the influences of physical factors on the distribution and zonation patterns of south african...

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The influences of physical factors on thedistribution and zonation patterns of SouthAfrican rocky-shore communitiesR. H. Bustamante , G. M. Branch & S. EekhoutPublished online: 08 Apr 2010.

To cite this article: R. H. Bustamante , G. M. Branch & S. Eekhout (1997) The influences of physical factorson the distribution and zonation patterns of South African rocky-shore communities, South African Journal ofMarine Science, 18:1, 119-136, DOI: 10.2989/025776197784160901

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S.Afr. J. mar. Sci. 18: /19-/361997

THE INFLUENCES OF PHYSICAL FACTORS ON THE DISTRIBUTIONAND ZONATION PATTERNS OF SOUTH AFRICAN ROCKY-SHORE

COMMUNITIES

R. H. BUSTAMANTE*, G. M. BRANCHt and S. EEKHOUTt

Vertical zonation and horizontal distribution patterns of both community biomass and species richness ofrocky-shore marine invertebrates and algae are described at a broad geographic scale for scven West andseven South-East Coast intertidal rocky-shore communities situated between southern Namibia andKwaZulu-Natal, South Africa. There were consistent patterns for community biomass and species richness, bothof which showed similar vertical and horizontal distributions in equivalent habitats, regardless of geographicallocation. This indicates that the processes which create these patterns operate and vary in a similar way, evenbetween different geographical regions. Multivariate techniques were used to assess, at a local scale, therelative importance of wave energy, rock temperature and shore elevation on the structuring and spatialvariability of community biomass. Direct gradient analyses revealed that wave action strongly influences thestructure of mid- to low-shore communities, whereas the interaction between rock temperature and shoreelevation (both of which influence desiccation potential) produces convergence of high-shore communities.There was a significantly positive relationship between wave action and the per-unit-area communitybiomass, and a negative relationship between shore elevation and biomass. The potential role that wavesmay play in determining overall intertidal productivity is discussed.

119

All species live in a characteristic limited range ofhabitats and, within their range, they tend to be mostabundant at their particular environmental optimum(Whittaker 1975). It has been consistently shown thatbiological communities exhibit trends along environ-mental gradients, regardless of the particularities oftheir habitat (Brown 1984). These "gradients" do notnecessarily have physical reality as continua in eitherspace or time, but are a useful abstraction for exploringthe distributions of organisms (Austin 1985). Whittaker(1967) developed the first quantitative approaches toecological gradient analysis to assist the interpretationof spatial changes in community composition in termsof species' responses to environmental variations.Such techniques can either be exploratory, i.e. toexamine how community composition varies withthe environment, or confirmatory, i.e. a means of testingthe effects of a particular environmental variable whiletaking into account the effects of other variables (TerBraak and Prentice 1988).

Numerical multivariate analyses have been longused in ecology to explore such gradients (see reviewof James and McCulloch 1990) and applied to a rangeof different marine communities (e.g. Field et at. 1982,McLachlan et al. 1984, Austen 1989, Kautsky andVan der Maare11990, van der Meer 1991, Castric-Feyand Chasse 1991, van Nes and Smit 1993, Santos1993), including intertidal rocky communities (e.g.Field and McFarlane 1968, Field and Robb 1970,

Kooistra et ai. 1989, Fuji and Nomura 1990). Allthese works have explored the importance of thejoint relationship between community data and envi-ronmental factors. Such analytical methods offersuccinct summaries of large datasets, and often playa creative role in suggesting causes; at a later stagethese can be formulated into new research hypothesesand causal models (James and McCulloch 1990), andthen subjected to experimental manipulation (Under-wood 1986).

The body of evidence relating to the ecologicalstructure and regulation of marine communities(especially intertidal ecosystems) has largely concen-trated on how particular species respond differentiallyto ecological processes such as disturbance, predation,competition or recruitment (e.g. Connell 1961,Paine 1966, Underwood and Denley 1984,Lubchenco 1986). Only recently have the effects of theenvironment on the regulation and structuring ofwhole marine benthic communities or species as-semblages been addressed (Menge and Sutherland1987, Menge and Farrell 1989, Menge and Olson1990, McGuiness 1990). However, intertidal ecolo-gists have long recognized that two of the most im-portant local physical forces structuring intertidalrocky shores are gradients of desiccation, whichproduce a vertical zonation, and the differentialeffects of wave forces that generate a horizontal zona-tion (Dayton 1971, Stephenson and Stephenson

* Formerly Coastal Ecology Unit, Zoology Department, University of Cape Town, Rondebosch 7701, South Africa; now Charles DarwinResearch Station, Puerto Ayora, Isla Santa Cruz, Gahipagos Islands, Apartado Postal 17-01-389], Quito, Ecuador E-mail:[email protected]

t Coastal Ecology Unit, Zoology Department, University of Cape Town, Rondebosch 7701 South Africa. E-mail: [email protected]

Manuscript received: October 1997

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120 South African Journal of Marine Science 18 1997

1972, Sousa 1979a, b, Underwood et al. 1983,Dayton et al. 1984, Menge and Sutherland 1987,Menge and Farrell 1989, Menge and Olson 1990).Those studies suggest that community structure(abundance and diversity of species) depends ona complex interplay between large-scale (e.g. envi-ronmental stress and productivity) and small-scaleprocesses (e.g. strong biotic interactions). The studieshave highlighted the need for further comparativestudies that simultaneously evaluate the contributionof environmental stresses at large and local scalesto variations in community structure (Dayton andTegner 1984, Menge and Sutherland] 987, Foster et al.1988, Menge and Olson ]990). However, compari-sons of particular environmental factors, such astemperature and wave action, are of little value whenthey are made between disjunct localities, becauseday-to-day changes in local weather can supersedeany observed differences. More fruitful are compar-isons within different localities (e.g. exposed v. shel-tered or high- v. low-shore), because they can bemade simultaneously under comparable conditions.

The rocky intertidal biota of southern Africa isamong the most varied in the world (Stephenson andStephenson ]972, Branch and Branch 198], Branchet al. ]994). These rocky shores have been the focusof extensive local ecological research, centred on theidentification of forces structuring rocky-shore com-munities. The majority of these works have dealtwith the identification of particular factors, includingseveral biotic interactions (Branch 1985, 1986, Branchet al. 1987, Bosman and Hockey 1988, Van Zyland Robertson 1991), abiotic factors (Field andMcFarlane 1968, Field and Robb 1970, McQuaid andBranch 1984, 1985, Huggett and Griffiths 1986,Bosman et al. 1987, Branch et al. 1987, McQuaidand Dower 1990, Field and Griffiths 1991), or acombination of abiotic and biotic factors (McQuaidet at. 1985, Griffiths and Hockey 1987). Griffithsand Branch (1991) concluded that physical factorscontrol the abundance and vertical zonation of domi-nant species, whereas subordinates are biologicalcontrolled. Among the physical factors, those authorsrecognized that wave action and desiccation areperhaps the most important. Despite the generalacceptance of theimportance of these factors, inSouth Africa and elsewhere (e.g. Lewis 1976,Underwood 1981, Foster et al. 1988, Menge andOlson 1990, McGuinness 1990), their variationamong sites, and comparisons at local and meso-geo-graphical scales are seldom documented.

The effects of the environment (leading to physio-logical and/or mechanical stress) have been incorpo-rated into general community models as independentvariables (Hairston et al. 1960, Connell 1975, Menge

and Sutherland 1976, 1987). To evaluate these models,it is necessary to quantify the main environmentalgradients independently and the community variationalong them. Moreover, this needs to be done at dif-ferent spatial scales (Menge and Sutherland 1987)before one can synthesize the main environmentalfactors (and their interactions) that influence variationin community structure.

The purpose of the present study is threefold:

(i) at a broad geographical scale, to describe, evaluateand compare zonational trends in biomass zona-tion and species richness of rocky intertidalcommunities at seven localities on the westcoast compared with seven localities on thesouth and east coasts of southern Africa;

(ii) to assess the relative importance of such physicalfactors as wave force, shore elevation and rocktemperature on species richness, biomass anddistribution at two specific but geographicallydisjunct localities, namely Groenrivier on theWest Coast and Port Elizabeth on the SouthCoast;

(iii) to relate zonation patterns of intertidal species toenvironmental variables at a local scale.

The study is exploratory and descriptive in natureand relies on direct gradient analyses to detect andexplore patterns in community structure and theircorrelations with physical variables. As such, it laysthe groundwork for developing specific hypothesesto explain community patterns, which can then betested experimentally.

MATERIAL AND METHODS

The sites

Data on zonation patterns were collected at 14 dif-ferent localities around the southern African coast(Liideritz, Port Nolloth, Tweepad, Rooiklippies,Spoegrivier, Groenrivier, Paternoster, Cape Infanta,Mossel Bay, Tsitsikamma, Port Elizabeth, Dwesa,Ballito Bay and Cape Vidal, see Fig. 1). Data arecompared in more detail from the intertidal rockyshores of Groenrivier (30°48'S, 1T30'W) on the WestCoast and from Port Elizabeth (34°00'S-26°37'W)on the South-East Coast (Fig. I). At each of theselocalities, either two or three sites were selected torepresent contrasting grades of wave action - i.e.sheltered boulder bays, semi-exposed rocky shores(in the lee side of kelp forests and present only onthe West Coast) and exposed rocky headlands. The

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1997 Bustamante et al.: Zonation of South African Intertidal Rocky Shores 121

S

NAMIBIA

LOderitz

Cape peninsu,a-l

Fa/seBay

KWAZULU·NATAL

SOUTH AFRICA

Port ElizabethTsitsikamma

/NO/ANOCEAN

ATLANTICOCEAN Kilometres

I . I . I . Io 100200 300

E

Fig. 1: The coast of southern Africa showing the study sites and other localities mentioned in the text

sites were chosen to ensure comparability in orienta-tion, slope (between IS and 45· inclination) and sub-stratum type (sandstone). Both localities experiencea similar semi-diurnal tidal regime and tidal ampli-tude, the latter being respectively 2.21 and 2.40 m atspring tide for Groenrivier and Port Elizabeth (SouthAfrican Navy 1993).

Data acquisition

The average (± 1 SE) values of community biomassper unit area for all sites were used to describe generalbiomass patterns in relation to rocky intertidal zona-tion (vertical and horizontal). Standard communitysurveys were carried out at each locality. In brief, ateach site, four replicate transects 15 - 30 m long

were laid down perpendicularly to the sea edge.Along each transect, eight quadrats (0.5 m2 each)were randomly placed, and the biomass contributionper species (converted to g·m-2 of ash free dry mass,AFDM), density, species richness (total number ofspecies per quadrat) and trophic structure were recorded.Only the data for the most important species wereemployed in the biomass analyses (i.e. those contri-buting >0.01 % to the total biomass, including infaunaland epibiont species). To document species richness,all species present in each quadrat were counted;small, cryptic species were also included, down to abody length of 1 mm. By confining the informationto the data obtained from quadrats, quantitativelyequivalent measures were obtained at all sites. It isrecognized, however, that this approach will havefailed to detect many of the rarer species, so that

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In total, 140 samples (70'm-2) were taken atGroenrivier and Port Elizabeth - the two particularlocalities where detailed environmental data weregathered. These yielded 101 algal and invertebratetaxa, all of which were used in the analyses of speciesrichness. For the biomass and multivariate analyses,only taxa that contributed >0.01 % to the total biomasswere induded - i.e. 38 and 34 taxa for Groenrivierand Port Elizabeth respectively. These taxa com-prised > 71% of the species richness and >95% ofthe total biomass recorded at each site during thesurveys. The contribution of individual species to thecommunity biomass ranged through five orders ofmagnitude (from 0.2 to c. I 700 g·m-2). Consequently,the biomass data were logarithmically transformed

Data analysis

.total biodiversity is underestimated. A more detailedaccount of the sampling methodology and a full datasetcan be found in Bustamante (1994).

At Groenrivier and Port Elizabeth, three environ-mental variables were recorded. At the positions ofall quadrats used to sample the biota, measurementswere made of (a) shore elevation (height) aboveMean Low Water Spring tide (MLWS), (b) rock tem-perature, and (c) wave force. Shore elevation wasmeasured using a water-level device which recorded thedifference in height between each sampled quadratand the zero level (MLWS). Wave force (measuredin N'm-2) was defined as the force exerted by wavesover a hollow hemispherical drogue, divided by thecross-sectional area of the drogue, and was measuredwith dynamometers, using a modified version of theJones and Demetropoulos (1968) apparatus, describedand tested by Palumbi (1984). At the position of eachquadrat, a series of three parallel dynamometers wasfastened to the rock surface perpendicularly to the di-rection of waves. The dynamometers were left insitu for a period of three days and the maximal waveforces exerted on the dynamometers during eachtidal cycle were recorded. For comparisons betweensites, absolute or average wave forces are frequentlynot critical (Denny 1988). However, simultaneousmeasurements and the use of identical drogues areabsolutely essential.

Rock temperatures were measured simultaneouslywithin each quadrat during low tide, every hour forthree consecutive days. Using epoxy glue, 30 Ga Type Tthermocouples were attached to the rock surface.Temperatures detected with these thermocoupleswere recorded by a Bat-12 Bailey Instruments digitalthermocouple reader.

(e) Exposed

(a) Sheltered

o

50 100 150 200 250 300ELEVATION ABOVE MLWL (em)

Vertical zonation of the average (±1 SE) biomass atseven localities on the west coast of southern Africa(clear symbols) on (a) sheltered, (b) semi-enclosedand (c) exposed shores. Solid symbols indicate thedata from Groenrivier. The trend lines were weight-

fitted to the total dataset with a 50% smoothing

3000

2000

1000

3000

Fig. 2:

c\J 1 (b) Semi-exposed'E• 3000Ol

~::20

1 L~~ 2000C/) jC/)« L1:2: 10000lD

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1997 Bustamante et at.: Zonation of South African 1ntertidal Rocky Shores 123

o

(a) Sheltered3 000 -

2 000

NE 1 000•OJ l;;.{:,~ ~ 40Ii.$Cf)Cf)

(b) Exposed«~ 3 000QCD

2 000

1 000


Fig. 3: Vertical zonation of the average (±1 SE) biomass atseven localities on the south-east coast of southernAfrica (clear symbols) on (a) sheltered and (b) ex-posed shores. Solid symbols indicate the data fromPort Elizabeth. The trend lines were weight-fitted to

the total dataset with a 50% smoothing

[loglo(x+l)] and standardized (proportions). Theordinal environmental variables (elevation, tempera-ture and wave action) were treated as continuousvariables.

To detect trends in the vertical distribution of bio-mass and of species richness, curves were fitted tothe plots by using the locally weighted least-squarederror method. This curve fit has no data restrictionsand has no parameters associated with it. The result ofthis curve fit is to plot a best-fit smooth curve throughthe centre of the data, or 50% smoothing. This is anextremely robust fitting technique and, unlike standardregression methods, is minimally sensitive to outliers(Press et at. 1986).

Linear regressions and univariate non-parametricanalyses of variance (ANOYA by ranks) with a-poste-

riori mean comparisons of main effects (Bonferronit-test) were performed for the comparison of shoreelevation, rock temperature and wave exposure betweenand within localities. All ANOVAs and regressionswere performed using Generalized Linear Models,GLM (SAS 1986).

To explore the joint relationship between the bio-mass of rocky intertidal species assemblages and theselected environmental variables, a multivariate (or-dination) direct gradient analysis was performed.Canonical Correspondence Analysis (CCA) was usedto correlate the biomass of the benthic communitywith the abiotic variables (Ter Braak 1986, Palmer1993). Direct gradient analysis was carried out usingthe average biomass per species at each height interval,for Groenrivier and Port Elizabeth independently.The environmental variables used in the analyses werethe maximum wave force, maximum rock temperatureand shore elevation. The computer package CANOCOv2.1 (Ter Braak 1987) was used to perform CCA(Ter Braak and Prentice 1988).

RESULTS

Biomass

When comparing all the localities around the coast,two different zonation patterns were detected forcommunity biomass, and these could be related todifferences in wave exposure. First, on sheltered shoresof both the West and the South-East coasts, communitybiomass was maximal on the low-shore, and decreasedexponentially upshore (Fig. 2a), although this patternwas less obvious on the South-East Coast (Fig. 3a). Atall shore heights, biomass was lower on the South-East coast than on the West Coast. Maximal valuesof 2 000 (± 445) g.m-2 were recorded on the WestCoast, but only 700 (±135) g.m-2 on the South-EastCoast. At shore height >50 em, in both West andSouth-East intertidal communities, the average biomassnever exceeded 450 (± 58) g.m-2• The upper limit ofintertidal biota was approximately 250 em aboveMLWS at both sites (Figs 2a and 3a).

Second, on semi-exposed and exposed shores onboth West and South-East coasts, biomass peaked inthe mid-shore (50-100 em). Low on the shore, bio-mass was intermediate between mid- and high-shorevalues (Figs 2b, c, 3b). The maximum biomass valueson the West Coast were 2 675 (± 168) and 3 726(± 150) g'm-2 for semi-exposed and exposed shoresrespectively, whereas the biomass on South-East Coastexposed shores never exceeded 2 500 (± 362) g'm-2

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124 South African Journal of Marine Science] 8 ]997

(a) Sheltered20

15

Cf)wc..>w

5 a..Cf)I.L.0II:Wco:;;E

(b) Semi-exposed~z

Cf) 20 IIw 0Uw 0a.. D CD [0Cf) 15 .D:JOI.L. • DO 00 U[]]

o coII: IT.JJJOuOw 10 o ~ 0(D ~I;0

0:2~ OJ 0 0z 5 00 ~1I00o 0 0

o ~~~M ----D_o .-:0 0

20o

15

10

5

(a) Sheltered

(c) Exposed


Fig. 4: Vertical zonation of the total number of species persampling quadrat at seven localities on the westcoast of southern Africa (clear symbols), on(a) sheltered, (b) semi-exposed and (c) exposedshores. Solid symbols indicate the data fromGroenrivier. The trend lines were weight-fitted to the

total dataset with a 50% smoothing

Fig, 5: Vertical zonation of the total number of species persampling quadrat at seven localities on the south-east coasts of southern Africa (clear symbols). on(a) sheltered and (b) exposed shores. Solid symbolsindicate the data from Port Elizabeth. The trendlines were weight-fitted to the total dataset with a

50% smoothing

(Figs 2 and 3). On the West Coast, intertidal commu-nities of the semi-exposed and exposed shores extendedsignificantly higher than on the sheltered shores(ANOVA, p < 0.001), the upper limit of the semi-exposed and exposed shores (350 cm) being signifi-cantly greater than that of sheltered shores (247 cm,Bonferroni t-test, p < 0.5, Fig. 2). Similarly, on theSouth-East Coast, exposed shores had a significantlyhigher upper limit (350 'cm) than sheltered shores(259 cm, Bonferroni t-test, p < 0.05, Fig. 3). At shoreheights >150 cm, average ,community biomass rangedbetween 74 and 420 g'm-2 and did not differ signifi-cantly between sites with different degrees of waveaction, or between localities.

In summary, the overall biomass was consistentlyhigher on the West Coast than on the South-EastCoast, higher at wave-exposed sites than sheltered

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/997 Bustamante et at.: Zonation of South African Intertidal Rocky Shores 125

Fig. 6: Maximum values recorded of (a) wave force and(b) rock temperature in relation to tidal elevation onexposed, semi-exposed and sheltered shores at

Groenrivier and Port Elizabeth

Species richness

On the West Coast, the maximum number of speciesper sample was 20, the highest values being reachedbelow the mid-intertidal (50-100 em above MLWStide) on semi-exposed and exposed shores (Figs 4b, c).Sheltered shores attained a maximum of only 14species, being achieved low in the shore (Fig. 4a).Similar patterns were found at exposed and shelteredshores of the South-East Coast (Fig. 5), except thatspecies richness was higher there than on the WestCoast. More specific examination of the two sites atwhich physical measurements were made, i.e. Groen-rivier and Port Elizabeth, revealed similar verticaldistribution patterns of species richness (Figs 4, 5).The vertical distribution of species richness thusparallels the patterns described for biomass.

Abiotic factors

The abiotic parameters measured at Groenrivier andPort Elizabeth are plotted in relation to shore eleva-tion in Figure 6. The maximum values of wave forcerecorded on exposed sites at Groenrivier (15000 N'm-2)were significantly greater (ANOYA, p < 0.0001) thanthose of sheltered shores (1 500 N·m-2). Semi-exposedshores experienced intermediate wave energies, witha maximum wave force of 7 000 N'm-2 (Fig. 6a).Similarly, exposed sites at Port Elizabeth (10 000 N'm-2)had significant greater wave forces (ANOYA,p < 0.0001) than sheltered shores (1 100 N·m-2). Thevertical distribution of wave force at exposed sitesfollowed a similar trend to that of community biomassand species richness (see Figs 2-5), i.e. mediumforces on the low-shore (0-20 em), and a peak onthe mid-shore, decreasing towards the high-shore. Onsheltered shores, there was no obvious vertical trendin the wave force distribution as elevation increased(Fig.6a).

There was a positive relation between the maximumrock temperatures and shore elevation at all sites(Fig. 6b). In the low-shore, rocks had a temperatureclose to that of sea water; higher up the shore, tem-peratures rose to 45"C. The overall rock temperaturesat Groenrivier (23.1 ± 8SC) and Port Elizabeth(30.9 ± 9.2°C) were marginally different (ANOYA,p < 0.049), but no differences were found betweentheir respective wave forces in habitats with corre-sponding exposure (ANOYA, p > 0.810). No greatsignificance can be attached to these differences,however, because prevailing weather conditions wouldhave strong influences on differences between regions.Within regions, temperature did differ on shoresexperiencing different grades of wave action, but noconsistent pattern emerged (Fig. 6b). At Groenrivier,semi-exposed shores were cooler than sheltered or

,.- -.

Groenrivier Port ElizabethExposed _ - - • - -Semi-exposed -Ir-

-0- - - c- - -

50 100 150 200ELEVATION ABOVE MLWL (em)

(a)

(b)

20

10

40 -

~ 30 -()~

•

wa::Jt;;:a:wCl...:2:wI-::.:::()

oa::2::J:2:X«:2:

~w 15000-()a:ou.w 10000-~:s:3 5000-:2:><«:2:

sites, and peaked Iowan the shore at sheltered sitesbut just below mid-shore on more exposed sites.

At both the localities studied in more detail, i.e.Groenrivier and Port Elizabeth, semi-exposed andexposed shores had intermediate levels of biomasson the low-shore «30 em), and maximum biomassbelow the mid-shore (50-100 em, Figs 2 and 3), andclosely followed the patterns described above for theWest and South-East coasts as a whole. Similarly, onsheltered shores at these two localities the biomasswas concentrated in the low-shore, followed by asharp up-shore decrease at Groenrivier (Fig. 2a), buta more gradual decrease at Port Elizabeth (Fig. 3b).The average community biomass was significantlygreater at Groenrivier than at Port Elizabeth (Fig. 3),at both exposed and sheltered shores (ANOYA,p < 0.001; Bonferroni t-test, p < 0.05).

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126 South African Journal of Marine Science ]8 ]997precluded the use of each of these factors in isolationas explanatory variables for local variation in com-munity biomass.

GROENRIVIER

Community structure and species composition

PORT ELIZABETH

On sheltered sites, 68% of the total communitybiomass was contributed by five taxa (Table I). These·were the kelps Ecklonia maxima and Laminaria pal-lida (combined 15.0%), the limpet Patella granatina(18.5%), which forms dense monospecific stands inthe low- to mid-shore (Bustamante et at. 1995), andlarge colonies of the polychaete Gunnarea capensis(17.8%). High on the shore the red alga Porphyracapensis (17.2%) formed dense patches. However,the species most frequently found in samples was thelimpet Patella granularis (12.1 %). The next mostfrequent species were the sea anemone Bunodactisreynaudii and two species of the scavenging whelksBurnupena spp. (B. cincta and B. catarrhacta), bothpresent in 9.9% of the samples.

On semi-exposed shores, 90% of the total communitybiomass accounted for three species, whereas a further24 different taxa contributed the remaining 10%(Table I). Of the dominant species, the limpetPatella argenvillei (29.9%) formed a conspicuousmonospecific band of c. 2 m width on the low-shore(Bustamante et ai. 1995). In the mid-shore, largecolonies of the polychaete Gunnarea capensis(35.5%) formed a complex mosaic with the alienmussel Mytilus galloprovincialis (25.0%). The most fre-quently encountered species in the samples wereP. granularis (17.1%) and M. galloprovincialis (11.0%).

In exposed sites, M. galloprovincialis (77.0%)dominated much of the entire mid- to low-shore,forming dense mussel beds which housed a number ofcryptic species. The mussel beds were interspersedwith patches of Gunnarea capensis (6.7%) and over-grown by epibiont algae «5%, Table I). The mostfrequently encountered species were the limpetp. granularis (16.1 %), the sea anemone Bunodactisreynaudii (13.8%) and the indigenous mussel Aula-comya ater (11.2%).

The community biomass of sheltered shores atPort Elizabeth was dominated by the colonial poly-chaete Pomatoleios kraussii (42.2%), several speciesof articulate coralline algae (14.7%), the red algaeGelidium spp. (7.6%), together with two limpets,Patella barbara and P. oculus, and the encrusting

(r2 = 0.367;p<0.02)

t+

t

4000 8 000 12 000 16 000MAXIMUM WAVE FORCE (N • m-2)

3 000

4000

5 000 (a)

2 000

1 000

3000

Fig. 7: Relationship between average (±1 SE) intertidalcommunity biomass and (a) maximum wave forceand (b) maximum rock temperature at Groenrivier

(solid symbols) and Port Elizabeth (open symbols)

exposed shores, which did not differ significantlyfrom one another (ANOVA, p > 0.05). At PortElizabeth, no significant differences were foundbetween sheltered and exposed shores (Fig. 6b).

The average community biomass was positivelycorrelated with maximum wave force and negativelycorrelated with maximum rock temperature at bothGroenrivier and Port Elizabeth (Fig. 7). There is anobvious inverse relationship between wave force androck temperature, one being negatively and the otherpositively related to tidal elevation. This situation

2 000

-0'

5 10 15 20 25 30 35 40 45MAXIMUM ROCK TEMPERATURE (OC)

~Clu.~(f)

~5 000 (b)oco

4000

N'E1 000

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o<"i-NN

I \0 V)odvi00N

1 1 1 V) "'"~~0\0N"'"

I I 1-0\-&<"iN

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Table III: Eigenvalues and percentage of variance accounted for by the four axes of the CCA ordination of samples andspecies scores for Groenrivier and Port Elizabeth

Groenrivier Pan ElizabethAxes

Eigenvalue % Variance Eigenvalue % Variance

I 0.805 43.9 0.816 36.42 0.559 30.6 0.661 29.53 0.306 16.7 0.472 21.04 0.162 8.8 0.293 13.1

Hildenbrandia sp. (Table II). All these species wereconcentrated low on the shore. The mid- and high-shore communities were characterized by numerousmobile grazers and predatory gastropods, but thesecontributed little to the total biomass. The mostfrequent species, however, were grazers, specificallytwo species of winkle, Oxystele variegata andO. impervia (combined 10.9%), the pulmonatelimpets Siphonaria spp. (8.7%) and the limpetsPatella oculus and Helcion spp. (8.0% each, Table II).

On the exposed sites at Port Elizabeth, as at Groen-rivier, >50% of the community biomass consisted offilter-feeders, in this case the mussel Perna perna(36.3%), the barnacle Tetraclita serrata (10.2%) andthe colonial polychaete P. kraussii (9.1 %), all con-centrated in the low- to mid-shore. However, the mostcommon species in the samples were P. granularis(8.4%), Burnupena spp. (6.6%) and Siphonaria spp.and P. perna (6.0% each, Table II).

Direct gradient analysis

The graphical results of the canonical correspon-dence analyses for the rocky communities associatedwith the environmental factors are presented inFigure 8. The figure displays the combined 2D-biplotof species (abbreviations), samples (numbers) andthe environmental vectors (arrows), where arrowsindicate the relative importance (length) and directionof each vector. At Groenrivier (Fig. 8a), the ordination

along the x-and y-axes explained 43.9 and 30.6% ofthe total community variance respectively (Table III).Similarly, in the ordination for the communities ofPort Elizabeth the same axes accounted for 36.4%and 29.5% of the total variance with respect to theenvironmental variables (Table III). For both localities,the first two canonical axes of the species ordinationwere significantly linked to the environmental variables(Monte Carlo permutation test, p < 0.01), and soindicate significant differences in the species compo-sition between shores of differing wave exposure.

At both sites, the separation of samples along thex-axis clearly illustrates the vertical zonation of thecommunity, with the low-shore samples being indicatedby smaller numbers (0, 1, 2) and positioned to theright where the x-axis is positive, whereas the largernumbers (5, 6, 7), indicating the high-shore samples,are placed to the left where the x-axis is negative(Fig. 8). Along the y-axes, the samples taken withineach of the different wave exposures group together,with the exposed sites at the bottom of the y-axis andsheltered sites at the top. The semi-exposed sites atGroenrivier occupied an intermediate positionbetween sheltered and exposed (Fig. 8a). Therefore, they-axis in both ordinations clearly indicates a gradientof wave energy.

At Groenrivier (Fig. 8a), the x-axis was significantlycorrelated with all environmental factors, the highestcorrelation being obtained with the interaction betweenelevation and rock temperature (r:: -0.812, p < 0.005,Table IV). Similarly, at Port Elizabeth (Fig. 8b), the

Table IV: Weighted correlation coefficients between the environmental variables and the first 2 axes of the CCA ordination.Degrees of freedom = (Number of samples - Number of factors)-1

Environmental Groenrivier (n=21) Port Elizabeth (n=14)variable

x-axis p y-axis p x-axis p y-axis p

Wave force 0.605 <0.005 -0.665 <0.001 0.502 >0.05 -0.842 <0.001Rock temperature -0.727 <0.005 -0.095 >0.5 -0.822 <0.001 -0.44] >0.05Shore elevation -0.71] <0.005 -0.504 >0.05 -0.834 <0.001 -0.398 >0.1Rock temp. x Shore elev. -0.812 <0.005 -0.390 >0.05 -0.888 <0.0005 -0.454 >0.05

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Fig. 8: Ordination diagram based on canonical correspondence analysis of the rocky intertidal communities at(a) Groenrivier and (b) Port Elizabeth with respect to three environmental variables (wave force, rock temperatureand elevation). Increasing numbers indicate the sampling stations from low- to high-shore in the different communities.Arrows show the magnitude (length) and direction of the environmental vectors. Full species/taxa names

corresponding to abbreviations are listed in Tables I and II

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1997 Bustamante et at.: Zonation of South African Intertidal Rocky Shores 131

highest and most significant correlation was betweenthe x-axis and the interaction of elevation and rocktemperature (r = -0.888, p < 0.0005, Table IV). They-axis was correlated only with maximum wave forceat both Groenrivier and Port Elizabeth (r = -0.665,p < 0.001 and r = -0.842, p < 0.001 respectively,Table IV). In short, the relative magnitude (length) ofthe different environmental vectors (arrows in Fig. 8)indicates that maximum wave force principally, andthe interaction between elevation and rock tempera-ture (second longest vector), were the most importantenvironmental factors in the ordination of the com-munities of both Groenrivier and Port Elizabeth.

In all samples taken in the high-shores of bothlocalities, the molluscan genera Littorina, Oxystele andSiphonaria were always represented, independentlyof wave exposure or geographic differences (Fig. 8),indicating convergence of the species assemblages inthe upper shore. Convergence is also illustrated bythe close positioning of the high-shore sites (6, 7, 8)in the ordination (Fig. 8). Conversely, completelydifferent pools of species characterized low-shoresamples (0, I, 2) experiencing different degrees ofwave action. Divergence of community structure istherefore a feature of the low-shore samples, and ismost obvious on the y-axis of the ordination and solinked to differences in wave exposure (Fig. 8). AtGroenrivier, several algae are clear indicators ofsheltered low-shore sites, together with the limpetP. granatina. At Port Elizabeth, this habitat supporteda different group of algae and two other limpets,Patella longicosta and P. oculus.

Semi-exposed low-shore sites featured an a'isemblageof kelps and Patella spp., including P. argenvillei,which is tightly associated with growths of the kelpsLaminaria pallida and Ecklonia maxima (Bustamanteet al. 1995).

The exposed shores were clearly characterized bythe presence of filter-feeders, especially the musselsA. ater and M. galloprovincialis at Groenrivier andthe mussel P. perna and the barnacles T. serrata andO. angulosa at Port Elizabeth (Fig. 8). These speciestend to be positioned near the end of the wave forcevector in the ordinations.

DISCUSSION

Patterns of vertical distribution of intertidal speciesassemblages have been intensely studied since theearly works on zonation (e.g., Stephenson 1942,Lewis 1964, 1976, Stephenson and Stephenson 1972,Moore 1975, Underwood 1978). In contrast, there islittle published information on horizontal zonationpatterns (Menge and Farrell 1989). In particular, the

quantitative responses of intertidal communities tohorizontal gradients have not been fully explored(Foster et at. 1988).

Southern African rocky intertidal communitiesshow consistent patterns of both vertical and hori-zontal biomass over spatial scales (Figs 2, 3). Twopatterns are consistent over large geographical scales.The first is that exposed shores support a muchgreater biomass than protected shores, a pattern pre-viously demonstrated on the cold-temperate shoresof the Cape Peninsula (McQuaid and Branch 1984).However, the "spread" of the biota from low- tohigh-shore indicates that the major concentration ofbiomass on semi-exposed and exposed sites occursconsistently between low- and mid-shore (Figs 2, 3).This contrasts with sheltered sites, where communitybiomass is concentrated on the low-shore. Althoughthere is no equivalent dataset available in the literature,biomass patterns can be inferred from descriptiveworks (e.g. Menge and Farrell 1989) and from esti-mates of relative abundance or percentage coverage.The vertical patterns on exposed shores found in thisstudy are generally comparable with those describedfor equivalent temperate regions in the South andNorth-Eastern Pacific (Santelices et at. 1977, Fosteret at. 1988, Menge and Farrell 1989) and the North-Western Atlantic (Menge 1976, Lubchenco andMenge 1978), where the low-shore appears to sup-port intermediate levels of biomass because of thedominance of a few species of encrusting algae andmobile species. There is convincing evidence that, in thelow-to-mid zones of rocky shores, biological inter-actions (either predation or competition) have impor-tant influences on community structure, with consumerscontrolling the abundance of space-occupying speciesin the low-shore while the mid-shore level is dominatedby sessile species, notably mussels and/or barnacles(Paine 1971, 1974, Menge 1976). However, a differentvertical distribution pattern has been described forexposed rocky shore in False Bay on the south coastof South Africa (McQuaid and Branch 1985), wherelarge colonies of sessile filter-feeding invertebratesand understory algal turf constitute the majority ofthe low-shore biomass. This latter situation indicatesthat consumers are not effective in controlling space-occupying species. Descriptions of part of the BritishIsles (Lewis 1964, Newell 1979) and South Australia(Stephenson and Stephenson 1972) suggest a similarpattern. Unfortunately, there is no information aboutthe species richness nor the degree of wave exposure ofthose communities, precluding a direct comparison.

Consistent vertical and horizontal patterns of thespecies richness were found independent of geogra-phi cal location (Figs 4, 5). Many of the more recentstudies of intertidal ecology have emphasized therole of scale in the maintenance and production of

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species diversity (e.g. Dayton 1971, Underwood andFairweather 1985, Petraitis et ai. 1989, Menge andOlson 1990). However, most of the comparative studiesfor patterns of species richness have failed to makecomparison between shores with comparable abioticenvironments (McGuinness 1990). Similarly, most ofthe studies of intertidal diversity do not include (ordo not mention) species occupying secondary sub-strata (e.g. Foster et ai. 1988, McGuinness 1990),leading to conclusions that are applicable only to thediversity of species occupying primary rock space.For example, the removal of mussels (space-dominantspecies) leads to an increase of the diversity of speciesusing rock as a primary substratum (e.g. Harger] 972,Paine 1971, 1974, Suchanek 1978, Paine et al. 1985),while decreasing the diversity of the epifaunal andinfaunal species associated within the mussel bed(Lohse 1993). In the present study, the consistency ofthe patterns of species richness is greatly strengthenedby the fact that all localities were compared withinequivalent physical environments (Figs. 4, 5) and allspecies living on secondary substrata were included.

The present findings confirm the prediction ofDayton and Tegner (1984) that many of the processesinvolved in the creation of patterns of species richnessand biomass act and vary at a local scale (i.e. at thescale of sites within shores). Wave action impactsstrongly on the low- to mid-shore community structureand causes the development of radically differentassemblages on a scale of tens of metres. This effectyields comparable responses over very large geographicscales, covering thousands of kilometres and threedistinct biogeographic provinces (Emanuel et ai. 1992).

The relative importance of the determinants of thezonation patterns (vertical and horizontal) for inter-tidal rocky-shore communities varies with scale (Daytonand Tegner 1984, McGuinness 1990, Menge andOlson 1990). Considered in more detail here are twoparticular localities where differences in communitystructure are influenced by coastal geomorphology(headlands, boulder bays, kelp beds, etc.) and, hence,differential wave forces (Fig. 6a). The magnitude ofthese local differences in wave forces will certainlybe greater than any that can be experienced betweendifferent geographical regions. Furthermore, the simplelocal effect of vertical environmental gradients (i.e.rock temperature, elevation and their interaction) onthe spatial distribution of the species assemblageswere consistently similar within localities and onlymarginally different between the disjunct geographicallocalities (Fig. 6b). This implies that the physiologicalstress imposed by tidal movements on intertidalorganisms, although operating at an extremely localscale, has comparable effects over large and meso-geographical scales.

Wave action is often considered as a stressingfactor that induces physical disturbance. Hence, it isexpected to cause random, localized mortality(Petraitis et al. ]989, McGuinness] 990). However,the present findings show that there is a positive re]a-tionship between the biomass per unit area and themaximum drag force exerted by waves (Fig. 7a).This relationship agrees with results reported byLeigh et ai. (1987) for the North-Eastern Pacific, wherethe sea palm Poisteisia palmaeformis producesextraordinary quantities of dry matter per unit area inwave-beaten sites. In summary, Leigh et al. (1987)conclude that wave energy enhances the productionof intertidal systems. This, together with the resultspresented here, is an important consideration thatneeds to be taken into account when deciding whichfactors (and their respective interactions) need to beincorporated into environmental stress models forcommunity regulation (e.g. Menge and Olson ]990).

The results of the direct gradient analysis support,with quantitative evidence, the traditional assumptionthat gradients of emersion and magnitude of waveforce are major local determinants of rocky intertidalcommunities (Menge and Farrell 1989). The analysesused only three simple environmental factors and asingle interaction, yet explained 65 and 74% of thevariance in community biomass recorded at two dis-junct geographicalloca]ities (Tab]e III).

The first gradient in the ordination diagrams (Fig. 8)was the desiccation gradient, as indicated by thearrows representing the rock temperature, elevationand their interaction. ]n addition, the overall communitybiomass (regard]ess of wave exposure) was negativelycorrelated with rock temperature (Fig. 7b). Fie]d andRobb (1970), using a quantitative indirect gradientanalysis, showed that this vertical gradient has a majoreffect on the intertidal species assemblages of therocky shores of False Bay (see Fig. 1). Although theanalyses by those authors were done using differentstatistical techniques and sampling procedures, and ona much more limited geographical scale, their resultsagree with the present findings. Unfortunately, thereare few equivalent multivariate community analyses forintertidal shores, the majority of such studies havingbeen devoted to soft-bottom or subtidal ecosystems(e.g. McLachlan et al. 1984, Gray et al. 1988, Dawson-Shepherd et ai. 1992, Van Nes and Smit 1993,Warwick and Clarke 1993). However, in all intertidalrocky shores that have been analysed in this manner,shore elevation plays an important role in explainingthe vertical changes in species composition (e.g.Kaandorp 1986, Koistra et ai. 1989, Takada andKikuchi 1990).

The second major gradient was one of wave energy,and yielded three (Fig. 8a) or two (Fig. 8b) distinct

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species assemblages. The fact that sessile filter-feedersare more abundant on exposed shores (McQuaid andBranch 1984, 1985, McQuaid et al. 1985) was alsoclearly shown in this analysis. On wave-exposedshores, filter-feeders contributed >67% of the com-munity biomass at both cold- and warm-temperatesites (Tables I, II). At Groenrivier the mussels A.ater and M. galloprovincialis and at Port Elizabeththe mussel P. perna and the barnacles T. serrata andO. granulosa were the dominant space-occupyingspecies, and prevailed where wave energy was greatest.This was noticeable in the ordinations (Fig. 8) inwhich these species were all placed close to the endof the wave force vectors. In part, this associationmay be related to the fact that wave action enhancesthe quantity and turnover of food particles for filter-feeders (Bustamante and Branch 1996). Mussel bedsprovide a suitable (shelter) microhabitat for severalco-occurring species that are seldom found living onthe bare rock. In the ordinations, cryptic species likethe nereid mussel worm P. variegata, the predatorywhelks Nucella spp. and predatory anemones (e.g.Bunodactis reynaudii) were all placed close to themussel species (Fig. 8). All of these species eithershelter among, or feed on, mussels.

The convergence of the upper shore and the diver-gence of low-shore species assemblages was evidentin the gradient analyses (Fig. 8). Convergence suggeststhat the ecological response of the upper shore com-munities to the constraints of this environment is inmany ways similar, as has been suggested by previousstudies (Stephenson and Stephenson 1972, Lubchencoet al. 1984, McGuinness 1990). Three molluscangenera consistently featured in high-shore samples,irrespective of their geographic situation or the degreeof wave action experienced: Littorina, Oxystele andSiphonaria. All are known to be very tolerant ofphysical stresses such as high temperature, desicca-tion and low salinity (Broekhuysen 1940, Branch etal. ]990). Frequently their densities were very high,although they contributed relatively little to the bio-mass.

Equally evident was the consistent divergence ofintertidal species assemblages in the lower shore,which can be related to differences in wave energy.For some species this has obvious explanations. Flat-bladed algae such as Vlva, Aeodes, Gigartina spp.and Iridaea, which are presumably vulnerable to waveaction, occurred low on the shore only at shelteredsites. The limpet P. granatina (noted for its low powersof attachment) was an indicator of sheltered condi-tions at Groenrivier, and two other limpets, P. long i-costa and P. oculus (also known to have low tenacity- see Branch and Marsh 1978), occupied shelteredshores at Port Elizabeth. Sessile filter-feeders over-

whelmingly dominated exposed low- to mid-shoresamples and are both strongly attached and stand tobenefit from wave action because it enhances theirfood supply. However, for many species, these are asyet no rational explanation for the preferences forparticular intensities of wave action.

In summary, the implications are that low-shorecommunities are determined largely by differences inwave action, whereas high-shore communities are in-fluenced by the uniform stress of high temperatureand desiccation.

In a similar study using a multivariate approach,Fuji and Nomura (1990) investigated the relation-ships between community structure and environmentalfactors (i.e. categories of wave force, height abovedatum and microtopography) for the rocky-shoremacrobenthos of southern Hokkaido, Japan. Theiranalyses did not include algae. The authors' mainconclusion was that community structure of themacrofauna is primarily influenced by microtopogra-phic characteristics, whereas the effects of wave forceand shore elevation were not apparent. However,their work only reflects the effects of their samplingprocedure. That is, at a particular site, they sampledwith different intensity (some microhabitats wereunder-represented) all possible distinct microhabitats,i.e. nip, bench, ledge, slope and boulders (Fuji andNomura 1990, Table I). In their analyses, each parti-cular microtopographic category was subjected to abroad range of wave-force categories (which werenot determined by direct in situ measurements), sothat wave force could not be used as a discriminatoryenvironmental variable. Consequently, their conclu-sion that differences in microhabitat explain most ofthe variation in intertidal community structure, over-riding the effects of other potentially important envi-ronmental factors, is a consequence of their methodo-logy more than anything else. This case illustrates theurgent need for standardized methods of samplingand analyses of benthic communities patterns (Mengeand Farrell 1989). Unfortunately, in contrast to ter-restrial ecology, the use of multivariate analyses indescriptive ecology is not well established in studiesof the structure and organization of marine commu-nities.

In relation to the main objectives of this study, dis-tinctive community structures were detected at a localscale, whose differences are strongly related to localenvironmental conditions. At this level of exploratoryanalysis, biotic interactions seem of secondary~-portance. Differences in community structure mayresult from the small-scale variation of such physicalfactors as tidal gradient and wave exposure (bothexplored in this study), and as well as other mechanicaldisturbances such as ice scour, river runoff, etc. (not

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covered here), that will "set the stage" for subsequentbiological interactions between the survivors of envi-ronmental constraints (Menge and Olson 1990).

ACKNOWLEDGEMENTS

We acknowledge the great help provided byT. Phillips, A. and R. Sakko, I. Rojas and L. Krugerduring most of the fieldwork. During the intertidalsurveys around the southern African coast, severalpeople helped us with the "wet and cold" fieldwork,among them M. L. Branch, A. Linton, C. Velasquez,E. Turner and R. Navarro, who are gratefullyacknowledged. We also acknowledge E. Moll of theBotany Department, University of Cape Town (UCT)for allowing us to use CANOCO. The final versionof this manuscript was critically read and greatlyimproved by Profs P. A. R. Hockey and J. G. Field(both of the Zoology Department, VeT). Financialsupport was provided by the UeT Research Committee,the Foundation for Research Development (FRD),the South African Network for Coastal and Oceano-graphic Research (SANCOR) and the Department ofEnvironmental Affairs and Tourism (DEA & T) inthe form of grants to GMB, and FRD and UCTResearch Scholarships to RHB and SE.

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AUSTIN, M. P. 1985 - Continuum concept, ordination methods,and niche theory. A. Rev. Ecol. Syst. 16: 39-61.

BOSMAN, A. L. and P. A. R. HOCKEY 1988 - Life-historypatterns of populations of the limpet Patella granularis:the dominant roles of food supply and mortality rate.Oecologia 75: 412-419.

BOSMAN, A. L., HOCKEY, P. A. R. and W. R. SIEGFRIED 1987- The influence of coastal upwelling on the functionalstructure of rocky intertidal communities. Oecologia 72:226-232.

BRANCH, G. M. 1986 - Limpets: their role in littoral and subti-dal community dynamics. TnThe Ecology of Rocky Coasts.Moore, P. G .. and R. Seed (Eds). New York; ColumbiaUniversity Press: 97-116.

BRANCH, G. M. 1985 - Competition: its role in ecology andevolution in intertidal communities. In Species and Specia-tion. Vrba, E. (Ed.). Pretoria; Transvaal Museum: 97-104(Transvaal Mus. Monogr. 4).

B~NCH, G. M., BARKA1, A., HOCKEY, P. A. R. andL. HUTCHINGS 1987 - Biological interactions: causesor effects of variability in the Benguela ecosystem? Tn TheBenguela and Comparable Eco-systems. Payne, A. I. L.,GuJland, J. A. and K. H. Brink (Eds). S. Afr. 1. mar. Sci. 5:425-445.

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the influences of physical factors on the distribution and zonation patterns of south african...

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