perturbation and recovery patterns of starfish-dominated intertidal assemblages in chile, new...

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Perturbation and Recovery Patterns of Starfish-Dominated Intertidal Assemblages in Chile,New Zealand, and Washington StateAuthor(s): R. T. Paine, Juan Carlos Castillo and Juan CancinoSource: The American Naturalist, Vol. 125, No. 5 (May, 1985), pp. 679-691Published by: The University of Chicago Press for The American Society of NaturalistsStable URL: http://www.jstor.org/stable/2461478 .

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Vol. 125, No. 5 The American Naturalist May 1985

PERTURBATION AND RECOVERY PATTERNS OF STARFISH-DOMINATED INTERTIDAL ASSEMBLAGES IN CHILE,

NEW ZEALAND, AND WASHINGTON STATE

R. T. PAINE,* JUAN CARLOS CASTILLO,t AND JUAN CANCINOt

*Department of Zoology, University of Washington, Seattle, Washington 98195; tLaboratorio de Zoologia, Departamento de Biologfa Ambiental y de Poblaci6nes,

Universidad Cat6lica de Chile, Casilla 114-D, Santiago, Chile

Submitted July 13, 1983; Accepted September 23, 1984

The definition of ecological stability continues to raise contentious but important issues. Sutherland (1981), Connell and Sousa (1983), and Peterson (1984) have recently dwelt on different aspects of the problem, and though not in complete agreement, their papers help to bring this elusive subject into sharper focus. Of particular interest are the nature and intensity of the forces potentially capable of altering the community composition, and whether alternative (stable) states might exist. As in Sutherland's view, the conclusions reached hinge critically on the temporal and spatial scale employed. Thus, one might require ". . . one turnover of all individuals of that species in the place" (Connell and Sousa 1983, p. 791). Another standard, and the one employed here, is Slobodkin's (1961, p. 30) criterion for ecological time "intervals of the order of ten times the length of one generation." Although the latter might be less strict, it is probably more biologically practical in that it does not require direct individual observation at the site, nor can it be vexed by the great longevity of many clonal or other potentially immortal organisms.

Here we compare the effects of removal of starfish from their native assemblages in three separate marine intertidal communities, paying special attention to changes subsequent to the starfish's return. These single-species removals define one kind of perturbation; independent observations on the resident assemblages can be used to quantify the rate and degree of response, that is, the assemblage's "stability." The removal of resident starfish species has been done in Washington State (Paine 1966, 1974), New Zealand (Paine 1971), and along the northeastern seaboard of North America (Warren 1936; Menge 1976; Lubchenco and Menge 1978; Peterson 1979). The result has been a dramatic change in the species composition of the assemblage from which starfish have been excluded: mussels of various species tend to monopolize the substratum to the detriment of many associated organisms. The generality of this response depends on three conditions being met: the existence of a competitively superior prey; the presence of a predator capable of controlling that prey's distribution and abundance; and

Am. Nat. 1985. Vol. 125, pp. 679-691. ? 1985 by The University of Chicago. 0003-0147/85/2505-0009$02.00. All rights reserved.



680 THE AMERICAN NATURALIST

sufficient recruitment of the competitive dominant, either from the plankton or by lateral migration, into the experimental site. Violation of any of these criteria is apt to modify substantially the usual result. Although these studies can be dimin- ished because they are pseudoreplicated (Hurlbert 1984), the pattern of response and change common to all makes their generality increasingly robust.

STUDY SITE

Most of the exposed shoreline of Chile would be described as outer coast, although measures of wave-generated forces are not available. We chose as our major observational and experimental station Punta el Lacho (lat. 33'30'S, long. 71'39'W), a rocky headland to the north of San Antonio, Chile. In general, the upper intertidal there is dominated by two species of chthamaloid barnacle, Jehlius cirratus and Chthamalus scabrosus. Beneath these is a band of the mussel Perumytilus purpuratus, its width varying as a function of habitat slope and exposure. The lower intertidal is a more heterogeneous landscape. The large laminarian alga Lessonia nigrescens, a species adapted to inhabit exposed sites (Santelices et al. 1980), can be abundant as can the equally impressive Durvillaea antarctica. The starfish Heliaster helianthus is commonly found at this level, although it can be observed foraging when immersed much higher in the intertidal. At the extreme low water mark of spring tides, the majority of space is covered by lithothamnioid algae. General descriptions of this community can be found in Alveal et al. (1973), Viviani (1975), and Castilla (1981).

THE Heliaster-Perumytilus RELATIONSHIP

Heliaster helianthus is the commonest intertidal starfish in Chile, at times attaining densities of 1 m-2 over broad areas (Paine and Suchanek 1983; this report). Heliaster spp. seem to be generalist predators. Heliaster kubiniji in the Gulf of California consumes predominantly barnacles (Dungan et al. 1982), although a broad range of other taxa drawn from at least three phyla are taken (Paine 1966). In Panama, H. microbrachius eats barnacles and mollusks (Menge 1982). The various reports from Chile (Viviani 1975; Castilla 1981; Paine and Suchanek 1983) reinforce the pattern: H. helianthus is a generalized consumer of marine invertebrates, including especially barnacles, a wide range of mollusks, and solitary tunicates. Table 1 gives our feeding observations, based on three sets of intertidal observations within a 2-yr interval.

Although we have not studied the food preferences of Heliaster, it is clear from table 1 that at Punta el Lacho a major component (59%-63%) of its observed adult diet is Perumytilus. This mussel is a characteristic species of the entire Chilean shore, although personal observation (R.T.P.) suggests that it occupies sig- nificantly more space toward the south. There are no conspicuous shell-length trends. Table 2 provides estimates of mussel population size structure based on replicate samples from three exposed coastal sites. Mussel size distributions appear relatively uniform; certainly, no one category predominates to the exclu- sion of others. Samples taken elsewhere in Chile confirm the suggestion that larger



TABLE 1

FEEDING OBSERVATIONS ON Heliaster helianthus FROM THE INTERTIDAL ZONE OF PUNTA EL LACHO

July 1974 Oct 1975 July 1976

No. of feeding Heliaster 141 74 73 Major prey

Barnacles Jehlius cirratus 19 75 107 Chthamalus scabrosus 28 134 9 Balanus laevis 10 1 8 Balanus flosculus 181 5 1 1 1 Austrobalanus psittacus 6 11

Mussels Perumytilus purpuratus 966 554 374 Semimytilus algosus 199 47 46 Brachidontes sp. 46 3 17

Other Chitons 14 2 6 Limpets 10 7 9 Herbivorous gastropods 161 3 20 Carnivorous gastropods 2 1 Fissurella spp. 4 Pyura chilensis 1 Tetrapigus niger 1 2 Total 1647 879 624

% of total as barnacles 15 30 24 % of total as mussels 74 69 70 % of total as Perumytilus 59 63 60

NOTE.-Observations were obtained throughout the area and therefore are representative rather than site-specific. Table entries are the total number of prey observed being eaten.

TABLE 2

SHELL LENGTHS OF LIVING Perumnytilus purpuratus AT THREE EXPOSED ROCKY INTERTIDAL SITES

ALONG THE CHILEAN SHORE

Islote Punta Perumytilus Antofagasta ConCon el Lacho Eaten by Shell Length (23?42'S) (32?52'S) (33030'S) Heliaster

(mm) N= 190 N= 114 N= 400 N= 252

< 10.0 19% 33% 31% 69% 10.1-15.0 7 8 18 11 15.1-20.0 12 13 21 7 20.1-25.0 7 7 13 6 25.1-30.0 17 29 13 3 30.1-35.0 31 10 4 2 35.1-40.0 7 0 0 1

NOTE.-The right-hand column gives the sizes of mussels observed to have been consumed by the starfish Heliaster helianthus. Entries are percentage of total.



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PERTURBATION AND RECOVERY PATTERNS 683

Perumytilus in the range of 25-40 mm shell length form the mussel matrix, within which many smaller conspecifics may exist. The final column gives the size distribution of Perumytilus observed being eaten by Heliaster at Punta el Lacho. Although these data are minimal (N = 252), they suggest that all sizes of mussels can be consumed. Data on other prey species also indicate that large-bodied individuals can be eaten: Concholepas, 50 mm; Enoplochiton, 150 mm; xanthid crab, 120 mm; fish (as carrion), 250 mm; and tunicates as large as 90 mm (Paine and Suchanek 1983). It seems reasonable to suspect, on observational grounds alone, that Heliaster could exert a significant influence on the distribution and abundance of Perurnytilus. The next section presents evidence exploring this possibility.

THE REMOVAL OF Heliaster

To examine the possible influence of Heliaster we chose a 63-M2 site which was protected from the immediate brunt of unrestricted wave action by a natural rock wall, though at times the site remained unworkable. A 27-M2 control was adjacent, though separated by a shallow surge channel. The experimental protocol involved measuring and removing Heliaster manually, and sampling both the experimental and control sites for a variety of conspicuous species at approximately monthly intervals (table 3). The removals were initiated in October 1975 and continued to mid-August 1977. Terminal observations were made in April-May 1981.

Observations on Heliaster.-Heliaster is a moderate-sized, highly vagile starfish. At the experimental site the mean diameter was 18.5 cm; the range in mean diameter, N = 21 censuses, was 15.0-20.6 cm; at the control, where starfish were individually measured only five times, 18.8-20.9 cm. Although Heliaster at the control appear marginally larger, the mean size is not statistically different (Mann-Whitney U, P > .10). The density of Heliaster resident on the control also indicates regularity. The control was censused 11 times (July 1976-August 1977, April 1981). The range of values is 0.56-1.15 Heliaster m-2 with a mean of 0.88 m-2. There is no hint of seasonality when seven winter samples (March-August) are compared with four summer ones (Mann-Whitney U, P > .10).

The data in table 3 provide one indication of the efficacy of the removals. In the removal area, there were 19 sampling intervals during the experimental period, with a mean of 33 (range, 14-72) days. The average immigration rate, based on the number removed at each date, was 0.128 Heliaster m-2mo-' and showed no seasonal trend. If the Heliaster numbers at the experimental site in October 1975 and April 1981 are representative, they suggest a density of 0.87 m-2, a value close to the mean value for the control (0.88 m-2). On the average, 0.064 immi- grants per m2 should appear by the midpoint of the first month following each removal; these represent about 7% of the normal density. Therefore, the program of continued removal achieved a 93% density reduction throughout the 22-mo experimental period.

Effects on the sessile biota.-We sampled the biota in both experimental and control areas using either haphazardly positioned 10 x 10-cm quadrats or repli- cated 1-m-long transects. Estimates of percentage of cover were obtained visually




90- . experimental, Perumyti/us

, control, Perumyti/us * * * I

. 50 0-

20

1- *experimental, chthamaloid barnacles| | l

10-

v control, chthamaloid barnacles

0- Al *' 1- ' * I . ' - ' ' ' ' * A| 'I L . A A. A - l . I.I Q N D J F M A M J J A S O N D J F M A M J J A April 1975 1976 1977 1981

FIG. 1.-Changes in percentage of space occupancy during and after the experiment by the 2 principal biological entities, mussels and barnacles. For analysis, see text. Vertical bars are I SE of estimate on either side of the mean (based on 4-13 samples); solid triangles indicate sampling dates; large stars identify dates on which experimental and controls differed.

in the quadrats, or by summing the proportion of the transect line touching a species. The topography of the experimental site was more varied than that of the control. We distinguished three levels at the removal site, and measured their height relative to mean low-tide level with a transit: above the original level of Perumytilus and essentially in the band of Jehlius cirratus (+ 1.56 to + 1.93 m); within the band of Perumytilus (+ 1.02 to + 1.56 m); and below this (0 to + 1.02 m) at a level characterized by the presence of Lessonia nigrescens. The control site is only comparable to the second of these in terms of topographic complexity and height. We therefore focus our attention on it, and minimally discuss changes in the lower zone. It should be noted that Perumytilus also increased subsequent to the removal in the highest level, the J. cirratus band. We attribute this effect to the presence of a shallow tide pool in which Heliaster found refuge; the pool's presence in effect extended the starfish's foraging range. We consider this an interesting but topographically local effect and do not mention it further.

The data taken within the normal domain of Perumytilus indicate (fig. 1) consis- tently higher coverage in the general absence of Heliaster for most censuses which include both the control and experimental sites. Average Perumytilus cover at the latter increased from 59% to 79% while average cover at the control varied between 59% and 67%. We evaluated these data in a variety of ways. The percent cover at the experimental site showed a tendency to increase through time




(Spearman rank-order statistic, r, = 0.97, N = 17, P < .01); no such trend characterized the control (r, = 0.39, N = 16, P > .05). Furthermore, the differences in Perumytilus cover between experimental and control sites also increased with time (rs = 0.92, N = 16, P < .01). When comparisons are made at individual censuses (t-tests), significant differences, P < .05, exist at all censuses made after October 1976 (fig. 1). We conclude that in the enforced absence of Heliaster, mussels tended to increase their domination of the surface.

Other changes at the experimental site either could have been anticipated or are uninterpretable. The second-most important and abundant space occupier, the chthamaloid barnacle Jehlius cirratus, declined in coverage throughout the experimental interval (Spearman rank-order statistic, rs = -.78, P < .02). Another barnacle, Chthamalus scabrosus, which tends to invade patches rapidly (Paine 1981), showed no such trends (rs .10, P > .10). No other species became at all abundant. Ulva sp. at one point occupied 4.8% of the space. Fleshy crusts of various species occupied 6.5% of the space and Ceramiumn sp. once accounted for another 7.8%. Even bare space itself, though usually present, ranged only between 0% and 6.8% and showed no trends. Although 17 other species were censused, the categories of free space, Perumytilus, and chthamaloid barnacles never accounted for less than 92% of the total. Forty-four mo after the removals ended, the control and experimental plots were essentially identical. The percent- ages of space covered by Perumytilus were once again indistinguishable (fig. 1) and the remaining space was usually either bare or occupied by chthamaloid barnacles. The barnacles had not converged with the control (fig. 1); however, the difference between 9% and 22%, though statistically significant, is not apt to persist or be of much consequence biologically.

In the lowest zone, Perumytilus was not recorded as a significant space occupier (>1%) in either October 1975 or April 1981. During the period of starfish removals, it came to occupy 8%-46% of the space. Other potential Heliaster prey also showed increases. Chthamalus scabrosus increased from a before-and-after abundance of 1% cover to an average of 4.6%; Austrobalanus psittacus from 3.8% to an average of 15.8%. From February to August 1977, however, the mean was 29.8%. The implications are that Heliaster not only determines the lower limit to Perumytilus, but also reduces the abundance of barnacles, especially Austro- balanus.

COMPARISON WITH OTHER STARFISH REMOVAL-RECOVERY PATTERNS

New Zealand.-For about 1 yr beginning in September 1968, the starfish Stichaster australis was excluded from an exposed shoreline on the west coast of New Zealand (details in Paine 1971). The site was abandoned in July 1969, and the starfish permitted to return. The initial treatment also involved the removal of the gigantic brown alga Durvillaea antarctica from a band beneath the existing bed of the zone-forming mussel Perna canaliculus. The changes in space utilization patterns during the experiment were striking. The entire area down to a point where it was no longer possible to exclude Durvillaea and remove Stichaster rapidly became a mussel monoculture. An adjacent control site retained its normal




TABLE 4

EFFECTS OF A REMOVAL OF Stichaster australis

DATE

Sept Mar May Sept Oct Feb Aug Jan % COVER 1968 1969 1969 1969 1970 1971 1976 1983

Perna 0 20 50 98 85 65 85 60 Durvillaea 85 15 0 2 5 25 10 35 Durvillaea

in control 85 100 100 95 90 100 80 100

NOTE.-Removal began in September 1968 and lasted about 1 yr. Details in Paine 1971. Despite return of the starfish by November 1969, the percent cover of Perna has remained high and that of Durvillaea low.

appearance: a dense band of Durvillaea throughout the lower intertidal with scattered Perna above. The site was photographed by friends occasionally in 1970 and 1971, and reexamined by us in July 1976 (R.T.P.) and late January 1983 (J.C.C.). Table 4 illustrates the recovery pattern: not only has Durvillaea failed to reestablish itself on the original experimental site, but Perna seems to be persist- ing. Clearly the 25-m2 site has not reverted to its original condition, despite the presence of 12 Stichaster in 1976 and 40 in 1983. It does appear, however, that Durvillaea is gradually encroaching on the mussel bed and that the site will eventually revert to its original condition.

Perna appears capable of rapid growth, and almost certainly attained sexual maturity at the experimental site within 2 yr, having reached an average shell length of 7.05 cm in the interval. This means that the Perna domination has already persisted about seven mussel generations (1969-1983) after the starfish were permitted to return. The reason for the apparent coexistence of prey and predator is probably related to Stichaster's tendency to consume smaller mussels (Paine 1971, fig. 5): large mussels thus come to predominate, form a matrix, and become self-perpetuating. Furthermore, assuming an annual reproductive effort by Durvillaea, the experimentally established Perna have resisted at least 14 annual episodes of spore invasion. The mechanism is unknown but could be similar to that identified by Paine and Suchanek (1983) for other matrix-forming invertebrates in which the associates of the matrix consume spores or sporelings and therefore prevent algal populations from becoming established or maintained. Since Durvillaea has a minimum generation time of 2 yr (Hay and South 1979), the alternative state (mussels) has persisted for approximately seven of their generations.

Washington State.-Pisaster ochraceus was initially removed from a rock platform in July 1963 at Mukkaw Bay (details in Paine 1966, 1974), and was kept removed manually until March 1968. The immediate result was successful invasion and retention of the space by Mytilus californianus. Since 1968 the site has been allowed to recover; censuses have been taken irregularly. Starfish returned immediately and had little apparent effect because those M. californianus forming the bed's matrix had become too large to be eaten (Paine 1976). Table 5 shows the




TABLE 5

PERSISTENCE OF Mytilus californianus IN THE PRESENCE OF Pisaster ochraceuls AT MUKKAW BAY

Area of Mean Length (cm) + I SD Density (N/M2) of Date Mussel Bed (m2) of Matrix Mussels Associated Pisaster

18 Mar 1968* 4.50 9.21 ? .62 0 26 Aug 1969 2.36 10.68 ? .57 3.3

3 Mar 1970 2.14 2.4 21 June 1970 12.03 ? .45 4.6

7 Feb 1971 2.25 1.5 7 Aug 1971 3.03 4.6 5 Sept 1971 12.10 ? .45

10 June 1972 2.64 13.04 ? .74 3.1 6 Apr 1973 2.44 12.50 ? .86 3.1

12 Sept 1973 2.65 4.8 9 Jan 1975 12.67 ? .62

27 Mar 1975 2.44 17 Apr 1976 2.07 21 May 1977 2.34 2.6 26 May 1979 1.96 3.5 6 Apr 1981 1.76 15.25 ? .71 1.9

10 June 1983 1.41 16.70 + 1.04 3.9 25 Aug 1984 1.41 18.3 ? .86 3.9

NOTE.-Starfish densities on the original, adjacent control site were 2.7 m-2 (SD = 0.6, N = 7; Paine 1974).

* Last data on which Pisaster was removed.

pattern of change in areas occupied by this "artificial" mussel bed since 1968. There has been no sustained increase in the area covered by mussels. There are signs of a persistent decrease, even after the area of mussels extracted for studies of population size structure (a cumulative total of about 0.25 M2) has been considered. The pattern would be reversed easily, however, if another major expansion comparable to 1971 occurred. We believe the area has not increased despite continued recruitment to the matrix (Paine 1976), because Pisaster (densities 1.5-4.6 M2) prune away smaller individuals at the bed's periphery. If the present pattern of decrease is maintained, the matrix mussels would be totally gone by early 1997, as estimated from a linear regression of bed size and age from August 1971 onward. At this point the site would again become indistinguishable from the adjacent control.

The persistence has already lasted a minimum of 8 mussel generations since starfish removal ceased, and perhaps as many as 16, given the rapid attainment of sexual maturity in M. californianus (Suchanek 1981). By 1997 these numbers would be 15 and 30. Another view of persistence is gained by noting the influence of physical disturbance on mussel bed structure. Paine and Levin (1981) cal- culated and empirically observed a minimal rotation or turnover period of about 7 yr for outer-coast mussels. This interval is the time lag between the initiation of a major disturbance and when the bed again becomes susceptible to disruption. By this criterion, the Mukkaw experimental site has persisted for three minimal cycles (1963-1984), although of course it has not been seriously disrupted. There have been no significant changes in the species composition or appearance of the




control since 1963 (Paine 1974, unpubl.), which continues as a phyletically varied collection of species. Small mussels (1-cm shell length) can be found, suggesting recruitment to the area. These are systematically eliminated by the resident Pisaster and a complex of other, smaller predators.

DISCUSSION

The rapid recovery of the Chilean assemblage to control levels subsequent to Heliaster's return contrasts with recoveries at our other sites. An alternative state has persisted since 1968 at Mukkaw Bay (table 5); Perna has maintained itself at Anawhata for at least 14 yr in the presence of Stichaster (table 4). We believe the reasons for these different recovery patterns reside in two related phenomena. First, in the artificially maintained absence of a critically important predator, two mussel species attained a size refuge (Paine 1976; Woodin 1978), permitting them later to coexist with their major predator. This did not occur in Chile, where Heliaster seems capable of consuming all Perumytilus including those larger individuals which form the mussel bed matrix (table 2). Second, mussels tend to recruit to the byssal fibers of their own species (Seed 1976), implying that once safely established at some site, given larval recruitment and survival, the local population could be self-perpetuating. This is clearly the case at Mukkaw Bay, and seems to characterize Anawhata as well. Revision to a "control" or normal state under such conditions can only be generated by physically induced stress, usually wave action, but thermal excesses or human exploitation should not be discounted.

Whether the Mukkaw Bay and Anawhata sites are alternative states, or evidence for multiple stable points (Sutherland 1974), is a function of which criterion one uses to define "stable." At both sites the mussel populations, though dwin- dling, seem capable of self-replacement. They have persisted for many minimal generation times, even using the loose definition of generation employed here, and would surely have persisted for a few even if more-rigorous demographic stan- dards were applied. They thus approach Slobodkin's (1961) criterion for ecological time. On the other hand, if one assessed adequately long persistence on the basis of at least one turnover of all individuals (Connell and Sousa 1983), neither of these mussel beds would constitute an alternative stable point or state. Evi- dence supporting this view is seen in table 5: the larger, matrix-forming mussels have not attained a shell-length asymptote, suggesting both continued individual growth and that they became established in the early phases of this manipulation.

Predator deletions and additions are perturbations in the sense of Sutherland (1981) because they potentially produce change. The deletion-wrought changes in these three assemblages are significant, and all have as a common mechanistic basis the tendency toward competitive monopolization of a spatial resource by some single species, following release from its controls. None of these communities is stable, as defined by the lack of change following the removal of these starfish. Since the communities are rich in species occupying and requiring pri- mary space, the reduction of the assemblage total by one species (the experimental removal) is minor relative to the magnitude of the induced change. Further-




more, it could be argued that since none of the removals was 100% efficient, the experimental procedure is best described as a numerical reduction, not a complete removal. Thus, at least initially, the species richness of control and experimental plots is identical. Although Orians (1975) has correctly noted that the experimental procedure itself is not independent of diversity, we believe that the lack of stability as expressed by the readily observable changes is the result of the alteration of one fundamental interaction, rather than a minor decrease in species richness. Our results support the conclusion of May (1973) and others that high species diversity in assemblages is unlikely to confer any special ability to resist change.

If we accept generation time as the yardstick for evaluating the temporal dimension of specific ecological processes, only the experimentally produced New Zealand and Washington State mussel assemblages can be considered stable, though all three mussel species, especially Perumytilus (Lozada and Reyes 1981), meet the requirements for short generation time of sexual maturity in their first year and frequent reproduction. Because these two assemblages have persisted and, like Sutherland's fouling assemblages, clearly have been bombarded unsuc- cessfully by spores or competent larvae of many other species, they can be considered stable in the face of two categories of perturbation, one of which is destabilizing under other conditions. Therefore, when a competitively dominant species becomes too large to be consumed, having attained the critical escape size, and if its own larvae can recruit effectively to that space, it can persist for many generations with its major predator. On the other hand, Perumytilus was incapable of maintaining its extended population in the presence of Heliaster: therefore it was unstable in one sense, suggesting that a persistent alternative stable point, that is, a state capable of both persistence through time and self- replenishment in space, is an unlikely possibility for this Chilean marine community. Our results, like those of Sutherland (1981), illustrate the difficulty in apply- ing the terms stable and persistent. Even when performing the simplest stability experiment practicable under natural conditions (single-species deletion), we have observed a range of effects. One of these, persistent stands of adult organisms, can serve as a major source of reproductive products, diversify the environment spatially and often provide a refuge for a host of associated species. As such, they are important biological entities; whether they constitute alternative states or persist for a sufficient interval to be classified as stable, being definition-dependent, seems of lesser significance.

SUMMARY

When starfish are removed from small portions (<63-M2 areas) of certain marine communities, mussels increase the percentage of space that they occupy. When compared to other studies in New Zealand and Washington State, new results from Chile indicate that none of these assemblages is stable when perturbed in this fashion. That is, all attain a different state within relatively brief periods. When starfish were permitted to return, we observed two different recovery patterns. In Chile, the experimental site converged rapidly toward the undisturbed control; at




the other sites, mussels too large to be eaten by starfish continued to dominate the space. The results indicate the importance of size escapes from predation for marine communities. Whether these persistent, but diminishing in spatial coverage, stands of mussels are alternative stable states or not is dependent on the definition of stability employed.

ACKNOWLEDGMENTS

R.T.P. takes great pleasure in acknowledging the opportunity to work with Chilean marine biologists. The chance was afforded, initially, by funding from the Interamerican Development Bank, and then by the National Science Foundation through grants GA41120 and DES 75-14378. J.C.C. greatly appreciates support from Pontificia Universidad Cat6lica de Chile through grant DIUC 62/82. C. H. Peterson and two anonymous reviewers substantially improved the paper. Field- work or discussions with K. P. Sebens, T. H. Suchanek, and M. Slatkin have been especially rewarding.

LITERATURE CITED

Alveal, K., H. Romo, and J. Valenzuela. 1973. Consideraci6nes ecologicas de las regi6nes de Valparaiso y de Magallanes. Rev. Biol. Mar. 15:1-29.

Castilla, J. C. 1981. Perspectivas de investigaci6n en estructura y dinamica de comunidades inter- mareales recosas de Chile central. II. Depredadores de alto nivel tr6fico. Medio Ambiente 5: 190-215.

Connell, J. H., and W. P. Sousa. 1983. On the evidence needed to judge ecological stability or persistence. Am. Nat. 121:789-824.

Dungan, M. L., T. E. Miller, and D. A. Thomson. 1982. Catastrophic decline of a top carnivore in the Gulf of California rocky intertidal zone. Science 216:989-991.

Hay, C. H., and E. R. South. 1979. Experimental ecology with particular reference to proposed commercial harvesting of Durvillaea (Phaeophyta, Durvillaeales) in New Zealand. Bot. Mar. 22:431-436.

Hurlbert, S. H. 1984. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54:187-211.

Lozada, E., and P. Reyes. 198 1. Reproductive biology of a population of Perurnytilus purpuratus at El Tabo, Chile. Veliger 24:147-154.

Lubchenco, J., and B. A. Menge. 1978. Community development and persistence in a low rocky intertidal zone. Ecol. Monogr. 59:67-94.

May, R. M. 1973. Stability and complexity in model ecosystems. Princeton University Press, Prince- ton, N.J.

Menge, B. A. 1976. Organization of the New England rocky intertidal community: role of predation, competition and environmental heterogeneity. Ecol. Monogr. 46:355-393.

1982. The effects of feeding on the environment: Asteroidea. Pages 521-551 in M. Jangoux and J. M. Lawrence, eds. Echinoderm nutrition. A. A. Balkema, Rotterdam.

Orians, G. H. 1975. Diversity, stability and maturity in natural ecosystems. Pages 139-150 in W. H. van Dobben and R. H. Lowe-McConnell, eds. Unifying concepts in ecology. Junk, The Hague.

Paine, R. T. 1966. Food web complexity and species diversity. Am. Nat. 100:65-75. 1971. A short-term experimental investigation of resource partitioning in a New Zealand rocky intertidal habitat. Ecology 52:1096-1106. 1974. Intertidal community structure: experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia 15:93-120.




. 1976. Size-limited predation: an observational and experimental approach with the Mytilits- Pisaster interaction. Ecology 57:858-873.

. 1981. Barnacle ecology: is competition important? The forgotten roles of disturbance and predation. Paleobiology 7:553-560.

Paine, R. T., and S. A. Levin. 1981. Intertidal landscapes: disturbance and the dynamics of pattern. Ecol. Monogr. 51:145-178.

Paine, R. T., and T. H. Suchanek. 1983. Convergence of ecological processes between independently evolved competitive dominants: a tunicate-mussel comparison. Evolution 37:821-831.

Peterson, C. H. 1979. The importance of predation and competition in organizing the intertidal epifaunal communities of Barnegat Inlet, New Jersey. Oecologia 39:1-24. 1984. Does a rigorous criterion for environmental identity preclude the existence of multiple stable points? Am. Nat. 124:127-133.

Santelices, B., J. C. Castilla, J. Cancino, and P. Schmiede. 1980. Comparative ecology of Lessonia nigrescens and Durvillaea antarctica (Phaeophyta) in central Chile. Mar. Biol. 59:119-132.

Seed, R. 1976. Ecology. Pages 13-65 in B. L. Bayne, ed. Marine mussels: their ecology and physiol- ogy. Cambridge University Press, Cambridge.

Slobodkin, L. B. 1961. Growth and regulation of animal populations. Holt, Rinehart & Winston, New York.

Suchanek, T. H. 1981. The role of disturbance in the evolution of life history strategies in the intertidal mussels Mytillis edulis and Mytillis californianus. Oecologia 50:143-152.

Sutherland, J. P. 1974. Multiple stable points in natural communities. Am. Nat. 108:859-873. 1981. The fouling community at Beaufort, North Carolina: a study in stability. Am. Nat. 118:499-519.

Viviani, C. A. 1975. Las comunidades marinas litorales en el norte grande de Chile. Publ. Ocas. Lab. Ecol. Mar., Iquique.

Warren, A. E. 1936. An ecological study of the sea mussel (Mytilus edulis Linn.). J. Biol. Board Can. 2:89-94.

Woodin, S. A. 1978. Refuges, disturbance and community structure: a marine soft-sediment example. Ecology 59:274-284.



perturbation and recovery patterns of starfish-dominated intertidal assemblages in chile, new...

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