring-shaped groove, the ‘limpet scar’, conforming to the shell margin and worn into the rock by slight movements of the shell. The exact fit between shell and rock reduces water loss during exposure and also lessens the danger of the shell being prised off the rock by predators. Even today the exact mechanism by which Patella finds its way back to its home remains unclear, but these brainless animals are capable of varying their route home. In some shore animals it is evident that the direction of their movements is related to factors such as light (phototaxes), gravity (geotaxes), lateral contact (thigmotaxes), humidity (hydrotaxes) or direction of flow of water (rheotaxes). This is a complex field of study because animal behaviour is seldom altogether consistent, varying from one individual to another and sometimes changing at different stages of the life history or  Benthic living: the seashore 271 reproductive cycle. It can also be modified or even reversed by alterations in the con- dition of the animal or the environment, for example, by changes of temperature or salinity, the animal’s need for food, its state of desiccation or its previous experiences. Nevertheless, it has been demonstrated that some shore creatures display patterns of movement which carry them into situations for which they are well suited and enable them to remain in appropriate zones despite their need to move about over the shore in search of food or for mating. Some examples from around the British Isles serve to demonstrate such behavioural modifications. The movements of Lasaea rubra are influenced by light, gravity and contact (Morton, 1960; Morton et al., 1957). This tiny bivalve is widely distributed throughout the littoral zone, extending to a high level and occurring mainly in the protection of crevices, empty barnacle shells and tufts of splash zone lichens especially species of Lichina. Lasaea makes temporary attachment by means of byssus but is capa- ble of moving freely over the surface by using its extensible foot to crawl on a mucus film. On a level surface Lasaea moves away from light, but on a sloping surface it climbs even against the light. Its response to lateral contact overrides the effects of both light and gravity, causing the animal to move into crevices and small holes. Laboratory experiments have shown that Lasaea will crawl into a narrow hole even downwards towards bright light. The Flat Periwinkle L. obtusata is numerous under cover of middle-shore seaweeds, where it usually matches the weed in colour and often also with respect to size of air blad- ders (Gill et al., 1976). On level surfaces it usually moves away from light. L. saxatilis extends high in the littoral fringe, showing a strong tendency to move towards light and to climb. L. littorea is widely distributed across the middle shore in both sheltered and moderately exposed situations. The direction of wave action is one clue whereby this snail, if displaced, moves towards its original level (Gendron, 1977; Williams and Ellis, 1975). Its movements have been studied on the Whitstable mudflats (Newell, 1958a,b) and found there to be related to the direction of the sun. In this locality the feeding excursions occur mainly during the periods shortly after the winkles are uncovered by the receding tide, or submerged when the tide returns. The majority of winkles on the mud move at first towards the general direction of the sun, but later they reverse their direction. They there- fore tend to retrace their course, their overall movement following a roughly U-shaped path which brings them back approximately to their starting point. These animals, accus- tomed to a horizontal surface, show no geotaxic responses, but experiments with other specimens collected from the vertical faces of groins demonstrate responses to both light and gravity, these too moving over a U-shaped track, at first downwards and later upwards. Looped tracks have been reported for a number of other shore creatures, in some cases orientated to light, in others to gravity and such behaviour has obvious advan- tages in enabling free-living animals to range about over the shore without moving too far away from the levels in which they find favourable conditions. 272 Elements of Marine Ecology The adults of Melarhaphe neritoides occur high in the littoral fringe, but their eggs and larvae are planktonic and settlement is mainly on the lower shore. The attainment of adult zonation is brought about by a combination of responses to light and gravity, modified by immersion (Fraenkel and Gunn, 1961). This tiny winkle is negatively geotactic and climbs upwards on rock surfaces. It is also negatively phototactic and so will move into dark crevices. But the reaction to light reverses if the animal is immersed in water while it is upside down. If its crevice becomes submerged, Littorina neritoides therefore tends to crawl out along the ceiling towards the light and then climb higher on the shore. Vision Some shore animals have sufficiently well-developed vision to be able to see nearby objects and direct their movements by sight. An example is the NE Atlantic amphipod T. saltator, which burrows in upper-shore sand in the daytime and emerges at night during low water to feed on the surface. These feeding explorations carry it well down the shore, but it eventually finds its way back to high-water level. If removed from its burrow during daytime and released lower on the shore on a firm, unbroken sand surface, irrespective of slope of the beach or direction of sun or wind, it tends to move over the surface towards the back of the beach, where it burrows on reaching the drier, looser sand. If both eyes are covered, the movements of Talitrus released low on the shore are haphazard and show no tendency to carry it back upshore. Experiments both on the beach and in the laboratory suggest that Talitrus is capable of seeing shapes (form vision), that certain shapes attract it and that its movements towards the top of the beach are probably associated with its ability to see the line of the backshore, even in dim, nighttime illumination. Pardi (1960) and others have studied the movements of Talitrus from various parts of the coastline when placed above high-water level. They have demonstrated that the animals generally move in a direction which would carry them towards the sea in the localities from which they were taken, even when removed to areas remote from the sea. Their orientation is based on their sight of the sun or, in shade, on their perception of the polarization of light from the sky. Even in animals bred in captivity in uniform light, which have never had previous sight of the sun or contact with the shore, the orientation shows once they are exposed to sunlight. 6.2 Rocky shores Rocky shores exist where the effect of waves on the coastline is mainly erosive, wear- ing down the softer materials and carrying them away, leaving the hardest rocks exposed. Most of the substratum is therefore stable and permanent, forming a secure surface upon which a variety of attached organisms can live and grow, for example  Benthic living: the seashore 273 seaweeds, barnacles, mussels and limpets. The appearance of the shore depends largely upon the type of rock exposed. Horizontal strata often erode to a stepped series of fairly uniform level platforms which provide little shelter from the waves. Tilted strata running across the shore usually produce a very varied shore with numerous protrud- ing rock ledges and overhangs and deep pools in the gullies between them. Certain types of rock erode to a smooth surface, while some laminated rocks readily gape to form deep narrow fissures. Rocky shores make an excellent habitat and are often heavily populated, especially in areas where there is sufficient wave action to keep the water well oxygenated and to continually replenish the supply of nutrients, so favouring algal growth. The algae provide a primary food supply for animals and copious additional food is available from the plankton. Rocks present a variety of habitable environments such as exposed rock faces, sheltered overhangs, crevices, deep or shallow pools, silt within fissures or under boulders, in the shelter of algae or in their ramifying holdfasts. Rocky shores with their many different microhabitats are able to support a wide variety of species with different requirements. The size and composition of rocky shore communities are profoundly influenced by the intensity of wave action, because this is one of the major factors determining the amount and type of seaweeds and other algae on the rocks. This is the case on rocky shores throughout the world, though other factors may be equally important in extreme environments, such as on ice-scoured Antarctic shores. Where wave intensity is moderate, large algae can attach and grow to some size without being torn away. A cover of sea- weeds provides shelter for many small animals which cannot tolerate complete exposure to air and sun, for example cnidarians, sponges, bryozoans and small crustaceans. Stronger waves prevent or limit the growth of seaweeds and the rock surfaces become dominated mainly by animals that have the ability to attach themselves firmly to the rock surface. Barnacles and limpets, or sometimes at the lower levels mussels, are predominant on many wave-exposed rocky shores. In extreme conditions of wave exposure, rock faces are swept virtually bare and the population is restricted to fissures and crevices. Because of the wet- ting effects of splash, heavy wave action tends to raise the levels to which sublittoral and intertidal populations extend up the shore and greatly increases the width and height of the splash zone. Where rocks meet intertidal sand or where sand is deposited between rocks, their lower parts may be kept bare by the scouring effects of wave-tossed sand. The intensity of wave action on a particular shore is a difficult parameter to evalu- ate in the field. Some information can be gained by studying nautical charts showing the direction that the shore faces and the likely fetch of the waves (distance over which the wind can blow to generate waves). Measurements of wave heights in the surf zone can be made using various instruments such as bottom-mounted pressure transducers (Inch, 2014), but a long run of data is needed at any one site to make an accurate estimation. However, for field ecologists there is an alternative approach 274 Elements of Marine Ecology where degrees of wave exposure are defined in terms of their biological effects. A bio- logically defined scale of exposure to wave action was first devised in the 1960s (Ballantine, 1961; Lewis, 1964) and modifications of the Ballantine scale are still used today. The Ballantine exposure scale was devised by studying the differences of popu- lation between exposed headlands and sheltered inlets and assigning numerical values for wave intensity to particular patterns of population, on the assumption that the dif- ferences are due mainly to wave effects. The most obvious contrast to be made is between shores where the rock surface is mainly encrusted with barnacles or mussels, that is barnacle-dominated and mussel-dominated shores, and those where the rocks are cov- ered by a copious growth of seaweeds, which are algal-dominated shores. The former occur where the force of wave action is too fierce to allow the survival of large sea- weeds, the latter where the intensity of wave action is much more gentle. 6.2.1 Shore zonation A vertical zonation of marine organisms, with different species dominating at different levels, is apparent on most seashores throughout the world, though it is most notice- able on rocky shores in temperate areas. Biological zonation in any habitat is driven by strong environmental gradients and is apparent in many habitats other than seashores. One of the most obvious examples is the changing vegetation from the top to the bot- tom of a mountain, driven largely by temperature changes (temperature decreases by roughly 1 C for every 300 m altitude gained). The most obvious driver behind sea- shore zonation is the length of time for which organisms are exposed to the air (emer- sion time). The lowest parts of the shore are uncovered only during the lowest spring tides, and then only for brief periods (Fig. 6.2). The highest levels are seldom fully Figure 6.2 A mixed rock and sediment shore on the island of Ulva, Inner Hebrides, Scotland at the time of ELWS.  Benthic living: the seashore 275 submerged and are mainly wetted by wave splash. Intermediate levels experience intermediate durations of alternating exposure and submersion. Even on nontidal shores there are gradients between permanently submerged and fully terrestrial condi- tions, with intermediate levels wetted by splash or irregularly covered and uncovered as wind action alters the water level. The requirements for life in air and water are so different that no organism is equally well suited to every level of the shore. Different levels are therefore occupied by different assemblages of organisms, each species having its main abundance within a particular zone, where conditions are most favourable for it. Exposure to air subjects shore organisms to detrimental effects, particularly drying out (Section 6.1.1) and changes in salinity (Section 6.1.4) and temperature (Section 6.1.2). Organisms living high up on the shore are exposed to air for long periods during spring tides and must therefore be able to withstand conditions of prolonged drying, extremes of tempera- ture and strong illumination. Direct wave impact is a relatively brief and infrequent hazard and strong wave action actually favours the upward spread of this population by increasing the height to which spray regularly wets the shore. Organisms living lower on the shore are only uncovered for a few hours or even minutes at a time and here the problems of desiccation, temperature fluctuations and excessive illumination are less severe. However, these organisms experience longer and more frequent peri- ods of wave action with the attendant risks of damage or dislodgement. Emersion-driven zonation is modified by several other biotic and abiotic factors, including grazing (Section 6.3.3), competition for space, predation (Section 6.1.8) and whether an organism can continue to feed when out of water. The final zonation pat- tern of the organisms on a particular shore is fine-tuned by all the factors that vary with height on the shore as well as these modifiers. However, although the tides exert a major influence on zonation, the distribution of shore species relative to particular tidal levels is by no means constant. Wide variations occur from place to place due to differences of geography, geology and climate. Factors which modify zonation and vary with locality include the intensity of wave action, the range of temperatures and humidities, the aspect of the shore with respect to the sun and prevailing wind, the type of rock or sediment, the amount of rainfall and freshwater run-off and the period of day or night when extreme low tides occur. Shore zone designations There are various different ways of designating shore zones. First, shores can be divided into physical zones according to tidal level, without reference to the biota. Tidal levels are measured above chart datum and are shown in Fig. 2.31 in Section 2.9.2, Tidal levels. Three main such zones are usually recognized: upper shore (from MHWN to MHWS), middle shore (between MLWN and MHWN) and lower shore (from MLWS up to MLWN). 276 Elements of Marine Ecology Second, using populations of organisms as a guide, early shore biologists divided the intertidal into three major zones (see Fig. 6.3). The highest zone, with the upper- most communities which require mainly aerial conditions, is called the ‘littoral fringe’. This zone is submerged only at spring tides or wetted only by wave splash (and today more usually called the splash zone). On very sheltered shores this zone is a narrow belt just below EHWS level, but it becomes higher and wider with increasing expo- sure to wave action, until, on the most wave-exposed rocky coasts, it lies entirely above EHWS level and may extend upwards for 20 m or more. This variation is shown in Fig. 6.3. Below the littoral fringe is the broad ‘eulittoral zone’, occupied by communities tolerant of short periods of exposure to air between tides, but requiring regular submersion on each tidal cycle, or at least thorough wetting. The eulittoral encompasses the major part of the shore. The low-shore zone is called the ‘sublittoral fringe’ and really forms part of the permanently submerged sublittoral zone. It is only exposed at spring low tides, extending approximately from ELWS (0 m) to MLWS. At their lowest levels the populations of the eulittoral zone overlap those of the sublit- toral fringe. The exact limits of physical zones are rarely measured by ecologists on site visits, who tend to estimate zones based on the populations present and it is these less exact, but often clearly visible, biological zones that are of greater ecological interest. These Lichens Barnacle zone Porphyra spp. Pelvetia caniculata Littoral fringe (splash zone) Fucus spiralis Mytilus edulis Fucus vesiculosus Ascophyllum nodosum Mastocarpus stellatus Fucus serratus Himanthalia elongata Alaria esculenta Laminaria digitata Saccharina latissima Eulittoral zone MHWS MHWS Littoral fringe Eulittoral zone Sublittoral fringe MLWS MHWS Sublittoral fringe Very exposed Increasing wave action Sheltered Figure 6.3 Diagram to illustrate how the distribution of some dominant seaweeds and animals of rocky shores varies with wave intensity.  Benthic living: the seashore 277 may span more than one physical zone but are closely related to tidal levels. The most usual recognized zones are the splash zone, upper, middle and lower shore (these three comprising the eulittoral) and the sublittoral fringe. Biological zonation is a feature of shore populations everywhere and since about the 1960s, many studies on this subject have been carried out around the world. Whilst zona- tion is a common feature between rocky shores in widely separated geographical regions, the actual zones and the species making them up can differ radically between regions and descriptive systems developed for one geographical area may not apply to another (Ingólfsson, 2005). On rocky shores, biological zones often show up as different coloured bands, a feature that is especially clear when viewed from above. In the splash zone and upper shore, green, orange and black lichens may show up. Barnacles form greyish bands and patches in the upper and middle shore. Different species of seaweeds, especially prom- inent brown species, may form wavy-edged bands whose species composition helps delin- eate and define upper, middle and lower shore. For example the upper level of Channel Wrack (Pelvetia canaliculata), a brown seaweed common on rocky NE Atlantic shores, can indicate where the landward edge of the upper shore, meets the splash zone. This species can survive for long periods out of water but does need occasional submersion. In the splash zone or littoral fringe only specialist species can thrive. On rocky shores marine lichens, gastropod molluscs and crustaceans are likely to be present, whilst on sediment shores amphipods commonly scavenge in the strandline. In areas exposed to strong wave action the splash zone extends well above extreme high tide level as already mentioned. The middle shore is home to the majority of shore organ- isms and in most places around the world, will almost always experience two low tides and two high tides in 24 hours, termed semidiurnal tides (see Section 2.9). On rocky shores around the world, key organisms include barnacles, polychaete worms with hard calcareous tubes, mussels, rock oysters and a wide variety of seaweeds. Standing on a rocky shore at similar latitudes in northern Europe and for example, Australia, similar subzones will often be apparent, though the species will differ. 6.2.2 Rocky shore zonation in the British Isles The zonation of algae (mainly seaweeds) and sessile animals such as barnacles is often clearly visible on rocky coastlines around the British Isles. Patterns of zonation vary on dif- ferent shores especially due to modification by the effects of wave exposure. An excellent summary of ‘typical’ patterns of zonation on wave sheltered, moderately exposed and exposed shores in this area, is given in Hawkins and Jones (1992). Classic early publications on zonation and distribution patterns that are still relevant today include Lewis (1964) and Ballantine (1961). Figs. 6.3 and 6.4 give a general indication of the zonation that might be expected on rocky shores in the southwest peninsula of the British Isles. Fig. 6.5 illustrates how some of the organisms involved interact within the rocky shore food web. 278 Elements of Marine Ecology MHTL MLTL MTL Verrucaria maura Pelvetia canaliculata Seaweeds Fucus spiralis F. vesiculosus + Ascophyllum F. serratus Himanthalia elongata Laminaria spp. Melaraphe neritoides Littorina saxatilis agg. Ligia oceanica Orchestia gammarellus Anurida maritima Chthamalus montagui Semibalanus balanoides Balanus perforatus Patella vulgata L. obtusata/ L. fabalis Animals L. littorea Phorcus lineatus Steromphala umbilicalis Nucella lapillus S. cineraria Mytilus edulis Chthamalus stellatus Calliostoma zizyphinum Halichondria panicea B. crenatus P. ulyssopensis Figure 6.4 Zonation of some common seaweeds and animals of rocky shores exposed to moder- ate wave intensities along southwest peninsulas of England and Wales. MHTL and MLTL are aver- age high and low tide levels respectively. MTL, Mean tide level. 6.3 Temperate rocky shores Temperate rocky shores, with their moderate climate and high biodiversity, have been and are well studied. There are numerous publications on the ecology, species compo- sition and zonation of such shores around the world. This section gives a general account of the roles played by key groups of species. An excellent and well-illustrated guide to the species, communities and zonation on rocky shores around the British Isles is given in Chapter 2 of Cremona (2014).  Benthic living: the seashore 279 Energy sources Solar radiation Stranded organic Plankton debris Producers Macroflora Microflora Detritus and associated bacteria Littorina Limpets Littorina Amphipods, Isopods Barnacles Mussels Herbivores obtusata Topshells littorea and other small Patella crustacea. Some pellucida polychaetes Lipophrys Eulalia pholis viridis Crabs Dogwhelks Starfish Predators Birds Sublittoral fish Bait Food Man Figure 6.5 Simplified food web of a rocky shore in the southwest of the UK. 6.3.1 Seaweed and lichen Large brown seaweeds (Phaeophyceae) are a feature of the middle parts of many tem- perate rocky shores round the world, wherever wave action is not too violent to allow their growth. The middle shore is typically covered by an often dense canopy of large, brown fucoid seaweeds (Fucales), sometimes called wracks (Box 6.4). The species involved differ around the world, but there can be remarkable similarities between temperate shores as far apart as Great Britain and New Zealand. Conspicuous in the sublittoral fringe, but usually uncovered only at spring low tides, are various species of large kelps, again represented by different species around the world, mainly Laminaria in the North Atlantic or, on the most wave-beaten rocks, Alaria esculenta. In the south- ern hemisphere, Ecklonia and Durvillaea are more or less the equivalents. In the British Isles another conspicuous brown species, Wireweed (Sargassum muticum), has spread around the southern half of England and throughout Ireland since the early 1970s. It has also reached some parts of western Scotland. As it cannot withstand exposure to air for very long, it is restricted to the lowermost parts of the shore but can also extend much higher 280 Elements of Marine Ecology BOX 6.4 Fucoid seaweeds in the British Isles. Look closely at a moderately exposed to sheltered rocky shore almost anywhere around the British Isles and you should be able to distinguish brown bands of fucoid seaweeds, each a slightly different colour, indicating the dominance of particular species at different shore levels. At the highest level there is the Channel Wrack, Pelvetia canaliculata, forming a narrow band along the upper edge of the upper shore, where it is wetted by salt spray, but only occasionally submerged. It has inrolled fronds to conserve water but can dehydrate down to a brittle, shrivelled state where it has lost up to 95% of its water content. It can still recover when wetted once again by a high tide or spray. Just below the Pelvetia zone towards the lower limit of the upper shore, there is often a nar- row zone of the Spiraled Wrack, Fucus spiralis. Below this, the greater part of the middle shore is covered with a mixed growth of Egg Wrack, Ascophyllum nodosum and Bladder Wrack, F. vesicu- losus, the former predominating in very sheltered areas and the latter in regions more open to waves. With its long, tangled fronds, Ascophyllum would soon be torn away from wave-exposed rocks. Both species have gas-filled bladders to hold their fronds erect whilst the tide is in to make the most of their short time underwater. Overlapping with A. nodosum and F. vesiculosus, but extending mainly across the lower shore, is a belt of Serrated Wrack, Fucus serratus. Thong Weed, Himanthalia elongata can flourish on lower shores with a wide variety of wave exposure, but may take the place of F. serratus under exposed conditions which the latter cannot tolerate. Under moderate and sheltered conditions it is outcompeted by F. serratus. by living in permanent rock pools. It was probably introduced with oysters imported from the Pacific and was first recorded on the south coast of Britain at Bembridge, Isle of Wight. If there is a dense canopy of seaweeds on a shore it will have material effects on the organisms living beneath, particularly in terms of shading, shelter and desiccation. When the tide is in, large seaweeds act in a similar way to the trees in a woodland, shading the rocks below them from sunlight. Seaweed fronds sweeping to and fro with wave action can prevent larval and spore settlement. With the tide in and the seaweed lying pros- trate, anything beneath the seaweed will be protected both from drying out and from predators. Beermann et al. (2013) found both positive and negative impacts of seaweed canopy on the settlement and establishment of barnacle larvae on a shore in Canada. Lichens are a common component of temperate rocky shores, forming bands and patches on upper shore and splash zone rocks. Lichens are well-known for their ability to survive in harsh environments and can flourish on rocks at the very top of the shore, where it is too dry for algae and seaweeds, but too salty for land plants. Many different salt-tolerant coastal species occupy this niche on rocky shores around the world. Some species can actu- ally extend down into the middle shore, especially on the sunny tops of rocky reefs and boulders. On exposed barnacle-dominated shores around the British Isles, tufts of the Black Lichen Lichina pygmaea are often common at this level. In the higher part of the upper shore (sometimes termed the littoral fringe), encrusting Black Tar Lichen Verrucaria maura often  Benthic living: the seashore 281 covers the rock in anything from small patches to extensive mats. Above this, within the splash zone and merging into the terrestrial realm, other more colourful lichens typically form a distinct zone of foliose and encrusting salt-tolerant species. Around the British Isles there will be yellow and orange crusts of Xanthoria and Caloplaca, grey lichens including Tephromela atra and right at the top of the splash zone and beyond, tufts of Sea Ivory (Ramalina spp.) (Fig. 6.6). Figure 6.6 Examples of communities within different rocky shore zones in the British Isles: (A) Splash zone lichen community, Outer Hebrides; (B) upper shore Pelvetia (left) and F. spiralis (right), west coast Ireland; (C) sheltered middle shore, F. vesiculosus and A. nodosum, west coast Ireland; (D) lower shore and sublittoral fringe, Dorset. 282 Elements of Marine Ecology 6.3.2 Barnacles Barnacles are a common sight on rocky shores, often covering large areas, especially in wave-exposed situations where seaweeds cannot gain a foothold. On temperate shores around the North Atlantic, sessile (stalkless) acorn barnacles (Balanomorpha) can reach densi- ties of 100,000 individuals per square metre. In the British Isles acorn barnacles dominate wave-exposed sites but also often form a distinct band on the upper shore at less exposed sites, where the middle shore is dominated by fucoid seaweeds. Pinnacles, ridges of rock or large boulders further down the shore are also usually covered in barnacles, because they are raised up and so are effectively at the same tidal height as the band on the upper shore. The shores of southern Australia can be subject to extremely strong waves and Surf Barnacles (Catomerus polymerus) are one of the few species that thrive on very exposed rock platforms. Whilst most intertidal barnacles have a low profile, which helps reduce drag on rocks pounded by waves, others solve the same problem by having a tough and flexible stalk. On shores along the wave-beaten Atlantic coasts of France, Portugal and Spain, stalked or goose barnacles often dominate. Species such as Pollicipes pollicipes have a tough, flexible stalk that can expand when the tide is in and contract when it is out. This species can withstand really heavy pounding by waves. In Galicia in northwest Spain, this species is harvested and the fishery is of great economic and social importance to the local people. The biology and identification of British intertidal barnacles is described in full in Southward (2008) and their identification in Hawkins and Jones (1992). S. balanoides is the most widespread species and is a northern boreal barnacle with its southern limits in the British Isles. Two species of Chthamalus are also common here, but these are essentially southern species from the Mediterranean and adjacent Atlantic coasts and the British Isles are at their northern limit. Unsurprisingly the southern Chthamalus can withstand higher temperatures and longer emersion than Semibalanus and often predo- minates on the upper shore, above the main zone of Semibalanus. Chthamalus is smaller and grows more slowly than Semibalanus and so whilst both genera occur on the mid- dle shore, here Semibalanus outcompetes Chthamalus for living space. In most British localities C. stellatus is limited to lower parts of the shore than C. montagui, mainly below mid-tide level, whilst C. montagui can extend right up into the splash zone. Chthamalus stellatus is usually most abundant on heavily wave-beaten coasts whilst C. montagui favours embayed sheltered situations. Again unsurprisingly the essentially northern Semibalanus is less abundant in southern parts of the British Isles than it is in Scotland, whilst the reverse is true for Chthamalus. The detailed geo- graphical distribution and shore height distribution of these three intertidal acorn bar- nacles result both from their temperature preferences and from competitive challenges. The most diverse populations of shore barnacles in the British Isles occur on the southwest peninsulas of England and Wales where an additional four species can be found, namely Perforatus perforatus, Balanus crenatus, Verruca stroemia and Austrominius mod- estus (Box 6.5). These species are not restricted to the southwest, but are often  Benthic living: the seashore 283 BOX 6.5 Nonnative ‘sleeper’ species. Austrominius modestus is an Australasian introduced intertidal barnacle, which is now wide- spread in northwest Europe. It first appeared in the British Isles in Chichester Harbour and the Thames estuary during World War II, probably arriving via shipping. Whilst it has per- sisted and has spread as far north as the Shetland Isles, it has not become particularly abun- dant in most places, though its wide tolerance of desiccation, silting, and variations in temperature and salinity means it sometimes outcompetes S. balanoides in sheltered areas such as estuaries. Its softer shell means it cannot survive in very wave-exposed places. It also has the advantage of a rapid growth rate and extended breeding season through the sum- mer months. However, although it has been in the British Isles since the 1940s, it is only since the mid-2000s that it has started to really increase in abundance in some areas, such as the Isle of Cumbrae in Scotland (Gallagher et al., 2015). This may be an example of a non- native species that, whilst well-established, has had to wait for a favourable (to it) change in environmental conditions before being able to compete effectively with native species. Witte et al. (2010) suggest that Austrominius may be an example of such a ‘sleeper species’ and that its exponential growth on the German Island of Sylt since 2007 is probably the result of a series of mild winters and warm summers. Increasing water temperatures associated with climate change may now be allowing this warm water species to proliferate. prominent there. In some localities B. perforatus virtually ousts Semibalanus. This larger species cannot withstand emersion for as long as Semibalanus and Chthamalus and so only occurs from the lowest levels of the shore up to about mid-shore level. Balanus crenatus is essentially a sublittoral species, intolerant of exposure to air. It may be found in rock pools or under algal cover very low on the shore round the British Isles. V. stroemia is a shallow-water species extending to the lower shore, where it is restricted mainly to pools or the underside of stones. 6.3.3 Grazers With a wealth of vegetation available on temperate rocky shores in the form of sea- weeds and other algae, it is hardly surprising that a wide variety of grazers is also found on such shores. As on land, grazers can have a dramatic effect on the vegetation and there will be a shifting balance between the two. Gastropod molluscs are the main grazers on temperate rocky shores. Armed with an effective grazing tool, the radula, which is unique to molluscs, these animals can scrape off the biofilm (see Section 7.3.2) on rocks, including seaweed sporelings, thus keeping some areas free from seaweed growth. They can also feed directly on seaweeds and smaller algae. Herbivorous winkles, limpets, ormers and top shells are typically common on temper- ate rocky shores. The different species within each group occur at different shore zones, as a result both of the zonation of their main food source and also their ability 284 Elements of Marine Ecology to spend time out of water. The zonation of periwinkles and limpets on rocky shores in the British Isles is described here as an example. Periwinkles (Littorinidae) Periwinkles, particularly species of Littorina, are very common on temperate rocky shorelines in the northern hemisphere. Several species occur on the coast of the British Isles but their taxonomic status can be problematic. Hawkins and Jones (1992) give basic and advanced identification tables for all species, but some of the specific names have since changed. Small Periwinkle Melaraphe neritoides: This tiny species lives mainly on the upper shore and in the splash zone, extending almost to the highest levels of wave splash. They are most numerous on shores exposed to heavy wave action and are often absent from sheltered regions. They live mainly tucked away in rock crevices, in dead barna- cle shells and amongst tufts of lichen and are consequently absent from most of the eastern part of the English Channel and southern part of the North Sea where suitable substrata are lacking. This species feeds on microalgae and lichens. Rough Periwinkle Littorina saxatilis group: Rough periwinkles are an aggregate of three species plus an ecotype and there has been much confusion of nomenclature. The group is often referred to as L. saxatilis agg. The current consensus is that there are three species within this group: L. saxatilis, L. arcana and L. compressa (was nigrolineata) (Hayward and Ryland, 2017). The species are very difficult to tell apart, especially in the field. However, these three species all have distinct grooves running round the shell and with practice can together be recognized as a group. The species now called L. saxatilis is the highest shore-living littorinid apart from M. neritoides and is mostly found in crevices at and above the Pelvetia zone, but can extend to the lower shore. This species is reproductively adapted to dry conditions by retaining the eggs in a brood pouch until they hatch into tiny crawling snails. Littorina arcana extends down from the upper shore to mid shore, where it overlaps with L. compressa. Not all shores support both species and L. compressa has a rather local distri- bution on moderately exposed to very exposed shores. The shell is distinctively ridged, light coloured and often patterned with dark spiral lines within the grooves. Unlike L. saxatilis, both L. arcana and L. compressa lay their eggs in damp crevices, but their young also hatch as crawling juveniles. At one time a fourth species, known as L. neglecta, was recognized. This tiny snail lives mostly in dead barnacle shells and also among mussel byssus and in Laminaria holdfasts and it is now known that individuals can belong to any of the other three species. They are not juveniles but become sexually mature at a tiny size due to their restricted habitat. This is the ecotype referred to in the preceding paragraphs. This aggregate of species demonstrates how complex and subtle differences in habitat and environment can be exploited to allow closely related species to thrive on one shore.  Benthic living: the seashore 285 Flat Periwinkles Littorina obtusata and L. fabalis: Flat Periwinkles are found on all British coasts but are more abundant in sheltered regions. This aggregate of two very similar species used to be referred to together as L. littoralis. Both species are found in the mid shore and have various colour morphs from yellow and orange to greenish and brown. The two species overlap but L. fabalis is much more common on the lower shore in the F. serratus zone. These two species make excellent crab food and the differences in their preferred shore levels seem to relate to this. L. obtusata is a relatively long-lived species surviving for at least 3 years and by living higher up the shore in the Ascophyllum nodosum and F. vesiculosus zone, it can better avoid being eaten as there are fewer predators, espe- cially crabs, than on the lower shore. It grazes on the algae amongst which it lives. In contrast, L. fabalis lives mainly on the lower shore amongst F. serratus, feeding on epi- phytes attached to the seaweed. It lives for only a year and times its reproduction for the winter period when many crabs migrate offshore. Edible or common periwinkle L. littorea: This is the largest and most easily identi- fied of the British periwinkles. It extends all the way from the upper shore down into the sublittoral and can be found everywhere except on very exposed shores. It can be present in very large numbers and as it feeds both by scraping the microflora from the rock surface and directly on fine red, green and brown seaweeds it can, like limpets, have an effect on algal abundance. It is often found on bare rocks and is especially numerous in gulleys or on the sheltered faces of boulders. This species has planktonic eggs and larvae. Limpets Limpets are significant grazers on rocky shores around the world and heavy grazing can prevent algal colonization, resulting in a patchy cover of seaweeds and a greater diversity of microhabitats (Fig. 6.7). This was well demonstrated in 1967 in the aftermath of the SS Torrey Canyon oil spill, when crude oil swamped shores in Cornwall, UK. The strong dispersants used to clean up the beaches, killed limpets and other grazers. As the shores Figure 6.7 Limpets are important grazers on rocky shores. (A) Radula scrape marks left by a graz- ing limpet; (B) intensely limpet-grazed boulder, Northumberland, UK. 286 Elements of Marine Ecology started to recover and without grazing pressure, fast-growing green algae grew over large areas, checking regrowth of longer-lived species. Edible periwinkles (L. littorea) are par- ticularly good at grazing on the young stages of common green algae such as Ulva spp. It took at least 10 years for full equilibrium to be restored. The most common and largest limpet on shores around the British Isles is the Common Limpet P. vulgata. This species roams the full extent of the shore from top to bottom and can be found on virtually all rocky shores in this region. Two other species of Patella have a more restricted distribution. The China Limpet Patella ulysso- pensis (was P. aspera) occurs on most suitable coasts around the British Isles but not between the Thames and the Humber on the east coast. It lives mainly below MLWN, but on exposed shores it can be found in mid-shore rock pools. In southwest Britain a third species the Black-footed Limpet, Patella depressa, occurs on moderately exposed to exposed shores in the middle and lower shore (Isle of Wight to Anglesey, absent in Ireland). On exposed shores, P. ulyssopensis is often the most common limpet species on the lower shore. P. depressa and P. aspersa are rarely found on sheltered shores, unlike P. vulgata. Limpets are themselves a key prey item for those animals that can penetrate their tough defences. On shores around the British Isles, Dog whelks (N. lapillus) will patiently drill through their shells and those of barnacles. Where there are plenty of limpets and barnacles, there is usually a good population of Dog whelks. The American Oysterdrill (Urosalpinx cinerea) feeds in a similar way along east coast USA, though it mainly feeds on oysters. On the Pacific coast of North America, the starfish Pisaster ochraceus can occur in high densities on rocky shores and although its main prey is mussels, it will also consume limpets if it can get them off the rocks. Limpets are also an important food source for Oystercatchers (Haematopus spp.) on both sides of the North Atlantic. These birds have strong beaks and can prise and smash the limpets from the rocks. 6.3.4 Rock pools Rock pools are an important feature of almost all rocky shores, except where the geology lacks depressions and irregularities where water from the receding tide could be retained. Pools provide a temporary refuge for many mobile animal species and a permanent home for many other animals and algae. When the tide is out, it is easy to see that many small seaweeds flourish in pools at much higher levels than they could otherwise and the shore can therefore support higher populations of seaweeds and the animals dependent on them for food and shelter. Rock pools also act as important refuges for juveniles of species normally living below shore levels, particularly some fishes (Fig. 6.8A). Here young animals are rela- tively safe from predators and they will only move offshore once they reach a certain  Benthic living: the seashore 287 Figure 6.8 (A) Bright green juveniles of Ballan Wrasse (Labrus bergylta) can commonly be found in pools around the British coastline in spring and early summer; (B) an exposed shore rock pool lined with encrusting calcareous algae and grazed by limpets the only foliose seaweeds to survive are those growing on the limpet shells themselves. (A) Courtesy Paul Naylor. size. Juvenile Lumpsucker (C. lumpus), Saithe (Pollachius virens), rocklings (Lotidae) and grey mullets (Mugilidae) are a common sight in rock pools around the British Isles. Living in rock pools is not always easy, especially in small pools and pools high up on the shore. Such pools can be subject to wide variations in temperature, salinity, pH and oxygen levels. Species that are structurally or physiologically adapted to more extreme conditions can thrive in the relative absence of competition and predation. The China Limpet P. ulyssopensis is an exposed rock pool specialist in that it can graze the hard calcareous algae (Corallinaceae) that often line such pools. It is one of the few grazing molluscs that can do so. Medium and high-level pools are often lined with this pink paint weed as it is often called, plus tufts of another calcium carbonate- containing alga, Corallina. These algae grow well in the absence of softer algae that are quickly gazed away by herbivores (Fig. 6.8B). 6.3.5 Under-boulder and crevice fauna Soft-bodied invertebrates such as sponges (Porifera), sea squirts (Ascidiacea), anemones and other cnidarians can only thrive on rocky shores if they are tucked away in damp crevices, under overhangs or on the undersides of boulders. Such sessile animals are mostly restricted to the lower shore and especially the sublittoral fringe. Large fissures and crevices can support microcosms of the communities found in the shallow sublit- toral. Boulders on exposed temperate shores are likely to be rolled by winter storms and whilst they provide a refuge for mobile animals such as crabs and amphipods, they are unlikely to have much growing attached to their under surface. However, stable boulders on moderately sheltered shores, but with strong currents running through when the tide is in, can support an amazing variety and quantity of attached animals (Fig. 6.9). 288 Elements of Marine Ecology Figure 6.9 Rich growths of encrusting sponges, colonial tunicates and hydroids on the underside of an intertidal boulder in the Farne Islands, UK. Some mobile intertidal species are specifically adapted to live in such habitats. Clingfish (Gobiesocidae) have flattened bodies and their pelvic fins are modified as suckers. Shore Clingfish (Lepadogaster purpurea) cling to the underneath and sides of wet boulders on the lower shore. The Broad-clawed Porcelain Crab (P. platycheles) also has a very flattened body and claws and can cling happily under rocks when the tide is out. It feeds mainly on the detritus that collects on its hairy claws and can remain hidden from predators even when the tide is in. 6.3.6 Mammals and birds Rocky seashores are an important habitat for seabirds and for seals and other pinnipeds worldwide. Many seabirds forage for food on rocky shores and are important predators in this respect, although usually present in smaller numbers than the large flocks of waders seen probing for worms and molluscs along sediment shores. True seabirds are inextricably linked to seashore and coast because cliffs, rocky stacks and islands, whilst not strictly part of the intertidal zone, provide safe breeding sites for many species. Rock ledges are used by Herring Gull (Larus argentatus), Great Black-backed Gull (L. marinus), Kittiwake (Rissa tridactyla), guillemots (Uria spp.), Razorbill (Alca torda), European Shag (Phalocrocorax aristotelis), gannets (Morus spp.) and others. Puffins (Fratercula spp.), many shearwaters and petrels and some penguins, nest in burrows often at the tops of rocky seashores or cliffs. Pinnipeds (seals, sealions, fur seals and walrus) rely on seashores both as places to haul out and rest and as breeding sites. Many species choose remote rocky shores as safe breeding sites and both adults and pups may remain ashore for several weeks. Whilst the majority of otters hunt in freshwater, there are a few species around the  Benthic living: the seashore 289 world that obtain most of their food from intertidal and shallow coastal waters and so can be considered as marine mammals. In Scotland, the Eurasian Otter (Lutra lutra) lives an almost entirely coastal existence and regularly catches intertidal fish such as the Butterfish (Pholis gunnellus). 6.3.7 Abundance scales for rocky shore organisms Student level methodologies for making detailed surveys of the abundance of rocky shore organisms and studying zonation patterns are well described in Hawkins and Jones (1992) and advanced methods for many different types of shore in Baker and Wolff (1987). Such methodologies usually involve the use of transects and quadrats to provide truly quantitative data and this can be very time-consuming. A faster method is to use a semiquantitative abundance scale, which estimates the density or cover of organisms, using between five and seven broad categories. For each abundance category, counts or percentage cover per unit area are defined for different groups of species. An abundance scale widely used in the UK is the SACFOR scale (Superabundant, Abundant, Common, Frequent, Occasional, Rare). An advanced version of this is shown in Table 6.1 and a simpler version using specific groups of organisms (e.g. limpets) can be found in Hawkins and Jones (1992). Using any scale requires familiarity with the various categories, which comes with practice. The scale has and can be adapted and the categories simplified for use in student or citizen sci- ence projects such as ‘The Shore Thing’ initiated by the UK’s MBA (Marine Biological Association) and previously operating around the British Isles (http://www.mba.ac.uk/ shore_thing). 6.4 Temperate sandy shores Sediment shores around the world vary from beautiful sandy beaches, beloved by sun- seeking holiday-makers, to black sticky mud, found in many estuaries and enclosed bays. There are all grades in between and these are often described in terms such as fine or coarse sand, sandy mud, or muddy sand. Such terms are often used by ecolo- gists working by eye and experience, using the terms to give an idea of the habitat in which they are recording. There are also precise definitions for sediment types, based on the sizes and relative quantities of particles as measured in dried and sieved samples (see Table 1.2 in Section 1.3.2). Seabed classification systems using both the type of substratum and the biota present are described in Section 7.2. Seashore sands contain particles of many types and sizes, often including silt and clay, deposited from many sources including cliff and rocky shore erosion and input from land and rivers. The main constituent of sand on coasts around the British Isles is fragmented silica and such yellow beaches often consist almost entirely of coarse siliceous sand. Add in silt, clay and organic debris to silica sand and you get much greyer and muddier beaches. Table 6.1 An advanced SACFOR abundance scale that can be used for both littoral and sublittoral taxa (Hiscock, 1996). % cover Growth form Size of individuals/colonies Density scale scale