275 5 Control of Community Structure CONTENTS 5.1 Introduction 277 5.2 Hard Shores 277 5.2.1 Interactions Between Plants and Animals 277 5.2.1.1 Grazing 277 5.2.1.1.1 Ecological categories of algae 277 5.2.1.1.2 Principal types of herbivorous grazers 277 5.2.1.1.3 Diets of grazers 278 5.2.1.1.4 Foraging behavior 278 5.2.1.1.5 Sit-and-wait grazers 280 5.2.1.1.6 Variability of foraging 280 5.2.1.1.7 Grazing and benthic microalgal distribution, biomass, and diversity 280 5.2.1.1.8 Algal defenses against grazing 280 5.2.1.1.9 Grazing and algal distribution 281 5.2.1.1.10 Contrasts in grazing on temperate and tropical shores 282 5.2.1.1.11 Gardening 284 5.2.1.1.12 Grazing and community structure 284 5.2.1.2. Algae and the Lower Limits of the Distribution of Limpets 288 5.2.2 Competitive Interactions 288 5.2.2.1 Introduction 288 5.2.2.2 Intraspecific Competition 289 5.2.2.3 Mechanisms for Reducing Intraspecific Competition 290 5.2.2.3.1 Larval settling patterns 290 5.2.2.3.2 Dispersal of adults 290 5.2.2.3.3 Dispersal along an environmental gradient 290 5.2.2.3.4 Avoidance or ritualization of combat 291 5.2.2.3.5 Difference in diet 291 5.2.2.4 Interspecific Competition 291 5.2.2.4.1 Competition between plants 291 5.2.2.4.2 Competition between species of grazers 291 5.2.2.4.3 Competition for space 293 5.2.2.4.4 Competition between plants and grazers 293 5.2.2.4.5 Competition between grazers and other organisms 294 5.2.2.4.6 Competition between plants and other organisms 294 5.2.2.4.7 Competition between sessile filter feeders 294 5.2.2.5 Processes Affecting the Outcome of Competition 294 5.2.2.5.1 Disturbance 294 5.2.2.5.2 Grazing and preference for different types of food 295 5.2.3 Predation 295 5.2.3.1 Introduction 295 5.2.3.2 Predation by Whelks 296 5.2.3.3 Predation by Highly Mobile Predators 297 5.2.3.4 Predation by Birds 297 5.2.3.5 The “Keystone Species” and “Diffuse Predation” Concepts 300 5.2.3.6 Impact of Predation on Community Structure 302 5.2.3.6.1 New England rocky intertidal 302 © 2001 by CRC Press LLC 276 The Ecology of Seashores 5.2.3.6.2 North American West Coast 303 5.2.3.6.3 Panamanian rocky shores 305 5.2.3.6.4 Temperate shore at Catalina Island 306 5.2.4 Human Predation on Rocky Shores 307 5.2.5 Environmental Heterogeneity and Community Structure, and Diversity 308 5.2.6 Persistence and Stability 308 5.2.7 Disturbance and Succession 311 5.2.7.1 Introduction 311 5.2.7.2 Size and Location of a Patch 312 5.2.7.3 Succession 313 5.2.7.4 Role of Recruitment in Succession and Its Impact on Community Structure 315 5.3 Soft Shores 317 5.3.1 Introduction 317 5.3.2 Experiments on Soft Shores and Caging Methodology 317 5.3.3 Grazing on Soft Shores 318 5.3.3.1 Introduction 318 5.3.3.2 Epibenthic Grazers 318 5.3.3.3 Epiphytic Grazers 318 5.3.3.4 Infaunal Grazers 319 5.3.4 Competition 319 5.3.4.1 Introduction 319 5.3.4.2 Intraspecific Competition 320 5.3.4.3 Interspecific Space Competition 320 5.3.4.4 Exploitative Competition for Food 320 5.3.4.5 Interaction Between Deposit and Suspension Feeders and Tube-Builders 322 5.3.4.6 Interference by Alteration of the Physical Environment 324 5.3.5 Predation 324 5.3.5.1 Introduction 324 5.3.5.2 Meiofaunal Predation 325 5.3.5.3 Predation by Infauna 326 5.3.5.4 Predation by Epifauna 326 5.3.5.5 Impact of Predation on Bivalves 328 5.3.5.6 Multiple Predation on Tidal Flats 328 5.3.5.7 Predation by Birds 328 5.3.5.8 Role of Predation in Structuring Soft-Bottom Communities 332 5.3.6 Influence of Resident Fauna on the Development of Soft-Bottom Communities 333 5.3.7 Role of Recruitment Limitation in Soft-Sediment Communities 335 5.3.8 Disturbance and Succession 335 5.3.8.1 Introduction 335 5.3.8.2 Disturbance 336 5.3.8.3 Levels of Faunal Disturbance 336 5.3.8.4 Impact of Disturbance on Productivity 336 5.3.8.5 Succession and Sediment Stability 337 5.3.8.6 Postdisturbance Responses of Microorganisms 337 5.3.8.7 Postdisturbance Response of Meiofauna 337 5.3.8.8 Postdisturbance Response of Macrofauna 337 5.3.8.9 Distribution along a Gradient of Organic Enrichment 339 5.3.8.10 Models of Postdisturbance Succession 343 5.4 Synthesis of Factors Involved in Controlling Community Structure 344 5.4.1 Hard Shores 344 5.4.1.1 Introduction 344 5.4.1.2 The Menge-Sutherland Model 344 5.4.1.3 The Relative Importance of Various Structural Agencies on the Vertical Distribution of Rocky Shore Communities 348 5.4.2 Soft Shores 348 © 2001 by CRC Press LLC Control of Community Structure 277 5.4.2.1 Introduction 348 5.4.2.2 Evidence of Distinct Correlation Between Infauna and Sediments 349 5.4.2.3 Processes that Determine the Sedimentary Environment 350 5.4.2.4 The Hydrodynamic Regime and Benthic Infaunal Species 351 5.4.2.4.1 Larval supply 351 5.4.2.4.2 Food supply 352 5.4.2.5 The Importance of Recuitment 352 5.4.2.6 Conclusions 352 5.4.2.7 Synthesis of Factors Determining Macrofaunal Community Composition on Soft Bottoms 353 5.1 INTRODUCTION In previous sections in this book, the emphasis has been on the impact of physical factors on the distribution of plants and animals on the shore. While these factors set the framework and define the limits over which the various life cycle stages of a particular species can exist, the patterns of distribution are subject to modification by a complex of interacting biological factors. Early studies (for example, reviews by Lewis, 1964; Stephenson and Stephenson, 1972) were oversimplifications relating distributions to tidal rise and fall and wave exposure, and much subsequent research has shown that interactions among species can profoundly modify distribution patterns, and often deter- mine these patterns (see reviews by Dayton, 1971; 1984; Connell, 1972; 1975; 1983; 1985; 1986; Underwood, 1979; 1985; 1991; 1992; 1994; Underwood and Denley, 1990). In this chapter we will be concerned with the pro- cesses that interact to ensure the persistence of species as members of shore communities and the maintenance of community structure. Concepts discussed include the ways in which plants and animals interact on the shore (including grazing, predation, and competition), the role of disturbance, and the interrelated ideas of succession and stability. While some of these processes operate on both hard and soft shores, there are considerable differ- ences between the two shore types that require their sep- arate consideration. 5.2 HARD SHORES 5.2.1 I NTERACTIONS BETWEEN PLANTS AND A NIMALS The interactions between plants and animals on rocky shores are complex. Of all the possible interactions, graz- ing has received the most attention. Research has focused on topics such as grazer diets, energy flow, foraging behavior, grazing and control of community structure, impacts of grazing on succession after disturbance events, grazing as a factor controlling the vertical distributions of macroalgae, macroalgae as habitats for invertebrate mac- rofauna and meiofauna, the impact of grazers on sessile animals, especially barnacles, competitive interactions, grazing, and algal functional morphology and chemistry. Space, however, will not allow the consideration of all these topics. 5.2.1.1 Grazing 5.2.1.1.1 Ecological categories of algae Three ecological groups of algae are recognized, each of which presents grazing animals with different problems. 1. Microflora. The film of diatoms, blue-green algae, and the spores and sporelings of mac- roalgae that carpet rock surfaces and the hard part of many animals. 2. Encrusting algae. Many kinds of calcareous (e.g., Lithothamnion) and noncalcareous “tar- crusts” such as Hildenbrandia form patches or continuous sheets on rocky shores. Gener- ally, the calcareous algae are restricted to low on the shore, except in rock pools or beneath macroalgae. 3. Erect, foliose algae. These can be either turf forming or occur as discrete individuals. They are subdivided into ephemeral, short-lived opportunistic species; longer-lived, larger peren- nial species; and epiphytes (species growing on other algae). Many are opportunistic species. 5.2.1.1.2 Principal types of herbivorous grazers Grazers eat both micro- and macroalgae; only parts of the latter may be consumed and the plants may survive the grazing. A great variety of grazers are found on rocky shores depending on tidal level, exposure to wave action, and geo- graphic location. They can be categorized as follows: 1. Littoral fringe species. The principal species worldwide are small snails, principally species in the Family Littorinidae. Other grazers high on the shore include omnivorous amphipods and isopods. 2. Eulittoral species. Molluscs are the dominant grazers. Prosobranch limpets are particularly © 2001 by CRC Press LLC 278 The Ecology of Seashores important in temperate regions (Branch, 1981). Trochids and mesogastropods, including some littorinids, are also major grazers (see Menge, 1976; Lubchenco, 1978; Underwood, 1979). At lower latitudes and in the Southern Hemisphere, pulmonate limpets such as Siphonaria spp. are important (Underwood, 1980; Branch, 1981; Underwood and Jernakoff, 1981). In some regions, e.g., the west coast of South America and Australasia, chitons are significant grazers (Boyle, 1977; Paine, 1980). Various crustaceans (classified as mesoherbivores) can be important grazers. They include amphipods (Pomeroy and Levings, 1980) and isopods (Nicotri, 1977, 1980), which can attain densities of thousands of animals m –2 , but due to their nocturnal activ- ity their abundance and importance have not been recognized. Decapods and fishes can also be important grazers, especially in tropical regions (Menge and Lubchenco, 1981). 3. Mid- and low-shore tide pools, sublittoral fringe, and sublittoral proper. Here the predom- inant grazers are regular sea urchins (Mann, 1977; Paine and Vadas, 1969; Dayton et al., 1984; 1992). Some grazing opisthobranchs, such as aplysiomorphs, bullomorphs, and sac- coglossans are also found here. On some shores, especially along the temperate West coast of the Americas and Australasia, abalones (gastropods of the genus Haliotis) are promi- nent herbivores feeding on drift algae. 5.2.1.1.3 Diets of grazers Mollusca: Most chitons, prosobranch limpets, and snails are generalist grazers, feeding on any microalgae or detri- tus available on the rock surface (Newell, 1979; Under- wood, 1979; Branch, 1981; Steneck and Watling, 1982). Much of the microalgal film consists of algal sporelings. Other molluscs, particularly mesogastropods, feed on large erect algae, rather than, or as well as, microflora or encrusting forms, and usually do exhibit choice in diet. Winkles and topshells in general prefer green algae to the tougher, unpalatable reds and browns (Lubchenco, 1978; Underwood, 1979). Siphonarian limpets feed mainly on greens such as Enteromorpha and Ulva (Underwood and Jernakoff, 1981). Some limpets and many snails such as Littorina obtusata and Lacuna spp. live and feed epiphyt- ically on a particular host alga (e.g., Branch, 1981; Under- wood, 1979). Most molluscan grazers are, however, extremely catholic in their feeding behavior eating the algae that are available if they can manage to eat them. Hawkins and Hartnoll (1983a) following Branch (1981) list four basic feeding patterns: (1) generalists feeding mainly on microalgae, detritus, and encrusting algae on the rock surface; (2) species feeding on macroalgae; (3) terrestrial species closely linked to a food plant; and (4) epiphytic stenotypic species that feed on their host plant. Echinoderms: Regular sea urchins are the major group of grazing echinoderms. Most species are subtidal and they are generalist browsers feeding on a wide variety of algae and also sessile encrusting animals (although most species have diets dominated by macroalgae). When food is abundant, they exhibit marked food preferences (Menge, 1976; Lubchenco, 1978; Sousa et al., 1981). They can also capture and feed on drift algae. Crustacea: There are two basic types of feeder: those that scrape the rock surface and those which feed on macroalgae. None of the latter seem to feed on a single species, but they often exhibit clear preferences both in the field and the laboratory. Fish: Few species of fish feed on intertidal algae in temperate regions, but fish grazing is very important in subtropical and tropical regions (e.g., Montgomery, 1980; Menge and Lubchenco, 1981), especially on coral reefs (Sale, 1980; John et al., 1992). In terms of their feeding methods, herbivorous fishes can be classified either as browsers or grazers (Russ, 1984; 1987; Horn, 1992). Browsers bite or tear off pieces from upright macroalgae and rarely ingest any inorganic material, whereas grazers feed on leafy, filamentous, or finely branched red or green algae (Klump and Polunin, 1990) and may ingest quanti- ties of inorganic material. Herbivorous fishes are more diverse in tropical than in temperate waters and few strictly herbivorous species are found beyond 40°N and S latitudes (Horn, 1989). Browsing species belong to the tropical Families Acanthuridae (sturgeon fishes), Pomato- centritidae (damsel fishes), and Signidae, the tropi- cal/warm temperate Families Grillidae, Odacidae, and Stichaeidae, among others. Grazing species belong to tropical Families Acanthuridae, Pomatocentridae, and Scaridae, the tropical/warm temperate Families Bleniidae and Mugilidae, and the temperate-zone Families Aplodac- tylidae and Grillidae, among others. On the West coasts of tropical and subtropical Africa, algivorous or omnivorous fishes often congregate in con- siderable numbers on broken rocky shores (John et al., 1992) where the physical relief affords them protection from carnivores. In the Caribbean they are associated with coral reefs rather than rocky shores. The majority of the species of nonterritorial fishes belong to two Families, the Acantharidae (sturgeon fishes) and Scaridae (parrot fishes). In addition there are the generalist herbivores belonging to the Family Pomacentridae (damsel fishes). These are territorial “gardening” species (see Section 5.2.1.1.4 Foraging behavior Chapman and Underwood (1992) recently reviewed for- aging behavior in marine benthic grazers. Two main aspects of foraging behavior relate to its temporal and © 2001 by CRC Press LLC 5.2.1.1.11). Control of Community Structure 279 spatial components. The temporal component covers vari- ations in the timing or rate of foraging, particularly diurnal or tidal rhythmicity. The spatial component concerns the distances and directions moved while foraging, and the occurrence or otherwise of homing to a fixed site. The timing of foraging: Temporal patterns of forag- ing activities have recently been reviewed by Hawkins and Hartnoll (1983a) and Little (1989). A great variety of patterns have been reported. Nevertheless, despite the complexity, certain trends can be observed. Nearly all grazers show a tidal correlation in their grazing pattern. The exception to this are species living high on the shore that respond quickly to external stimuli like wave wash, the weather, or periods of submergence. Low-shore ani- mals are often more predictable in their temporal patterns, frequently showing circatidal rhythms on the rising and falling tide, remaining inactive at low and high tide. Other low-shore species, e.g., the limpet Patella miniata, feed independently of either time of day or the tide (Branch, 1971). Some subtidal grazers also show circadian patterns of foraging. The New Zealand sea urchins Evechinus chlo- roticus and Centrostephanus coronatus are nocturnal graz- ers, remaining immobile during the day. Foraging patterns: Nearly all benthic grazers move in order to feed and their movement patterns during feed- ing depend on their distribution and the distribution and abundance of their food. Foraging patterns can be classi- fied as follows: 1. Free range foraging: Where the animals (e.g., many gastropods) are surrounded by food, they do not need to search for it, and any movements made are essentially foraging excursions. While the movements are random in orientation and extent (Underwood and Chapman, 1985; 1989), over longer periods they do tend to remain within a general area of the shore, usually within a vertical belt. 2. Foraging in response to patchy distribution of food: If the food is patchily distributed, some grazers make directional foraging movements. Chemical cues are thought to be important in the location and choice of preferred species of algae (Imrie et al., 1989; Norton et al., 1990). Many species of sea urchins will cover large distances in search of patchily distributed algal food and will form feeding aggregations around individual food items when these are located (Schiel, 1982; Choat and Andrew, 1986; Vadas et al., 1986). 3. Foraging in response to distribution of a shel- ter: Many benthic grazers are limited in the range over which they can forage because of the need to return to shelter, or a different microhabitat after foraging. Many species, par- ticularly limpets, “home” to specific sites (Branch, 1975b), whereas others return to par- ticular habitats different than those in which they feed, e.g., crevices, erect algal shelter (Chelazzi et al., 1985). Homing also occurs in siphonarian limpets, chitons, and some gastro- pods. Figure 5.1 illustrates the homing of a group of Patella vulgata on one high tide. The widespread occurrence of homing indicates that it must be of considerable advantage to the species con- cerned. The benefits that have been suggested fall into two basic categories. The first relates to the exploitation and availability of resources. A fixed location provides a starting point for better relocation of preferred feeding areas (McFarlane, 1980). It could also maintain a bene- ficial even spacing of the individuals that would optimize the use of resources for grazing (Underwood, 1979). The second category of benefits relates to the reduction of physical stress. Continuously returning to a fixed base ensures that the animal remains at a level on the shore where it can survive environmental stress. For limpets on an irregular substrate, homing permits a good fit between the margin of the shell and the rock surface. This good fit should improve protection against preda- tion, dislodgement by wave action, and desiccation (Branch, 1981). FIGURE 5.1 The homing excursions of a group of the limpet, Patella vulgata, recorded by hourly observations during a day- time submersion; the squares indicate the home sites. (Redrawn from Hartnoll, R.G. and Wright, J.R., Anim. Behav., 25, 808, 1977. With permission.) © 2001 by CRC Press LLC 280 The Ecology of Seashores Some limpets establish territories around their home scars (Branch, 1971), usually on patches of their preferred algal food. They vigorously defend both territories and food against invading animals, pushing and occasionally dislodging invaders. The large limpet Lottia gigantia maintains a territory on a patch of the encrusting alga Ralfsia around its home scar (Stimson, 1970; 1973), defending this against encroachment by pushing out invading Lottia, smaller limpets such as Acmaea digitalis, and sessile animals such as mussels. 5.2.1.1.5 Sit-and-wait grazers These species, rather than searching, wait for food in the form of drift algae to come to them. Prominent sit-and- wait grazers are sea urchins and abalones. 5.2.1.1.6 Variability of foraging Foraging activity in many species appears to be extremely labile, varying from place to place and from time to time (Hawkins and Hartnoll, 1983a; Little, 1989). Some species change feeding patterns at different seasons because of either changes in activity or changes in the availability of food. For example, the sea urchins Strongylocentrotus droebachiensis and S. franciscanus feed on a range of attached algae, but have a preference for Nereocystis (Vadas, 1977). This alga is an annual and it dies back each winter. In summer the urchins mainly eat Nereocystis and a variety of other algae. In winter Nereocystis forms a smaller proportion of their diet. Many species also show changes in diet foraging behavior as they grow larger. 5.2.1.1.7 Grazing and benthic microalgal distribution, biomass, and diversity Hunter and Russell-Hunter (1983) found that grazing by the gastropod Littorina littorea on benthic microalgae (aufwuchs) grown on glass surfaces resulted in substantial changes in the bioenergetics and community structure of the microalgae. At all grazing densities (13 to 504 snails m –2 ), the standing crop of the benthic microalgae was markedly reduced compared to that on control (ungrazed) substrata. Both in situ dry mass and organic carbon per square decimeter decreased as snail density increased; however, nutritional quality was improved with an increase in the density of grazers. Carbon per unit dry mass of the benthic microalgae was higher at all grazer densities than for controls, and nitrogen per unit dry mass increased as grazer density increased. The C:N ratio of the benthic microalgae decreased from 10:1 at 13 snails m –2 to 2:1 at 504 snails m –2 . Both microalgal abundance and richness decreased as Littorina density increased. Grazing reduced the number of taxa to 50% of that of control substrates at low snail densities and to <30% of that of controls at high densities. Five taxa (including the genera Achanthes, Nitzschia, Amphora, and Cocconeis) appeared to resist grazing and in terms of number of cells cm –2 , comprised 73% of the cells on highly grazed substrata, compared to 7.9% on control substrata. Other species that feed in a similar manner to the littorinids (by using their radulae to scrape the surface of the rock) consume benthic microalgae and the micro- scopic of sporelings include limpets, siphonariids, and chitons. Most such species have a major impact on mac- roalgal colonization, depending on the degree of grazing pressure they exert. Grazing pressure is a function of grazer density and behavior. Density can be influenced by the density of predators (generally carnivorous gastro- pods) as well as the life histories and the recruitment success of the grazers. It is also influenced by the avail- ability of suitable microhabitats, such as crevices, barnacle cover, or algal canopy. Other factors include: (1) height on the shore (many species only graze when submerged); (2) weather (including season); and (3) degree of wave exposure, as heavy wave action can inhibit grazing. 5.2.1.1.8 Algal defenses against grazing There are three basic ways in which macroalgae can sur- vive herbivore grazing: they can escape grazing by using refuges in time and space; they are able to tolerate grazing; or they can deter herbivores (Hay and Fenical, 1988; 1992). Spatial escape is achieved by growing at a level on the shore inaccessible to grazers, or growing in inacces- sible crevices. Temporal escape can be achieved by grow- ing and reproducing at times when grazing pressure is low. Tolerance of grazing may involve growing at a rate that compensates for tissue loss. Other algae that may be inten- sively grazed maintain a holdfast or encrusting base that can regenerate when grazing pressure is lessened. Some algae have a growth form that deters grazers. For example, grazers have difficulty in penetrating the encrusting calcified thalli of some calcareous red algae. In such algae the growth layer or meristem and the con- ceptacles (bearing the reproductive organs) are in pits and are thus protected from grazing. Many coralline algae such as Corallina have a large proportion of structural tissue, but also low growth rates and low reproductive output. Hay and Fenical (1992) have recently reviewed chem- ical defenses developed by algae to combat grazing. In the field, seaweeds are attacked by many species of her- bivores; this is especially true on species-rich coral reefs where rates of herbivory are higher than for any other known habitat (Carpenter, 1986; Hay, 1991). Thus, to be advantageous in such a habitat, a defensive compound would have to function against a broad range of herbi- vores. Several experimental field studies demonstrate that common seaweed metabolites are often able to do this (Hay and Fenical, 1988; Hay, 1991). As examples, when the following secondary metabolites were coated on the palatable sea grass Thalassia and placed on shallow por- tions of Caribbean coral reefs, all significantly decreased © 2001 by CRC Press LLC Control of Community Structure 281 the amount of plant material lost to herbivorous fishes: pachydictyol-A from brown algae in the family Dictyo- taceae, cymopol from the green alga Cymopolia, stypot- riol from the brown alga Stypopodium, and elatrol and isolaurinterol from red algae in the genus Laurencia (Hay et al., 1987). To date, over 40 pure compounds from a variety of seaweeds have been tested in the field on Caribbean and Pacific coral reefs, or in the laboratory against fishes, sea urchins, crabs, amphipods, or polychaetes (Hay, 1991; 1992; Steinberg, 1992). Although many seaweed second- ary metabolites are broad-spectrum deterrents, several have no known effects against herbivores, and few, if any are deterrents to all herbivores. Herbivore size and mobility are often correlated with resistance to seaweed chemical defenses. Small, second- ary herbivores (mesograzers) that live on the plants they consume often preferentially consume, or specialize on seaweeds that are chemically defended from fishes. These mesograzers avoid or deter predators by associat- ing with chemically noxious host plants and may use compounds that deter fishes as specific feeding or host identification cues. 5.2.1.1.9 Grazing and algal distribution It has been generally accepted that the upper limits of intertidal algae are set by physical factors, while the lower limits are set by biological interactions such as grazing, predation, and competition (see Section 2.7). However, while physical factors are of major importance in control- ling upper limits, it has become evident that grazing also plays a major role in determining algal upper limits (Underwood, 1980; Underwood and Jernakoff, 1981; 1984; Hawkins and Hartnoll, 1983a; Jernakoff, 1983). Upper limits and grazers — One of the most notable features of the rocky shores of New South Wales, Austra- lia, is the fairly abrupt upper limit of foliose macroalgae at the top of the extensive algal beds on the lower shore (Underwood, 1981b). Above this limit on sheltered shores, grazing gastropods are abundant, and the only algae are crustose species (Underwood, 1980). When cages and fences prevented grazers from entering some areas of the shore, there was rapid development of foliose algae (Underwood, 1980; Jernakoff, 1983). These plants could survive at levels much higher than they were normally found, provided grazers were absent. Intensive grazing by the gastropods remove virtually all the sporelings and microscopic stages of the algae. Southward and Southward (1978) document the rais- ing of the upper limits of various low shore red algae and the brown algae Himanthalia and Laminaria following massive mortality of limpets, topshells, and Littorina spp. following the Torrey Canyon oil spill (Figure 5.2). Other algae such as Fucus serratus, Palmaria palmata, and Dumontia have all grown more abundantly higher up the shore than normal after limpet removal experiments (Hawkins, 1981a; Lubchenco, 1980). On the Pacific coast of the U.S., ephemeral algae such as Enteromorpha and Porphyra survive the summer in areas from which grazers, such as littorinids and limpets and also crabs (Pachygrap- sus) and dipteran larvae, have been excluded (Robales and Cubit, 1981). Lower limits and grazers — Many species of algae will grow profusely at lower levels on the shore than normally occupied if grazing lessens or stops due to nat- ural causes or experimental removal of grazers. This is particularly true of North Atlantic ephemeral algae, which are the initial colonizers in grazer exclusion experiments (e.g., Ulothrix spp., Blidingia minima, Enteromorpha spp., Porphyra spp.) (Menge, 1976; Lubchenco, 1978; 1980: Little and Smith, 1980; Hawkins and Hartnoll, 1983a). Similar results in molluscan removal experiments have been found in other areas around the world in Australasia (Underwood and Jernakoff, 1981), South Africa (McQuaid, 1980; Branch, 1981), and on the Pacific coast of North America (Dayton, 1971; Paine, 1980). In conclusion, grazing is in many instances as impor- tant as competition or physical factors in determining the vertical distribution patterns of algae, though grazing can act in concert with competition or modify competitive ability (Lubchenco, 1980). Figure 5.3 plots models of variation in grazer importance at various levels on the shore and their relationship to food availability. Food availability increases downshore (Figure 5.3A). On the Pacific coast of North America, grazing declines into the mid-sublittoral zone and then declines again into the deep sublittoral (Foster, 1992). On northeastern Atlantic shores (Hawkins and Hartnoll, 1983a), grazing is most important in the high- and mid-eulittoral and in the mid- to deep- sublittoral, and the algal assemblage in the splash zone is limited directly by physiological stress. Duggins and Dethier (1985), by manipulations of the density of the chiton Katharina tunicata, studied its impact on the species composition and abundance of algal assemblages in the San Juan Islands, Washington, U.S.A. over a period of ten years. K. tunicata ranges from about 0.5 m above, to 1.0 m below mean lower low water (MLLW). Prominent algae here are the perennial intertidal kelps Hedophyllum sessile, Alaria, Laminaria, and Nereo- syctis. Over the ten-year period, algal abundance and diversity increased in the areas where Katharina was removed; algae of most functional groups proliferated and a multistoried intertidal kelp bed eventually developed. In areas where Katharina were added, the abundance of all plants except crusts, diatoms, and surfgrasses decreased and overall diversity declined. Control sites underwent year-to-year fluctuations in the abundance of the most conspicuous algae, H. sessile, but otherwise remained © 2001 by CRC Press LLC 282 The Ecology of Seashores unchanged. It is clear that this grazer has a considerable impact on the diversity and abundance of the algae in the areas in which it grazes. Levings and Garrity (1984) investigated the impact of the pulmonate Siphonaria gigas in the mid-intertidal on rocky, wave-exposed shores on the tropical Pacific coast of Panama. On these coasts, erect macroalgae and sessile invertebrates are rare; crustose algae covers 90% of the rock surface. The relative abundance of a common blue-green algal crust (Schizothrix calcicola?) is nega- tively correlated with Siphonaria’s abundance. Large- scale removals of the limpets caused rapid increases in the percent cover of Schizothrix and concomitant decreases in other crusts, but no changes in the abun- dance of erect algae or sessile invertebrates. Removal of Siphonaria also (1) increases recruitment of crustose algae and barnacles into new rock and plexiglass sur- faces, and (2) decreases the abundance of a calcified form of Schizothrix. 5.2.1.1.10 Contrasts in grazing on temperate and tropical shores Brosnan (1992) has drawn attention to the contrast in zonation patterns and the nature of herbivorous grazers on tropical and temperate shores. Overall, herbivorous fish are more common in the tropics, while invertebrate grazers dominate temperate shores; this difference is responsible for much of the variation in algal composition and abun- dance between tropical and temperate shores. Brosnan (1992) presented a generalized model to predict the dis- FIGURE 5.2 Grazing and zonation of low shore algae, Cape Cornwall, wave-beaten rocks: sketches showing changes in zonation after the Torrey Canyon disaster: upper — the situation in May 1968, 13 months after all herbivores (limpets, topshells, littorinids) had been killed by dispersants; lower — nine years later in May 1977, showing more normal conditions after full return of herbivorous populations; upper limits of Laminaria digitata and Himanthalia were 1.5 to 2 m higher in Spring 1968 than in Spring 1977; MT, mean tide level; LWS, mean low water springs level. (Redrawn from Southward, A.J. and Southward, E.C., J. Fish. Res. Bd. Canada, 35, 698, 1978. With permission.) © 2001 by CRC Press LLC Control of Community Structure 283 tribution of algal types in relation to herbivore size and efficiency (Figure 5.4). When herbivorous fish are abundant, algal growths will not compensate for herbivory — such shores appear barren or dominated by grazer-resistant crustose forms. If slower-moving invertebrate grazers predominate, the greatest effects occur where algal growth is too slow to compensate for herbivory (e.g., the upper shore, especially during the tropical dry season). Grazer impact increases as algal growth rates increase (e.g., lower down the shore and during the wet season (Lubchenco, 1980; Underwood, 1980; Cubit, 1984). As fish forage frequently on tropical shores, they have a less patchy appearance than on temperature shores (e.g., Gaines and Lubchenco, 1982; Menge et al., 1985; 1986a,b). Seasonality on tropical shores will be less pro- nounced as any increase in algal biomass will be quickly eaten, and herbivores will limit the upper distributions of algae more frequently than on temperate shores. In addi- tion, competition among foliose algae should be less important. On temperate shores where molluscs domi- nate, seasonal effects in algal abundance are more pro- nounced as algal productivity often exceeds grazing (Underwood, 1980; 1981; Underwood and Jernakoff, 1981; 1984: Branch, 1986), and other factors (e.g., com- petitive and physical) are relatively more important in setting distributional limits. This is because at low pri- mary productivity, spatial and temporal plant escapes will be important and will tend to result in patchy algal dis- tributions. At high growth rates, algae will be more evenly distributed as productivity will exceed herbivory and algae will dominate spatially. Tropical shores will be located in the right rectangle in Figure 5.4, but their mid- to upper zones could oscillate back and forth between the upper left and lower left rectangles during the wet and dry seasons. A second prediction of the model relates to herbivore size and the rate of resource renewal. Fast-growing algae will be able to support larger-sized grazers than will slow- growing algae. Larger grazers should be more prevalent lower on the shore, and smaller grazers higher up. Large limpets such as Patella cochlear are found low in the intertidal zone where their persistence depends on high algal productivity, while smaller littorinids are found high on the shore. On most shores this pattern applies, although other factors such as desiccation are involved. FIGURE 5.3 A graphical summary or model of variation in grazer importance and its relationship to food availability on semiprotected shores in the northeastern Pacific, and a comparison with the model of Hawkins and Hartnoll (1983). (a) Changes in food availability (solid line: maximum availability with bars representing variation; dashed line: effect of increased desiccation). (b) Changes in grazing importance at the spatial scale of assemblage (solid line: minimum importance with bars representing variation; dashed line: effect of reduction in algal availability due to desiccation). (c) Hawkins and Hartnoll’s (1983) model of grazer importance. ? = lack of information. (Redrawn from Foster, M.S., in Plant-Animal Interactions in the Marine Benthos, John, D.M., Hawkins, S.J., and Price, J.H., Eds., Clarendon Press, Oxford, 1992, 72. With permission.) © 2001 by CRC Press LLC 284 The Ecology of Seashores 5.2.1.1.11 Gardening Grazers that influence the composition or growth of algae are often referred to as “gardeners.” Branch et al. (1992) define this behavior as: “modification of plant assem- blages, caused by the activities of an individual grazer within a fixed center, which selectively enhances particu- lar plant species and increases the food value of the plants for the grazer.” Three major groups of animals have been recorded as gardeners. Tropical reef fish (mainly poma- centrids) are well-documented examples (see Branch et al., 1992 for a list of references). Individual fish defend patches of algae, aggressively repelling other fish and sea urchins. The result is the development of small algal assemblages different than those in the surrounding area. Some limpets also garden. In California the giant lim- pet Lottia gigantea maintains a territory with a fine algal film and excludes other grazers from this territory. It also hinders invasion of its gardens by sessile species (Stimson, 1973). The South African limpets Patella longicostata and P. tabularis have specific associations with the encrusting alga Ralfsia verrucosa and also defend their gardens against other grazers (Branch, 1975b,c; 1976; 1981). The South African limpet Patella cochlear, which lives in dense aggregations, has a narrow fringing garden around each limpet of fine red algae, usually Herposiphonia her- ingii or Gelidium micropterum, the latter apparently only occurring in these gardens (Branch, 1975c). The third example comprises the nereid polychaetes Platynereis bicanaliculata and Nereis vexillosa, which catch drifting fragments of green algae and attach them to their tubes, which are embedded in soft sediments. The attached algae provide a predictable food supply. As the nereids interact aggressively, their tubes are spaced out, helping to restrict the use of the algae to the individuals gardening them. Most gardens consist of opportunistic, fast-growing species — often filamentous, delicate red or green algae, but sometimes encrusting forms. Gardens increase local productivity relative to that in adjacent areas (Figure 5.5) (Montgomery, 1980; Klump et al., 1987; Russ, 1987). This shift is brought about by the nature of the algae involved, and because they are maintained in an early rapid phase of growth by continual grazing. Apart from their higher productivity, algae in the gardens of fish species have a higher proportion of protein, and lower ash content and C:N ratios than algae outside the territories (Montgomery, 1980; Klump et al., 1987; Russ, 1987). Outside damselfish territories, algal biomass is low (Figure 5.5) and is dominated by encrusting corallines. Inside territories, biomass rise and become dominated by filamentous forms. Limpets present a different picture and appear to intensify grazing pressure within their gardens by concentrating on a small area. Algal biomass is invari- ably lower in their gardens than in adjacent areas (Figure 5.5). They do, however, enhance productivity. 5.2.1.1.12 Grazing and community structure Patchiness is a fundamental feature of rocky shore com- munities. Such patchiness can be due to a variety of causes, including grazing. One of the best documented examples of the role of grazing in creating patchiness is on moder- ately exposed shores in the British Isles where Patella spp. FIGURE 5.4 A model of algal composition and distribution in relation to herbivore type (mollusc or fish, and algal productivity). This model predicts outcomes of interactions between herbivore type and algal productivity. When fish are more important (right rectangle), shores have a uniform appearance (bare space or crustose algae), competition between foliose algae is predicted to be low, and herbivory is important at all tidal heights. When slow-moving molluscan grazers predominate, their effectiveness depends on algal growth rates, and this in turn affects the relative importance of competition and physical stress. (Redrawn from Brosnan, D.M., in Plant-Animal Interactions in the Marine Benthos, John, D.M., Hawkins, S.J., and Price, J.H., Eds., Clarendon Press, Oxford, 1992, 111. With permission.) © 2001 by CRC Press LLC [...]... sequences as described above Removal of the dominant macroalgae also initiates successional events The rate of recovery for the impact of harvesting will largely depend on the sizes of the cleared patches and the type of harvesting regime (i.e., whether removal is total or partial) and the the capacity of the algae for vegetative growth 308 5. 2 .5 The Ecology of Seashores ENVIRONMENTAL HETEROGENEITY,... Carcinus maenus, the whelk Thais emarginata, and the gastropod Conus ebraeus 5. 2.2.4 Interspecific Competition The outcome of interspecific competition will vary with the nature of the species involved, the means of competition, the kind of resources competed for, and the amount of overlap of the niches of the species (Branch, 1984) Where competition is extreme, it can result in the exclusion of the weaker... negative The variety of these indirect effects was due to both consumer-prey interactions among the consumers, and competitive or commensalistic interactions among the sessile prey Comparison of the sum of the effects of each of the single consumer groups (i.e., the sum of the effect observed in treatments with one group absent, three present) with the total effects of all consumers (i.e., the effect... Cellana among the barnacles (Figure 5. 11) Figure 5. 11A shows that the mortality of P latistrigata increased if all or half The Ecology of Seashores of the barnacle cover is removed, due to C tramoserica invading the area This interspecific interaction is further complicated by the presence of the common predatory gastropod Morula, which attacks the barnacles Following an increase in the numbers of Morula,... 1984; Moran, 1985c; Fairweather, 1987) The impact of M marginalba on the assemblages of prey depends indirectly on the availability of crevices, prevailing conditions of desiccation and wave shock, and the densities and preference ratings of the available prey (see Fairweather et al., 1984; Fairweather, 19 85; 1987; 1988a,b; Moran, 1985a,b,c) In experimental removal of Morula (Fairweather, 1986), it... occurs in the middle and upper balanoid zone of the rocky shores of the Cape of Good Hope, South Africa Two areas were compared, the mid-balanoid zone and the upper Littorina zone Ten prey species were recorded (Figure 5. 13) The principal prey species in the mid-balanoid zone was the barnacle Tetraclita serrata, while on the upper shore it was the winkle Littorina africana knysnaensis Predation in the Littorina... in a mosaic of differently aged patches (Connell, 1961a; Dayton, 1971) Typically, investigators determine the effect of consumers by examining the responses of the system in the absence of the predators However, predation intensity varies from the extremes of no effect vs a normal effect In order to gain a clear understanding of the patterns of community structure as a result of the impact of predators,... at the beginning of the study in 1983, when the intertidal community was dominated by mussels, to values of ca H = 2 toward the middle of the study in 1984 (which coincided with the maximum predatory impact of C concholepas), and subsequently decreased to ca H = 0 .5 at the end of the study in 1987, when the mid-intertidal community was dominated by barnacles Fissurelid (keyhole) limpets are among the. .. barnacles in the mid-shore, tubeworms in gastropod pools and the mid-shore) When young individuals occurred in these areas, the whelks normally ate them all In another series of experiments (Fairweather, 1987), either barnacles, limpets, or tubeworms were added to sites where they were quickly consumed by the whelks that were present McQuaid (19 85) investigated the differential effects of predation by the intertidal... Results of observations and experiments by Whitman (1987) indicated that storm-generated dislodgement of mussels overgrown by kelps was the mechanism reducing the ability of Modiolus to maintain and hold space in the shallow kelp zone Removal of sea urchins Strongylocentrotus droebachiensis from the lower edge of the kelp zone resulted in the downward shift of kelp to a 12 . 5- m depth, demonstrating that the . 324 5. 3 .5. 2 Meiofaunal Predation 3 25 5.3 .5. 3 Predation by Infauna 326 5. 3 .5. 4 Predation by Epifauna 326 5. 3 .5. 5 Impact of Predation on Bivalves 328 5. 3 .5. 6 Multiple Predation on Tidal Flats 328 5. 3 .5. 7. 328 5. 3 .5. 7 Predation by Birds 328 5. 3 .5. 8 Role of Predation in Structuring Soft-Bottom Communities 332 5. 3.6 Influence of Resident Fauna on the Development of Soft-Bottom Communities 333 5. 3.7 Role of. Determine the Sedimentary Environment 350 5. 4.2.4 The Hydrodynamic Regime and Benthic Infaunal Species 351 5. 4.2.4.1 Larval supply 351 5. 4.2.4.2 Food supply 352 5. 4.2 .5 The Importance of Recuitment 352 5. 4.2.6