Rocky Shores        Of all the intertidal shores, those composed of hard material, the rocky shores-particularly those of the temperate zones-are the most densely in­habited by macroorganisms and have the greatest diversity of animal and plant species. They con­trast sharply With the almost barren appearance of the surface of sand and mud shores. It is these densely populated, topographically diverse, and species-rich rocky areas that have fascinated ma­rine biologists and ecologists for many years. In the last 30 years, these areas have been the subject of several classic studies that have enhanced our understanding of how these associations of species interact to maintain or change the commu­nity. It should be noted at the outset that these in­tertidal rocky areas differ fundamentally from the

subtidal rocky areas discussed in Chapter 5. Most of the dominant organisms of intertidal rocks are solitary or clonal animals, whereas subtidal rocks seem dominated by colonial encrusting animals.



One of the most striking features of any rocky shore anywhere in the world at low tide is the prominent horizontal banding or zonation of the organisms. Each zone or band is set off from those adjacent by differences in color, morphology of the major organism, or some combination of color and morphology. These horizontal bands or zones succeed each other vertically as one progresses up from the level of the lowest low tides to true ter­restrial conditions (Figures 6.7, 6.8). This zonation on intertidal rocky shores is similar to the zonation pattern one observes with increasing elevation on a mountain, where the different horizontal zones of trees and shrubs succeed each other vertically until, if one progresses far enough, permanent snow cover is reached. The major difference be­tween these two areas is the scale. Mountain zones are perhaps kilometers in extent as opposed to in­tertidal zones extending a few meters vertically.



Rocky intertidal zones vary in vertical extent, depending on the slope of the rocky surface, the tidal range, and the exposure to wave action. Where there is a gradual slope to the rock, individ­ual zones may be broad. Under similar tidal and ex­posure conditions on a vertical face, the same zones would be narrow. In the same manner, ex­posed areas have broader zones than protected shores, and shores with greater tidal ranges have broader vertical zones (Figures 6.4, 6.8).

Of course, these striking bands may be inter­rupted or altered in various places wherever the rock substrate shows changes in slope, composi­tion, or irregularities that change its exposure or position relative to the prevailing water movement.

The fact that these prominent zones can be ob­served on nearly all rocky shores throughout the world under many different tidal regimes led Stephenson and Stephenson (1949) to propose, after some 30 years of study, a "universal" scheme of zonation for rocky shores (Figure 6.9). This uni­versal scheme was really a framework using com­mon terms that would allow comparison of diverse areas. It established zones based on the distribu­tional limits of certain common groups of organ­isms and not on tides. It reflects the knowledge of the Stephensons, and other intertidal ecologists, that distribution patterns of the organisms and zones vary not only with tides, but with slopes and exposure. Therefore, under similar tidal conditions there could be different bandwidths due to differ­ent exposures or slopes of rocks. It was this univer­sal scheme that established a standard format for describing shore zonation, replacing a bewildering host of schemes and names established by earlier biologists.

The Stephensons' scheme has three main divi­sions of the intertidal area. The uppermost is termed the supralittoral fringe. Its lower limit is the upper limit of barn4eles, and it extends to the upper limit of snails of the genus Littorina (periwinkles). The dom­inant organisms are the littorine snails and black en­crusting lichens (Verrucaria type). The extreme high water of spring tides reaches part of this zone, but most of its water comes from wave splash. Above this zone is the terrestrial or supralittoral zone.

The middle part of the intertidal is termed the midlittoral zone and is the broadest in extent. Its upper limit coincides with the upper limit of bar­nacles, while its lower limit is the point where

zone is often subdivided and contains a host of different organisms. Perhaps the only universally present dominant group are the barnacles.

The lowest zone of this scheme is the infralit­toral fringe, which extends from the lowest low tide up to the upper limit of the large kelps. This is an extremely rich zone composed of organisms that can tolerate only limited exposure to air. It is really an intertidal extension of the infralittoral zone (Stephensons' term) or what we know as the sublittoral area.

Although Stephensons' scheme did set forth a means for describing zonation on rocky shores, it does not offer an explanation of why the zonation occurs. It is this explanation of zonal patterns that intrigues many marine biologists.



Causes of Zonation

Whereas it is fairly easy to recognize and measure the extent of the zones on a rocky shore, it is more difficult to find suitable explanations for why or­ganisms are distributed in these zones. Physical and biological factors can be considered to explain the phenomenon. We shall take up each in turn.

Upper-limit barnacles

Equinoctial high-water spring tides



 A = Supralittoral (spray) zone A' = Supralittoral fringe

B = Littoral zone

B' = Midlittoral

C = Infralittoral zone C = Infralittoral fringe


FIGURE 6.9 Stephensons' universal scheme of zonation for rocky shores. (From R. L. Smith, Ecology and field bi­ology, 3d ed., Figure 8-4. Copyright © 1980 by Robert

Leo Smith. Reprinted by permission of Harper & Row Publishers, Inc.)

large kelps (Laminaria, etc.) reach their upper­most distribution. This

nalus is


Equinoctial low-water spring tides



PHYSICAL FACTORS The most obvious expla­nation for the occurrence of the zones is that they are a result of the tidal action on the shore and re­flect the different tolerances of the organisms to in­creasing exposure to the air and the resultant desiccation and temperature extremes. One diffi­culty with this explanation is that the rise and fall of a tide tend to follow a smooth curve with, no ob­vious sharp breaks corresponding to the often sharp boundaries observed in the intertidal zones. If, however, one observes a whole series of such tidal curves, such a series of breaks does become apparent. For example, Figure 6.10a gives a typical tidal curve for a mixed tide area on the California coast. Figure 6.10b gives the maximum time of continuous submergence for various tide levels. The graph shows that there are certain points on this curve that reflect sharp increases in exposure to air. This can also be deduced from Figure 6.1Oa, which represents a single typical lunar tide cycle. Consider an organism at point X on the graph. At this point, the tide will cover the organism at least once every six hours. If, however, the organism moves up only a few inches, the tide will not cover it for 12 hours. There is a great change in exposure time with a very short vertical movement. Points exhibiting sharp increases in exposure time over short distances have been termed critical tide levels by Doty (1946) and were offered as one of

the early explanations for the zonation patterns de­scribed previously. In this explanation, it is impor­tant to remember that it is not the tide alone that causes the limit but the fact that, at these critical points, the organisms are subjected to greatly in­creased time in the air; hence, they experienced greater temperature fluctuations and desiccation.

The critical tide hypothesis has been tested in var­ious places by several scientists since its original pro­mulgation by Doty in 1946. In general, it is difficult to find good correlations, particularly at the lower tide levels. This lack of good correlation can be partly attributed to the diverse topography of the dif­ferent shores and to the variation in exposure. Thus, a species may be able to exist above the critical tide level if the rocky shore is exposed to persistent vio­lent wave action, which would throw water up higher and decrease desiccation. Similarly, caves, overhangs, and crevices remain moist when ex­posed areas are dried out; thus, organisms are able to persist above the critical tide level. The effects of differences in topography and exposure suggest, however, that the ultimate upper limits are set by cer­tain physical factors: desiccation and temperature.

We have previously noted that desiccation is a serious problem. Several natural observations, as well as field experiments, have suggested that des­iccation can set the upper limits to organisms and zones. In the North Temperate Zone, for example,

rocks that have a north-facing slope often have the same organism occurring higher than do adjacent south-facing slopes. Since such rocks experience no difference in wave exposure or tides, the only reason for the height difference is that north faces dry out more slowly than south faces. Similarly, field experiments by Frank (1965) and others in which water was slowly dripped down slopes have resulted in the organisms extending higher up (Figure 6.11). In other experiments, organisms were transplanted above their normal positions. Notable in this respect are barnacles, which can­not move. When transplanted by Foster (1971) above their normal tidal height, they died. Younger barnacles died more quickly than older ones. Again, desiccation can be suspected.

Along with desiccation, and often acting in con­cert with it, is temperature. As noted previously, aer­ial temperatures have ranges that may exceed the lethal limits; hence, intertidal organisms may die from either freezing or "cooking." Upper limits of zones in part may be attributed to the tolerable tem­perature limits of the intertidal organisms. In addi­tion, high temperature promotes desiccation, and the synergistic effect of these factors may be even more devastating than each acting alone. The lack of abundant organisms on rocky intertidal shores of the tropics may be at least partly the result of desicca­tion combined with heat and ultraviolet light stress.

Finally, sunlight may act adversely to limit organ­isms on the shore. Sunlight includes wavelengths in the ultraviolet (UV) region that can harm living tissue. Water absorbs these wavelengths and pro­tects most marine animals. However, intertidal ani­mals have direct exposure to such rays at low tide. The higher an organism is in the intertidal, the greater the exposure to these rays. At present, there is little information concerning whether UV radiation controls distribution of organisms, but the recent finding of UV-absorbing compounds in shallow-water organisms suggests its importance. Light also has been suggested as a regulator of the distribution of intertidal algae. This has to do pri­marily with the spectral quality of the light. As noted in Chapter 1, different wavelengths of light are absorbed differentially by water. In the case of intertidal algae, those that need light of longer wavelength (reds) that are absorbed most quickly by water would tend to be found higher in the in­tertidal. When submerged, they would not be too deep for the penetration of red light (about 2 m). Since the main intertidal algae belong to three dif­ferent groups-reds, browns, and greens-each of which has a slightly different absorption spectrum, it might be thought that they would be arranged along a depth gradient. In such a gradient, the green algae would be expected to be the highest, because they absorb mainly red light; the brown next; and the red algae deepest, because they ab­sorb mainly the deep, penetrating green light. This, however, is not the case. The intertidal algae are a mixture of all types at most levels. This is likely due to the interaction of other factors and the physiology of the algae. It points out again the fallacy of attempting to explain patterns of species distribution with only single factors when a multi­tude are acting at all times.

Although there is a large body of evidence that physical factors are the strongest determinants of the upper limits of organisms, there may be alter­native explanations, many of which have not been investigated. Underwood and Denley (1984) point out that other processes are at work in the high intertidal that may be confused with physical effects. For example, some animals in the high intertidal, particularly sessile filter feeders, may be killed by starvation during long periods of calm weather because they are not covered with water long enough to feed. Similarly, grazing animals may be absent, not because they cannot tolerate the physical factors, but because their algal food is ab­sent, perhaps killed by severe physical factors. Finally, in the case of larvae settling out of the plankton, they may choose not to settle in the area, in which case the upper limit is set by processes affecting larval settlement. In one in­stance reported by Underwood (1980), the upper limit of several algal species in Australia was di­rectly due to grazing by gastropods. In each of these cases, the upper limits of the organisms are the result of biological and physical factors acting either independently or together.

BIOLOGICAL FACTORS Although the early work in the intertidal focused on the importance of physical factors in setting the zonal patterns, more recent work has begun to clearly establish the great importance of a number of biological fac­tors in setting various observed distribution pat­terns. In general, these biological factors are more complex, often subtle, and closely linked to other factors. This is probably why we have only re­cently begun to understand how they act. The major biological factors are competition, preda­tion, grazing (herbivory), and larval settlement. We shall discuss them in order.

Competition for a certain resource does not occur if the resource is so plentiful that adequate supplies of it are available for all species or individ­uals. In the rocky intertidal zone, only one re­source is commonly in limited supply and that is space. This is perhaps the most restricted area in the marine environment; at the same time, it is densely populated, at least in the temperate zone. As a result, there is an intense competition for space that has resulted in observed zonal patterns.  

On the intertidal shores of Scotland, there is a distinct zonation of barnacles with the small

 Chthamalus stellatus living in the highest zone and the larger Balanus balanoides occupying the

 major portion of the midintertidal. Studies done by Connell (1961) showed that Chthamalus larvae settled out throughout the zones occupied by both barnacles but survived to adulthood only in upper

zones. The reason for the disappearance in the midlittoral region was due to competition from Balanus balanoides, which either overgrew, up­lifted, or crushed the young Chthamalus. Balanus was prevented from completely eliminating Chthamalus, because unlike Cbthamalus, Balanus did not have the tolerance to drying and high tem­peratures that prevailed at the higher tidal levels; hence, it could not survive there. Here, then, is a case where the zonation is at least partially a func­tion of biological competition (Figure 6.12).

Intertidal algae, particularly those on temperate shores, also often show abrupt limits to their upper and lower distribution. Earlier, these limits were ascribed to critical tide levels, but it has also been suggested that this could be due to competi­tion for space or access to light. In two experimen­tal studies done on the Pacific coast of North America, evidence of competition was found. Dayton (1975) found that the dominant kelps­Hedophyllum sessile, Laminaria setchelli, and Lessionopsis littoralis-all outgrew and outcom­peted certain smaller species in the lower inter­tidal. These smaller species were generally fast-growing species, that quickly colonized open areas. As noted in Chapter 1, they are oppor­tunistic or fugitive species. Among the three dominants, Hedophyllum was outcompeted by the other two, and they dominated the areas. The second study was done in the subtidal, where Vadas (1968) found that the giant kelp Nereocystis outcompeted and overgrew the brown alga Agarum. On the New England coast, studies of tide pool algae by Lubchenco (1978) indicated that Enteromorpha intestinalis was a dominant space competitor as opposed to Chondrus crispus. In the absence of grazers, E. intestinalis would quickly outcompete Chondrus and take over the space. These few studies suggest that competition among algal species may be more widespread than originally assumed and may be a fertile ground for future ecological work.

 Competition among the mussel Mytilus califor­nianus and several species of barnacles on the Pacific coast of Washington (Plate 40) is a more complex example. In this case, studies by Dayton (1971) and Paine (1966, 1974) have shown that M californianus is the dominant space competitor on open coast shores.'' Given enough time and free­dom from predators, the M. californianus eventu­ally overgrow and outcompete all other macro­organisms and take over substrates throughout most of the midintertidal. Mytilus californianus takeover is, however, slow. Wherever open space occurs, it may be rapidly colonized by other organ­, isms, including three species of barnacles: Balanus landula, B. cariosus, and Pollicipes polymerus.

ese, in turn, displace any rapidly growing algal

species. The barnacles persist only until the mus­sels enter. The mussels outcompete and destroy the barnacles by settling on top of them and smoth­ering them. Since nothing appears to be large enough to settle and smother the M. californianus, they remain in control of the intertidal space. Given this competitive edge, it would appear that eventually the rocky Pacific coast of Washington could be a monotonous band of M. californianus. It is also curious that M californianus forms dense clumps or bands only in the intertidal, though it is perfectly capable of living subtidally. Since it is a premier space competitor, why this abrupt lower limit? The reasons for this have to do with other bi­ological factors that prevent such resource monop­olization, namely predation.

The role of predators in determining the distrib­ution of organisms in the intertidal and the zonal patterns is best documented for the Pacific coast of Washington and is discussed here as an example of how complex biological interactions create the prevailing distributions (Plates 41 and 47).

The dominant abundant intertidal animals on the Pacific coast other than the space-dominating Mytilus californianus are the barnacles Balanus cariosus and Balanus glandula. These latter two species occur abundantly in the intertidal region even though they are competitively inferior to M. californianus, because a predatory starfish, Pisaster ochraceus, preferentially preys on M. cali­fornianus, preventing it from completely over­growing the barnacles (see Plate 40). Pisaster ochraceus is a voracious predator of mussels, con­suming them at a rate that prevents them from oc­cupying all the space.

At the same time, Balanus glandula is found primarily as a band of adults in the high intertidal, while Balanus cariosus occurs as scattered, large individuals or clumps in the midintertidal. This pat­tern, as Connell (1970) has shown, is also due to predation. Balanus glandula, like Chthamalus in Scotland, is capable of living throughout the inter­tidal zone and, indeed, settles throughout. The same is true for B. cariosus. That both show a re­stricted distribution is due to predation by three species of predatory gastropods of the genus Nucella: N lamellosa, N. emarginata, and N. canaliculata. The abundance and motility of these predators is such that they are capable of com­pletely consuming all the young B. glandula set­tling out in the midintertidal in 12-15 months. Balanus glandula survives only in a narrow band at the top of the intertidal, where the Nucella species are prevented from entering because of ex­cessive desiccation. In the case of B. cariosus, however,. the situation is somewhat different. There is no high level refuge for this barnacle, and, as with B. glandula, the young are consumed by the Nucella. Size is the defense for B. cariosus. Once it reaches two years of age, it is too large for Nucella to attack (Figure 6.13). The only mystery is how B. cariosus survives the Nucella for two years. It may have to do with periodic events like big freezes at low tide. As a result, the pattern of distribution for B. cariosus is random clumps of large, older barnacles.

It is not known what regulates Nucella popula­tions, but they are preyed on by large Pisaster and are also vulnerable to periodic events, such as freezing during winter low tides. Such periodic events may reduce the population by such a signif­icant amount that the Balanus cariosus could suc­cessfully establish themselves in an area. This may explain the differences among various shores with respect to the abundance of this barnacle.

Although it prefers mussels, Pisaster ocbraceus can consume Nucella and barnacles of any size and is the primary predator of small- and medium­sized Mytilus. It is the top predator in the system. Because of its ability to influence the structure of the entire intertidal community by consuming Mytilus and preventing monopolization of the space, it has been called by Paine (1966) a key­stone species as defined in Chapter 1.

The reason the upper intertidal is a refuge from perdators is that Pisaster and Nucella can feed only when the tide is in, and they require a long period to attack their prey successfully. The short period of immersion of the upper intertidal does not allow sufficient time for them to make success­ful forays into that area. In subtidal areas, unlimited time is available; hence, the starfish have sufficient time to attack and consume their prey. It is proba­bly for that reason that Mytilus, for example, do not extend into the subtidal areas, even though they can live there; hence, it is the reason for the sharp lower boundaries to the zonation of this species (Figure 6.13).

The situation regarding the importance of the interaction of mussels and starfish in structuring intertidal rocky communities of the Pacific coast of Washington has a confounding factor that sug­gests how difficult it is to understand how com­munities are structured and to extrapolate results from one area to another. Paine et al. (1985) have followed up on the earlier studies in Washington with similar studies of starfish removal from inter­tidal shores in Chile and New Zealand to assess the universality of the results obtained earlier in Washington. In Chile, the dominant space occu­pier was the mussel Perumytilus purpuratus, and its predator was the sun star Heliaster helianthus. In New Zealand, the mussel was Perna canalicu­lus, and the predator was the sea star Stichaster australis. When predator removal studies were done in these areas and compared to Washington, a notable difference occurred. In Washington and New Zealand, when the starfish were permitted to return to the areas from which they were formerly excluded, the mussel community persisted in mo­nopolizing the space they had occupied when the starfish were excluded for as long as 14-17 years. In other words, there was no quick return to the conditions seen in control areas where predators were always present. By contrast, in Chile, when starfish were returned to the excluded areas, the community rapidly returned to the condition of the undisturbed control. What are the reasons for this difference? Paine et al. (1985) suggest that the main reason is that in Washington and New Zelnd the mussels were able to attain a size dur­mg the absence of their main predator such that, when the predators were reintroduced, the mus­sels had grown to such a size that they were im­mune to predation. In the case of Chile, Perumytilus  never reaches a size at which it is im­mune to predation; hence, the quick return to a "normal" pattern. These results, in turn, suggest that in Washington and New Zealand the commu­nity will not return to the pre-exclusion state until the current large mussels either die or are re­moved by some other destructive event, such as wave action or crushing by wave-borne objects (see p. 248). This may take years. Whereas we may expect all three of these communities to eventu­ally converge to their "normal" condition, the time involved may be markedly different. In the case of Washington and New Zealand, this may lead to an 

intertidal with a mosaic of patches-some com­pletely dominated by mussels and others with scattered clumps, depending on the conditions and length of time the dominant predator was ex­cluded.

Menge (1976) and Lubchenco and Menge (1978) have also demonstrated that predation is important in setting zonal patterns in the intertidal of the North Atlantic Ocean. In the low intertidal of New England, the competitive dominant species is Mytilus edulis. Mytilus edulis is able to outcompete and eliminate the barnacle Balanus (Semibalanus) balanoides and the alga Chondrus crisp us. It is pre­vented from doing so by the starfish Asterias forbesi and A. vulgaris and the snail Nucella lapillus, all of which prey on M. edulis. Where these predators are absent-namely, in the most exposed, wave-beaten areas-M. edulis eliminates Balanus and Chondrus. The exposed, wave-beaten areas exhibit a zonal pat­tern in which the low intertidal is an M. edulis band, while in protected areas a diverse lower zone exists with Mytilus, Balanus, and Chondrus pre­sent (Figure 6.14).

An unexplained anomaly of the previous pat­tern is found in the very sheltered bays of New England. In these areas, Petraitis (1987) has demonstrated that the barnacle Balanus bal­anoides and the mussel Mytilus edulis are the most common organisms in the lower intertidal, where perennial algae are rare. This is a condition similar to the exposed outer shores, where preda­tors are absent. However, here predators are abun­dant. The herbivorous gastropod Littorina littorea is thought to be responsible for the lack of algae, but the presence of the barnacles and mussels can­not be accounted for by a lack of asteroid preda­tors nor by a refuge in size, since the starfish are capable of consuming all size classes.

The presence of the above mentioned anom­alies in the keystone species concept has caused some researchers to question its usefulness, partic­ularly how it should be defined and the generality of its occurrence. It is appropriate to briefly dis­cuss these points.

At its inception by Paine (1969), the keystone species concept was defined as a single carnivore that preferentially preyed on and controlled the abundance of a prey species that, in turn, could competitively exclude other species and so domi­nate the community. It was subsequently used by

other workers to refer to such noncarnivorous species as herbivores, mutualists, prey, etc.; hence, confusion arose. Menge et al. (1994) have rede­fined the keystone species concept as originally stated and have clarified it by defining two other predator-prey relationships that are not keystone relationships. Diffuse predation is a condition where the total predation is strong and capable of controlling the abundance of a competitively dom­inant species but in which the predation is spread over several predators, not just one. If the total ef­fect of predation on the competitive dominant prey is low such that predation does not alone control the abundance, the condition is called weak predation.

The large geographical extent of the Pisaster­Mytilus community, extending from Alaska to Baja California, suggested to Paine (1969) that this key­stone species concept, at least for this interaction, might hold true throughout the range. Subse­quently, however, others such as Foster (1990) have questioned whether this generality could be maintained, particularly when Pisaster and Mytilus abundances are so variable in different ge­ographic areas. Also, in southern California, it ap­peared that spiny lobsters, not Pisaster, were controlling the mussels.

In a recent test of the generality of the keystone concept, Menge et al. (1994) investigated the high temporal and spatial constancy of the lower limits of Mytilus distribution at several sites in Washington and Oregon in which the abundance of Pisaster showed enormous variation. They com­pared sites that varied in size from meters up to kilometers, adding a question of scale that had not been posed earlier. They found that while Pisaster predation varied dramatically, they were able to conclude that Pisaster behaved as a keystone species, eliminating Mytilus at exposed sites. At more protected sites, however, Pisaster predation was much weaker and variable, and Mytilus was controlled by other factors, such as recruitment and burial by sand.

It seems safe to conclude that the keystone species concept, at least for temperate rocky shores, remains a valid concept. At the same time, it is not a universal concept, and its occurrence is variable within the geographic range of the species or communities in question. It may be replaced under certain environmental conditions by other community regulatory mechanisms, such as diffuse or weak predation or physical factors.

A central theme of marine intertidal ecology, as argued by Connell (1975), is that wherever preda­Von is reduced, competition will be increased. Indeed, the previous examples demonstrate this. It is well, however, to remember that this is not the inevitable result of predator removal. For example, Keough and Butler (1979) removed predatory starfish from pier pilings in Australia and found no changes in the, invertebrate populations or any in­crease in competition. This indicates an important principle: the relative importance of biological fac­tors and physical factors on rocky shores varies over relatively short distances. The variation is both vertical and horizontal. Therefore, one can­not extrapolate from single experimental studies done on small areas to form models for the organi­zation of large geographic areas of the intertidal. .The role of grazers or herbivores in regulating upper and lower limits of algal species is well stud­ied and documented, and evidence suggests this process may also be important. Whereas a number of animals graze on intertidal algae, relatively few grazers seem abundant enough to significantly alter or determine community structure. The dom­inant grazers are various gastropod mollusks, cer­tain crustaceans, sea urchins, and fishes. The relative importance of these groups varies latitudi­nally and vertically in the intertidal zone (Figure 6.15). Their relative abilities to keep algae in check may also vary.

Data on the importance of grazing were late in being reported (not until well after World War II). In the past 20 years, however, considerable evidence has been accumulated by various methods-experimental removals of grazers, caging experiments, natural disasters-so our un­derstanding of the role of gazing is now fairly well advanced. Grazing affects a number of parameters, including algal zonation, species diversity, patchi­ness, and succession. Before the implementation

of various experimental methods, it was assumed that in the intertidal the upper limits of the domi­nant algal species on rocky shores were a function of the species' ability to tolerate various physical factors. On the other hand, lower limits of algal species distribution seem not to be set by physical factors, because most algae grow faster when ex­perimentally transplanted to lower levels or when they are grown constantly submerged.

Since most algae do grow better when set lower in the intertidal or submerged, why don't we find them there naturally? The answer coming from many researchers is that they are grazed out. For example, in various experiments that have re­moved grazing animals, the result has been the ap­pearance lower on the shore of a number of algae otherwise restricted to higher levels, where graz­ing is less intense. This has been shown by Lubchenco (1978, 1980) to be true for Chondrus in New England, where the main grazer is the urchin Strongylocentrotus droebachiensis. Himmelman and Steele (1971) found the same thing for the alga Alaria esculenta in Great Britain, where S. droebachiensis is also responsi­ble (Figure 6.16).

Grazing may also determine the community structure. For example, Dethier and Duggins (1988) removed the chiton Katharina tunicata from the low intertidal in Washington state, and the site developed from an area with few macro­

scopic scopic plants into a kelp bed dominated by the kelps Hedopbyllum sessile, Alaria marginata, and Nereocystis luetkeana. However, a similar removal of Katharina from a low intertidal area in Alaska did not result in development of a kelp bed, sug­gesting again that it is unwise to generalize from local experiments to broad geographical areas.

Grazing may also set the upper limits of algal distribution. One of the more interesting pieces of evidence supporting this comes from the Torrey Canyon oil spill disaster of 1968. This spill killed the main intertidal molluscan grazers on the shores of southern England. Southward and Southward (1978) documented a subsequent rise in the upper limits of a number of intertidal algae. Following the return of the limpets and other grazing gastropods, the algae were once again grazed down.

The mechanisms by which the removal of graz­ers facilitates the upward or downward extension of algae vary. In the simplest case, the algae are directly limited by the grazer. In other cases, the absence of the grazers may permit a rapid estab­lishment of ephemeral algae, in turn, trapping moisture and permitting the newly settled spore­lings of the dominant algae to survive. In still an­other scenario, the upward extension of algae may be seasonal due to changes in grazing pres­sure. For example, Castenholz (1961) showed that a summer decrease in high intertidal diatom cover was due to a summer increase in Littorina grazing activity in contrast to the less active winter condi­tion. In a more complicated situation, grazing and physical factors interact. Hay (1979) found that in New Zealand the alga Durvillea extended its range upshore in the winter, when grazers were absent, but was cut back in the summer by a com­bination of increased grazing and desiccation at the higher levels.

Surprisingly enough, some of the limits of algae are set by the effect bf the algae themselves on po­tential grazers. In New Zealand, for instance, Underwood and Jernakoff (1981) showed that the downshore extensions of the main gazing limpets, Cellana and Patelloida, are limited by certain algae. In this case the algae settle and grow faster than the limpet grazers can remove them. As a result, the algae form a `substrate that prevents the limpets from attaching, so they cannot enter the area and gaze. Obviously, in this kind of situation there is a continuum. At some level, there is a balance point defining one area where grazers are more efficient at grazing than the algae are at growing, thus elimi­nating the algae. At the other extreme, the algae grow faster and exclude the limpets by creating an unsuitable surface for attachment.

Another consideration in the zonation of algae species is the ability of some algae to grow fast enough to escape grazing by becoming too large for the grazers to feed on. In these cases, the algae will mature only in areas where the grazers are low in density or restricted from grazing during some seasons; thus, the algae can reach a size at which they are immune to grazing.

So far we have considered grazing and its effects on vertical zonation patterns. Grazing may, how­ever, also affect the horizontal patterns of zonation-patterns that have as the dominant phys­ical factor the variation in wave action. The best studied examples come from the Atlantic coast of Europe. Here, the more exposed coastlines have the intertidal dominated by mussels, barnacles, and limpets, whereas the more sheltered shores are covered with dense stands of fucoid brown algae. From various removal experiments and nat­ural experiments, such as the Torrey Canyon oil spill, a conceptual model to explain this has been developed by Southward and Southward (1978). Very simply, this model says that on sheltered shores limpets and other grazers are rare (but see preceding section on New England sheltered shores). This permits the algae to grow and flour­ish. Furthermore, the algal canopy reduces the ability of limpets to settle on the shore. On ex­posed shores, the limpets are abundant and graze out the algae, leaving the shore dominated by mus­sels and barnacles. On the opposite side of the Atlantic, in New England, limpets are rare and the dominant grazer, the snail Littorina littorea, de­creases in abundance in waveswept areas. As a re­sult, the community changes, going from exposed to sheltered conditions, are attributable not to grazing but to physical factors and predation, as noted previously.

We should not leave this issue of grazing with­out discussing a final subject, namely, the defenses of the algae to grazers. We cannot assume that algae are completely without protection from graz­ing. Indeed, they are not. The most obvious adap­tations to grazing are morphological, and one of the most common is the laying down of calcium carbonate in the tissues. Calcium carbonate re­duces the palatability of algae to grazers and makes the grazer exert more energy in feeding. Furthermore, Steneck (1982) has even shown for one coralline alga, Clathromorphum, that the meristem tissue and reproductive sites are all on the underside and protected from grazing. Growth form may also discourage grazing. Hay (1981) has shown, for example, that formation of short turfs in algae reduces grazing mortality. Still other algae, such as the Pacific coast Egregia, have consider­able structural or "woody" tissue when mature; this may deter grazers.

Chemical defenses are also common. Many algae contain noxious or toxic compounds. For ex­ample, on the Pacific coast of North America the genus Desmarestia contains concentrated enough sulfuric acid to erode the calcium carbonate teeth of the grazing urchin Strongylocentrotus fancis­canus. Other algae contain various alkaloids, phe­nolic compounds, and halogenated metabolites.

Finally, there are evolved defenses in the life histories of certain algae. Some algal species are able to exist in at least two growth forms, one a low "crust" and the other an upright frondose form. In areas with heavy grazing pressure, the slow-growing but grazer-resistant crusts predomi­nate, but in areas of low grazing pressure or in areas from which grazers have been excluded, the frondose forms increase. Littler and Littler (1980) have suggested that having these two alternative growth forms in a single species is a strategy of bet hedging. The frondose form has fast growth and high competitive ability but low grazing resistance. The crust form, on the other hand, has slow growth rates and competitive ability but high graz­ing resistance. Another life history feature that may have evolved in algae to cope with grazing is re­production. Many algae, particularly those that are favored by grazers because of their high fraction of digestible material and low fraction of structural tissue, have evolved the opportunistic habit of high reproductive output. This also makes them successful in colonizing newly available space. Quick maturity and high reproductive output mean that these species should be able to colonize an open area and reach maturity quickly before the grazers find and decimate them. Other species have evolved the opposite, or K-selected, features. They are relatively slower growing, perennial, and long-lived. To survive pressure from grazers, these algae either have evolved chemicals that make them unpalatable or grow large enough to be im­mune from grazers. Large size usually also means an enhanced competitive ability, at least for light.

We can conclude this section on grazing by looking briefly at the geographical variation in grazing and its effects on various kinds of commu­nities. Beginning with the temperate zone, grazing is one of the main structuring agents of the rocky intertidal on the Atlantic shores of Europe and the Pacific shores of North America. On the Pacific coast of North America, a large number of species of limpets plus a few species of crabs and sea urchins are responsible for controlling community structure. Fewer grazers, primarily limpets and other snails, exist on the European shore, but they are efficient at structuring the communities. Grazing is less important on the Atlantic coast of North America where limpets are rare and the major grazer, the snail Littorina littorea, seems less efficient than Patella in Europe. Grazing becomes less important as one moves poleward in the Atlantic. In the Southern Hemisphere, the in­tertidal zones of Australia and New Zealand are strongly structured by grazing and also have a high diversity of grazing species. Generally, as one moves toward the equator, the importance of graz­ing increases and so does the variety of grazing or­ganisms. Crabs and fishes become more important as grazers in the tropics. The rocky intertidal in the tropics has been considered relatively barren due to the extremes of the physical factors acting there, but the large number of grazers suggests grazing may be more important (see following sec­tion on tropical shores). Additional work is needed to clarify this situation.

We can summarize the effects of grazing in the three intertidal zones defined by the Stephensons to create a general framework for the North Atlantic Ocean as a model or example of how graz­ing acts. In the supralittoral fringe, grazers are ei­ther uncommon or have little time to graze. The rigorous and stressful physical environment is thus the most important agency causing changes in algal composition. The midlittoral zone is dominated by barnacles and mussels but is strongly influenced by gastropod grazers, primarily limpets, and may vary in algal cover depending on exposure. This, in turn, may limit the numbers of gastropods. Barnacles, however, may also be present due to the ability of limpets and other grazers to keep the competing algae in check. In the sublittoral fringe, the algal growth exceeds the capabilities of the grazers to control it. Therefore, the competition for space and light among the various algae is the dominant inter­action that structures communities at this level. These various factors and their relative importance are summarized in Figure 6.17.

The ability of larvae of various benthic inverte­brates to select areas on which to settle has been known for more than half a century (see Chapter 1). However, the importance of this choice to the eventual structure of intertidal communities has re­mained obscure due to the difficulty of working with larvae under natural conditions. Several stud­ies recently have, however, demonstrated the im­portance of this selection ability. In Australia, the larvae of the barnacle Tesseropora rosea settle only where adults occur; thus, the distribution of adults is not the result of competition with other barnacles outside their range. Moreover, the upper and lower limits on the shore are not set by physi­

cal factors, but by settlement of the larvae.

Furthermore, the barnacle larvae were found by Denley and Underwood (1979) to avoid settling on substrates already occupied by other organisms. A more comprehensive example, also from Australia, includes a second barnacle, Chamaesipho columna. In New South Wales, Underwood and Denley (1984) report that shores protected from wave shock have grazing gastropods as dominants, but where there is moderate wave action, the mid­shore is dominated by Chamaesipho. On the most exposed areas, Tesseropora occupies midtide levels and Chamaesipho the upper reaches. Neither bar­nacle settles into the areas dominated by grazing gastropods, even if the grazers are removed. On ex­posed shores, neither settles into areas occupied by the adults of the other species. In other words, this whole intertidal zonation pattern is structured by the patterns of larval choice and not by predation, competition, or grazing.

Larval recruitment can be variable in time and in space. This variability has been documented, and its importance to the intertidal community structure can be significant. In some years, any given intertidal area may experience poor recruit­ment due to bad combinations of weather, repro­duction by adults, larval mortality in the plankton, such water conditions as wave action, and so forth. The result is few survivors and a de­crease in biological interactions, such as preda­tion, competition, and grazing. In other years, favorable physical conditions may swamp an area with recruits, leading to increased competition or predation and probable changes in the adult pop­ulation and the community. As a result, the same area may have a community that not only differs in composition over time, but may change in rela­tive numbers of individuals. The importance of competition, predation, and grazing in determin­ing the structure of the community will also, therefore, change.

Gaines and Roughgarden (1987) have demon­strated another significant factor that can lead to variation in larval recruitment. They were able to show that the juvenile rockfish that inhabit the kelp forest immediately offshore of the intertidal zone in central California are significant predators of the larvae of the intertidal barnacles. The fish are capable of reducing the number of recruits to 1/50 of the number that would settle in the ab­sence of the fish. The number of barnacle larvae that actually make it across the kelp bed depends on the stock of rockfish, which, in turn, is a func­tion of the extent of the kelp forest. Whenever the kelp forest is decreased, as in El Nino years, the rockfish also decrease, which leads to good barna­cle recruitment and vice versa. In this scenario, the dynamics of the intertidal communities are directly coupled to another community, namely, the kelp forest (see Chapter 5 for factors influencing kelp forest dynamics).

This great spatial and temporal fluctuation in the settlement of larvae of the dominant intertidal organisms means that the importance of competi­tion, predation, and grazing are likely to be vari­able. It is difficult to generalize about the effects of competition, predation, and grazing if the num­bers of prey or potential competitors are also un­predictable. Although it is considered by some to

be a "nuisance" in the setting up of experiments, this irregularity of appearance of various dominant intertidal invertebrates is a fact of nature and must be considered in any attempt to understand the structuring process in the intertidal zone. In other words, the irregular occurrence in a community of a numerically important, competitively dominant, or keystone predator should lead to a variety of dif­ferent outcomes from experimental studies done in the area because of variations in the intensity of biological interactions resulting from the larval re­cruitment patterns.

In an attempt to sort out the relative impor­tance of competition, predation, and larval recruit­ment to the structure of rocky intertidal communities, Menge (1991) undertook a multiple regression analysis of these factors for New England and Panama shores. The results' indicated that recruitment in New England explained 11% and predation and competition 50-78% of the structure, whereas in Panama recruitment ex­plained 39-87% and predation and competition only 8-10% of the structure. If these figures hold true for other areas, this may indicate a fundamen­tal difference in the structuring forces in temper­ate and tropical intertidal areas.

Tide pools

A characteristic feature of many rocky shores is the presence of tide pools of various sizes, depths, and locations. Certain conditions affecting life of tide pools differ markedly from the surrounding inter­tidal and necessitate a separate discussion here. Our remarks in this section will be restricted to those pools that undergo a complete interchange with the ocean water during the tidal cycle (Figure 6.24). It should be pointed out at this juncture that the biotic communities of tide pools and the fac­tors influencing their structure are less well under­stood and studied than those of the emergent rocky surfaces. It has even been suggested that tide pools do not represent an intertidal habitat be­cause they are never exposed to the air during a tidal cycle. However, the fluctuations in physical and chemical factors in tide pools are a function of the tidal cycle; hence, it seems logical to consider them in this chapter. Furthermore, many of the or­ganisms found in tidal pools are similar to those found on the adjacent exposed rock.

At first glance, tide pools appear more or less ideal places for aquatic organisms seeking to es­cape the harshness of the intertidal during its ex­posure to air. In reality, however, escape from such physical factors as desiccation may mean exposure to others that operate more severely in tide pools. 

Tide pools vary a great deal in size and in the volume of water they contain. Since water is a great moderator of harsh physical conditions, the larger the pool and the greater the water volume, the less the fluctuations in physical factors. Other factors in addition to volume influence the physical and chemical conditions of the water held in a tide pool. These include the surface area, depth of the pool, height in the intertidal, exposure to wave ac­tion and subsequent splash, degree of shading, and drainage pattern. In addition, the physical and chemical environment of tide pools can vary verti­cally with depth and horizontally across the pool. Finally, all physical factors may fluctuate diurnally and seasonally. Given all these variables, Metaxas and Scheibling (1993) suggest that it is unlikely that any two tide pools will be similar in all characteris­tics; therefore, individual pools are unique physi­cally. If this is true, it means ecologists cannot replicate experimental manipulations in different tide pools and may be a significant reason why there has been so little experimental ecological work done on pools. It may also be the reason why most studies have been primarily descriptive.

Three major physical factors are subject to vari­ation in tide pools. The first is temperature. Whereas the ocean itself is a vast reservoir that heats and cools very slowly and usually within very narrow limits, the same is not true of tide pools. These relatively small bodies of water are subject to more rapid changes. Shallow tide pools exposed to the sun on warm days may quickly reach lethal or near lethal temperatures. Similarly, tide pools in cold temperate or subpolar regions may have temperatures in the freezing range in winter. An additional problem is temperature fldc­tuation. The pool may either heat up or cool down over a several-hour period while exposed to the air, but when the tide returns, it will be flooded with ocean water. This will suddenly change the temperature of the whole pool. Variations in daily temperature in a tide pool can be as much as 15°C, depending on its height in the intertidal, volume, degree of shading, and wave exposure. Finally, change in temperature dur­ing exposure at low tide may cause temporary thermal stratification of the pool. Organisms in­habiting such pools must still be adapted to con­siderable temperature fluctuation.

The second factor to vary in pools is salinity. During exposure at low tide, tide pools may heat up, and evaporation occurs, increasing salinity. Under hot tropical conditions, the salinity increase can be dramatic enough to reach the point of pre­cipitating out salt. The opposite situation is the case when heavy rains occur at low tide and flood

pools with fresh water, dramatically lowering the salinity. Fluctuations in salinity in tidal pools vary with the position of the pool on the shore and the other factors mentioned, but values that have been measured have ranged between 5-25 psu. Salinity stratification also may develop in the pool due to fresh water runoff during heavy rains or as a result of freezing in winter and evaporation in summer. Again, tide pool animals and plants may have to be adapted to wider ranges in salinity than typical ma­rine or intertidal organisms. As before, when the tide returns, the pool will be flooded with seawa­ter at some point, and there will be an abrupt re­turn to normal conditions.

The final physical factor undergoing change in pools is oxygen concentration. Since the amount of oxygen that can be held in seawater is a function of temperature, it follows that tide pools that heat up during exposure to the air will lose oxygen. Under normal conditions, this may not be serious enough to produce oxygen stress, but if the pool is crowded with organisms, it may produce a stress situation. For example, a pool filled with algae that was exposed at night would produce a situation in which the lack of photosynthesis coupled with high respiration could reduce the oxygen level sig­nificantly. Oxygen level has been recorded falling to only 18% of saturation in tropical tide pools. It is also possible to develop an oxygen stratification in the water column of certain pools.

Tide pools are areas of refuge from desiccation for intertidal organisms, but in turn, these organ­isms suffer from rapid changes in temperature, salinity, and occasionally oxygen; thus, the fauna and flora is restricted to those organisms able to tolerate such ranges.

The organisms that inhabit tide pools are similar to those on the adjacent emergent substrates but often with differences in abundances between the pools and exposed surfaces. For example, several genera of algae, such as Spongomorpha and Corallina in the intertidal of Maine, Prionitis in Washington, and Fucus in Nova Scotia, are more abundant in pools. Other species are either absent or occur in lower numbers in pools than on ex­posed surfaces. An example is the alga Asco­pbyllum nodosum in New England. Finally, the oc­currence of tide pools permits some organisms to extend their range upward in the intertidal beyond the levels to which they would be limited on the adjacent emergent surface. This is true for a great many algae and invertebrates and is particularly true for many fishes.

Zonation patterns have been described for tide pool organisms both within the intertidal zone and vertically within the tide pools. Along the inter­tidal gradient such green algae as the genera

Enteromorpha, Cladophora, and Chaetomorpha,

dominate the upper tide pools, while such brown algae as Fucus and Laminaria, and the red corallines, such as Lithothamnion and Corallina, are abundant in the lower intertidal pools. Benthic invertebrates also show a zonation. High pools are inhabited by littorine snails, whereas low tide pools have a greater diversity of snails and all in­vertebrates. Fish zonation in tide pools has not been quantitatively documented according to Metaxas and Scheibling (1993), but qualitatively, there is a decrease in the number of species with increasing height of the pool. In general, both in number of species and biomass, high tide pools are depauperate compared with lower level pools.

The role of biological interactions in determin­ing the community structure of tide pools is poorly documented when compared to the studies for the exposed rocky intertidal. This is due not only to a relative lack of studies, but also to the variability among adjacent tide pools at the same intertidal level when subjected to experimental manipula­tion. Such variability has precluded obtaining sta­tistically significant results in many cases, although correlative data often indicate a trend. We discuss some of these data here.

Herbivory has similar effects in tide pools to those recorded for the emergent rock surfaces, namely, the altering of macroalgae abundance. For example, Paine and Vadas (1969) demonstrated that the removal of sea urchin grazers from tide pools in Washington resulted in increases in macroalgae. Similarly when Lubchenco (1978) added littorine snails to a pool, the density of the dominant alga Enteromorpha was reduced, whereas when she removed littorines from a pool dominated by the alga Chondrus crispus, the den­sity of Chondrus decreased. In Nova Scotia, Chapman and Johnson (1990) found that littorinid snails had a negative effect on the abundance of several species of the brown algal genus Fucus, a positive effect on the ephemeral algae, and no ef­fect on the crustose alga Hildenbrandia.

Very few studies have investigated the role of predation in structuring tide pool communities. Indeed, there seem to be no well-documented ma­nipulative studies. The few studies that have been done suggest that addition of predators to pools re­duces the abundances of various prey organisms, but whether or not the predator exerts control of the community structure is uncertain.

The evidence for the importance of interspe­cific competition in regulating community struc­ture in tide pools is also sparse. Lubchenco (1982) and Chapman (1990) have both demonstrated de­creases in canopy cover in Fucus due to competi­tion with ephemeral algae. Kooistra et al. (1989) have shown competitive dominance as indicated by overgrowth for the alga Halichondria panicea in tide pools in Brittany, France.

Although recruitment can be a significant fac­tor in structuring tide pool communities, no studies have considered this factor directly. Similarly, there is little or no information about the role of disturbances, particularly large-scale episodic events, in the structuring of tide pool communities.



Marine Science              Name___________Pd___

Rocky Shores Reading                          Part 1


  1. How do rocky shores compare with sand and mud shores?


  1. What types of animals dominant the intertidal rocks?


  1. What types of animals dominant the subtidal rocks?



  1. What is the most striking feature of any rocky shore?



  1. How is one zone different from another?



  1. Compare and contrast rocky shores with mountains?



  1. What are 3 ways rocky intertidal zones vary?




  1. What conditions may alter the bands or zones?



  1. In the Stephenson’s scheme, there are three main divisions. What are they?



10 Describe each zone discussed in question 9



Physical Factors-that cause zonation


11      What does desiccation mean?



12     What does critical tide levels mean?



13     Why is the “critical tide hypothesis” difficult to prove or disprove?



14     Why is there height difference among the same organisms that grow on north-facing slopes as opposed to south-facing slopes?



15     What  is the single determinant factor of the upper limits of organisms in the intertidal zone?