effects of patch-size on the structure of assemblages in rock pools

ELSEVIER Journal of Experimental Marine Biology and Ecology,

197 (1996) 63-90

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

Effects of patch-size on the structure of assemblages in rock pools

A.J. Underwood*, G.A. Skilleter

Institute of Marine Ecology, Marine Ecology Laboratories, A II, University of Sydney, Sydney, NSW 2006,

Ausfralia

Received 3 January 1995; revised 28 June 1995; accepted 11 August 1995

Abstract

Rock pools represent patches or islands of habitat different from the surrounding shore. They contain diverse assemblages of invertebrates and algae. The shape, size, height on the shore and exposure to waves are considered important influences on the abundances of organisms. In studies of natural pools, these factors are confounded because pools are rarely comparable; they differ in size, position on the shore and history of colonization. To solve this, experimental pools of different diameters (I 5, 30 and 50 cm) and depths (5, I5 and 30 cm) were drilled in sandstone rocky shores in Botany Bay, New South Wales, Australia. Replicate pools of each size were made in each of 24 randomly-chosen sites, six sites representing each combination of two heights (mid and low) on the shore and sheltered versus wave-exposed habitats. The influence of diameter of the pool is examined here, using data from a total of 360 experimental pools. Despite a 2-3-fold increase in surface-area of pools with increased diameter, there was no difference in densities of most taxa examined (gastropods, a starfish, sessile invertebrates, algae). An exception was foliose algae, the cover of which was generally greater low on the shore and in 50 cm than 30 cm diameter pools. There were also consistently more species in any stratum (i.e., depth in a pool) in the wider pools. There were approximately 25-50% more species in the widest than the narrowest pools, consistently from season to season and year to year. There were, however, significantly fewer species per unit area of a given stratum in pools of 50 versus 30 versus I5 cm diameter. These results require further investigation in relation to different theories to explain species-area relationships. Multivariate analyses revealed no influence of diameter on the structure of assemblages of organisms in pools of different diameter. This was true for different strata in pools and at mid- or low-shore positions on exposed or sheltered shores. Diameter of pools thus had remarkably little influence on the organisms; those effects found were consistent. Experimental pools were shown to be effective for testing hypotheses about proposed influences on the ecology of inhabitants. The findings about diameter of pools greatly simplify analyses of influences of depth and physical features of the surrounding habitat.

*Corresponding author. Fax: (61) (2) 351-0612

0022-0981/96/$15.00 0 1996 Elsevier Science B.V. All rights reserved

SSDI 0022-098 I (95)OO 145-X

64 A.J. Underwood, G.A. Skilleter 1 J. Exp. Mar. Bid. Ed. 197 (1996) 63-90

Keywords: Experimental; Intertidal; Patchy habitats; Rock pool; Spatial variability; Species richness

1. Introduction

Rock pools, isolated microcosms of submerged habitat in the surrounding emergent substratum, have rarely been examined quantitatively to determine the processes creating and maintaining the structure of populations and assemblages of organisms occupying them (Dethier, 1984). Large spatial and temporal variability in these assemblages (e.g., Astles, 1993; Metaxas et al., 1994) and the difficulty of obtaining suitable ‘replication’ of pools (Dethier, 1984; Metaxas and Scheibling, 1993) have contributed to our poor understanding of the ecology of assemblages in these habitats, despite the fact that they are almost ubiquitous in their occurrence on rocky shores throughout the world.

Rock pools are ‘islands’ of one habitat encompassed by a different region. The organisms in rock pools are not exposed to such harsh physical conditions during low tide as are the plants and animals living on the surrounding rocky surfaces. Thus, pools may serve to provide refuges for many intertidal species and for individuals of subtidal species that venture to higher regions on a shore (e.g., intertidal algae, Underwood and Jemakoff, 1984; whelks, Moran, 1985; Fairweather, 1988). These features also mean that rock pools may be useful models for other types of patchy habitats, including real islands, National Parks and reserves and patches of forest, habitats less amenable to experimental manipulation (e.g., Wiens et al., 1993). An understanding of the ecology of such insular patches is vital if we are to understand the impacts of human activities causing fragmentation of habitat (Wilcox and Murphy, 1985). One additional advantage that arises from using rock pools as models for other patchy habitats is that they may provide more reliable models than, say, true islands. True islands tend to have ‘hard edges’ (Stamps et al., 1987a) and predictions derived from these habitats may not be readily applied to species which occupy softer-edged insular patches of habitat (Stamps et al., 1987b). Rock pools on shores in New South Wales are likely to represent soft-edged habitats to species occupying them because many of these species can also be found on the surrounding emergent substrata (Underwood, unpublished data).

Many of the existing models describing the dynamics of marine organisms in patchy intertidal habitats have been derived from so-called Type I patches (Connell and Keough, 1985; Sousa, 1985), areas of empty space surrounded by a matrix of organisms (e.g., Dayton, 1971; Levin and Paine, 1974; Connell, 1978; Suchanek, 1978; Paine and Levin, 1981; Sousa, 1984; see also the reviews in Pickett and White, 1985). There have been few studies to compare predictive models generated from these studies with results for Type II patches, isolated patches of a new habitat (but see Sousa, 1979a,b; Keough, 1984b; McGuinness, 1987a,b). Studies of Type II patches have largely been restricted to assemblages on intertidal boulders or on subtidal bivalve shells. Rocks pools are clearly recognisable as a Type II habitat in that they are isolated from other patches of similar habitat by the relatively inhospitable surface of the rock platform. Pools therefore provide an ideal opportunity to increase our knowledge about the processes which

A./. Underwood, G.A. Skillerer I J. Exp. Mar. Biol. Ecol. 197 (1996) 63-90 65

structure the biota in Type II patchy habitats and compare these results with the better

understood Type I habitats. One aspect of the dynamics of patchy habitats, frequently mentioned (see reviews in

Pickett and White, 1985) but rarely examined specifically, is the effect of size of patch on the composition of the associated assemblages, as opposed to simply examining the total number of species in a patch (Keough, 1984b). For a number of different reasons, the number of species generally increases with the size of a patch (see, for review, McGuinness, 1984). This in turn increases the potential number of inter-specific interactions (Keough, 1984b) with possible concomitant effects on the abundance of individual taxa. An understanding of the dynamics of these patches must, therefore, also incorporate analyses of changes in the composition of the assemblages. Given the range in sizes of patches that occur naturally in different habitats (Connor and McCoy, 1979), it is necessary to quantify the relationship between patch-size and the abundance of individual taxa in order to propose models to explain observed differences in the composition of assemblages found there.

For rock pools, there are two components comprising the ‘size’ of a patch, the diameter of the pool (e.g., Bennett and Griffiths, 1984) and its depth (e.g., Droop, 1953). Each of these variables may lead to differences in the structure of the assemblages in rock pools but there have been no studies which have specifically attempted to determine the contribution of each of these factors to the observed patterns. One of the primary reasons behind this lack of a systematic approach to understanding the importance of size on the dynamics of rock pool ‘patches’ may be the difficulty in unconfounding the two variables in natural pools. As noted above, no two natural pools are quite the same, so it is difficult, if not impossible, to obtain data from replicate natural pools where one of these variables is held constant while allowing the other to vary (e.g., constant depth, but variable diameter). Further confounding any comparisons is the variability associated with ‘replicate’ pools often being found at different heights on the shore or different exposures to waves. Both factors have been described as important for the fauna and flora in pools (e.g., Johnson and Skutch, 1928; Metaxas et al., 1994).

The solution to the problem of natural pools being different in size (diameter and depth), shape, height on the shore and history of colonisation is to make pools of appropriate sizes and shapes where and when they are needed. In this way, variables that have been claimed to influence patterns of assemblages can be controlled in replicate sets of pools in orthogonal arrays of the various factors. This allows different features of pools to be separated in tests of hypotheses about causes of patterns in assemblages in pools.

Here, we describe the influence of one variable, the diameter of the pool, on the assemblages of invertebrates and algae in pools of various depths. By use of experimental pools, we were able to separate variability among pools and to unconfound differences due to different heights on the shore, wave-exposure and depth of the pools. In general, larger numbers of species are found in larger patches of habitat. If this is true for assemblages in rock pools, there should be more species in pools of larger diameter, when depth, period of colonisation and time of formation of the pools are held constant. This hypothesis is tested in the present paper. Other components of size of pools, relating to their depth, will be described elsewhere. Here, pools are treated as patches of

66 A.J. Underwood, G.A. Skilleter I J. Exp. Mar. Biol. Gal. 197 (1996) 63-90

different sizes (diameters). At any given depth in any pool, the hypothesis that number of species should increase with increasing diameter can be tested without being confounded by depth.

2. Materials and methods

2.1. Study sites and experimental pools

Experimental pools were constructed during 1986 on sandstone shores in the Cape Banks Scientific Marine Research Area (Botany Bay, New South Wales, Australia). All details of the construction of the pools are not described here (Underwood, data not shown) but an array of pools of different diameters (15, 30 or 50 cm) and depths (5, 15 and 30 cm) were cored out of the rock using diamond-corers. Although pools were cored over a period of about 9 months, all pools were completely cleansed of any colonists by scraping, scrubbing with concentrated hydrochloric acid so that they began colonisation in December/January !986/ 1987.

Altogether, there were 24 sites (each approximately 10 X 5 m along and across the shore, respectively). These sites were 10-100 metres apart along the shore. Six sites were randomly chosen to represent each of the four combinations of low- (0.92-2.25 m above local datum, Indian Low Water of Spring tides) and mid-shore (1.16-2.54 m above I.L.W.S.) habitats in wave-exposed locations and low- (0.64- 1.27 m above I.L.W.S.) and mid-shore (0.98-1.77 m above I.L.W.S.) habitats in sheltered locations. As much as was practicable, sheltered and exposed sites were interspersed along the shore. Whatever the actual height on the shore, low-shore sites were in areas dominated by foliose algae, tubeworms or the tunicate Pyura stolonifera (Underwood, 1975, 1981; Underwood and Jernakoff, 1981, 1984). Mid-shore sites had a typical mid-shore assemblage of encrusting algae and grazing gastropods or the barnacle Chamaesipho

tasmanica (in sheltered areas) or barnacles Tesseropora rosea and Catomerus polymerus (in exposed areas), as in Underwood ( 198 1) and Fairweather and Underwood ( 199 1).

Experimental pools were scattered haphazardly about 1.35 m apart over each site. For this paper, the pools examined were 15 cm diameter, 5 cm deep (three replicates per site); 30 cm diameter, 5, 15 or 30 cm deep (two replicates of each per site) and 50 cm diameter, 5, 15 or 30 cm deep (two replicates per site), a total of 15 pools per site and 360 experimental pools altogether. In a survey of 246 natural pools along the shores where experimental pools were built, 93% were shallower than 30 cm depth and 77% were narrower than 50 cm diameter. Thus, experimental pools represented the great majority of those occurring naturally.

In each pool, depths were sampled in a stratified design. The top 5 cm (i.e. the entire depth of a 5 cm deep pool) was sampled separately because this stratum could be compared across pools of all depths. The next 10 cm (5- 15 cm from the top) could be compared for pools of depth 15 or 30 cm. In 30 cm deep pools, the deepest stratum (15-30 cm from the top) was also sampled. In all pools, the base was sampled separately. This stratification from the top of pools downwards, rather than the bottom upwards, is appropriate and will be justified elsewhere.

A.J. Underwood, G.A. Skilleter 1 J. Exp. Mar. Biol. Ecol. 197 (1996) 63-90 61

In this paper, we use data from periods when colonization was substantially complete and assemblages were no longer changing much in terms of composition of species. These data were from October 1989 to July 1990, some 33 to 43 months after the pools were initially cleared. Although there is no room here to provide all the data necessary to support this statement, by about 30 months from initial construction and clearing, experimental pools had assemblages very similar to those of similar-sized natural pools. The composition of species was very like that in natural pools and more importantly, variations in abundances of species from pool to pool, site to site and time to time were large, as documented in detail for natural pools on the same shores by Astles (1993).

The sides of pools were sampled using an inverted periscope, 8.0 X 5.5 cm in cross-section and about 45 cm long. A mirror reflected the view of a 4 X 4 cm quadrat (see Astles, 1993). Covers of algae and encrusting animals (sponges, bryozoans, etc.) were estimated as the number out of ten dots on the front of the periscope that were over the organism, multiplied by ten to give percentages. All mobile animals in the field of view were counted. Percentage covers and counts were averaged for each stratum from 3, 4 or 6 randomly-placed periscope quadrats in 15, 30 and 50 cm diameter pools, respectively. Where the periscope landed on large mobile animals, they were carefully removed or the periscope was moved to an immediately adjacent position. Then, the numbers of larger animals (snails, limpets, worms, individually recognizable algae, crabs, starfish, etc.) were counted for the whole stratum and converted to density per unit area.

The flat bases of pools were sampled in the same way, except that instead of a periscope a 6 cm diameter viewing tube was used to gain a clear view through the water. It had a 4 X 4 cm quadrat in its lid. Again, 3, 4 or 6 quadrats were sampled depending on the diameter of the pool.

2.2. Statistical analyses

2.2.1. Univariate measures

The effects of diameters of rock pools on the structure of populations and assemblages of organisms in these habitats were analysed using twelve variables representing different functional groupings of organisms. These were: mobile animals (represented by a patellid limpet, Cellana tramoserica, a trochid gastropod, Austrocochlea constricta and a herbivorous starfish, Patiriella exigua); sessile animals (represented by the total percent cover of all sessile animals, the numbers of a serpulid worm, Galeolaria

caespitosa and the numbers of the barnacle Tesseropora rosea); foliose algae (total percent cover of all foliose algae); encrusting algae (represented by total percent cover of all encrusting algae and by the percent cover of two abundant taxa, Ralfsia verrucosa and pink encrusting algae, a mixture of coralline species indistinguishable in field sampling); total number of all species. The total number of species was examined in two ways, corrected and uncorrected for area of the stratum sampled.

We examined the differences among diameters for: 5 cm deep pools, 3 diameters ( 15, 30 and 50 cm diameters); 15 cm deep pools, 2 diameters (30 and 50 cm diameters); and 30 cm deep pools, 2 diameters (30 and 50 cm diameters). Within each of these three sets, we examined the effects of diameters for each of the different strata sampled separately

68 A.J. Underwood, G.A. Skilleter I J. Exp. Mar. Biol. Ecol. 197 (1996) 6-g-90

because different strata within a single pool are not independent of each other (Underwood, data not shown). The different depths of pool have different numbers of strata available so for each of the three sets of pools, different numbers of strata were examined. In 5 cm deep pools, we examined the upper 5 cm and the basal stratum. For 15 cm deep pools, there was an extra stratum, the lower 10 cm, giving three strata. For the 30 cm deep pools, there was an upper 5 cm, a middle 10 cm, the lower 15 cm and the base, four strata in total.

We were concerned that a detailed analysis of data at one time may not be very representative of patterns of distribution and abundance of organisms (although there is little average temporal variation in sets of natural pools; Astles, 1993). We also wished to be sure that any successional changes were complete. Therefore, for all combinations of dependent variables, depth of pool and individual stratum, we examined data collected on three separate occasions, October 1989, January and July 1990. The same pools were necessarily sampled on each occasion so data from individual times are not independent and separate analyses were done for the three dates. In total, we did 324 separate univariate analyses of variance to test whether there were significant effects of diameter of pool on the structure of populations and assemblages of organisms in these habitats.

2.2.2. Multivariate measures In the majority of univariate analyses, there were significant effects of height on the

shore and/or levels of exposure on the abundance of individual taxa and on species richness within the different groups of rock pools. Effects of diameters on the structure of the assemblages within pools were therefore examined separately for each of the four different combinations of exposure and height (e.g., mid-shore exposed, mid-shore

sheltered, etc.). Data were analysed using non-metric Multi-Dimensional Scaling ordination (nMDS)

using the Bray-Curtis similarity measure on double square root transformed abundance data, followed by an analysis of rank similarities (ANOSIM; Clarke, 1993). Data of two types are mixed in these analyses (percentages in the range O-100 and counts in the range O-575). There is no mathematical or statistical reason that these should not be analysed together but obviously those with the largest range (in this case densities) must have a greater influence on outcomes than the other. This is somewhat mitigated by using double square-root transforms. Here, the densities had the greater range and may therefore have greater influence on outcomes than the data on percentages.

3. Results

3.1. Univariate measures

3.1. I. Mobile animals: Cellana tramoserica, Austrocochlea constricta and Patiriella exigua

There was a striking lack of consistent effects of diameter on the abundance of any of the mobile animals examined. Of the 27 analyses examining the effects of diameter on

A.J. Underwood, G.A. Skilleter I J. Exp. Mar. Biol. Ecol. 197 (1996) 63-90 69

Table 1

Example analysis of mean abundance of Cellana tramoserica in 15 cm deep pools with different diameters in

October 1989

Source df MS F P F versus

Exposure: E 1 46 256

Height: H 1 104 286

Site(E X H):S(EH) 20 23 602

Diameter:D 1 3392

EXH 1 57 693

EXD 1 6 180

HXD 1 6 807

D X S(EH) 20 221

EXHXD 1 14 657

Residual 48 3 676

1.96 >0.15 4.42 CO.05

6.42 <O.OOOl

2.78 >O.lO 2.44 >O.lO

5.06 CO.05

5.57 CO.05

0.33 >0.95

12.00 -Co.005

VW WW Residual

D X S(EH)

S(EH) D X S(EH)

D X S(EH)

Residual

D X S(EH)

The complete analysis is shown here to illustrate the full design for the experiment (data were untransformed;

n = 2 replicate pools in each site). There were six independent sites in every combination of exposure

(sheltered versus exposed) and height (mid-shore versus low-shore).

the abundance of each of these species, only eight showed significant effects of diameter, either as a main effect or as an interaction (as in the example in Table 1,

Cellana tramosericaj. Where there were significant differences due to diameter no consistent patterns could

be associated with pools of different depths. For example, in shallow pools (5 cm deep), for October 1989 and January 1990, the mean abundance of C. tramoserica in the basal stratum of pools differed among the three diameters but the differences varied between heights on the shore and exposures. The means showed no consistent differences among the three diameters.

In October 1989 on exposed shores, there were no significant differences among the three diameters (SNK tests on means averaged over both heights on the shore; Fig. 1) but on sheltered shores, the smallest pools (15 cm diameter) had significantly more C. tramoserica than either of the larger diameters. In contrast, in January 1990 there were significantly more C. tramoserica in the largest pools in exposed sites (50 cm diameter; Fig. 1).

Similarly, in October 1989, in the upper 5 cm stratum of 15 cm deep pools, there were significantly more C. tramoserica in 30 cm than in 50 cm diameter pools. In January 1990 and July 1990, however, this was only true for sites on exposed shores (Fig. 2). On sheltered shores, there were no significant differences between the two diameters and in fact, there was an opposite trend (more limpets in 50 cm than 30 cm diameters) in July 1990. There was a similar lack of consistent pattern in the differences among diameters of pool in the abundance of Austrocochlea constricta and Patiriella exigua.

3.1.2. Sessile animals: total percent cover of all sessile animals, numbers of Galeolaria caespitosa and Tesseropora rosea

There were no consistent effects of diameter on the percent cover of sessile animals in the different groups of pools. Only 7 of 27 analyses showed significant effects of diameter as a main effect or as an interaction with other factors. Five of these significant

70 A./. Underwood, G.A. Skilleter I .I. Exp. Mar. Bid. Ed. 197 (1996) 63-90

150

100

"E $ 50 a

$ z

3 O

6 20

t

f

2 15

10

5

0

October 1989

a T a

January 1990

b

I

a

i

15 30 50 15 30 50 exposed sheltered

Diameter of pools (cm)

Fig. 1. Mean ( + SE) number of Cellana rramosericu (adjusted to per m’) on basal stratum of 5 cm deep pools,

IS cm, 30 cm or SO cm diameter, in October 1989 and January 1990 (n = 24 pools, pooled across mid- and

low-shore sites for each exposure). Letters above the histograms indicate groups of means identified as

significantly different (P < 0.05) by SNK tests; treatments with the same letter were not significantly different

(P > 0.05). Each set of adjacent bars was analysed in a separate SNK test.

effects were in 30 cm deep pools but, in all cases, multiple comparisons of means showed that differences between the two diameters (30 and 50 cm) varied between heights or exposures or from time to time. Sometimes there was a trend for greater cover of sessile organisms in the larger diameter pools but often the opposite was true. There were rarely any significant differences among the pools (Fig. 3).

The number of Galeolaria caespitosa varied as a function of diameter (main effect or in interactions) in 15 of 27 analyses. Eight of these involved an interaction whereby the effect of diameter varied among the replicate sites within Height by Exposure combinations for 15 cm deep pools. That is, any differences between the two diameters depended on which sites were being examined. If there were no overall difference


1501 a October

a

T

30 50 30 50

exposed sheltered


January a a

July 1990

a

Fig. 2. Mean ( + SE) number of Cellana tramoserica (adjusted to per m’) on stratum 5 of I5 cm deep pools,

30 cm or 50 cm diameter, in October 1989, January 1990 and July 1990 (n = 24 pools, pooled across mid- and low-shore sites for each exposure). Other details as in Fig. 1.

between the pools of different diameters, there should be an equal probability that in any site either the 30 or the 50 cm diameter pools would have a larger mean number of Galeolaria (i.e., 12 sites should have abundances greater in 50 cm than in 30 cm diameter pools and 12 sites should show the opposite pattern). We determined the number of sites (out of the 24 in the experiment) where, in 15 cm deep pools, abundance in 50 cm diameter pools was greater than that in 30 cm diameter pools.

In October 1989 and January 1990, 50 cm pools were more likely to have more Galeolaria than 30 cm pools (x2 = 4.44, 5.40; P < 0.05 for October 1989 and January 1990, respectively) but in July 1990 this pattern no longer existed (x2 = 1.72; P > 0.05). This pattern of differences between diameters among the different sites was not evident for the 5 cm nor the 30 cm deep pools.

72 A.J. Undrrwood, G.A. Skilleter I J. Exp. Mar. Biol. Ed. 197 (1996) 63-90

b

04 30 50 30 50 30 50 30 50 30 50 30 50 mid IOW mid low mid IOW

October 1989 January 1990 July 1990


Fig. 3. Mean ( + SE) percent cover of sessile species on basal stratum in 30 cm deep pools, 30 cm or SO cm

diameter, in October 1989, January 1990 and July 1990 (n = 24 pools, pooled across exposed and sheltered

sites for each height). Other details as m Fig. I.

Only 7 of 27 analyses (not shown here, to save space) of the abundance of the barnacle Tessevaporu TOSea showed signilicant effects relating to diameter of pool. Four analyses showed significant effects at the smallest spatial scale of Sites (within Exposure by Height) but these occurred for different depths of pool, in different strata and at different times, again demonstrating the lack of consistency in the results.

3.1.3. Foliose u&e: total percent cover of all foliose algue In general, whenever there were differences among diameters, 50 cm diameter pools

had greater mean cover of foliose algae than did 30 cm diameter pools (Fig. 4 and Fig. 5). 14 of the 27 analyses showed significant differences between diameters or interactions of diameter with other factors (Table 2).

For example, on the basal stratum of 5 cm deep pools, foliose algae were in greater cover in larger pools in low-shore, but not mid-shore sites (Fig. 4). In the deeper parts (stratum 30) of deeper pools (30 cm deep), there were generally greater covers of foliose algae in the wider pools (Fig. 5). There was an apparent tendency for the mean cover of algae to differ among diameters more often for the basal parts of pools regardless of their depth. Thus, in Table 2, the cover of foliose algae was more likely to be significantly different in basal and the deepest strata of pools than in the shallower strata. Such patterns are to be considered elsewhere; this study is focused on differences due to the diameter of the pools.

There were, however, numerous inconsistencies. Either there were no differences (Table 2) or there were differences in mid-shore sites (Fig. 6). In no case was there a significantly larger cover in 30 cm than in SO cm diameter pools.


70

60

50

October 1989

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30

20

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July 1990

a T a

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Fig. 4. Mean ( + SE) percent cover of foliose algae on basal stratum of 5 cm deep pools, 15 cm, 30 cm or 50

cm diameter, in October 1989, January 1990 and July 1990 (n = 24 pools, pooled across exposed and sheltered

sites for each height). Other details as in Fig. I.

3.1.4. Encrusting algae: total cover of all encrusting algae, cover of Ralfsia spp. and pink encrusting algae

Neither the total percent cover of encrusting algae nor the covers of the two most abundant taxa, Ralfsia verrucosa and pink encrusting algae, varied in any consistent way with different diameters of rock pool. Relatively few analyses (fewer than 25% of all analyses) for any of these taxa showed significant effects of diameter as a main effect or as an interaction with other factors. These significant results occurred in different strata, depths of pools and times of sampling with no pattern. The lack of consistent patterns

74 A./. Underwood, G.A. Skilletrr I J. Exp. Mar. Bid. Ed. 197 (1996) 63-90

October 1999

30 1 a T b

m Q) 35 v)

g 30

,o

6 25

G 20

g 15 0 E 10

z 5

$ 0 a

35

30

25

20

15

10

5

0

b

30 50 exposed

bJuly 1990

30 50 sheltered

of pools (cm)

Fig. 5. Mean ( + SE) percent cover of foliose algae on stratum 30 of 30 cm deep pools, 30 cm or 50 cm

diameter, in October 1989, January 1990 and July 1990 (n = 24 pools, pooled across mid- and low-shore sites

for each exposure). Other details as in Fig. I.

indicated that the diameter of the pool had no real influence on cover of encrusting algae.

X1.5. Number of species Although results were not consistent for all strata and there were some interactions

with height and exposure (Table 3), there were usually more species in wider pools (Fig. 7 and Fig. 8). For the shallow (5 cm deep) pools, there were significantly more species in 30 and 50 cm wide pools than in the narrowest (15 cm wide) pools (Fig. 7). There were more species in 50 cm than 30 cm wide pools but this was only occasionally significant (Fig. 7). In the deeper pools, there were always more species in 50 cm wide than in 30 cm wide pools and this was usually a significant difference (Fig. 8).

A.J. Underwood, G.A. Ski&to- I J. Exp. Mar. Biol. Ecol. 197 (1996) 63-90 75

Table 2 Analyses of mean percent cover of foliose algae in pools with different diameters for three times

5 cm deep pools

Diameter

EXD

HXD

D X S(EH)

EXHXD

15 cm deep pools

Diameter

EXD

HXD

D X S(EH)

EXHXD

30 cm deep pools

Diameter

ExD

HXD

D X S(EH)

ExHXD

5 15 30 B

Tl T2 T3 Tl T2 T3 T1 T2 T3 Tl T2 T3

* **

DNE *

*

DNE *** *** ***

*** *** ***

DNE

*

*

*

*

*

*** * *** ** ** *** *

** ***

Only results for levels of the analyses relating to diameter or an interaction involving diameter are shown.

Different depths of pools have different strata available: DNE indicates this stratum did not exist for that depth

of pool (data were untransformed; n = 2 replicate pools). T1 = October 1989, T2 = January 1990, T3 = July

1990. In this and subsequent tables: *P < 0.05; **P < 0.01; ***P < 0.001; blank = not significant, P > 0.05.

Where there were interactions with height or exposure, there were still always more species in wider pools (Fig. 9). Patterns in numbers of species with respect to depth, stratum, exposure or height on the shore are not considered here; only the influence of diameter is interpreted.

Because there were generally more species in the wider and therefore larger pools, the numbers of species were corrected for area of each stratum in each pool (by dividing by

the area). In these analyses, there were always more species per unit area in narrower pools (Fig. 10). This was always significant (or significant as an interaction with exposure or height and occasionally among sites; Table 4). Where there were interactions, the pattern was always for more species in narrower pools (Fig. 11).

3.2. Multivariate measures

Only 2 of 72 analyses of rank similarities (ANOSIM) showed a significant effect of diameter on the structure of the assemblages found in the different groups of rock-pools. There was no evidence to suggest that the composition of the assemblage found in pools of different size varied in any manner consistent with increasing diameter. The

16 A.J. Underwood, G.A. Skilleter I J. Exp. Mar. Bid. Ed. 197 (1996) 6.3-90

A

a

Exposed

b

Sheltered

30 50 mid

a


Fig. 6. Mean ( + SE) percent cover of foliose algae on basal stratum of 30 cm deep pools, 30 cm or SO cm

diameter, at mid- and low-shore sites m January 1990. (A) Exposed sites; (B) sheltered sites (n = 12 pools, 2

pools from each of 6 sites for each combination of height and exposure). Other details as in Fig. I.

variability among pools of the same diameter was as large as any differences among the different diameters (Fig. 12 and Fig. 13).

Each combination of height and exposure was analysed separately (see Section 2) but these analyses used data pooled across all six sites within each combination. Thus, there was the potential for any overall differences among diameters to be obscured because of substantial variability in the structure of assemblages from site to site (equivalent to Diameter X Site interactions in a univariate analysis). We examined this by analysing subsets of data from the pools at a single site. Data from several randomly-chosen sites were examined. Although there were few pools in each site, there was no indication that different diameter pools at any single site had a different composition (Fig. 14).

A.J. Underwood, G.A. Skilleter I J. Exp. Mar. Biol. Ecol. 197 (1996) 63-90 II

Table 3

Analyses of mean number of species (uncorrected for area sampled) in pools with different diameters for three

times. Other details as in Table 2.

Stratum

5 15 30 B

Tl T2 T3 Tl T2 T3 Tl T2 T3 Tl T2 T3

5 cm deep pools

Diameter

EXD

HXD

D X S(EH)

EXHXD

15 cm deep pools

Diameter

EXD

HXD

D X S(EH)

EXHXD

30 cm deep pools

Diameter

EXD

HXD

D X S(EH)

EXHXD

DNE DNE *** *** *** *** *** ***

* *

*

DNE ** *** **

*

** *** ** *** *** * *

* * **

4. Discussion

In this study, there were very few indications that size of pool, measured as diameter had any influence on abundance of organisms. This paucity of consistently significant effects of the diameter on the abundance of most taxa in rock pools is surprising given the apparent prevalence and importance of patch-size in other habitats, terrestrial or marine (Pickett and White, 1985). These reviews have illustrated the various interactions between disturbance and patch-size and subsequent effects on the structure of the assemblages occupying the patches. For example, in some intertidal boulder fields, smaller boulders are more frequently disturbed due to wave action than larger ones (Sousa, 1979a). The assemblages on these boulders show distinct patterns related to the size of the boulder (representing a patch of habitat) and this can be best explained by models relating to disturbance (Sousa, 1979b).

Over the range of sizes of pools we examined (15-50 cm diameter, 176.7-1963.5 cm2 plan surface area), any effects of disturbance were not modified by this component of size of patch. The relatively few effects seen here cannot be used, however, to infer that disturbances were not occurring in these habitats. Unlike Dethier’s (Dethier, 1984) reasoning, the definition of disturbance must be independent of the organisms or assemblages under examination (McGuinness, 1987a). Our data indicated that whatever

A.J. Underwood, G.A. Skilleter I .I. Exp. Mar. Biol. Ecol. 197 (1996) 63-90

20

15

10

5

0

2c

I ‘U 15

P 6 10

i

f 5

z’ 0

20

15

10

5

0

October 1989 B

January 1990

b 15

10

5

a

July 199C

20

15

10

5

0 15 30 50

b b

15 30 50


Fig. 7. Total ( + SE) number of species (uncorrected for area) in stratum 5 (A) and basal stratum (B) of 5 cm

deep pools, 15 cm. 30 cm or 50 cm diameter, in October 1989, January 1990 and July 1990 (n = 48 pools,

pooled across all 24 sites).

the processes structuring the pools, they were not affected by the diameter of pools in such a way as to lead to significant changes in abundance of most taxa.

The only functional group or individual taxon that showed a consistent effect of patch-size on abundance was foliose algae although even for these, there was substantial variability depending on the particular types of pool being examined. Where there were differences in response between mid- and low-shore pools, those low on the shore had an increasing cover with increasing patch-size while high on the shore there were no differences (see Fig. 4). McGuinness (1987a) found a similar difference between high and low shore in the effect of patch-size (for intertidal boulders) on an abundant foliose alga, Polysiphonia sp. High on the shore, there was no relationship between patch-size


l4 1 October 1989

b

12

10

8

6

4

2

0 30 50

‘4 1 January 1990

,L b “I

.g 12

g 10 u)

6 8

; 6

f 4

: 2

0

14 - July1990 b

12

10

8-

6-

4.

2.

0 - 30 50


Fig. 8. Total ( + SE) number of species (uncorrected for area) in basal stratum of 30 cm deep pools, 30 cm or

50 cm diameter, in October 1989, January 1990 and July 1990 (n = 48 pools, pooled across all 24 sites). Other details as in Fig. 1.

and cover of the algae but low on the shore there was a strong relationship between the two although he found the opposite pattern to ours. In his study, McGuinness (1987a) found that Polysiphonia sp. occupied about 3 1% of the space on smaller rocks but decreased to nearly zero on larger rocks. It is impossible to propose coherent explanatory models for why algae should respond so differently on boulders and in rock-pools, given the vast range of differences between these two habitats.

Foliose algae were more abundant in pools lower than higher on the shore, a result entirely consistent with Underwood and Jernakoff (1984) who also examined experimental pools although theirs were only 2 cm deep. In the absence of grazing gastropods, there was considerably greater cover of foliose algae in pools low than high

80 A.J. Underwood, G.A. Skilhter / J. Exp. Mar. Biol. Ecol. 197 (1996) 6.3-90

October 1989

30 50 exposed

30 50 sheltered

6

k 20 2

;

16

8

B

b

January 1990 a

exposed- sheltered- low mid


b

sheltered- low

Fig. 9. (A) Total ( + SE) number of species (uncorrected for area) on stratum 30 of 30 cm deep pools, 30 cm or

SO cm diameter, in October 1989 (n = 24 pools, pooled across mid- and low-shore sites for each exposure). (B)

Total ( + SE) number of species (uncorrected for area) on basal stratum of IS cm deep pools, 30 cm or SO cm

diameter, in January 1990 (n = 12 pools, 2 pools from each of 6 sites for each combination of height and

exposure). Other details as in Fig. I.

on the shore. Where grazers were allowed into pools, they had a much smaller impact on foliose algae at lower than higher levels (Underwood and Jernakoff, 1984). Thus, algae, even in the presence of grazers, can colonize and survive better in pools lower on the shore which is probably attributable to the greater opportunities to grow in the lower parts of the shore (Underwood and Jernakoff, 1984).

Further explanations for the relationship between patch-size and abundance of foliose algae will not be dealt with in detail here. The patterns relating to diameter were


20

15 1 October 1989

20

15

10

5

0

January 1990

a

a

July 1990

a

a

15 30 50 15 30 50 exposed sheltered


Fig. 10. Total ( + SE) number of species (corrected for area) on stratum 5 of 5 cm deep pools, 15 cm, 30 cm or

50 cm diameter, in October 1989, January 1990 and July 1990 (n = 24 pools, pooled across mid- and

low-shore sites for each exposure). Other details as in Fig. 1.

complicated by interactions with exposure and height on the shore and these will be covered elsewhere (Underwood, data not shown).

The only other variables we analysed which showed similar consistency in the effects of patch-size were numbers of species (or species richness) and density of species (species cmP2). Species may be distributed among patches of different size in two ways (Keough, 1984b). First, they can be arranged at random with respect to patch-size with larger patches having more species due to sampling effects (see also McGuinness, 1984). Second, particular species may be found disproportionately on patches of a certain size

82

Table 4

A./. Underwood, G.A. Skilleter I J. Exp. Mar. Biol. Ecol. 197 (1996) 63-90

Analyses of mean number of species (corrected for area sampled) in pools with different diameters for three

times. Other details as in Table 2.

Stratum

s 15 30 B

Tl T2 T3 Tl T2 T3 Tl T2 T3 Tl T2 T3

5 cm deep pools

Diameter * * * EXD *

HXD

D X S(EH)

EXHXD

I5 cm deep pools

Diameter ***

EXD

HXD

D X S(EH)

EXHXD

30 cm deep pools

Diameter ***

EXD

HXD

D X S(EH)

EXHXD

*** ***

*

***

*

*** *

*** *

*

*** *** *** *

*** *** *** * *

**

*** *

*

DNE ***

DNE *** *

*** ** *** *** ** *

* ** *

*** ***

*** **

***

** *

*** *

*** **

**

*** ** *

(Keough, 1984b). Here, the latter arrangement would be detected as significant differences in the composition of the assemblage in different sized pools.

In almost all circumstances, the number of species increased with increasing diameter of rock pool, yet we detected no significant differences in the structure of the assemblages in different sized pools using multivariate analyses. Although these results do not specifically test the null model of random placement (see Coleman et al., 1982; McGuinness, 1984), they suggest that more complicated models to explain the species- area relationships do not need to be invoked.

When the number of taxa per unit area was analysed, there were significantly more species in the narrower pools. This difference represented an increase of about 50% in the number of species from the narrowest to the widest pools (see Fig. 7 and Fig. 8).

This finding is interesting with respect to theories concerning patterns of species-area relationships. The general finding of increased number of species with increasing size of

habitat (e.g., the review of McGuinness, 1984) is well-known. In general, two components of increased area are implicated, area per se and the inclusion of greater diversity of habitats in areas of larger size. There is no widespread consensus on how to interpret these because they are often correlated. Some authors (e.g., Johnson and Raven, 1973) consider them to be equivalent because increased area of islands is always associated with increased structure of micro-habitat. Others have considered them inevitably correlated but the species respond to increased availability of habitats (Johnson and Simberloff, 1974; Simberloff, 1974) or survive better because larger areas


a

30 50 30 50 mid low

20 B

15 1 a 10

5

0

; 20

f 15 z’

10

5

0

30 50 mid

C a

b

30 50

20 D exposea

l5fi A 1

a T

b

30 50 sheltered

a

0 30 50 30 50 3050 3050

exc;d- exprsed- sheltered- sheltered- low mid low


Fig. 1 I. Total ( + SE) number of species (corrected for area). (A) Stratum 15 of 15 cm deep pools in July 1990

(n = 24 pools); (B) basal stratum of 30 cm deep pools in October 1989 (n = 24 pools); (C) basal stratum of IS cm deep pools in January 1990 (n = 24 pools): (D) Stratum 15 of 30 cm deep pools in July 1990 (n = 12

pools). Other details as in Fig. 1.

support larger and genetically more variable populations less likely to go extinct (e.g., Brown, 1971; Johnson and Raven, 1973). Yet other interpretations treat the two components as separate and diversity of habitats to be the crucial issue (Hamilton et al., 1963). Some authors have, however, found effects of area alone (Simberloff, 1976).

The results here suggest two interpretations. First, many (in fact, the majority) of species are found in all pools, regardless of their diameter. The addition of more area in a wider pool of a given depth makes some but not a pro rata difference to the number of

84 A.J. Underwood, G.A. Skilleter I J. Exp. Mar. Biol. Ecol. 197 (1996) 63-90

A

Mid Exposed

A

. Low Exposed

,

.

Mid Sheltered

. %OA .o n B CT;w.boA A

. O A . AA 0

0

. AS . .

Low Sheltered

July 1990, 5 cm deep pools, stratum 5

n =15cm; 0=30cm; A=50cm

Fig. 12. nMDS ordination on fourth root transformed species abundance data from stratum 5 of 5 cm deep

pools in July 1990. There were six independent sites in every combination of exposure (sheltered versus

exposed) and height (mid-shore versus low-shore). II = 18 for IS cm diameter pools; n = 12 for 30 and 50 cm

diameter pools. See Section 2 for details.

species. This is not consistent with random placement of species which predicts pro rata decreases in number of species with decreasing area (e.g., McGuinness, 1984).

The present results are much more in line with some of the models proposed by conservation ecologists. For example, May (1994) proposed a ‘rule-of-thumb’ which, when inverted from his use of it, suggests that about 50% of species might be preserved

in only 10% of an area (Shafer, 1990). If a large proportion of the species in large pools are ubiquitous, then a large proportion of them must also be present in small pools, leading to the sorts of results described here.

Where area alone is the important influence, equilibria1 theory predicts that sampling standardized areas of patches of habitat of different sizes should lead to more species per unit area where the patches are larger (Kelly et al., 1989; Kohn and Walsh, 1994). The opposite occurred here supporting that area, per se, is not the factor determining number of species.

Yet, in these experimental pools, the surface areas were created at the same time and are featureless, the surfaces are smooth and uniform (absolutely for 15 and 30 cm diameter pools, created by diamond corers). Thus, for any given depth (i.e., in a

A.J. Underwood, G.A. Skilleter 1 J. Exp. Mar. Biol. Ecol. 197 (1996) 63-90 85

.

. .O t O

Mid Exposed

. 0

0m .

0

0 00 00 0” n n

Low Exposed

. .

I ao 0

0 .

0 n m .

%“” O . 0

0 0

Mid Sheltered

n

.o 0 o- . om so

0 00 w n 0

n 0

0 0

July 1990,30 cm deep pools, stratum 5

W=30cm; 0=50cm

Fig. 13. nMDS ordination on fourth root transformed species abundance data from stratum 5 of 30 cm deep

pools in July 1990. Other details as in Fig. 12.

particular stratum) in a pool, it is unrealistic to propose that pools with greater diameter can contain an increased diversity of habitats.

More and more, the generality of processes and patterns originally described at a

n =15cm; 0=30cm; A=50cm

Fig. 14. nMDS ordination on fourth root transformed species abundance data from stratum 5 of 5 cm deep pools in July 1990 showing each of the mid-shore exposed sites (see Fig. 12) separately. n = 3 for 15 cm

diameter pools; n = 2 for 30 and 50 cm diameter pools. See Section 2 for details.

86 A.J. Underwood, G.A. Skilleter I .I. Exp. Mar. Biol. Ecol. 197 (1996) 63-90

single (or a few) site(s) or on a single occasion, is being challenged through investigations of higher-order interactions between spatial and/or temporal scales and supposed explanatory models (e.g., kelp beds, Foster, 1990; Kennelly and Underwood, 1992, 1993; subtidal algal assemblages, Schiel, 1990; soft-sediments, Peterson and Beal, 1989; rocky intertidal habitats, Fairweather and Underwood, 1991; see also, for reviews, Underwood and Denley, 1984; Underwood and Petraitis, 1993). These studies have almost universally shown that it is extremely difticult and premature to propose general models for the structure of assemblages in marine habitats based on observations made at a small number of sites or on only a few occasions.

Many previous studies (e.g., Femino and Mathieson, 1980; Huggett and Griffiths, 1986; Kooistra et al., 1989; Benedetti-Cecchi and Cinelli, 1992; Parker et al., 1993; Metaxas et al., 1994) have only examined rock pools at one or a few sites and have described patterns of structure in the observed assemblages based on these restricted data (but see Dethier, 1982, 1984; Astles, 1993). It is difficult to see how these data could then be used to formulate more general models about the processes structuring assemblages in rock pools, even though this is usually the goal of such studies.

The present work demonstrates a fundamental difference in approach to that used in most previous studies on the structure of assemblages in rock pools. Here, when examining the effects of patch-size (diameter) on these assemblages, we have only described examples where significant results involving diameter were consistent across several different spatial scales, at many sites and among different times. Thus, we have not described each and every significant result of the 324 analyses of variance because few of these were repeated on many occasions, nor at many of the twenty-four sites. We have, therefore, avoided identifying ‘important’ (Foster, 1990) processes based on results from a limited number of sites or times.

A similar approach was used by Foster (1990) when he compared twenty different rock platforms on the coast of California. He found that he could not readily explain observed patterns of distribution of potentially competing species of algae on the basis of competitive interactions he had previously demonstrated experimentally at only one of these sites (Foster, 1982). The conclusion was that the relative importance of competition between these species of algae was small on the basis of the proportion of sites in which the process could explain observed patterns of abundance. Similarly, we found that particular patterns of abundance which may ostensibly have been related to the diameter of pools at a few sites or even at one height on the shore, were not repeated at other sites. If this aspect of patch-size cannot reliably explain patterns of abundance of taxa in rock pools found on shores spread over approximately one kilometre, then it is extremely unlikely that it would be able to provide generalisations applicable to other sections of the coast nor to other coastlines.

There was also considerable variability at the scale of replicate pools in the abundance of individual taxa and in the structure of the entire assemblage. Small-scale variability may be a characteristic of patchy marine habitats (see also McGuinness, 1987a, intertidal boulders; Keough, 1984a,b, subtidal epibiotic sessile assemblages; Astles, 1993, natural rock pools). The existence of variability at several different spatial scales further emphasises the need for any explanatory models to be based on observations from each of the appropriate scales (Andrew and Mapstone, 1987).


Sampling in natural rock pools (see references above) has shown that assemblages in pools are variable within and between different exposures and heights on the shore. Previously, it has been impossible to unconfound whether these differences were due to position or some component of ‘patch size’. Any two natural pools may vary not only in their position on a shore but also in their depth and diameter. Our results demonstrate experimentally that one of these measures of patch size, diameter, is not important in determining the abundance of most common taxa found in pools across many sites on a rocky shore.

This conclusion strongly implicates the effects of depth as a primary source of variability in the structure of these little-understood habitats. Before the patterns of increasing numbers of species in assemblages of pools of different sizes can be understood, two aspects of the depth of pools must be analysed. Increased depth of pools obviously increases the area of substratum for pools of a given diameter. Deeper pools, however, also add complexity of habitat by provision of deeper habitats (i.e., more strata). The roles of these two components of depth and their interactions as influences on assemblages in pools will be considered elsewhere with the influences of wave- exposure and height on the shore. This analysis is made much simpler by the elimination of diameter of pools as an important influence on most of their inhabitants.

Acknowledgments

This work was supported by funds from the Australian Research Council (Program Grant and Special Investigator Awards to AJU) and from the Institute of Marine Ecology. We are grateful to many people for help with sampling but particularly K. Astles who worked on all aspects of the project. We thank Dr A.J. Butler for advice and Drs M.G. Chapman and W.P. Sousa for their comments on the manuscript.

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