Short-term effects of sessile organisms on colonization of intertidal boulders

J. Exp. Mar. Biol. Ecol., 1988, Vol. 116, pp. 159-175

159

Elsevier

JEM 001033

Short-term

effects of sessile organisms intertidal boulders

on colonization

of

Keith A. McGuinness Institute of Marine Ecology, University of Sydney, Sydney, New South Wales, Australia

(Received 10 July 1987; revision received 19 November 1987; accepted 7 December 1987) Abstract: This study examined how the sessile organisms on boulders (algae on the tops; polychaetes, bryozoans, ascidians, and sponges on the undersides) influenced the rates of colonization of other species. Experiments showed that the sessile organisms occupying space on the undersides of boulders reduced the rate at which other sessile species recruited. This was true for rocks in their normal orientation and for those which had been experimentally overturned and disturbed. This preemption of space reduced diversity on the undersides of boulders low on the shore where space was in short supply. Grazers and predators (primarily molluscs) moved more quickly onto rocks with sessile organisms than onto those without and the rate of recolonization also varied with rock size. Thus, observed patterns in number and abundance of species with rock size were at least partially due to selection among rocks by these species. High on the shore rocks of medium size (300-600 cm’ in surface area) had more species. This pattern is often explained by the intermediate disturbance model (as the result of the interaction of disturbance and competition) but here it resulted from selective colonization of different sized rocks. Overall, the sessile organisms on boulders influenced their colonization by other species. This influence is important since these communities are often disturbed and frequently recovering from disturbance. Key words: Colonization;

Disturbance;

Intertidal boulder; Mobile organism; Preemptive competition;

Sessile organism

INTRODUCTION

Considerable attention has been given to the ways in which the organisms in a place affect the arrival and/or survival of other individuals (e.g., Connell & Slatyer, 1977; Sousa, 1979a; Green & Schoener, 1982; Turner, 1983; Johnson & Mann, 1986). The results of such interactions have various consequences for the rates and nature of changes within the community (Sutherland, 1974; Connell & Slatyer, 1977; Jackson, 1977; Green & Schoener, 1982; Connell & Keough, 1983). Sequential nonseasonal changes within an assemblage are generally referred to as succession and three mechanisms for such changes have been suggested - facilitation, tolerance, and inhibition (Connell & Slatyer, 1977). Inhibition - also called preemptive competition (Underwood & Denley, 1984) - has been shown for many sessile communities on marine hard substrata (e.g., Dayton, 1971; Denley & Underwood, 1979; Sousa, 1979a; Turner, Correspondence address: K.A. McGuinness, Institute of Marine Ecology, Zoology Building, A08, University of Sydney, Sydney, New South Wales 2006, Australia. 0022-0981/88/%03.50 0 1988 Elsevier Science Publishers B.V. (Biomedical Division)

160

K.A.

McGUINNESS

1983 ; see Underwood & Denley, 1984). Instances of facilitation, where the organisms present aid the recruitment of others, are also known (e.g., Dayton, 1971; Gallagher et al, 1983). These processes are usually studied within a group of sessile species but such interactions may also occur between sessile and mobile species. For example, the colonization of parts of rocky shores by grazers may be facilitated by the presence of algae as food (Underwood, 1979), though the movements of grazing molluscs may also be hindered by foliose macroalgae {Underwood & Jernakoff, 1981; Fletcher, 1984). Many communities are frequently affected by physical disturbances which damage or kill organisms and free resources within the community (Connell, 1978; Sousa, 1984). Since these communities are often recovering from recent disturbances the process of recolonization is of particular importance; the rate of recovery will be a function of the extent to which organisms remaining inhibit or facilitate the recruitment of other individu~s (Connell & Slatyer, 1977). This is clearly the case for communities on intertidal boulders. These are continually disturbed by physical factors - such as sand and waves - which dislodge, damage, or kill mobile and sessile organisms (Sousa, 1979a,b; Lieberman et al, 1984; McGuinness, 1987b). The aim of this study was to determine the effects of the sessile species on boulders on the rate of colonization by other organisms. I sought answers to the following three questions. First, would the sessile species already present on the upper and lower sides of a boulder reduce the rate at which others recruited to that surface? Second, would the species characteristic of one side of the boulder after overturning alter the rate of recruitment of species characteristic of the other side? For example, after a boulder was overturned, would the algae characteristic of its (previously) upper surface affect the subsequent r~rui~ent of sessile animals to the underside? [Other workers have discussed the effects of overturning rocks without considering whether the space is immediately available for settlement (e.g., Osman, 1977; Sousa, 1979a,b).] Finally, would the colonization of a boulder by mobile forms - grazers and predators - be influenced by the sessile species present? This info~ation is needed to underst~d how the different processes which affect the organisms on these boulders (e.g., disturbance, habitat structure, grazing; see McGuinness, 1987a,b; McGuinness & Underwood, 1986) interact to determine the observed community structure. Further, these interactions are important for a general understanding of the role of disturbance and subsequent recolonization in natural communities.

METHODS STUDY

SITES

Boulder fields on two shores were studied, Cape Banks and Long Reef. Both were on the southeastern coast of Australia near Sydney, New South Wales, and are described elsewhere (McGuinness, 1984, 1987a; McGuinness & Underwood, 1987).

COLONIZATION

OF BOULDERS

161

Briefly, each shore had two boulder fields separated by an expanse of platform free of rocks. One of these fields was low on the shore (0.2-0.3 m above MLW) and the other higher (0.6-0.9 m above MLW); these will be referred to as the “low-shore” and “high-shore” areas, respectively. The boulders studied were usually in the size range 20-1500 cm2 in upper surface area. They were oval in plan view and were flattened so that upper and lower surfaces could always be distinguished. There are few seasonal patterns in the disturbance or colonization [with the major exception of the tube-worm Gale~laria cues~itosfl Savigny (O’Donnell, 1986)] of these boulders (McGuinness, 1987a; see also underwood, 1980; Jemakoff, 19X5), so experiments were started when convenient. The experiments done were short-term (ranging in duration from 3 wk to 3 months) but this is realistic given that many rocks on these shores are disturbed three to four times a year (McGuinness 1987a). In fact, experiments were concluded as soon as any of the rocks used were disturbed. PREEMPTION

BEFORE OVERTURNING

The effects of the organisms occupying space on the colonization of other species were examined in two similar experiments. The first examined the effects of macroalgae on the recruitment of species to the tops of rocks using large rocks (size > 2000 cm2) with nearly complete cover (> 95 %) of one or other of the two major occupants of space in the low-shore area - a foliose species, Polysiphonia sp., and an encrusting species, Ra&kia sp. (MeGuinness, 1987a). On each boulder, I cleared three small (2 x 2 cm) and three large (4 x 4 cm) patches. Three undisturbed control patches of each size were also randomly placed on each of the boulders (marked as described below). Altogether there were six boulders; three with Ralfsia and three with Polysiphonia. In addition, to control for the effects of the scraping itself, I also scraped patches on three initially bare rocks, brought down from above the high-water mark. A comparison of scraped and unscraped patches on these bare rocks provided a partial test of whether or not scraping altered the surface of the rock in a way that affected the recruitment of organisms (also see Discussion). The second expe~ment tested whether bryozoans and spirorbids - major occup~ts of space underneath boulders - affected recruitment to the undersides. Three replicate rocks (size > 2000 cm’) with a large number of colonies of the bryozoan VaZdemunitella valdemunita (Banta) and great cover of spirorbids were found (the spirorbids were a complex of two species - Janua pseudocorrugata Bush and Pileolaria pseudomilitaris Thiriot-Quievreux - indistinguishable in the field). On each replicate rock three patches were cleared in bryozoan colonies and three others cleared amongst the spirorbids (the two treatments could be placed on the same rocks because both species were abund~t together). Only small patches (2 x 2 cm) were created because colonies were not big enough for large patches to be cleared. Control undisturbed patches were marked on randomly selected colonies on the same boulders. In all cases, the cover of a patch before clearing was > 90 %. As before, patches were scraped on the undersides of bare rocks as partial controls for scraping.

162

K. A. McGUINNESS

The rocks were photographed at the start of the experiment (7 October 1983) and the positions of the various patches were marked on scale maps drawn from these photographs. Undisturbed (i.e., uncleared) control patches were also marked on the maps at this time. I used these maps to locate and sample the patches at later times. This method avoided having to mark the rocks and possibly disturb the organisms. These experiments were done in the low-shore area at Long Reef because the species examined were most abundant on this shore (McGuinness, 1987a) and recruitment was greater low on the shore (McGuinness, unpubl. data). Large boulders were used in order to minimize disturbance by waves and sand. PREEMPTION AFTER OVERTURNING

The aim of this experiment was to test the hypothesis that the organisms present on one side of the rock would, after being overturned, retard the recruitment of the species typical of the other side. Accordingly, I found eight large rocks (Z 1000 cm2) with great (> 90%) cover of algae on the upper surface (predominantly Ralfsia, PoIysiphonia, and the crust Hildenbrandia prototypus Nardo) and sessile animals on the lower surface (primarily the spirorbids, bryozoans, and the sponges Baja/us sp. and Trachyopsis halichondroides). One half of each surface of four of these rocks was scraped clear of organisms (half-cleared rocks). Each of the half-cleared rocks was photographed and overturned. The other four rocks were simply photographed and overturned. These were controls to determine whether I damaged the organisms on the nominally untouched half of the manipulated rocks in the process of scraping the other half. If there was no damage, there would be similar recruitment to the unscraped halves of both half-cleared and control rocks (note that I was only interested in disturbance to the existing organisms which altered their resistance to recruitment by other individuals). As in the previous experiment, bare rocks from above the high-water mark, each with half of the upper and lower surfaces scraped, were used to determine whether the surface was altered in any biologically significant fashion. Recruiting organisms were counted in five replicate randomly placed 4 :X4-cm quadrats in each half of the top and bottom of the boulder (a total of 20 quadrats per boulder). This experiment was also done in the low-shore area, started on 20 September 1983 and done at Cape Banks for convenience. The rocks in this experiment were smaller than those in the previous experiment because few manageable rocks with a surface area of z 2000 cm2 were present at Cape Banks (the different sizes are unimportant because the abundance of species, and the disturbance of rocks, reach an asymptote at a rock size of z 800-1200 cm2; McGuinness, 1987a). This and previous experiments were designed to have both cleared and uncleared patches on the same boulder. Because recruitment varies greatly among boulders (McGuinness, 1987b), this design leads to a more powerful test of the effects of clearing than one in which the treatments are on different boulders.

COLONIZATION RECOLONIZATION

OF BOULDERS

163

OF BOULDERS BY MOBILE SPECIES

The aims of this experiment were to determine the rate at which grazers and predators colonized cleared boulders and whether this was in~uen~ed by the presence of sessile organisms. Three treatments were used: control rocks, which were not disturbed (other than when sampling); cleared rocks, which had all mobile organisms removed from them; and bare rocks, which were brought into the area from above the high-water mark and intermingled with the other boulders. (Note that the bare rocks may differ from the control and cleared rocks for reasons other than the absence of sessile organisms; see Discussion.) Earlier work suggested that the response of the mobile species might depend on rock size (McGuinness, 1987a,b), so within each of the three treatments there were four replicate rocks of three sizes: small (mean surface area = 100 cm2, SE = 6) medium (mean surface area = 365 cm2, SE = 15) and large (mean surface area = 866 cm2, SE = 43). The experiment was done in the high- and low-shore areas at Cape Banks - the boulder fields where grazers and predators were most abundant - and started on 5 September 1983. After 1, 3, and 18 days, the numbers of all the mobile species were recorded. In addition, I estimated the percentage of the underside of each boulder that was buried in sand (methods in McGuinness, 1987a) to determine whether rocks in all treatments rested on the substratum in a comparable fashion and allowed similar access to organisms. STATISTICAL ANALYSES

The results of experiments were analysed by appropriate ANOVAs (Wirier, 1971) with a significance level (a) of 0.05. Data were transfo~ed as lnfx + 1) when Cochran’s test indicated that vari-iances were heterogeneous (Winer, 197 1). If variances remained heterogeneous at the 0.05 level but not at the 0.01 level, then the smaller value of cI(0.01) was used forF tests, following Underwood (1981). Student-Newm~-Keuls (S-N-K) tests were used after the ANOVA to compare means, at the significance level used for the F tests (0.05 or 0.01). All factors in analyses were fixed except the replicate rocks used in experiments which, since they were randomly selected from those available, were a random factor (Winer, 1971). Further, except for the last experiment, the “rocks” factor was nested within other treatments (see tables of analyses for details).

RESULTS PREEMPTION

BEFORE OVERTURNING

There was no colonization by sessile species on the tops of rocks in either cleared or control patches by the end of this experiment (55 days), though small amounts of the foliose macroalga Ulva lactuca L. had arrived elsewhere (i.e., outside the cleared patches). The only change to occur was the slow closing of the cleared patches by ingrowth of the algae from the edges.

K.A. McGUINNESS

164

Three sessile species did recruit to patches on the undersides of the rocks - the spirorbids, Galeolaria, and the barnacle Tetraclitellapurpurascens (Wood) - but only the spirorbids were abundant enough for analysis. It was impossible to distinguish new spirorbids from those already present, so recruitment was inferred from increases in abundance by subtracting the number initially present from counts at later times. There were similar numbers of spirorbids in cleared and control patches on bare rocks at the two times sampled, indicating that scraping did not alter, either favourably or unfavourably, the surface of the rock (Fig. 1; scraped vs. unscraped within bare rocks

~

9

BP

27 DAYS

M

Iir SP

BP

BA

55 DAYS

Fig. I. Mean number of spirorbids . cm-’ recruiting to patches in spirorbids (SP), in bryozoans (BR), and on bare rocks (BA) after 27 and 55 days (+ SE): D , scraped patches; 0 , control (unscraped patches).

factor in Table I). In contrast, there was greater recruitment into patches cleared within either bryozoan colonies or spirorbids than into control patches (Fig. 1; scraped vs. unscraped within occupied rocks factor in Table I). By 55 days, the location of the cleared patch affected the number of spirorbids settling (bryozoan vs. spirorbid factor in Table I). There was greatest recruitment into patches cleared amongst other sp~orbids, few individu~s recruited on bare rocks, and rec~itment into patches in bryozoan colonies was intermediate between these extremes (Fig. 1). PREEMPTION

AFTER

OVERTURNING

As in the previous experiment, the only colonization of the tops of rocks was by a small amount of Ulva; again, this was too little for analysis. Furthermore, only one sessile animal, Galeolaria, recruited to the undersides of rocks. At neither 45 days

COLONIZATION

165

OF BOULDERS

TABLE I ANOVAs on the number of spirorbids recruiting to patches on the undersides of boulders: bare refers to patches on bare rocks and occupied to patches within bryozoans or spirorbids. There were three scraped and three unscraped (control) patches on each of three boulders (note that patches within bryozoans and spirorbids were on the same rock). The table shows the significance of each factor and the percentage of the total variation attributable to it; the total sum of squares is given in parentheses at the foot of the table (total). Data were transformed as ln(x + 1) to stabilize variances (homogeneous by Cochran’s test). In this and ah following tables: NS = non significant, *Pi 0.05, **P < 0.01, ***P < 0.001. Source

df

Among all cells Bare vs. occupied rocks Within bare rocks Scraped vs. unscraped (SC) Replicate rocks SC x R Within occupied rocks Bryozoan vs. spirorbid (B/S) Scraped vs. unscraped (SC) Replicate rocks B/S x SC B/S x R SC x R B/S x SC x R Residual Total

(phmned comparison

Percentage of variation

17 1 5

27 days

55 days

74.5*** 35.1***

65.1*** 9.8***

1 2 2

0.0 NS 5.89 0.8 NS

1 1 2 1 2 2 2

2.2 NS Is.!%*** SO** 0.0 NS 1.5 NS 0.1 NS 2.5 NS

0.5

NS

26.2*+* 0.3 NS

11

36 53

25.5 100.0 (76.45)

6.0* 19.2*** 1.5 NS 0.0

NS

0.5 NS 1.6 NS 0.1

NS

34.3 100.0 (91.24)

I: = 0.07, df = 1, 9, NS) nor 76 days (planned comparison

F = 0.92, df = 1, 60, NS), was there a difference in recruitment between either half of

the control rocks and the unscraped portion of the half-cleared rocks; thus, there was no damage to the organisms on the unscraped half during scraping the other half. There were no effects of clearing space at 45 days, though there were si~i~~~t differences among rocks in the intensity of recruitment (rocks within control rocks factor in Table II). Clearing did, however, have an effect after 76 days (B/H x S/U within manipulated rocks factor in Table II) with more worms recruiting to the cleared half of the half-cleared boulders (S-N-K tests on means in Fig. 2). These differences were apparently simply due to the preemption of space, since the worms recruiting to control boulders were on bare space amongst the algae. There was also greater recruitment to the unscraped half of the bare rocks (S-N-K tests on means in Fig. 2). Thus there was potentially an artifact due to scraping but, since this reduced recruitment, the results remain valid.

166

K. A. McGUINNESS TABLE II

ANOVAs on the number of Guledaria recruiting to the undersides of boulders after overturning: control

refers to uncleared rocks; type refers to either bare or ham-cleared rocks (co~ectiveiy calfed others). Five patches were sampled on each of the four control, bare, and half-cleared rocks. One rock was lost from each of these groups part way through the experiment reducing the df for some sources of variation at 76 days (indicated by /). Data were transformed as In(x + 1) to stabilize variances (homogeneous by Cohran’s test). Format as for Table I. Source

df

Percentage of variation 45 days

Among all cells Control vs. other rocks Within control rocks Rocks (R) Within m~ip~ated rocks Bare vs. half-cleared (B/H) Scraped vs. unscraped (S/U) Rocks (nested in B/H) B/H x S/W S/U x rocks Residual Total

19

76 days

49.9*** I

0.0

34.5*** 6.5*

NS

3 3

12.s***

1.8 NS

1 1 614 1 614

3.6 NS 1.5 NS 24.-l*** 0.3 NS 7.0 NS

1.6 NS 0.6 NS 7.6 NS

IS/l1

80160 99174

45 DAYS

50.1 lOO.0(39.61)

I_ BA

-76

”

iYS

13.3

NS

3.1

NS

65.5 loo.0 (28.17)

BA

Fig. 2. The density of Gale&r& (mean number .crn-’ + SE) on the new underside of experimentally overturned boulders: C were control boulders overturned but with existing organisms left attached (thus there were two unscraped halves); SC were boulders which had one half of the upper and lower surfaces cleared of organisms (by scraping); and BA were bare boulders from above the high-water mark which also had one half of each surface scraped.

COLONIZATION RECOLONIZATION

161

OF BOULDERS

OF MOBILE SPECIES

Analyses of the percentage of the undersides of the rocks buried in sand showed that, while there was a difference among treatments after 1 day (bare = 6%, defaunated = 302, control = 33 %), this disappeared by 3 days (overall mean = 11%) indicating that by this time the imported bare rocks were resting on the substratum in the same way as other rocks in the area (Table III). Accordingly, results of S-N-K tests are only presented for 3 and 18 days.

TABLE III Results of ANOVAs ofthe percentage ofthe undersides of rocks in removal experiment treatments (control, cleared, bare rocks) buried in sand after 1 and 3 days. Data at 3 days were transformed as ln(x + 1) to stabilize variances (homogeneous by Cochran’s test). Source

Treatment (T) Area (A) Size (S) TxA TxS AxS TxAxS Residual Total

df

2 1 2 2 4 2 4 54 71

Percentage of variation 1 day

3 days

12.1* 0.3 NS 12.4* 4.8 NS 2.9 NS 0.8 NS 1.9 NS 64.8 100.0 (87045)

1.2 NS 19.2*** 12.7*** 1.2 NS 2.5 NS 12.7*** 2.5 NS 48.0 100.0 (171.2)

Grazers quickly colonized the boulders in this experiment, though significant differences among some treatments in the number and abundance of species did persist until 18 days (Fig. 3, Tables IV-VII). The cleared rocks were colonized faster than the bare rocks : after only 1 day, the cleared rocks in most places had the same number of species as controls (Fig. 3, Table IV). The only exception was the large rocks in the low-shore area, initially the situation with the greatest number of species. The bare rocks, in contrast, consistently had fewer species than cleared rocks or the controls, however, by 18 days these differences were only significant for medium and large boulders low on the shore (Table V). It is interesting to note that the number of grazing species in the high-shore area at Cape Banks was greatest on the medium-sized boulders (Fig. 3). Furthermore, this pattern was reestablished on the cleared rocks within 1 day and developed on bare rocks within 3 days (Fig. 3, Table V). Low on the shore, large boulders consistently had most species (Fig. 3). The abundances of four of the commoner grazers were significantly affected by the treatments, with differences persisting to 18 days for three of these species (Tables VI-VII). The neritacean Nerita atramentosa Reeve responded consistently, being less

K. A. MEGUINNESS

168

1

1

5 4

HIGH

I

I

I

1

3

I

18

TIME (days)

Fig. 3. The mean number of grazing species ( . rock - ‘) present at the start of the experiment and after 1, 3, and 18 days on boulders high and low on the shore: Kl , unmanipulated control boulders; , boulders with all mobile species removed at the start of the experiment; I , bare boulders from above the high-water mark; S, small; M, medium; L, large (see text for actual sizes of rocks). The SE bars apply to all means at a time.

TABLE IV

Results of ANOVAs of effects of treatments in removal experiment (control, cleared, bare rocks) on mean number of mobile species on rocks after 1, 3, and 18 days. Data were transformed as ln(x + 1) to stabilize variances (homogeneous by Cochran’s test). Source

Treatment (T) Area (A) Size (S) TxA TxS AxxS TxAxS Residual Total

Percentage of variation

df

2 1 2 2 4 2 4 54 71

1 day

3 days

18 days

38.2*** 2.3* 17.3*** 5.8** 4.8* 3.5* s.4** 19.7 100.0 (156.4)

36.9*** 0.6 NS 16.4*** 1.2 NS 6.3* 4.3 NS 1.4 NS 32.9 100.0 (184.9)

15.9*** 1.2 NS 37.8*** 3.2 NS 4.6 NS 5.7*+ 5.5* 27.1 100.0 (162.4)

COLONIZATION

169

OF BOULDERS

abundant on bare rocks than on cleared and control rocks at 3 days but equally abundant in all treatments by 18 days (Tables VI-VII). Ausm~~chba constricta Lamarck, a trochid, was initially least abundant on all sizes of bare rocks but by 3 days TABLE V Results of S-N-K

tests on mean numbers of grazing species recolonizing boulders after 3 and 18 days (at

P = 0.05). The test at 3 days was on the ~eatment x size interaction, the test at 18 days on the treatment x area x size interaction. The untransformed mean number of species is given, though tests were done on transformed data ( = signifies no significant difference). Area

Rock-size

Control

Small Medium Large

0.94 2.44 3.31

= = >

1.50 2.44 2.19

> 0.13 > 0.75 > 0.81

Small Medium Large

1.63 2.25 2.38

= = =

1.38 3.00 2.38

= 0.38 > 1.75 > 1.13

Small Medium Large

0.67 3.50 4.75

= > >

1.25 2.17 3.38

= 0.75 = 2.00 > 2.00

Cleared

Bare

After 3 days

After 18 days High

Low

all large rocks had similar numbers. The relationship for small and medium rocks varied with area on the shore (Tables VI-VII). The response of the littorinid Bembicium nanum Lamarck varied with time (Table VII). It was initially less abund~t on bare rocks but only in the high-shore area where it was more common; after 3 days, this difference between areas vanished. By 18 days, it had become equally numerous on all small and large rocks, but medium bare rocks still had smaller densities than the other treatments. CeZZunatr~mo~eric~ (Sowerby), a limpet, was slow to colonize ah rocks. After 3 days, it was still absent from cleared and bare rocks high on the shore, and significantly less abundant in these treatments than in controls in the low-shore area where it was more common (Table VII). After 18 days, it was more abundant on cleared rocks than on bare rocks, but had still not reached the numbers present in controls. There were too few predators for an analysis of the number of species to be meaningful and so only the abundance of the whelk Morula marginalba (Blainville) was examined. Its behaviour was consistent; it was always equally abund~t on cleared and control rocks but was never found on bare rocks (Table VII).

**a

_ _

_ _

Area (A) Size (S)

TxA TxS AxS TxAxS

1

Treat (T)

Time (days)

-

_ ***

***

-

**

_

_

*

_ -

**

*

* **

_ _

*W

-

** **

**

*

_

* * *

a**

1

_

*

* *

***

3

18

3

1

3+

18

Bembicium

Austrocochlea

Nerita

_

**

_ **

*

18

_

*** *** * ** *

*HZ

l++

-

* -

z+++ ** *

3

Cellana

-

-

*W *** * **

18+

*

** *

I+

_

-

* **

3++

Morula

_

* **

18

Results of ANOVAs of effects of treatments (control, cleared, bare rocks) on abundance of five gastropods. A dash means that the factor or interaction was not significant (at P = 0.05). Data were transformed as ln(x + 1) to stabilize variances. Even after transformation, variances in some analyses were heterogeneous (by Cochran’s test). These are indicated by symbols next to the time when heterogeneity was present: + = significant at P = 0.05, + + = significant at P = 0.01. See Methods for procedures used in these instances.

TABLE VI

3 K

2

8 c

F ? zz

COLONIZATION

171

OF BOULDERS

TABLE VII Results of S-N-K tests (at P = 0.05) on mean densities (.m-*) of five mobile gastropods recolonizing boulders after 3 and 18 days. Untransformed means are given, though tests were done on transformed data. When variances were heterogenous, a significance level of 0.01 was used for the S-N-K test (see Methods and Table VI). Means for the two areas and three rock sizes were pooled when ANOVAs (Table VI) indicated that these factors did not interact with treatments. Area

Rock size

Control

Cleared

Bare

Nerita

Pooled

268

=

330

>

30

Small Medium Large Small Medium Large Small Medium Large

107 20 19= 25 51 21 63 30 47

= =

= =

23 6

= = = = = =

242 48 I=1 0 111 11 196 106 23

= > = > = =

0 0 26 0 75 60

Pooled Pooled

Pooled Small Medium Large

34 8 71 21

< = = =

68 10 58 38

> = > =

8 25 6 4

High Low High Low

Fooled Pooled Pooled Pooled

7

=

0

40 > lO= 71 >

Pooled

Pooled

After 3 days Austrocochlea

Aher 3 days

High

Low

After 18 days

Pooled

Bembicium

ARer 3 days After 18 days

Cellana

After 3 days ARer 18 days

=

0

6 = l=O 19 >

0 0

26

0

Morda

After 18 days

7

=

>

DISCUSSION COLONIZATION

BY SESSILE SPECIES

Experiments showed that the recruitment of at least some species to the undersides of rocks was reduced if the space was already occupied, by organisms characteristic of either the upper or under surface. At Long Reef, more spirorbids settled into patches cleared in bryozoans, or amongst other spirorbids, than onto individuals of either of these species. At Cape Banks, Galeoiaria became more abundant on that half of the overturned rocks which had been cleared of algae. This has been found previously for tube-building polychaetes (Zotolli & Carriker, 1974) and also for other forms, such as barnacles (Denley & Underwood, 1979), fohose macroalgae (Sousa, 1979a; Turner, 1983), ascidians, and sponges (Su~erI~d, 1974). This preemption of space is only likely to be important low on the shore, since only here was space in short supply (McGuinness, 1987a). Within this area, the effect was

172

K. A. McGUINNESS

import~t both before and after boulders were disturbed and overturned, though probably for different sizes of rock. Large boulders were rarely disturbed and all of the underside may be occupied by sessile animals, with some ascidian and sponge colonies overgrowing other species and occupying much space (McGuinness, 1987a). Thus, diversity was less on these rocks than on smaller boulders where space was still available and species were not excluded by preemptive competition (see also McGuinness, 1984, 1987b). In contrast, preemption after overturning may be more important for small boulders. Cover on the tops of boulders was not related to rock size and averaged x70%, though it may be up to 100% (~cGuinness, 1987a). Small rocks (Z 50 cm2> were overturned once every 1-2 months and the encrusting algae which usually dominate space (McGuinness, 1987a), may take longer than this to decay or be removed by animals or abrasion, Thus, this space may only rarely be available for settlement. An interesting aspect of the second experiment was that the spirorbids became much more abundant in cleared patches on already occupied rocks at Long Reef than on initially bare rocks. Conceivably, the spirorbids avoided these bare rocks because they differed in some way from others in the area: perhaps the microbial film which induces settlement in many marine larvae (e.g., Knight-Jones, 1951; Crisp & Ryland, 1960; Meadows & Williams, 1963), was absent, though this usually develops within a few days (MacLulich, 1987; Scheltema, 1974). At Cape Banks, however, GaleoZaria recruited equally to scraped patches on rocks low on the shore and those imported from above the high-water mark, suggesting that there were no adverse effects of the latter rocks (unless these effects differed between shores or species). Another expl~ation for the patterns of rec~itment of the spirorbids concerns their reproductive behaviour. Spirorbids brood their eggs and release iarvae which may be able to settle almost immediateIy (Fauchald, 1983). Thus, the bare rocks may simply have been further from the source of potential colonists; i.e., further from the adult spirorbids. Recruitment to patches cleared in bryozoans, w IO-15 cm from adult spirorbids, was less than amongst spirorbids but greater than on bare boulders, supporting this interpretation. Alternatively, the pattern might be caused or exaggerated by the tendency for polychaete larvae of some species to settle near adults (Scheltema, 1974; Ten Hove, 1979). The lack of recruitment of algae to the tops of rocks in these experiments was not surprising. It was not because the time scale of the experiment was too short; Ulva can develop 100% cover on boulders within 20 days (Underwood, 1980; McGuinness, unpubl. data). Grazers were not deliberately removed from the rocks and any dislodged inadvertently could have recolonized rapidly. These grazers are quite capable of preventing the growth of foliose macroalgae on the boulders (Und~ood, 1980; Underwood & Jeruakoff, 198 1). When Underwood (1980) excluded grazers from cleared areas of the open platform, l/ha developed 100% cover within 1 month. This suggests that preemption of space was less important for the tops of boulders, and the major determinants of algal abundance and diversity here were grazing and exposure to air during low tide (Underwood, 1980; Underwood & Jernakoff, 1981,

COLONIZATION

OF BOULDERS

173

1984; McGuinness, 19878). These results are also consistent with Underwood’s (1980) finding that Hjide~bra~d~, which is also common on boulders, did initially retard the growth of Ulv~but that eventually cover in areas with and without the crust was similar. Further, a great cover of Ulva did not affect the rate at which Hildenbrandia recolonized primary space; Ulva simply occupied secondary space. COLONIZATION

BY MOBILE

SPECIES

The sessile species present on boulders also influenced the rate of colonization by mobile organisms. Boulders with sessile organisms were colonized faster than those without. Even after 18 days, several gastropods were less abundant on bare rocks than on cleared or control boulders in at least some situations. This could again be an experimental artifact: rocks from above the high-water mark may have differed from others in some way - apart from the absence of sessile organisms - which affected the behaviour of the mobile organisms. There was no difference in shape or surface heterogeneity (McGuinness, unpubl. data) but it is possible that they carried a repellent substance. For the latter explanation to be true, however, the effect of this substance would have to vary among species and also depend on the size of rock and the area on the shore (Tables VI-VII). A simpler inte~retation of the results is that grazers and predators selected amongst boulders on the basis of the organisms present. Apparently, the patterns in the diversity and abundance of mobile species resulted from the responses of the individuals to the rocks and the other mobile and sessile organisms on them. The slower colonization of the bare boulders suggests that much of the selection that occurred was on the basis of food. This might also be responsible for the different relationships between density and rock size observed (see also McGuinness, 1987a). Small rocks are emersed for significantly shorter periods at low tide (McGuinness & Underwood, 1987) and could develop different amounts or types of food (and see Underwood, 1984b). Underwood (1979) hypothesized that some patterns in the distribution of grazing gastropods might result from behavioural responses to the presence of food, but noted the paucity of relevant data. The present results support this view and suggest that other studies of these interactions are needed. High on the shore at Cape Banks, the grazing assemblage is typically most diverse on medium-sized rocks (Fig. 3; McGuinness, 1984). The usual explanation for this pattern is the intermediate disturbance model (Connell, 1978; Sousa, 1979a): small rocks had few species because they were frequently disturbed and large rocks had few because, in the absence of disturbance, some species outcompeted others. Certainly, small rocks are more frequently disturbed (Sousa, 1979a; McGuinness, 1987a) and more species did accumulate on experimentally stabilized boulders (McGuinness, 1987b). However, disturbance could not be responsible for fewer species on small rocks in the present study because no rocks were overturned until after 3 days but the pattern was established on cleared boulders within 1 day. (This does not mean that disturbance was in general unimportant for this assemblage, merely that it was not responsible for this particular short-term pattern.) Nor was the reduction in diversity on large boulders

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the result of competition for food because this is not intense enough to produce an effect within a few days {Underwood, 1978, 1984a). Thus, this “intermediate disturbance pattern was caused by the behaviour of the grazers and did not result from the factors postulated by the model to be responsible. This emphasizes the importance of studying the process of recolonization after disturbance, and of usiug experiments to manipulate existing organisms to determine their effects on the recruitment of other individuals. Here, such experiments have led to a greater underst~d~g of the causes of patterns in the diversity and abundance of organisms in these communities.

ACKNOWLEDGEMENTS

I was supported during this work by a Commonwealth Post~aduate Research Scholarship and a University of Sydney Research Grant. Thanks are due to A. J. Underwood for discussions concerning this work. My thanks to L. S. Stocker, and to P. G. Fairweather, C. H. Peterson, W. P. Sousa, and A. J. Underwood for comments which greatly improved this paper.

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