Experimental Investigations of Disturbance and Ecological Succession in a Rocky Intertidal Algal Community
Abstract
The study investigates mechanisms of ecological succession in a rocky intertidal algal community via field experiments in southern California.
The study site is an algal-dominated boulder field in the low intertidal zone.
The major natural disturbance is the overturning of boulders by wave action, which clears space.
Algal populations recolonize cleared surfaces through vegetative regrowth or spore recruitment.
Experimentally cleared boulders and concrete blocks are initially colonized by a mat of the green alga, Ulva.
Perennial red algae, such as Gelidium coulteri, Gigartina leptorhynchos, Rhodoglossum affine, and Gigartina canaliculata, colonize the surface in the fall and winter after clearing.
Without further disturbance, Gigartina canaliculata gradually dominates, holding 60-90% of the cover after 2-3 years, persisting through vegetative reproduction and resisting invasion by other species.
Diversity increases initially but declines as one species monopolizes space.
The study found that Ulva inhibits the recruitment of perennial red algae by competing for settling space, a key feature of succession.
Ulva is a superior competitor for space, reproducing year-round and quickly establishing on cleared substrates, preempting colonization by perennial red algae with seasonal recruitment and slower growth.
Selective grazing on Ulva by the crab, Pachygrapsus crassipes, breaks this inhibition, accelerating succession to a red algae community.
Grazing by small molluscs, particularly limpets, has no long-term effect but temporarily enhances barnacle recruitment by clearing space in the algal sporeling and diatom mat.
Middle successional red algae also slow the invasion and growth of the late successional dominant, Gigartina canaliculata, which replaces them due to greater resistance to desiccation and epiphyte overgrowth.
The study's results do not support the classical facilitation or tolerance models of succession.
Early colonists resist rather than facilitate later colonists' invasion.
Early colonists are not killed by direct interference competition with late successional species; instead, they inhibit their recruitment and growth.
Successional sequences occur because early species are more susceptible to environmental rigors and natural enemies compared to late species.
Late species colonize and mature when early species die and open space. Direct competition with surrounding adult plants of late successional species only contributes to the decline of remaining early species late in succession.
Studies in other communities support this inhibition model.
Key words: algae, community structure, competition, desiccation, disturbance, diversity, dominance, epiphytes, grazing, rocky intertidal, succession.
Introduction
The study of temporal changes in community structure began with North American plant ecologists in the early 20th century (Cowles 1899, Cooper 1913, Clements 1916).
Clements (1916) viewed community development as an emergent property analogous to an organism's embryological development.
With exceptions (Gleason 1926, 1927, Egler 1954), his view was widely accepted, leading to succession being seen as a closed-system deterministic process (Drury and Nisbet 1973).
This resulted in generalizations about successional trends and mechanisms (Odum 1969) based on a tenuous homology between spatial vegetation zones and long-term vegetation sequences on a single site (Gleason 1927, pp. 320-324).
Little evidence supports these generalizations, especially when succession is viewed in the context of individual species' life histories (Drury and Nisbet 1973, Horn 1974, Connell and Slatyer 1977).
Many mechanisms proposed to explain changes in ecological communities after a disturbance remain untested.
Most succession research has been in terrestrial communities, mainly forests and abandoned old-fields, where only the earliest stages are amenable to experimentation.
Later successional stages and mechanisms are not directly observed because later-appearing species persist longer than any ecological study.
Recently, tests of successional theory have been conducted in communities where succession is relatively short, like the marine rocky intertidal (Dayton 1971, 1975, Menge 1975, Lubchenco and Menge 1978).
This paper is the first of two (Sousa 1979) on the dynamics of algal-dominated communities in marine intertidal boulder fields.
Sessile species arepatchily distributed in successional states. Each boulder's top surface is a habitat patch varying in size and age.
Together, they form a mosaic analogous to the patch structure of intertidal mussel beds modeled by Levin and Paine (1974).
Small boulders are more susceptible to wave disturbance than larger ones, renewing space in a space-limited system.
Boulder fields are excellent systems to experimentally investigate species interactions in both undisturbed patches and the role of disturbance in maintaining diversity.
Most algal succession studies on denuded surfaces in the rocky intertidal reveal common recolonization features.
Algal species that arrive first on a large opened space do so because of evolved life history characteristics:
Propagules are produced in large numbers during most seasons.
High vagility.
Rapid growth to maturity.
Relatively short-lived populations.
The cosmopolitan "weedy" species of the seashore include members of the green algal genera, U/ca and Enterolnorplia.
These species possess flagellated motile spores and are usually the first algal colonists (after an initial cover of colonial diatoms) to colonize denuded surfaces in the marine rocky intertidal (Haton 1938, Rees 1940, Northcraft 1948, Castenholz 1961, Menge 1975, and others).
These pioneer species settle densely and grow quickly, securing most of the available canopy space.
Sometime later, large perennial brown or red algae, which tend to have larger and less motile spores, become established, replacing the earlier colonists.
Reproduction and recruitment in these perennial species is usually more seasonal than in the green algae.
This group is composed of both the species which will eventually come to dominate the space as well as others which will not persist in the climax community in the absence of disturbance.
The paper presents data on algal recolonization patterns following a disturbance and experimental investigations of the mechanisms that drive these successional changes.
A companion paper (Sousa 1979) presents correlative data and experimental corroboration of the role of disturbance in maintaining diversity in this system.
Study Site
Intertidal boulder fields comprise much of the rocky shore of southern California.
They often occur near points where rocks have been deposited at the mouths of creek beds.
The study site was established in one of these areas at Ellwood Beach, California (34^025'N, 119^041'W) located within the Santa Barbara Channel approximately 9 km west of the University of California, Santa Barbara (Fig. 1).
Sandstone boulders overlie a gently sloping shale platform which extends into the low intertidal zone (from -0.30 m to +0.30 m above mean lower low water, hereafter MLLW).
This habitat is bordered on the landward side by a sand beach and on the other sides, at lower tidal levels, by beds of the surf grass, Phyllospadix torreyi, in sand areas and patches of the brown alga, Egregia laevigata, on rock substrates.
After large winter rainstorms, freshwater runoff from a nearby intermittent stream flows across the beach and out into the rocky intertidal to the east of the main study area.
Though the latter area appeared unaffected, the density of grazers, particularly of sea urchins and crabs, was much reduced in an adjacent boulder field, presumably a result of these periodic inundations.
There was no observable difference in the algal species composition in these two areas.
Wave exposure and disturbance of boulders
Ellwood is protected from the effects of large summer swells by the Channel Islands located approximately 35-40 km offshore.
Little boulder movement occurs here during summer months (May through October).
Winter storms (November through April) out of the northwest frequently produce mid-channel wind waves in excess of 2.4 m in height or swells greater than 1.5 m in height which overturn many boulders (Sousa 1979).
When a boulder is overturned, the algae and sessile invertebrates on its top surface are killed in whole or part by a combination of sea urchin grazing (if urchins are present), anoxia, light levels below compensation intensity, and mechanical damage caused by abrasion.
The length of time that a boulder remains overturned determines the intensity of disturbance and thus the amount of space renewed.
If this time is relatively short, the residents may simply be damaged, and open space is recolonized primarily by vegetative regrowth of surviving individuals.
At the opposite extreme, if boulders remain overturned a long time, all the algae may be killed and recolonization accomplished completely by propagules from the outside.
Tidal exposure and desiccation stress
Climatological stress is highly seasonal because most winter low tides at or below 0.0 m MLLW occur in the late morning and afternoon between the months of October and March.
The actual number of hours of exposure is sometimes reduced when high seas are generated by storm conditions but this does not substantially change the general pattern of daytime exposure to air during winter months.
Strong winds and intense sunlight often coincide with late morning and afternoon low tides causing severe desiccation and death of both plants and animals.
In the early winter (October-January) several red algal species, including important canopy species in this zone, are defoliated by a combination of this desiccation stress and simultaneous attack by large numbers of the small herbivorous snail, Lacuna unifasciata (W. P. Sousa, personal observation).
The effect of Lacuna will be described in more detail later.
As a consequence, during winter months, algal abundances are reduced and free primary space (i.e., space not covered by the algal canopy) increases.
Populations of most herbivores are also reduced during winter months.
Most summer (April-September) low tides at or below 0.0 m MLLW occur in the early morning and during the night when physical conditions are benign.
Algal growth is most rapid and herbivores most abundant during this period.
Algae which defoliated during the winter regrow from a low tuft of short branches or a perennating holdfast in the spring.
Available free space is less than during winter months.
Data on these trends will be presented later.
Animal and plant communities
The area of the boulder field between 0.0 and +0.30 m above MLLW (approximately 1500 m^2) is covered by an algal association dominated by the red alga, Gigartina canaliculata, on stable substrates (Table 1).
This association contains about 30 species of macro-algae but this study was limited to those which comprised at least 5% of the cover on the substrates sampled.
Smaller (less stable) boulders contain various mixtures of Gigartina canaliculata, Gigartina leptorhynchos, Gelidium coulteri, Rhodoglossum affine, Ulva spp., Centroceros clavulatum, Corallina 'ancou'eriensis, and the barnacle, Chthamallis fissius.
During benign summer months, Laurencia pacifica and Gastroclonium coulteri may also be present.
The anemone, Anthopleura elegantissimna, never covered more than 5% of the space on boulders in this habitat and was not studied in any detail.
The mussel, Mytilus californianus, is the potential competitive dominant at this level (Paine 1974). However, it is absent from this site due presumably to intense predation by octopuses, starfishes, and predatory snails.
At or below 0.0 m MLLW, this algal association grades into one which is dominated by the red algal species, Gastroclonium coulteri and Laurencia pacifica (Table 1).
This zone is not extensive in area, ending abruptly at the lower edge of the boulder habitat (approximately -0.45 m below MLLW) where a bench of soft shale sparsely covered with encrusting coralline algae, Phyllospadix torreyi and Egregia laevigata extends into the subtidal.
Hereafter, sessile species will be referred to by their generic names, except for the two species of Gigartina for which both genus and species names will be used.
Large herbivores present in the Ellwood boulder field include the sea urchin, Strongylocentrotus purpuratus, the sea hare, Aplysia californica, the lined shore crab, Pachygrapsius crassipes, and several species of fish including the adult opaleye, Girella nigricans, the monkey-face eel, Cebidichthvs viola ceus, and the top smelt, Atherinops affinis.
Small grazers include the limpets, Notoacneca fenestrata, Collisella strigatella, and Collisella scabra, the chiton, Mopalia inuscosa, the volcano limpet, Fissurella volcano, hermit crabs, Pa gurus spp., and the snail, Lacuna uni- Jatsci(lta.
Juveniles of the herbivorous snail, Tegula fienebralis, recruit to this zone but are completely eliminated by predators (Fawcett 1979).
Densities of the more abundant of these herbivores were sampled cooperatively with M. Fawcett and S. Schroeter, whose studies on populations of herbivores at the Ellwood site coincided with this study of the algal community (Fawcett 1979).
A uniform grid (25 x 60 m in area) of 28 permanently marked 0.25-M2 quadrats was established across the boulder field.
The quadrats were sampled for limpets and chitons in January 1975, May 1975, November 1975, and January 1976.
The number of sea urchins in the same quadrats was counted on the January 1975 and May 1975 dates.
Accurate estimates of the densities of the crab, Pach- vgrapsuls cr(lssipes, are difficult to make.
Crude estimates which undoubtedly underestimate their abundance were obtained by carefully searching randomly laid 1-M2 quadrats in August 1976 (four quadrats) and January 1977 (15 quadrats).
Sea hares, mostly Aplysia californica, in the 1500-rM2 grid area were periodically counted between April 1975 and February 1977.
Only a single pair of mating Aplysia vaccaria was observed in August 1975.
The abundance of all these grazers except for sea urchins and sea hares (Table 2) was greatest at the spring and summer sampling dates.
Sea urchin densities were nearly identical in the two sea- sons in which they were sampled.
The abundance of sea hares fluctuated erratically with no clear seasonal trends.
The greatest number of sea hares was recorded in April 1975 while the number in April 1976 was one of the lowest of that year.
Mating in these hermaph- rodites began in May of each year and egg masses laid on algae were found between May and December.
Small juveniles (2-5 cm long) were very rare until the winter and spring of 1977 when a large number could be located with relatively little searching effort.
The snail, Lacuna unifasciata, was not sampled quantitatively.
Snails laying egg masses on Gigartina canli(ulata in May and June of 1975 and 1976 were observed.
Their populations became very dense between September and December of each year, inflicting heavy grazing damage to most of the algal species I studied.
This damage does not kill perennials, which regrow the following spring.
The snails graze small holes in the thallus; the weakened branches are torn off and carried away by waves.
Shortly after winter defoliation, the snails largely disappeared.
General Methods
Settling surfaces
One method of documenting seasonal recolonization patterns of denuded boulders is to overturn many boulders at different times of the year and monitor subsequent colonization.
This approach has two drawbacks:
It would be extremely destructive to the habitat.
It was difficult to find a sufficient number of boulders similar enough in size, surface texture, and composition to act as true replicates.
To satisfy these latter requirements, 165-cm2 concrete blocks were used as settling surfaces.
Though some previous workers (MacGinitie and MacGinitie 1968, p. 91) have warned of the potentially lethal nature of chemicals which leach from concrete, no evidence of this was observed during the study.
As will be seen later, the successional patterns observed on concrete blocks did not differ in any obvious way from those which occur on natural boulder surfaces.
Most experiments using the surface of natural boulders were conducted in 100-cm2 clearings in beds of algae.
These plots were cleared by removing as much algae as possible with a putty knife, then burning off the remainder with a propane torch.
Subsequent observations revealed no vegetative regrowth of algae within the plots, indicating that the burning had been effective.
The corners of all plots were marked with stainless steel screws or Sea-Goin Epoxy Putty (Permalite Plastics Corporation, Newport Beach, California 92668).
Estimaution oJ'percent co01er and numbers of plants
The percent cover of a sessile species is a measure of its relative abundance and use of space.
Two methods were used to estimate cover.
Concrete blocks and experimental plots on boulders were photographed periodically and the percentage covers of each macro-algal species and of the barnacle, Chthamnalus, were estimated by a point sampling technique using 100 uniformly positioned points superimposed on the projected image.
The number of points which hit each species is an estimate of its cover.
A systematic sampling design often gives an estimate of percentage cover which has a smaller variance than if a random pattern were used (Greig-Smith 1964, Snedecor and Cochran 1967).
It does, however, have two potential disadvantages:
If there is some periodic variation in the spatial pattern of the cover being estimated which matches that of the sample spacing, then bias will be introduced. No pattern in the algal canopy which was likely to induce bias in this manner was observed.
There is no reliable way of estimating the standard error of the mean of a sys- tematic sample, although in most cases it will be small- er than that for a random sample. Approximate values were calculated by applying the usual formula for the standard error of a random sample to the cover esti- mates obtained with the uniform grid of points.
The positioning of the points over the projected image was shifted haphazardly each time a slide was analyzed to reduce any potential serial correlations in the data from successive sampling dates.
When inclement weather or a dense overlying canopy precluded photography of the cleared plots or concrete blocks, the percent cover was estimated vi- sually in the field with the aid of plexiglass quadrats subdivided into 100 squares.
By simultaneously using both techniques on the same sampling date it was found that the two estimates differed by less than 5%.
Dayton (1971, 1975) using similar methods reported the same precision in his visual estimates of percent cov- er.
All statistical comparisons of percent cover data were performed on values normalized with an arcsine transformation (Sokal and Rohlf 1969).
Since plants of the species studied often have many basal branches making it difficult to enumerate indi- viduals, I counted distinct holdfasts as separate plants.
This method probably underestimates the actual num- ber of individuals as adjacent holdfasts may fuse into one.
There is no bias between treatments in this re- spect as all were conducted in 100-cm2 areas over the same period of time.
Manipulations oJ (lge(
To study interactions between different species of algae, a number of selective removals were performed.
Plants were removed from the experimental plots using forceps or a scalpel.
Because of rapid recruitment of some species and/or regrowth of plants from por- tions of surviving holdfasts, removals had to be re- peated on each sampling date.
When plants had to be marked individually, color-coded, numbered Brady Wire Markers were cemented to the dried rock surface near the holdfast of each plant with Loctite 404 epoxy adhesive (Loctite Corporation, Newington, Connecticut 0611 1).
Algal sporelings were experimentally transplanted algal sporelings by chipping off small pieces of rock to which they were attached and cementing these chips to the surface of other boulders with Sea-Goin Epoxy Putty.
Manipulations of grazers
To assess the effects of grazing on patterns of algal succession, the densities of herbivores were experimentally manipulated.
Grazing by the limpets, Notoactnea fe- nestra ta, Collise/la striga tella, and Collisella scabra, was prevented using a technique devised by Cubit (1974).
A 3-cm-wide ring of copper paint was applied to four sides of each concrete block from which lim- pets were to be excluded. Limpets do not cross the barrier because of the toxic and/or electrolytic prop- erties of the copper.
In addition, strips of copper were painted on two sides of a second group of blocks to which limpets were allowed access.
This partial ap- plication was intended to serve as a control for any influence the presence of copper ions might have on the recruitment or growth of algae.
See Cubit (1974) for details concerning the components of the paint mixture.
The effects of larger grazers were studied by using cages.
Cages were used either to exclude herbivores and thus prevent their grazing on experimental plots, or to enclose them and thus ensure that the plots were grazed.
To control for the effects of shading by the cage roofs, cages with openings in the sides allowing access to all grazers were constructed.
Possible cage effects will be discussed later.
The cages were 0.6 m on a side and 0.45 m high. They were constructed of 1.25- cm-wide Vexar mesh (DuPont Corporation) wired to a 5 x 10 cm mesh vinyl-coated hardware cloth frame with stainless steel wire.
Cages were secured in place and supported by 1.25-cm-diameter reinforcing bars driven into the soft shale platform underlying the boul- der field at Ellwood.
Patterns of Recolonization following a Disturbance
Disturbances in boulder fields create openings which vary in size from small holes in the algal canopy to entire surfaces of boulders being wholly or partially cleared.
Recolonization usually begins soon after space is cleared.
The resultant patterns and mecha- nisms of change in species composition depend in part on the size of the initial clearing and whether adult plants surround the opening or not.
Recolonization of large clearings
When a boulder remains overturned for a long period of time (i.e., more than 2 mo), all of the sessile organisms on what used to be its upper surface are killed.
When the boulder is reflipped and stabilized, the entire surface is bare and recolonization begins.
The seasonal recruitment patterns of algae and sessile invertebrates were documented and the species interactions which influence the sequence of coloniza- tion on bare surfaces were examined by establishing a series of concrete blocks in the Ellwood boulder field at approximately +0.15 m above MLLW tidal level.
Replicated sets of concrete blocks were placed in the intertidal on 16 September 1974, 15 January 1975, and 31 May 1975.
While all sets began with six replicate blocks, some were lost or damaged during winter storms, reducing the minimum number of replicates to four at later sampling dates.
The percentage covers of all sessile species which averaged at least 5% cover on a set of blocks are plot- ted in Fig. 2.
These plots are for unmanipulated blocks set out on the September 1974, January 1975, and May 1975 dates, respectively.
Though a cover of diatoms dominated by Navicula spp. and Lici-nophora spp. usually developed first on a block or cleared boulder, this phenomenon was not studied in any detail.
In each set of blocks, the green alga, Ulva, recruited and grew to dominate soon after the blocks were es- tablished.
On the September blocks, the cover of Ulva declined during the physically harsh months of Janu- ary through May 1975 when the lowest tides occurred in the afternoon.
Surviving Ulva plants form a 1-cm- high turf during harsh winter months while the same thalli can grow to be 20 cm long during the summer.
As tides shifted to night and early morning hours in the summer, and physical conditions became more benign, U/va rerecruited and grew rapidly, holding 50% of the cover on the September blocks in August 1975.
This cover gradually declined again until Ulva had essentially disappeared from these blocks by Oc- tober 1976.
By this time, four species of perennial red algae had recruited and grown to cover most of the space on the blocks.
Ulva dominated the January blocks during the early summer of 1975 (June-August) but declined to about 15% cover by March 1976.
It then underwent a second increase in abundance be- tween June and August 1976 and disappeared by the late fall, 1976.
There was no corresponding increase in Ulva on the September blocks, indicating that the canopy of red algae probably interfered with the re- cruitment and growth of Ulva.
U/va covered nearly 90% of the space on the May blocks between August 1975 and January 1976.
It declined somewhat in the winter of 1975-76 and disappeared during the late fall of 1976.
On the September and January blocks, the barnacle, Chthalnalu/s, held approximately 35% and 50% of the space, respectively, during the winter months of 1974- 75.
These barnacles settled into small openings in the cover of Ulva and diatoms created by the grazing ac- tivities of limpets.
This effect of limpet grazing will be discussed in greater detail later.
By August 1975, the cover of barnacles had disappeared from both block sets.
Only the empty tests of dead barnacles remained.
Barnacles did not recruit to the May blocks during 1975 and held less than 10% of the space on those blocks in March of the winter of 1976.
During the fall and early winter months of 1974-75 four species of perennial red algae, Gigartina canali- culata, Gigartina leptorhynchos, Gelidiumn, and Rho- doglossuin recruited to the September blocks.
Their settlement is far more restricted seasonally than that of either Chthainalus or Ulva. Settlement occurs in the fall and early winter when space is available for colonization due to the defoliation of the algal canopy.
Blocks exposed for settlement in January and May 1975 were not colonized by any of these red algae during the late winter of 1975.
Not until the fall and early winter of 1975-76 did these species recruit to the January and May blocks.
By February 1977, these four species had grown to comprise most of the algal cover on these blocks, but strong dominance by any one species had not developed by the time the study was ended.
Strong dominance by G. canaliculata did develop slowly on the unmanipulated September blocks.
The G. canaliculata canopy increased in cover during the benign summer months when the thalli grew rapidly but declined in the harsh winter months (February through April of 1975 and 1976) when its branches defoliated.
There was almost no decline in the cover of this plant, however, in the fall and winter of 1976- 77 as it had by that time secured 55% of the primary space on the blocks.
Though the recruitment of this species to the blocks was predominantly from spores, I did see several instances in which branches from plants on neighboring boulders became attached at their distal ends to the sides of a concrete block.
These branches became detached from their parent plants and developed into new individuals.
This form of colonization may be relatively common under natural conditions.
It should be noted that a crustose Petrocelis stage has not been identified for any of the red algal species in this study; all have erect tetrasporic plants (West 1972, W. P. Sousa, personal observa- tion).
The three other species of perennial red algae which recruited to the September blocks in the fall and winter of 1974-75 underwent seasonal fluctuations in abun- dance throughout the 2^1/_2 yr study, eventually de- clining to less than an average of 10% cover by Feb- ruary 1977.
After recruiting to the September blocks in the fall-winter 1974-75, G. leptorhynchos increased slightly to more than 10% cover by August 1975.
It then declined in cover to near zero in late October 1975, but rerecruited in the winter of 1976.
These plants grew to cover nearly 40% of the space on the September blocks in April 1976.
This cover declined again throughout the summer of 1976, remaining near 10% cover into February of the 1977 settlement season when strong dominance by G. canaliculata was de- veloping.
Gelidiumn showed seasonal fluctuations in abundance which differed somewhat from those of G. leptorhynchos.
Gelidiumn covered nearly 10% of the space on the September blocks by October 1975.
By March 1976, most of this cover had disappeared but the growth of surviving and newly recruited plants during the next summer resulted in an average of 20% cover of Gelidium in October 1976.
Once again this cover declined dramatically to about 5% by February 1977 as G. canaliculata dominated the surfaces of the blocks.
The seasonal decline in abundance of G. lep- torhynchos and Gelidium coincided with their over- growth by various species of epiphytes.
This phenom- enon will be discussed in detail later.
Rhodoglossum never increased above an average of 10% cover throughout the study and I could not detect any marked consistent fluctuation in its abundance.
In summary, shortly after a block is established in the low intertidal it is colonized (independent of sea- son) and dominated by the early successional species, U/ea.
The barnacle, Chtharnalus, may also be abun- dant, depending upon what season the block is estab- lished and whether limpets are present.
These early species gradually disappear from the blocks after undergoing several seasonal pulses in recruitment and growth.
In the first fall and winter, the block is colo- nized by four species of perennial red algae, three of which fluctuate in abundance seasonally, reaching their peak abundances in the middle of the succes- sional sequence (hereafter referred to as middle successional species), while the fourth, Gigartina ca- naliculata (late successional species), gradually in- creases in cover and dominates, holding 55% of the space after 30 mo.
Recolonization of' small clearings
Small bare patches in a bed of the dominant algal species, Gigartina canaliculata, are sometimes cleared when a loose rock is lifted by waves and strikes the surface of a larger, more stable boulder.
Small open- ings may also be created when a large boulder over- turns for a short period of time so that when it is re- flipped, most of the canopy recovers vegetatively except for small areas where intense urchin grazing or abrasion occurred.
Late in a successional sequence, large clearings become a mosaic of small openings. Some are filled with early or middle successional species, others are bare, and all are surrounded by adults of the late successional alga.
The successional processes which occur in small openings in a canopy of adult plants are qualitatively different from those which operate when a completely denuded boulder is recolonized.
In small openings, the canopy of surrounding plants grows long and covers the cleared patch during summer months.
In the winter the surrounding plants defoliate, opening the patch to sunlight and colonization.
In addition to colonization from planktonic propagules, vegetative reproduction occurs.
Adult plants of Gigartina canaliculata have the capacity to spread vegetatively across the rock surface by rhizoid-like basal branches that can attach to the surface at their distal ends and then sprout branches at the point of contact, creating an entirely new plant.
In this way, surrounding plants slowly en- croach into and eventually fill the opening.
To study the dynamics of colonization within small openings, a number of 100-cm2 plots were cleared in solid beds of G. canaliculata on a group of large stable boulders in February 1975.
To examine mainly plant- plant interactions, all small molluscan grazers, includ- ing limpets and chitons, were removed at each sam- pling date from all plots.
Patterns of recolonization of small clearings in beds of Gigartina canaliculata are shown in Fig. 3.
An im- portant feature of small clearings is the fluctuating can- opy of surrounding G. canaliculata plants, which dur- ing the summer months of 1975 and 1976 covered nearly 100% of the space in the plots.
UOva recruited to the plots in March 1975 shortly after clearing.
Its abundance remained low, an average of approximately 10% cover, until January 1976 when the G. canali- culata canopy defoliated, opening the plots to the light.
Subsequent recolonization and growth of newly recruited and surviving U/va plants caused its cover to increase to 30-40% in the plots.
This cover of U/va gradually disappeared by November 1976 as the can- opy of G. canaliculata redeveloped.
The middle successional red alga, G. leptorhynchos, recruited into the plots in the fall and winter of 1975-76, but never comprised more than 10% cover throughout the study.
For unknown reasons, recruitment of Gelidiuln, Rho- doglossuin, and of the barnacle, Chtharnalus, to these plots was very low and none of these species reached an