the crustose coralline alga, phymatolzthon foslie ......growing fleshy algae. it is of interest to...

.I. Exp. Mar. Biol. Ecol., 1986, Vol. 96, pp. 127-146 Elsevier

127

JEM 641

THE CRUSTOSE CORALLINE ALGA, PHYMATOLZTHON Foslie, INHIBITS

THE OVERGROWTH OF SEAWEEDS WITHOUT RELYING ON

HERBIVORES

CRAIG R. JOHNSON’ and KENNETH H. MANN’ Department of Biology, Dalhousie Universily, Halgax, Nova Scotia, Canada B3H 4Jl

(Received 15 August 1985; revision received 19 November 1985; accepted 18 December 1985)

Abstract: When surfaces of boulders covered with Phymatolithon Foslie were compared with boulders of bare granite in a grazer removal experiment, the biomass of recruited fleshy algae was significantly lower on the Phymatolithon, being on average less than half that on the granite. This inhibitory effect was not species specific; the species composition and species diversity on the two substrata were similar. S.E.M. studies indicated that the surface of Phymatolithon is unstable in that epithallial cells slough off frequently. There are also numerous chalky white scales on the crust surface, up to N 1 mm diameter and lo-15 cells thick, that are easily dislodged. We suggest that, although the possibility of chemical inhibition cannot be ruled out, the instability of the surface crust contributes significantly to inhibition of algal settlement on Phymatolithon. There was no evidence of dieback of Phymatolithon crusts during the 16 months of the experiment.

Key words: coralline alga; epithallial sloughing; antifouling effect; seaweed recruitment; grazer dependence; Phymatolithon

Crustose coralline algae, which are cosmopolitan and abundant in the subtidal, are slow growing calcareous plants with a hard surface suitable for the attachment of faster growing fleshy algae. It is of interest to know how they compete with fleshy seaweeds and survive under these circumstances. Several experimental studies have indicated that in the absence of grazers to remove fleshy macroalgal epiphytes from crust surfaces, crustose corallines become overgrown and eventually die (Adey, 1973; Littler & Doty, 1975; Wanders, 1977; Paine, 1980; Steneck, 1982). Also, Vine (1974) and Littler & Doty (1975) showed that crusts would not settle and establish on primary substrata unless herbivores were present to limit the development of fleshy algae. Consideration of these kinds of observations has led Paine (1980) and Steneck (1983) to suggest that coralline crusts are dependent on grazers to maintain their surfaces free from fouling by competitively superior but grazer-vulnerable fleshy seaweeds. Steneck (1983) contends that, herbivory aside, corallines have no other effective means of limiting fouling by epiphytes. In contrast, Masaki et al. (1981, 1984) reported that sloughing of epithallial cells from the surface of the crust of Lithophylfum yessoense was sufficient to

’ Present address: Department of Fisheries and Oceans, Marine Ecology Laboratory, Bedford Institute of Oceanography, P. 0. Box 1006, Dartmouth, Nova Scotia, Canada B2Y 4A2.

0022-0981/86/$03.50 0 1986 Elsevier Science Publishers B.V. (Biomedical Division)

128 CRAIG R. JOHNSON AND KENNETH H. MANN

prevent fouling by the kelp Laminaria japonica when herbivores were absent. Others have also hypothesized that shedding of epithallial cells might be effective as a mechanism against fouling by epiphytes (Adey, 1964, 196613, 1973; Johansen, 1981; Littler & Littler, 1984) and sessile invertebrates (Padilla, 1981; Breitburg, 1984).

Recent mass mortalities of the sea urchin Strongylocentrotus droebachiensis (Mtiller) in the nearshore rocky subtidal of Nova Scotia (see Miller & Colodey, 1983; Scheibling & Stephenson, 1984; Jones, 1985; Jones & Scheibling, 1985; Jones et al., 1985) left coralline algae the conspicuously dominant taxon until fleshy seaweeds began to reappear for the first time in over a decade (Moore & Miller, 1983; Johnson, 1984; Miller, 1985). In this paper we test, and reject, the null hypothesis that the structure of the successional seaweed community which developed following the demise of the urchins was not influenced by coralline algae in the absence of grazers. We suggest that when herbivores are absent (1) coralline algae may exert a significant effect on the structure of seaweed assemblages by inhibiting algal recruitment, (2) that the mechanism for this antifouling effect may be sloughing of epithallial cells from the surface of the crust, and (3) that since many species of crustose corallines slough epithallial cells, are adapted to low light levels, and apparently thrive beneath dense canopies and turfs, there is no case for a general application of the “grazer-dependent” hypothesis for the maintenance of coralline crusts.

METHODS

SITE DESCRIPTION AND EXPERIMENTAL DESIGN

The experimental site was near Mill Cove in St. Margaret’s Bay on the Atlantic coast of Nova Scotia (44”35’30”N : 64”03’42”W). The site is moderately exposed with a granite boulder substratum to % 15 m depth. By early 1982 all hard substrata, including coralline crusts, supported an extensive growth of mainly Iilamentous fleshy seaweeds that had grown up following the disease-induced mortality of the sea urchins. Encrusting corallines cover nearly all of the hard substrata in St. Margaret’s Bay below 5 m depth, and at Mill Cove covered > 91 y0 of the boulder surfaces (estimated October 1983 from a sample of25 0.25-m’quadrats; quadrats were divided into 100 0.05 x 0.05 m squares, and the proportion of coralline cover in each estimated as l/8,2/8, . . ., 8/8 and summed).

Species of Phymatolithon always occupied the tops of boulders (see p. 13 l), and the experiment compared the biomass of fleshy seaweed species that recruited onto bare (overturned) boulders and Phymatolithon crusts. Eighteen groups of 10 experimental boulders were positioned at z 10 m depth in June 1982. The rocks were large enough (Z 0.20-0.35 m diameter) that they did not move in heavy surge, and the groups were positioned l-2 m apart. Each group of 10 consisted of five rocks with z 100% cover of crustose corallines, and five which had been overturned to expose their bare underside surfaces. The rocks were not shaded by seaweeds or other boulders. All rocks were collected at z 10 m depth, and all manipulations were performed at this depth.

CORALLINE ALGA INHIBITS SEAWEED RECRUITMENT 129

First, the experimental rocks were scrubbed thoroughly over their entire surface with wire brushes to remove all foliose algae and sediment. Initially and on each sampling visit, limpet, ~otoac~uea tes~di~al~ (Muter), chiton, Toni~ella rubra (Linnk), and sea urchin, Strongylocentrotus droebachiensis grazers were removed from the experimental rocks and from an area x0.6 m around each group. In 1983 the growth of algae concealed small numbers of newly recruited grazers, on both substratum types, which reached a maximum density of < 10 per experimental rock in August. It was assumed that the low numbers of very small herbivores on the exp~~rnent~ surfaces had a negligible effect on seaweed recruitment. During the fast 4 months of the experiment removal of grazers was performed monthly, but it was evident that even at this time of the year (the peak of grazer activity) removals at this frequency were unnecessary since the migration of limpets, chitons and sea urchins onto the experimental rocks was neg~~ble. All sea urchins were newly settled animals (l-2 mm diameter), they were never found on the upper experimental surfaces but were always cryptic under rocks, and their modal size attained only w 5 mm diameter before the cohort disappeared (R.E. Scheibling, pers. comm.). Although grazing in the experimental plots by fishes and amphipods might have occurred, it was never observed. Furthermore, there is no evidence that these grazers might be specifically associated with either granite or coralline substratum, therefore their grazing activities, if occurring at all, would not confound the fixed treatment (substratum) effect.

On each of six occasions (see Figs. 1,2), one of the initial 18 groups of rocks was selected haphazardly, and the individual rocks sealed in separate containers underwater for transport. Portions of rocks to be excluded from analysis (e.g. undersides and sides overlaid by adjacent rocks) were delineated unde~ater with oil pastel crayon, The mean experimental area per rock was 325 cm2 (SE = 15). All non-crustose macroalgae on the experimental surfaces were removed, identified, dried at x 80 “C, and weighed. Numbers of plants were not counted as the morphology of several of the species made it impossible to identify individuals. Algae were identified according to the taxonomy given in South & Hooper (1980), but species of Antit~~n~on and Antitha~nio~ella were pooled under the generic assemblage Antitha~nion spp. Substratum areas were determined by dividing each surface into approximately flat sections or sections with curvature in only one plane, tracing these sections onto acetate sheets, and converting the weight of the tracings to an area from a predetermined regression function. Final results were expressed as dry weight per m2. Thus, on any one sampling date, tive replicate observations of each seaweed species on the two experimental substrata (granite + Phpatolithon) were obtained. In analyzing these data, the Shannon index of diversity (tlr’) and measure of evenness (J’) were used (both discussed by Pielou, 1978).

A supplementary experiment was conducted to control for the possibility that the bare undersides of overturned rocks might possess chemical characteristics to promote or inhibit seaweed settlement and growth, and thus bias the primary expe~ment. Twenty bare rocks were brought from the splash zone above the high intertidal adjacent the Mill Cove site in September 1982, and placed at z 10 m depth with a second group of 20


overturned rocks collected at z 10 m depth. All rocks were scrubbed with wire brushes in the manner described previously, and were also maintained clear of grazers. Ten rocks of each treatment were selected haphazardly at the end of October 1983 and the biomass of seaweed species on each rock determined as described above.

STATISTICAL

For parametric tests, data were transformed in an attempt to achieve homoscedasti- city and a normal distribution of error terms. Unless stated otherwise, transformations were successful in meeting these requirements. In the text, tr~sfo~ations are described in terms of the untransformed variate, Y. For the multivariate analysis of variance (MANOVA), several changes were made to the raw data in attempting to circumvent problems of heteroscedasticity in dispersion matrices and non-normality of residuals. In the primary experiment, data from the first two sampling dates in the incipient stages of the experiment, and 10 species rarely encountered (Table I) were excluded from the analysis. Also, dimension reduction of the remaining 12 species was attempted by performing an R-type (Legendre & Legendre, 1983) principal components analysis (PCA) on a mean variance-covariance matrix obtained by averaging the eight group dispersion matrices (4 dates x 2 substrata = 8 groups). Since the first four principal components accounted for 97.1% of the raw dispersion, thus representing a parsimonious but quite satisfactory description of the data complex, the MANOVA was conducted on these principal components to test for date and substratum effects.

A similar procedure was adopted in analyzing data from the supplement~y experiment. Again, rare species were excluded (Table IV), and a MANOVA was conducted on the first three principal components (which absorbed 99.4% of the total dispersion) generated by a PCA of the mean variance-covariance matrix obtained by averaging the two group dispersion matrices. In addition to facilitating reduced dimensionality, combining PCA with MANOVA in this manner has the added advantage that since the principal axes are orthogonal and uncorrelated, and therefore independent, a unique transformation may be applied to each variate (principal component) independently (see Press, 1972).

SCANNING ELECTRON MICROSCOPY

The surface of Phymatolithon crusts were examined for evidence of sloughing of surficial cells. Samples of live crust chipped from boulder substratum at Fink Cove (~40 km south east of Mill Cove) at z 10 m depth were collected into separate containers for transport, rinsed in sea water, either (1) air-dried overnight or (2) fixed overnight in half-strength Karnovsky’s solution (Karnovsky, 1965) in 0.2 M cacodylate buffer, washed in the buffer, dehydrated in a graded ethano1 series, and then critical point-dried. Dried specimens were sputter coated with gold-palladium (60 : 40) before examination with a Bosch and Lomb Nanolab 2000 S.E.M.


RESULTS

INCIDENCE AND DISTRIBUTION OF CORALLINE GENERA

Crustose corallines in St. Margaret’s Bay are primarily represented by the genera Clathromorphum Foslie, Lithothamnium Philippi, and Phymatolithon Foslie, the dominant species being Clathromolphum circumscriptum (Strbmfelt) Foslie, Lithothamnium glaciale Kjellman, Phymatolithon laevigatum (Foslie) Foslie and P. rugulosum Adey. The relative abundance of these genera on the experimental rocks was 72.3 y0 Phymatolithon, 26.7% Lithothamnium, and only 1.0% Clathromorphum. The latter occurred in small patches usually not larger than lo-30 mm diameter. The top surface and uppermost regions of the sides of rocks was covered mostly by Phymatolithon, whereas Lithothamnium was

largely restricted fo a relatively narrow band around the base of rocks immediately above the rock-sediment interface. Thus, since Phymatolithon was the only genus comparable with the bare rock surfaces in terms of area and aspect, the other two genera were excluded to avoid bias stemming from differences in orientation to light and area available for colonization.

DIVERSITY AND TOTAL BIOMASS

Qualitative differences among the bare granite and Phymatolithon experimental substrata in the number and identity of fleshy seaweed species encountered were minor (Table I), and can be attributed to effects of chance in settlement since the species that were not ubiquitous on both substratum types were rare. Moreover, the species absent from coralline crusts on the experimental rocks were all found growing on Phymatolithon nearby. Similarly, there was little difference in the diversity and evenness of abundance of species that established on the crust and granite surfaces (Fig. 1).

However, conspicuous differences were evident in the total biomass of seaweeds that recruited onto the two substrata (Fig. 2). The substratum x date interaction was highly significant (ANOVA, transformation = Y ’ 235, F = 6.83, P < O.OOl), and Tukey’s test indicated that by August 1983 a significantly greater biomass of fleshy algae had recruited to the bare rock surfaces than to an equivalent area of Phymatolithon. The decline in standing biomass after August 1983 reflects deterioration of the summer annuals.

MULTIVARIATE ANALYSIS; RESPONSES OF INDIVIDUAL SPECIES

Each principal vector generated in the PCA had only one species with a high loading, and the species was different for each vector. This indicated that, in decreasing order of importance, Ceramium rubrum, Bonnemaisonia hamifra, Polysiphonia nigrescens, and Desmarestia viridts were responsible for most of the variance within date-substratum groups. These were also the most abundant species recorded at any time during the experiment (Table II).


The MANOVA of the first four principal components also identified a highly significant date x substratum effect (Table III). Furthermore, the univariate ANOVAs within each of the main and interaction effects suggested that the first three principal components were significant components of variance within the main effects. Since each principal component had only a single, and different, species with a high loading, it may be concluded that the three species Ceramium rubrum ( w PCl), Bonnemaisonia hamifra (z PC2) and Polysiphonia nigrescens (z PC3), in decreasing order of importance, were largely responsible for the observed differences in the two substrata. (It should be noted that although transformations of the principal components achieved normality of error terms of the marginal distributions, some heteroscedasticity was still evident after transformation. While this may reduce the efficiency of the test, it is unlikely to affect the interpretation of the results in this case.)

The rank order of importance of these three species as indicated by the PCA matched

TABLE I

Occurrence of species of fleshy algae on Phymatolithon and bare granite substrata in an experiment examining influence of coralline crusts on recruitment of seaweeds in the absence of grazers: + , species

recorded; -, species not recorded; *, species included in principal components analysis.

Substratum

Species Granite Phymatolithon

Chlorophyta Cladophora spp.

Phaeophyta Ectocarpus spp. Acrothrix novae-angliae Stictyosiphon spp. Desmarestia vin’dis Tilopteti mertensii Sphacelaria cirrosa Sphacelaria firrcigera

Sphacelaria plumosa Halopteris scoparia Petalonia fascia

Rhodophyta + Bonnemaironia hamifra

Cysloclonium purpureum * Chondrus crispus * Antithamnion spp. * Callithamnion spp. * Ceramium rubrum

Polysiphonia Jrexicaulis Po&siphonia harveyi

* Polysiphonia nigrescens * Polysiphonia urceolata * Rhodomela confervoides

+ + + + + + + + + +

+ + + + + + +

+ + +


exactly the rank of their overall abundance on the experimental surfaces (see Table II), suggesting that among these species, the difference in biomass on the two substrata was approximately proportional to their abundance. Moreover, it was evident from the relationship between the biomass on Phymatolithon and that on granite that this trend was reasonably consistent among all of the more common (biomass 2 1.0 g dry wt * m - 2, species. This relationship was approximately linear (9 = 0.79, and showed that the biomass of a seaweed species on Phymatolithon was, on average, z 46 y0 of its biomass on an equivalent area of granite (Fig. 3). Considering (1) the similarity in the

diversity and evenness of the seaweed community on both substrata, (2) the corre- spondence of the rank of species abundances with their rank in importance in contri-

o-9

0.8

0.7

0.6

o-5

0.4

0.3

0.2

0.1

M Diversity - Phymatolithon

. 0 Evenness - Phymatolit hon

.- - -0 Diversity - granite

@- - --o Evenness - granite

I

I I

II I I I l l l l 11 l l l I I I1 J J ASONDJ FMAMJJ A S 0 N

1982 1983

Fig. 1. Diversity (H’) and evenness (J’) of fleshy seaweed species recruited on bare granite surfaces and

on Phymatolithon crust in the absence of grazers.


Biomass of seaweed

g dry weight O-lm2

16 -

15 -

14 -

13 -

12 -

II -

IO -

9-

8-

7-

6-

5-

4-

3-

2 -

I -

I I I I I I I I I I I I I I l I JJASONDJ F M A M J J A S 0 N

1982 1983

Tukey’s classification -

P4 gl PI P3 P2 g4 g2 g3

Fig. 2. Total biomass of all fleshy seaweed species recruited on bare granite substratum and on an equivalent area of Phymatolirhon crust in the absence of grazers: bars are SE; homogeneous subsets of substratum-date groups according to Tukey’s classification are given (U = 0.05, transformation = ln( I’)).


TABLE II

Mean biomass (g dry wt -rnm2) of commonest seaweed species recruited onto bare granite (G) and ~~y~~~~~?~u~ (P) substrata in the absence of grazers: data from samples taken during incipient stages of

the experiment are not included.

Species

Phaeophyta Acroth& novae-angiiae St~ctyos~~on sp. ~esmarestia vi&& Tilopteris mertensii

Rhodophyta Bonnemaisonia hamifera Chondrus crzpus Anthihamnion spp. Cal~thamnion sp. Ceramium rubrum Polysiphonia nigrescens Polysiphonia urceolata Rhodomela confervoides

Date (no. of days since start of experiment)

21 Sept. ‘82 7 Mar. ‘83 9 Aug. ‘83 20 Oct. ‘83

(1~~ (267) (4221 (494) -__l_ll

G P G P G P G P

1.4 1.4 0.0 0.0 0.1 0.0 0.0 0.0 0.2 0.0 0.0 0.0 0.0 0.0 0.6 0.8 0.0 0.0 0.2 0.0 14.3 0.0 0.0 0.0 0.2 0.1 0.2 1.9 0.0 0.0 0.0 0.0

1.7 0.8 0.0 0.4 55.0 22.9 10.7 4.5 0.0 0.0 0.0 0.0 0.0 0.0 1.2 0.1 0.0 0.0 1.5 2.1 0.7 0.0 0.0 0.0 8.3 12.1 3.5 0.0 0.0 0.0 1.3 0.4 3.3 3.9 62.7 43.5 52.2 13.2 4.7 0.2 0.0 0.0 0.1 0.5 3.5 1.0 29.4 6.1 0.0 0.0 0.0 0.5 0.1 0.2 0.7 0.1 0.0 0.0 0.0 0.1 0.1 0.4 1.8 0.1

t

Biomass on Phymatolithon

5o ( g dry weight 1.0 me21

*

Biomass on granite (g dry weight 1.0 ms2)

Fig. 3. Relationship between biomass of seaweed species on Phymatolithon and biomass on granite substrata (for species 2 1.0 g dry wt .rn-a substratum),


buting to the differences in seaweed biomass on the two substrata, and (3) the approximate linear relationship between seaweed biomass on the two substrata, suggests that the inhibitory effect of Phymatolithon on the biomass of seaweed recruits was similar for all algae encountered.

TABLE III

Recruitment of fleshy seaweeds onto bare granite and Phymatolithon substrata: two-way MANOVA of first four principal components (PCl-PC4) in date (4) x substratum (2) model; unique transformations were applied to each principal component; viz., lnl Y-51 for PCl, PC2 was not transformed, and ln(Y + 10) for PC3 and PC4; levels of significance are: ***PS 0.001; ** 0.001 <PI 0.01; * 0.01 i P i 0.05; ns = P 2 0.05; each PC had only a single species with a high coefficient, showing that PC1 x biomass of Ceramium rubrum, PC2 z Bonnemaiconia hamifra, PC3 % Polysiphonia nigrescens, and PC4 x Desmarestia

viridti.

Source Test F P

Date (adjusted for substratum) Hotelling’s trace 25.3 ***

Wilk’s lambda 26.8 ***

Substratum (adjusted for date) Hotelling’s trace 6.9 ***


Date x substratum (adjusted for date and substratum) Hotelling’s trace 3.5 ***


Univariate tests within main effects Source Variable F P

Date PC1 45.1 ***

PC2 40.0 ***

PC3 23.9 ***

PC4 2.6 ns

Substratum PC1 16.2 ***

PC2 4.5 *

PC3 9.6 **

PC4 0.1 ns

Date x substratum PC1 3.3 *

PC2 4.2 *

PC3 7.0 ***

PC4 1.3 ns

ASSESSMENT OF BIAS IN SETTLEMENT AND GROWTH OF SEAWEEDS ON

OVERTURNED ROCKS

Of the 23 species recorded in the secondary experiment comparing the recruitment of seaweed species on the bare surfaces of granite rocks obtained from the splash zone and on overturned subtidal rocks, 22 were encountered on the intertidal boulders, but only 15 were recorded from the overturned rocks (Table IV). Although most of the seaweeds limited to a single substratum were relatively rare on the experimental

CGRALLINE ALGA INHIBITS SEAWEED RECRUITMENT 137

surfaces, this result suggests that recruitment was lower on the overturned rocks than on the boulders brought from the splash zone. Moreover, quantitative analysis indicated that there were highly significant differences in the abund~ces of the common (Table IV) species that settled on the two substrata (one-way MANOVA of first three

TABLE IV

Mean biomass of seaweed species recruited onto granite boulders brought from the intertidal (splash zone) and onto overturned subtidal granite rocks in the absence of grazers: *, species included in principal

components analysis.

Chlorophyta * Cladophora spp.

C~etomo~ha spp. ~izoclonium spp.

* Spongomorpha spp.

Phaeophyta Ectocatpus spp.

+ Stictyosiphon tortilis * ~e~re~.a aAleata + Resmarestia v&id& * Chorda j&m * Laminaria longicruti

Saccothiza dermatodea * Sphacelak &rosa * Sphace1an.a furcigera * Sphacelaria phmosa

Halopteris scoparia

Rhodophyta Bannemaironia hamgera

* ~~st~on~rn pu~ur~m Chondrus cr&pus

+ Callithamnion sp. * Ceramium rubrum * Polysiphonia nigrescens * Polesaw wceolatu * ~odomela confervoides

Dry weight (g. m-*)

Intertidal Subtidal rocks rocks

2.11 0.01 0.08 0.39

0.02 1.02 2.10 4.93

64.43 1.20

0.53 0.04 0.02 0.05

0.13 4.89 0.01 2.68 0.95

82.05 0.51 2.46

0.13

0.22 0.26

-

4.54 0.02 0.17 1.34

2.35

1.07 0.36

55.43 0.34 0.51

principal components; for Hotelling’s trace and Wilk’s lambda F = 9.68, P < 0.001, ~~sfo~ations were Ini Y-201 for PC1 and PC3, and InI Y/ for PC2). A sign~c~tly greater biomass of algae recruited onto rocks brought from the intertidal than to an equivalent area on the scrubbed undersides of overturned subtidal rocks. This difference is suprising since all of the boulders were granite and the only difference was in their collection sites. Although the surfaces of the overturned rocks may have been anoxic initially, after the scrubbing treatment all sulphides etc. should have been oxidized within


24 h. It is possible that the anaerobic undersides did not originally support a bacterial population suitable for seaweed colonization (e.g. see Scheer, 1945). However, while this result is somewhat enigmatic, it clearly implies a conservative bias in the primary experiment. The differences in the abundance of seaweed species recruiting to equivalent areas of Phymatolithon and bare granite surfaces can be expected to be at least as great as that observed between Phymatolithon and the bare surfaces of overturned rocks.

SURFACE STRUCTURE OF PHYMATOLZTHON CRUSTS

Scanning electron microscopy indicated that the epithallus of Phymatolithon is continuously disintegrating. Groups of epithallial cells with their covering cuticle (Fig. 4A) may cleave and be lost as small scales. However, in all specimens examined epithallial cells were rarely encountered, and the occurrence of primary pit connections at the uppermost surface of the majority of surface cells (Figs. 4A-C) showed that the epithallus had been sloughed from most of the surface. Furthermore, the calcareous

Fig. 4. S.E.M.s of the surface of Phymatolithon crusts showing: A, a small group of epithallial cells covered by cuticle (cu) surrounded by an area from which the epithallus has been lost: B, primary pit connections (pp) indicating loss of epithallial cells; C, a section of crust from which the epithallus has been lost showing an abundance of coccoid, rod-shaped and filamentous bacteria (ba) within the concavities of dead cells (in some of which the inner cell wall (ic) is visible); D, a multilayered ‘scale’ which has been broken to reveal

thickness; specimens in A-C critical point-dried; specimen in D air-dried.


walls of the surface cells in these regions were themselves crumbling and appeared unstable (Figs. 4A-4C). It is unlikely that the unstable nature of the walls of the surface cells of ~~~~ff~5~j~~5~ was an artifact of prep~ation, since the surface cells of Lithothamnium prepared in the same way appeared much more robust.

There was evidence of a second type of shedding of cells. The surface of most crusts supported chalky white scales (indicating groups of dead cells) that were visible to the naked eye (up to = 1 mm diameter) and which were readily removed with the tip of a needle. These flakes were lo-15 cells thick and many appeared to be epiphytic conspecifics (Fig. 4D).

DISCUSSION

MECHANISM OF INHIBITION OF SEAWEED RECRUITMENT BY ~~Y~~~~~~~~O~

We suggest that inhibition of establishment of fleshy algae on Phymato~jthon crusts is largely the result of sloughing of epithallial cells from the crust surface. Albeit the possibility of chemical inhibition cannot be excluded, there is little doubt that the surface of this crust is unstable. Our observations are in accord with those of Adey (1964,1973), who reported that sloughing of epithahial cells by Phymato~~th~~ can occur at such a rate that frequently there is no epi~~um remaining over relatively large areas. The profusion of bacteria in most dead surface cells (Fig. 4C) parallels the observations of Millson 8c Moss (1985) who suggested that bacterial invasion of the epithallial cells of Phymatolithon lenormandi accelerates epithallial degradation. Shedding of the larger multi-layered scales (Fig. 4D) would exacerbate the effect of epithallial sloughing. Al~ough not quitted, it was clear that for those species where indi~du~s could be discerned, fewer plants grew on the crusts than on the bare granite.

Others have also hypothesized that epithallial shedding in crustose (Adey, 1964, 1966b, 1973; Johansen, 1981; Littler & Littler, 1984) and articulated corallines (Borowitzka & Vesk, 1978), and analogous sloughing of epidermal tissue by fleshy red and brown seaweeds (Filion-My~ebust & Norton, 198f ; Sieburth & Tootle, 1981; Moss, 1982; Russell 8z Veltkamp, 1984), calcareous green algae (Borowitzka & Larkum, 1977), and sea grasses (Jagels, 1973), serves as an innate antifouling mechanism. More importantly, Masaki et al. (1981, 1984) demonstrated unequivocally that surlicial sloughing by Lithophyllum yessoense prevented fouling by Laminaria jap5njca and microorg~isms. It is noteworthy that Padilla (198 1) found that dense patches of diatoms grew on crust-removal areas but not on live crusts in adjacent control areas. Similarly, Breitburg (1984) observed a ten-fold increase in the number of algal recuits on bare rock relative to coralline crusts in the absence of grazers, but this difference was not significant.

The di.tTerence in biomass of seaweeds that recruited to the granite and Phymat~~~thon substrata is unlikely to stem from differences in surface rugosity, since the grain size of both experimental surfaces was considerably > 0.5 mm. Surface particle size appears to have greatest effect on the settlement of seaweeds in the size range O-O.5 mm (Foster, 1975; Harlin & Lindbergh, 1977 and references).


HERBIVORES, SLOUGHING OF EPITHALLIAL CELLS AND CRUST SURVIVAL

Experimental studies have identified two ways in which coralline crusts overcome the problem of fouling by epiphytes. Masaki et al. (1981, 1984) have shown that epithallial sloughing may be sufficient to prevent fouling, whereas others have found that the establishment, growth and survival of crusts requires the presence of herbivores (Adey, 1973; Vine, 1974; Littler & Doty, 1975; Wanders, 1977; Paine, 1980; Steneck, 1982). Paine (1980) and Steneck (1983) extrapolated from these latter kinds of results to suggest dependence of coralline crusts on herbivory in general. Implicit in Steneck’s (1983) assertion that crusts have no intrinsic ability to limit fouling by epiphytes, is that corallines may influence the structure of fleshy seaweed assemblages only indirectly via their interactions and associations with grazers.

It is clear from the present study that (1) by limiting algal cover Phymatolithon has a direct impact on the structure of seaweed communities and that (2) survival of Phymatolithon is not dependent on grazers to remove epiphytes from the crust surface. There was no evidence of necrosis or mortality of either Phymatolithon or Lithothamnium crusts on the experimental boulders during the 16 months of the experiment. In the work of others, crust mortality as a result of algal growth has been demonstrated within 3 months of grazer removal (Wanders, 1977; Paine, 1980; Steneck, 1982). The fact that Phymatolithon and Lithothamnium appeared healthy after 16 months leads us to suppose that adverse affects of overgrowth of algae were unlikely to occur in the future. Both species have thrived beneath dense kelp cover from at least 1968 up to the present at Boutilier’s Pt. in St. Margaret’s Bay, this being an area not subject to urchin grazing and therefore which had an algal cover during the whole of that period (see Mann, 1972; Bernstein et al., 1981). Similar to our results, Padilla (1984) found no change in the cover of coralline algae within herbivore exclusion cages over a nine month period, and within urchin removal areas over two years, relative to controls. Breitburg (1985) also reported that corallines established and grew on settling plates in the absence of herbivores, although cover of crusts was greater on grazed plates.

How widespread is the necessity of grazers for crust survival among corallines? There is much evidence to indicate that for many crustose corallines, there is no obligate requirement of herbivory for survival. Among crusts for which the surface structure has been examined, most have an unstable epithallium which is regularly sloughed (Table V). Species such as Clathromorphum circumscriptum (for which Steneck (1982) demonstrated a dependence on grazing by limpets) which have lost the ability to cleave surficial cells, clearly constitute a minority among corallines (see also Johansen, 1981). Morse & Morse (1984) have also noted that most coralline crusts slough surface layers, and suggested that it is this action that exposes chemical inducers for the settlement of invertebrate larvae.

Certainly coralline crusts do not require absolute protection from colonization by macroalgal epiphytes to remain viable. We have already mentioned the persistence for nearly two decades of extensive cover of Phymatolithon and Lithothamnium beneath a


dense canopy at Boutilier’s Pt. At other sites in St. Margaret’s Bay where dense kelp cover had been present for > 18 months, corallines covered 98 % of the hard substratum and the only areas of dead crusts were those directly beneath La~ina~a holdfasts

TABLE V

Incidence of sloughing of epithallial cells from the surface of coralline crusts

Species Epith~i~ sloughing Reference

Lithophylloideae Dermatolithon litorale Lithophyllum congestum Lithophyl~um incrustans Lithophy~um o~murai Lithophyl~m yessoense Lithophyllum sp. Pseudohthophyllum orbicatum

Mastophoroideae Neogoniolithon sp.

yes &meson (1982) yes Steneck & Adey (1976) Yes Giraud & Cabioch (1976) 3-s Ma&i et al. (1984) yes Masaki et al. (1981, 1984) yes Morse & Morse (1984) yes Adey (1966b)

IlO Masaki er al. (1984)

Melobesioideae Clathromo~hum ~ir~u~~~~rn Clathromorphum parcum Leptophytum laeve Lithothamnium coralloides Lithothamnium glaciale Lithothamn~~ japonicum L~hot~rnni~ ~eno~andii Li~othamnium sp. (Pacific) Lithothamnium spp. (in general) Neopolyporolithon reclinatum Phymatolithon laevigatum Phymatolithon lenormandi Phymatolithon rugulosum Phymato~hon spp. (in general)

ll0

IlO

9s yes yes yes yes yes Yes yes yes Yes Yes Yes

Adey (1973); Steneck (1982) Adey & Johansen (1972) Adey (1966~) Adey & McKibbon (1970) Morse & Morse (1984) Masaki er al. (1984) Giraud & Cabioch (1976) Morse & Morse (1984) Adey (1964) Adey & Johansen (1972) Adey (1964) Millson & Moss (1985) Adey (1964) Adey (1964; 1973)

(Johnson, 1984). On the south shore of Nova Scotia, coralline crusts thrive beneath dense and long-lived turfs of Chondm crispus (A.R.O. Chapman, pers. comm.). Indeed, the occurrence of extensive cover of healthy corallines (crusts and articulate forms) beneath dense stands of seaweeds in both the subtidal (Adey, 19&a, 1970 ; Adey eb al.,

1977; Moreno & Sutherland, 1982; Reed & Foster, 1984; Santelices & Ojeda, 1984a,b) and intertidal (Adey, 1966a,c; Littler, 1973; Adey & Vassar, 1975; Dayton, 1975; Adey et al., 1977; Southward & Southward, 1978; Ralfaelli, 1979; Ojeda & Santelices, 1984; Hawkins & Harkin, 1985), is widely documented. Of greater significance is that many intertidal corallines are obligate understorey species in that their survival depends on the presence of a dense overstratum of non-calcareous seaweeds (presumably to reduce the effects of desiccation), and therefore on the absence or only minimal levels of


herbivory. Several workers have found that when thick intertidal seaweed cover is removed, either artificially or by introducing grazers, understorey coralline species suffer extensive dieback (Dayton, 1975; Southard & Southward, 1978; Ojeda & Santelices, 1984; Hawkins & Harkin, 1985; Hawkins & Hartnoll, 1985).

That many coralline algae are adapted to low light intensities is also well established from bathymetric distribution surveys and physiological studies. Many crustose corallines grow at depths of 40-50 m and below (Johnson, 196 1; Adey, 1964, 1966a, 1971; Adey & MacIntyre, 1973; Lang, 1974; Sears & Cooper, 1978); verily the deepest macroalga recorded is a crustose coralline, which Littler et al. (1985) recently found growing in abundance on primary substratum at 268 m. Physiological studies have also shown that many coralline crusts can grow at low light levels (Adey, 1970, 1973; Littler, 1973 ; Adey & Vassar, 1975; Johansen, 198 l), and several have reported photoinhibition at moderate to high light intensities (Adey, 1970; Littler, 1973).

We contend then, that while the survival of some species of crustose corallines may depend on herbivores to prevent their overgrowth by fleshy seaweeds, many are able to survive in the absence of grazers by limiting fouling through sloughing of their epithallial cells, and in their ability to grow at relatively low light intensities. It seems that grazer dependence may apply to a small number of crust species that have lost the ability to slough their surlicial cells (e.g. Steneck, 1982), and in circumstances in which the rapid establishment and growth of dense algal turfs swamps the antifouling ability of corallines that are unable to grow at low light levels (e.g. Vine, 1974; Wanders, 1977; Paine, 1980).

Steneck (1983) argued that the frequent association of well developed coralline bottoms with areas of intensive herbivory and sparse macrophyte cover (e.g. Paine & Vadas, 1969; John & Pople, 1973; Branch, 1975; Dayton, 1975; Lawrence, 1975; Lubchenco, 1978; Brock, 1979; Vance, 1979; Ayling, 1981; Hay, 1981; Hagen, 1983; Hay et al., 1983; Himmelman et al., 1983; Littler & Littler, 1984; Masaki, 1984; Ojeda & Santelices, 1984; Breitburg, 1985), and the manifestation of morphological and anatomical features that afford crusts a high degree of resistance to grazing (e.g. Steneck, 1982, 1983; Steneck & Watling, 1982; Littler et al., 1983a,b; Littler 8z Littler, 1984; Padilla, 1984; Breitburg, 1985), signifies an ‘inextricable link’ of crust and herbivore. Paine (1980) considered the promotion by coralline algae of the settlement and metamorphosis of a variety of invertebrate grazers (e.g. Barnes & Gonor, 1973; Morse et al., 1979; Steneck, 1982; Rumrill & Cameron, 1983; Morse & Morse, 1984) as indicative of ‘positive interdependence’ of the two. We emphasize that the associations of crustose corallines with herbivores and the many adaptations of crusts to grazers, or even co-evolved mutualism between coralline and herbivore (see Paine, 1980; Steneck, 1982; Morse & Morse, 1984), does not exclusively infer or convey logical primacy to the hypothesis of grazer dependence. The associations of corallines with herbivores, their adaptations to withstand grazing, and their intrinsic antifouling ability are complementary in their effects in reducing overgrowth by other species. Moreover, in view of the spatial and temporal patchiness that is typical of herbivore populations,


a mechanism effective in reducing fouling in the absence of grazing is likely to be of considerable adaptive value and be favoured by natural selection. In summary, considering their high abundance worldwide, their interactions and associations with a diverse assemblage of invertebrate grazers, their ability to limit potential invertebrate competitors (Padilla, 1981; Breitburg, 1984) and their innate antifouling ability, crustose corallines amount to a guild of prominent ecological significance in shaping the structure of shallow hard-bottom communities.

ACKNOWLEDGEMENTS

We thank W. P. Young, J. Smith, B. Gill, S. F. Watts and J. Houston for diving and field assistance, C. Bird for help in identification of algae, C.A. Field for statistical advice, and C. Mason for preparing specimens for the S. E. M. A. R. 0. Chapman, I. A. McLaren and E. L. Mills provided useful criticism at all stages of the study, and the comments of two anonymous reviewers helped greatly to improve the manuscript. The work was supported by a Natural Sciences and Engineering Research Council Operating Grant awarded to K. H. M., and C. R. J. was supported by an Izaak Walton Killam Memorial Scholarship. This paper was written while C. R. J. was in receipt of a Visiting Fellowship from the Department of Fisheries and Oceans Canada at the

Bedford Institute of Oceanography.

REFERENCES

ADEY, W. H., 1964. The genus Phymatolithon in the Gulf of Maine. Hydrobiologia, Vol. 24, pp. 377-420. ADEY, W.H., 1966a. Distribution of saxicolous crustose corallines in the northwestern north Atlantic. J.

Phycol., Vol. 2, pp. 49-54. ADEY, W.H., 1966b. The genus Pseudolithophyllum (Corallinaceae) in the Gulf of Maine. Hydrobiologia,

Vol. 27, pp. 479-497. ADEY, W. H., 1966~. The genera Lithothamnium, Leptophylum (nov. gen.) and Phymatolithon in the Gulf of

Maine. Hydrobiologia, Vol. 28, pp. 321-370. ADEY, W.H., 1970. The effects of light and temperature on growth rates in boreal-subarctic crustose

corallines. J. Phycol., Vol. 6, pp. 269-276. ADEY, W. H., 1971. The sublittoral distribution of crustose corallines on the Norwegian coast. Sarsiu,

Vol. 46, pp. 41-58. ADEY, W.H., 1973. Temperature control of reproduction and productivity in a subarctic coralline alga.

Phycologia, Vol. 12, pp. 11 l-l 18. ADEY, W. H. & H. W. JOHANSEN, 1972. Morphology and taxonomy ofCorallinaceae with special reference to Clathromorphum, Mesophyllum, and Neopolyporolithon gen. nov. (Rhodophyceae, Cryptonemiales), Phycologia, Vol. 11, pp. 159-180. ADEY, W. H. & I.G. MACINTYRE, 1973. Crustose coralline algae: are-evaluation in the geological sciences,

Geol. Sot. Am. Bull., Vol. 84, pp. 883-904. ADEY, W.H. & D. L. MCKIBBON, 1970. Studies on the maerl species Phymatolithon calcareum (Pallas) nov.

comb. and Lithothamnium corulloides Crouan in the Ria de Vigo. Bot. Mar., Vol. 13, pp. 100-106. ADEY, W. H. & J. M. VASSAR, 1975. Colonization, succession and growth rates of tropical crustose coralline

algae (Rhodophyta, Cryptonemiales). Phycologia, Vol. 14, pp. 55-69. ADEY, W.H., P.J. ADEY, R. BURKE & L. KAUFMAN, 1977. The Holocene reef systems of eastern

Martinique, French West Indies. Atoll Res. Bull., No. 218, pp. I-40.


AYLING, A.M., 1981. The role of biological disturbance in temperate subtidal encrusting communities. Ecology, Vol. 62, pp. 830-847.

BARNES, J. R. & J. J. GONOR, 1973. The larval settling response of the lined chiton Tonicella lineata. Mar. Biol., Vol. 20, pp. 259-264.

BERNSTEIN, B.B., B.E. WILLIAMS & K.H. MANN, 1981. The role of behavioral responses to predators in modifying urchins’ (Strongylocentrotus droebachiensb) destructive grazing and seasonal foraging patterns. Mar. Biol., Vol. 63, pp. 39-49.

BOROW~TZKA, M.A. & A.W.D. LARKUM, 1977. Calcification in the green alga Halimeda. I. An ultrastructural study of thallus development. J. Phycol., Vol. 13, pp. 6-16.

BOROWITZKA, M.A. & M. VESK, 1978. Ultrastructure of the Corallinaceae. I. The vegetative cells of Corallina officinalis and C. cuvierii. Mar. Biol., Vol. 46, pp. 295-304.

BRANCH, G.M., 1975. Intraspecific competition in Patella cochlear Born. J. Anim. Ecol., Vol. 44, pp. 263-281.

BREITBURG, D.L., 1984. Residual effects of grazing: inhibition of competitor recruitment by encrusting coralline algae. Ecology, Vol. 65, pp. 1136-l 143.

BREITBURG, D.L., 1985. Development of a subtidal epibenthic community: factors affecting species composition and the mechanisms of succession. Oecologia (Berlin), Vol. 65, pp. 173-184.

BROCK, R. E., 1979. An experimental study on the effects of grazing by parrotfishes and role of refuges in benthic community structure. Mar. Biol., Vol. 51, pp. 381-388.

DAYTON, P.K., 1975. Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecol. Monogr., Vol. 45, pp. 137-159.

FILION-MYKLEBUST, CC. & T.A. NORTON, 1981. Epidermis shedding in the brown seaweed Ascophyllum nodosum (L.) Le Jolis. Mar. Biol. Letters, Vol. 2, pp. 45-51.

FOSTER, M. S., 1975. Regulation of algal community development in aMacrocystispyr$ra forest. Mar. Biol., Vol. 32, pp. 331-342.

GIRAUD, G. & J. CABIOCH, 1976. Etude ultrastructurale de l’activite des cellules superficielles du thalle des Corallinactes (Rhodophycees). Phycologiu, Vol. 15, pp. 405-414.

HAGEN, N.T., 1983. Destructive grazing of kelp beds by sea urchins in Vestljorden, northern Norway. Sarsia, Vol. 68, pp. 177-190.

HARLIN, M.M. & J.M. LINDBERG, 1977. Selection of substrata by seaweeds: optimal surface relief. Mar. Biol., Vol. 40, pp. 33-40.

HAWKINS, S.J. & E. HARKIN, 1985. Preliminary canopy removal experiments in algal dominated communities low on the shore and in the shallow subtidal on the Isle of Man. Bot. Mar., Vol. 28, pp. 223-230.

HAWKINS, S. J. & R.G. HARTNOLL, 1985. Factors determining the upper limits of intertidal canopy-forming algae. Mar. Ecol. Prog. Ser., Vol. 20, pp. 265-271.

HAY, M. E., 1981. Herbivory, algal distribution, and the maintenance of between-habitat diversity on a tropical fringing reef. Am. Nat., Vol. 118, pp. 520-540.

HAY, M. E., T. COLBURN & D. DOWNING, 1983. Spatial and temporal patterns in herbivory on a Caribbean fringing reef: the effects on plant distribution. Oecologia (Berlin), Vol. 58, pp. 299-308.

HIMMELMAN, J.H., A. CARDINAL & E. BOURGET, 1983. Community development following removal of urchins, Strongylocentrotus droebachiensti, from the rocky subtidal zone of the St. Lawrence estuary, eastern Canada. Oecologiu (Berlin), Vol. 59, pp. 27-39.

JAGELS, R., 1973. Studies of a marine grass, Thalussiu testudinum. I. Ultrastructure of the osmoregulatory leaf cells. Am. J. Bot., Vol. 60, pp. 1003-1009.

JOHANSEN, H.W., 1981. Coralline algae, afirst synthesis. CRC Press, Boca Raton, 239 pp. JOHN, D.M. & W. POPLE, 1973. The fish grazing of rocky shore algae in the Gulf of Guinea. J. Exp. Mar.

Biol. Ecol., Vol. 11, pp. 81-90. JOHNSON, C. R., 1984. Ecology ofthe kelp Laminariu longicrurfs and its principal grazers in the rocky subtidal

of Nova Scotia. Ph.D. dissertation, Dalhousie University, Halifax, Nova Scotia, Canada, 280 pp. JOHNSON, J. H., 1961. Limestone-building algae and algal limestones. Colarado School of Mines, Colarado,

297 pp. JONES, G. M., 1985. Parumoeba invadens II. sp. (Amoebida, Paramoebidae), a pathogenic amoeba from the

sea urchin Strongylocentrotus droebachiensir in eastern Canada. J. Prorozool., Vol. 32, pp. 564-569. JONES, G.M. & R.E. SCHEIBLING, 1985. Paramoeba sp. (Amoebida, Paramoebidae) as the possible

causative agent of sea urchin mass mortality in Nova Scotia. J. Parasirol., Vol. 71, pp. 559-565.


JONES, G. M., A. J. HEBDA, R. E. SCHEIBLING & R. J. MILLER, 1985. Histopathology of the disease causing mass mortality of sea urchins (Strongylocentrotus droebachiensis) in Nova Scotia. J. Invertebr. Pathol., Vol. 45, pp. 260-271.

KARNOVSKY, M. J., 1965. A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J. Cell Biol., Vol. 27, p. 137A.

LANG, J.C., 1974. Biological zonation at the base of a reef. Am. Sci., Vol. 62, pp. 272-281. LAWRENCE, J.M., 1975. On the relationships between marine plants and sea urchins. Oceanogr. Mar. Biol.

Annu. Rev., Vol. 13, pp. 213-286. LEGENDRE, L. & P. LEGENDRE, 1983. Numerical ecology. Developments in environmental monitoring, Vol. 3.

Elsevier Scientific Publishing Co., Amsterdam, 419 pp. LITTLER, M.M., 1973. The population and community structure of Hawaiian fringing-reef crustose

Corallinaceae (Rhodophyta, Cryptonemiales). J. Exp. Mar. Biol. Ecol., Vol. 11, pp. 103-120. LITTLER, M.M. & M. S. Don, 1975. Ecological components structuring the seaward edges of tropical

Pacific reefs: the distribution, communities and productivity ofPorolithon. J. Ecol., Vol. 63, pp. 117-129. LI~LER, M. M. & D. S. LITTLER, 1984. Models of tropical reef biogenesis: the contributions of algae. Prog.

Phycol. Res., Vol. 3, pp. 323-364. LITTLER, M. M., D. S. LITTLER & P.R. TAYLOR, 1983a. Evolutionary strategies in a tropical barrier reef

system: functional-form groups of marine macroalgae. J. Phycol., Vol. 19, pp. 229-237. LITTLER, M. M., P.R. TAYLOR & D. S. LITTLER, 1983b. Algal resistance to herbivory on a Caribbean Barrier

Reef. Coral Reefs, Vol. 2, pp. 11 l-l 18. LITTLER, M.M., D. S. LITTLER, S.M. BLAIR & J.N. NORRIS, 1985. Deepest known plant life found on an

uncharted seamount. Science, Vol. 227, pp. 57-59. LUBCHENCO, J., 1978. Plant species diversity in a marine intertidal community: importance of herbivore

food preference and algal competitive abilities. Am. Nat., Vol. 112, pp. 23-39. MANN, K.H., 1972. Ecological energetics of the seaweed zone in a marine bay on the Atlantic coast of

Canada. 1. Zonation and biomass of seaweeds. Mar. Biol., Vol. 12, pp. l-10. MASAKI, T., D. FUJITA & H. AKIOKA, 1981. Observation on the spore germination of Laminaria japonica

on Lithophyhum yessoense (Rhodophyta, Corallinaceae) in culture. Bull. Fat. Fish., Hokkaido Univ., Vol. 32, pp. 349-356.

MASAKI, T., D. FUJITA & N.T. HAGEN, 1984. The surface ultrastructure and epithallium shedding of crustose coralline algae in an ‘Isoyake’ area of southwestern Hokkaido, Japan. Hydrobiologia, Vol. 116, 117, pp. 218-223.

MILLER, R. J., 1985. Succession in sea urchin and seaweed abundance in Nova Scotia, Canada. Mar. Biol., Vol. 84, pp. 275-286.

MILLER, R. J. & A. G. COLODEY, 1983. Widespread mass mortality of the green sea urchin in Nova Scotia, Canada. Mar. Biol., Vol. 73, pp. 263-267.

MILLSON, C. & B.L. MOSS, 1985. Ultrastructure of the vegetative thallus of Phymatolithon lenormandii (Aresch. in J. Ag.) Adey. Bot. Mar., Vol. 28, pp. 123-132.

MOORE, D. S. & R. J. MILLER, 1983. Recovery ofmacroalgae following widespread sea urchin mortality with a description of the nearshore hard-bottom habitat on the Atlantic coast of Nova Scotia. Can. Tech. Rep. Fish. Aquat. Sci., No. 1230, 94 pp.

MORENO, C. A. & J.P. SUTHERLAND, 1982. Physical and biological processes in a Macrocystis pyrifera community near Valdivia, Chile. Oecologia (Berlin), Vol. 55, pp. l-6.

MORSE, A.N.C. & D.E. MORSE, 1984. Recruitment and metamorphosis of Haliotis larvae induced by molecules uniquely available at the surfaces of crustose red algae. J. Exp. Mar. Biol. Ecol., Vol. 75, pp. 191-215.

MORSE, D.E., N. HOOKER, H. DUNCAN & L. JENSEN, 1979. y_Aminobutyric acid, a neurotransmitter, induces planktonic abalone to settle and begin metamorphosis. Science, Vol. 204, pp. 407-410.

MOSS, B. L., 1982. The control of epiphytes by Halidrys siliquosa (L.) Lyngb. (Phaeophyta, Cystoseiraceae). Phycologia, Vol. 21, pp. 185-188.

OJEDA, F. P. & B. SANTELICES, 1984. Ecological dominance of Lessonia nigrescens (Phaeophyta) in central Chile. Mar. Ecol. Prog. Ser., Vol. 19, pp. 83-91.

PADILLA, D. K., 1981. Selective agents influencing the morphology of coralline algae. M. SC. dissertation, Oregon State University, Corvallis, Oregon, U.S.A., 80 pp.

PADILLA, D. K., 1984. The importance of form: differences in competitive ability, resistance to consumers and environmental stress in an assemblage of coralline algae. J. Exp. Mar. Biol. Ecol., Vol. 79, pp. 105-127.


PAINE, R.T., 1980. Food webs: linkage, interaction strength and community infrastructure. J. Anim. Ecol., Vol. 49, pp. 667-685.

PAINE, R. T. & R. L. VADAS, 1969. The effects of grazing by sea urchins, Strongylocentrofus spp., on benthic algal populations. Limnol. Oceanogr., Vol. 14, pp. 710-719.

PIELOU, E. C., 1978. Population and community ecology:principles and methods. Gordon & Breach, New York, 424 pp.

PRESS, S. J., 1972. Applied multivariate analysis. Holt, Rinehart & Winston, New York, 521 pp. RAFFAELLI, D., 1979. The grazer-algae interaction in the intertidal zone on New Zealand rocky shores.

J. Exp. Mar. Biol. Ecol., Vol. 38, pp. 81-100. REED, D. C. & M. S. FOSTER, 1984. The effects of canopy shading on algal recruitment and growth in a giant

kelp forest. Ecology, Vol. 65, pp. 937-948. RUMRILL, S. S. & R. A. CAMERON, 1983. Effects of gamma-aminobutyric acid on the settlement of larvae

of the black chiton Kathanna tunicata. Mar. Biol., Vol. 72, pp. 243-247. RUSSELL, G. & C. J. VELTKAMP, 1984. Epiphyte survival on skin-shedding macrophytes. Mar. Ecol. Prog.

Ser., Vol. 18, pp. 149-153. SANTELICES, B. & F.P. OJEDA, 1984a. Effects of canopy removal on the understory algal community

structure of coastal forests of Macrocysris pyriferu from southern South America. Mar. Ecol. Prog. Ser., Vol. 14, pp. 165-173.

SANTELICES, B. & F.P. OJEDA, 1984b. Population dynamics of coastal forests of Macrocystis pyriferu in Puerto Toro, Isla Navarino, Southern Chile. Mar. Ecol. Prog. Ser., Vol. 14, pp. 175-183.

SCHEIBLING, R. E. & R. L. STEPHENSON, 1984. Mass mortality of Strongylocentrotus droebachiensis (Echinodermata : Echinoidea) off Nova Scotia, Canada. Mar. Biol., Vol. 78, pp. 153-164.

SEARS, J.R. & R.A. COOPER, 1978. Descriptive ecology of offshore, deep-water, benthic algae in the temperate western North Atlantic Ocean. Mar. Biol., Vol. 44, pp. 309-314.

SIEBURTH, J. M. & J. L. TOOTLE, 1981. Seasonality of microbial fouling on Ascophyllum nodosum (L.) Lejol., Fucus vesiculosus L., Polysiphonia lanosa (L.) Tandy and Chondrus crispus Stackh. J. Phycol., Vol. 17, pp. 57-64.

SOUTH, G.R. & R.G. HOOPER, 1980. A catalogue and atlas of the benthic marine algae of the island of Newfoundland. Memorial Univ. Newfoundland Oct. Pap. Biol., No. 3, 136 pp.

SOUTHWARD, A. J. & E. C. SOUTHWARD, 1978. Recolonization of rocky shores in Cornwall after use of toxic dispersants to clean up the Torrey Canyon spill. J. Fish. Res. Board Can., Vol. 35, pp. 682-706.

STENECK, R. S., 1982. A limpet-coralline alga association: adaptations and defenses between a selective herbivore and its prey. Ecology, Vol. 63, pp. 507-522.

STENECK, R.S., 1983. Escalating herbivory and resulting adaptive trends in calcareous algal crusts. Paleobiology, Vol. 9, pp. 44-61.

STENECK, R. S. & W. H. ADEY, 1976. The role of environment in control of morphology in Lithophyllum congesturn, a Caribbean algal ridge builder. Bo?. Mar., Vol. 19, pp. 197-215.

STENECK, R.S. & L. WATLING, 1982. Feeding capabilities and limitations of herbivorous molluscs: a functional group approach. Mar. Biol., Vol. 68, pp. 299-319.

SUNESON, S., 1982. The culture of bisporangial plants of Dermatolirhon litorale (Suneson) Hamel et Lemoine (Rhodophyta, Corallinaceae). Br. Phycol. J., Vol. 17, pp. 107-I 16.

VANCE, R. R., 1979. Effects of grazing by the sea urchin, Centrostephanus coronatus, on prey community composition. Ecology, Vol. 60, pp. 537-546.

VINE, P.J., 1974. Effects of algal grazing and aggressive behaviour of the fishes Pomacentna lividus and Acanthurus sohal on coral-reef ecology. Mar. Biol., Vol. 24, pp. 131-136.

WANDERS, J. B. W., 1977. The role of benthic algae in the shallow reef of Curacao (Netherlands Antilles) III: the significance of grazing. Aqua?. Bat., Vol. 3, pp. 357-390.

the crustose coralline alga, phymatolzthon foslie ......growing fleshy algae. it is of interest to...

Documents