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Estuarine, Coastal and Shelf Science 64 (2005) 658e670
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Spatial variability of intertidal rocky shore assemblagesin the northwest coast of Portugal
R. Araujo a,b, I. Barbara c, I. Sousa-Pinto a,d, V. Quintino b,*
a CIMAR, Centro Interdisciplinar de Investigacao Marinha e Ambiental, Rua dos Bragas, 289, 4050-123 Porto, Portugalb Departamento de Biologia, Universidade de Aveiro, CESAM, Centro de Estudos do Ambiente e Mar, Campus Universitario de Santiago,
3810-193 Aveiro, Portugalc Departamento de Bioloxia Animal, Bioloxia Vegetal e Ecoloxia, Campus da Zapateira, s/n. 15071 A Coruna, Spain
d Departamento de Botanica, Faculdade de Ciencias, Universidade do Porto, Rua do Campo Alegre, 1191, 4150-181 Porto, Portugal
Received 20 September 2004; accepted 18 March 2005
Available online 7 July 2005
Abstract
The spatial variability of rocky shore assemblages of the northwest Portuguese coast was studied in a total of 12 transects, visited
twice between March and August 2003. Each transect was positioned from the upper to the lower shore and four replicate samples(50! 50 cm) were taken at each visually identified assemblage. Multivariate analysis was used to test the null hypothesis of nosignificant differences among assemblages located on different heights along the transect and among assemblages located at the same
height on different transects. The distribution pattern of organisms along the height was not consistent across transects andsignificant variability could be found in assemblages located at the same height on the shore. Globally, the variability from the lowerto the upper shore (vertical axis) was larger than from transect to transect (horizontal axis) but the distribution pattern along height
was clearer in sheltered transects than in exposed ones. The heterogeneity in composition between the visually identifiedassemblages, within the same transect, was, however, the major source of variability in the study area. In the rocky intertidalnorthwest coast of Portugal, where tidal amplitude is broad and extremely wave-exposed sites are scarce, height above chart datum
was the most important factor determining the distribution and species composition of the assemblages. However, variability alongthe horizontal axis was also significant and should be considered in studies of spatial patterns of distribution of organisms withinthis area.� 2005 Elsevier Ltd. All rights reserved.
Keywords: macroalgae; spatial variability; intertidal; marine; NW Portugal
1. Introduction
Intertidal rocky coastlines are heterogeneous envi-ronments that support a wide variety of living forms. Inthese systems organisms are distributed in a particularway, occurring at specific levels along a height axis, from
* Corresponding author. Victor Quintino, Departamento de Biol-
ogia, Universidade de Aveiro, CESAM, Centro de Estudos do
Ambiente e Mar, Campus Universitario de Santiago, 3810-193 Aveiro,
Portugal.
E-mail address: [email protected] (V. Quintino).
0272-7714/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2005.03.020
the lower to the upper shore (Underwood, 1981;Ballesteros, 1995; Thompson et al., 2002). The observa-tion of these distribution patterns led to the develop-ment of several models of vertical zonation of organismson rocky shores. These models usually consider threemain zones on the shore, in relation to a gradient ofemersion/desiccation, containing distinct organisms: theupper shore, the midshore and the low shore (Stephen-son and Stephenson, 1949; Lewis, 1964; Peres andPicard, 1964; Seoane-Camba, 1969). Nevertheless,some authors considered these general zonation schemes
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over-simplified, given that elevation above chart datumalone could not explain all the variability encountered indistribution patterns and abundance of benthic organ-isms (Underwood, 1981; Boaventura et al., 2002).
Causes underlying the distribution patterns of organ-isms in intertidal rocky systems have been approached bymany authors. Examples include the role of competition(Schonbeck and Norton, 1980; Kastendiek, 1982;Jenkins et al., 1999a,b), herbivory and predation(Moreno and Jaramillo, 1983; Underwood, 1998; Wil-liams et al., 2000), settlement and recruitment (Connell,1985; Kaehler and Williams, 1997; Jenkins et al., 1999c,2000), height above chart datum (Schonbeck andNorton, 1978; Underwood, 1978; Bockelmann et al.,2002) and gradient of wave exposure (Underwood, 1981;Menge et al., 1993).
More recently, the role of small-scale topographyheterogeneity in regulating species distribution andabundance was investigated (Bourget et al., 1994;Archambault and Bourget, 1996; Thompson et al.,1996; Lapointe and Bourget, 1999; Williams et al.,2000). Species distribution can change over very smallspatial scales if the complexity of the habitat is high(Benedetti-Cecchi and Cinelli, 1997). In fact, mosaics oforganisms are an obvious feature of intertidal habitats,mainly at low levels on the shore (Menge et al., 1993).
Recent studies report on the variability in verticalpatterns of distribution of organisms among sites and inthe species composition of assemblages within the samelevel on the shore (Benedetti-Cecchi and Cinelli, 1997;Menconi et al., 1999; Kelaher et al., 2001). InMediterranean rocky systems, for example, Benedetti-Cecchi (2001) found more vertical than along-shorevariations at small scales but this tendency was notconfirmed at larger spatial scales.
Qualitative descriptions of intertidal rocky shoreassemblages for the Portuguese coast have been pro-vided by some authors (Boaventura et al., 2002).However, quantitative data on spatial patterns ofdistribution of organisms are scarcer. Examples includethe work of Boaventura et al. (2002), who reported onsignificant differences between the upper and the lowerparts of the midshore zone and between midshoreassemblages of the northern and southern coasts ofPortugal. No study ever addressed which of thesevariability axes is strongest on the Portuguese coast:the vertical axis, from the upper to the lower shore,versus the horizontal axis, across the shore, at the sameheight. The main objective of this work was toquantitatively analyse the distribution patterns of in-tertidal organisms along horizontal and vertical gra-dients, in a 60 km stretch of the northwestern coast ofPortugal. Different scales of variability were analysed:global horizontal and vertical variability along the studyarea, variability among and between different heights onthe shore and variability within transects.
2. Material and methods
2.1. Study area
The tidal regime along the Portuguese coast is semi-diurnal with the largest tidal range during spring tides of3.5e4 m. The northwest rocky shores are typicallygranite and the coast is exposed to the prevailingnorthwest oceanic swell, which can reach values over5 m in the winter. Sea surface temperature variesbetween 13 �C and 20 �C.
The northern Portuguese rocky intertidal ecosystemsare divided into three major zones, as described ingeneral zonation schemes by Stephenson and Stephen-son (1949), Lewis (1964), Peres and Picard (1964) andSeoane-Camba (1969). The uppermost zone of the shoreis dominated by incrustant lichens such as Verrucariamaura, Lichina pygmaea and Lichina confinis and by thegastropod Melaraphe neritoides. In the colder seasons,this level is also colonized by Porphyra linearis. Sessilefilter feeders such as Patella sp., Chthamalus sp. andMytilus sp. are the most common organisms at midlevels on the shore of exposed zones, brown algae suchas Fucus spiralis, Fucus vesiculosus, Ascophyllum nodo-sum and Pelvetia canaliculata being the predominantorganisms in sheltered midshore environments. Thelower littoral is characterised by the presence ofa considerable diversity of turf forming algae andcanopy species like Saccorhiza polyschides, Laminariaochroleuca, Laminaria hyperborea, Bifurcaria bifurcata,Chondracanthus acicularis and Himanthalia elongata.
2.2. Sampling
Sampling occurred in 12 sites, placed betweenMoledo (41 �50#5$N, 8 �52#18$W) and Apulia(41 �29#14$N, 8 �46#58$W) (Fig. 1). At each site thesampling points were positioned along a transectextending from the upper to the lower shore. Eachtransect was visited twice, between March and August2003. The positioning of transects was chosen accordingto the presence of extensive rocky shore systems and wasrestricted to bedrock. Rock pools were not considered inthis study. The study area comprehends exposed,moderately exposed and sheltered habitats.
In all transects, four replicate samples were taken ateach visually identified assemblage (homogeneous mac-roalgal assemblages) (Schils and Coppejans, 2003). Theunit sample, each replicate, corresponds to a quadrateof 50! 50 cm, divided into 25 sub-quadrates of10! 10 cm. The quadrates were placed randomlywithin each assemblage (Dethier et al., 1993). Percentcover was assessed by means of non-destructivemethods, by counting the number of sub-quadratesoccupied by each species and giving 4% cover toeach sub-quadrate. Whenever necessary, sampling was
660 R. Araujo et al. / Estuarine, Coastal and Shelf Science 64 (2005) 658e670
Moledo
Cepães
Apúlia
Amorosa
Montedor
Forte do Cão
Viana do Castelo
Vila Praia de Âncora
S. Bartolomeu do Mar
9°5'0"W 9°0'0"W 8°55'0"W 8°50'0"W 8°45'0"W
41°30'0"N
41°35'0"N
41°40'0"N
41°45'0"N
41°50'0"N
0 4 8 12 Km
Fig. 1. Study area. Transects distanced less than 50 m are marked in the same locality. The transects studied were: Moledo, Vila Praia de Ancora 1
and 2, Forte do Cao 1 and 2, Montedor 1 and 2, Viana do Castelo, Amorosa, S. Bartolomeu do Mar, Cepaes and Apulia.
stratified in different layers and the upper visible layer ofmacroalgae was distinguished from substrate cover,being estimates of percent cover made for each layerseparately (Dethier et al., 1993). Four replicates weretaken per assemblage on each sampling occasion.
The specimens which could not be identified in thefield were collected and identified in the laboratory. Allmacroalgae were identified to species level except for thegenus Ulva. Only sessile animal species were consideredin this study and were identified to the genus level. The
lichens Verrucaria maura, Lichina pygmaea and Lichinaconfinis were also considered.
Littoral level was calculated in relation to chartdatum. Height on the shore of the sampled communitiesvaried between 0 and 6 m above chart datum.
The concept of community used in this study is basedon the knowledge that species aggregate in a particularway in relation to biological factors and environmentalgradients, making it possible to recognize mosaics ofcommunities whose dominant species lead to the notion
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of homogeneous macroalgal assemblages (Turner andLucas, 1985; Menge et al., 1993; Ballesteros, 1995).
In this study the number of assemblages sampled inthe lower shore was higher than in the other levels, dueto the wider diversity of assemblages found in thatzone.
2.3. Data analysis
Data analysis was performed with non-parametricmultivariate techniques using the PRIMER software(Clarke and Gorley, 2001).
Samples similarity was calculated with the BrayeCurtis coefficient, after log (xC 1) data transformation.Non-metric multidimensional scaling (nMDS) was usedto produce two-dimensional ordination plots.
One-way ANOSIM (Clarke and Warwick, 2001) wasused to test the null hypothesis of no significantdifferences between: (1) sampling occasion; (2) assemb-lages located on different heights along transects evertical gradient; (3) assemblages located at the sameheight on different transects e horizontal gradient and(4) visually identified assemblages within the sametransect.
ANOSIM test produces a statistic (R-statistic) thatlies in the range (�1;1). Values of RZ 1 are obtainedonly when all replicates within groups are more similarto each other than any replicates from different groups(Clarke and Warwick, 2001).
To test the null hypothesis 1, samples were groupedinto a sampling occasion factor and the comparison wasmade between each visually identified assemblage withinthe same transect, and between each height class, alsowithin the same transect. This test also included thecomparison of the whole transect, sampled on the twooccasions. Only the global R-value for each height classand for the whole transect will be presented, given theelevated number of assemblages under test. To test forthe null hypothesis 2, a height factor was established,with the classes: below 1 m, 1e2 m, 2e3 m and above3 m. All the unit samples (each individual50 cm! 50 cm quadrate) obtained within each heightclass were regarded as replicates of the same heightfactor, independently of belonging or not to the samevisually identified assemblage. This analysis was con-ducted separately for each transect and for the wholegroup of transects. This test was conducted with thedata collected on the first sampling occasion. To test thenull hypothesis 3, a transect factor was considered. Allunit samples within the same transect and height classwere regarded as replicates. This test was conductedseparately for each of the four height classes. For thistest, only the global R-value (Clarke and Warwick,2001) for each height class will be presented, given thevery large number of possible pairwise comparisonsbetween transects (66). To assure data independence
from the previous test, this analysis was conducted withthe data collected on the second sampling occasion. Totest the null hypothesis 4, the unit samples were groupedinto an assemblage factor. The assemblages werevisually identified in each transect. Not all the assemb-lages are present in all transects. This analysis wasconducted separately for each transect, comparingpotentially distinct assemblages located on the sametransect. This test was conducted with data from six outof the 12 transects visited on the first sampling occasion,chosen randomly. Only the global R-value for eachtransect is presented. A similar test was conducted tocompare the same assemblage located on distincttransects. This analysis was conducted with datacollected on the first sampling occasion, from theremaining six transects.
The Primer Routine Relate was also used to test therelationship between the succession of communitiesalong height and a seriation matrix, representing thesampling sites according to this factor. This testproceeds by calculating and testing the significance ofa Spearman rank correlation between the two matrices(Clarke and Warwick, 2001).
3. Results
Concerning the variability between samples taken atthe same sites on different occasions, no significantdifferences were found between each transect (Table 1)or between some of the height levels (Table 2). However,significant differences were found between some of thevisually identified assemblages on the two samplingoccasions. In spite of presenting similar percent cover ofthe dominant species, these assemblages showed highvariability in the species composition and percent coverof the accompanying species. Higher on the shore, nosignificant differences could be found between the
Table 1
One-way ANOSIM. Global R-values and associated probability for
the comparison between the same transect sampled in the two
occasions. In this test, the null hypothesis was never rejected
Transect Global R p
1 0.069 0.71
2 �0.081 0.93
3 �0.027 0.61
4 �0.027 0.69
5 �0.07 0.73
6 0.059 0.15
7 �0.208 0.77
8 0.064 0.06
9 �0.114 0.98
10 �0.250 0.99
11 �0.064 0.89
12 �0.122 0.92
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majority of the visually identified assemblages on thetwo sampling occasions. These assemblages have muchlower diversity of the accompanying species. As anexample from one of the transects, the low shoreassemblage dominated by Chondrus crispus presenteda total of 26 accompanying species in the four replicates,while the high shore assemblage dominated by Pelvetiacanaliculata had only a total of five accompanyingspecies in the four replicates. Overall, the lack ofsignificant difference between the two sampling occa-sions allows using all the data to test different null
Table 2
One-way ANOSIM. Global R-values and associated probability for
the comparison between the same height levels sampled in the two
occasions. The null hypothesis was not rejected for the lowest (!1 m)
and the highest (O3 m) height levels. *non-significant
Height (m) Global R p
!1 0.005 0.32*
1e2 0.079 0.005
2e3 0.159 0.001
O3 �0.011 0.56*
hypothesis, without introducing significant variabilityrelated to the temporal gap between the collections ofthe two data sets.
The ordination diagrams of the individual transectsshow that height above chart datum may play differentroles in different transects. The relationship betweenassemblages and height on the shore was not the samefor all transects, as shown in the ordination diagramsdepicted in Fig. 2. The worst relationship was encoun-tered for transects illustrated in Fig. 2a and b, whereasfor those illustrated in Fig. 2cef, the relationship wasmuch clearer. In Fig. 2e and f, the variability among thesamples taken at the same height on the shore was alsoimportant, mainly at mid and higher levels. Table 3presents the Spearman rank correlation calculatedbetween the BrayeCurtis similarity matrix from in-dividual transects and a seriation model matrix accord-ing to the position of the sites along the height on theshore. The values obtained corroborate the MDS plotsand clearly indicate that the distribution of theassemblages does not show the same relationship tothe height factor across transects. Both results suggest
<1m 1 - 2m 2 - 3m 3 - 4m 4 - 5m
Stress: 0,09
Stress: 0,12
Stress: 0,07
Stress: 0,07Stress: 0,07
Stress: 0,11
Fig. 2. Two-dimensional nMDS ordinations for six of the 12 transect studied. Each point refers to a single replicate and each symbol to a different
height on the shore. Data from the first sampling occasion. (a) Moledo; (b) Apulia; (c) Montedor 1; (d) Vila Praia Ancora 1; (e) Vila Praia Ancora 2;
(f) Amorosa.
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an interaction between the two main factors and as suchthe test of the null hypothesis of no differences amongtransects was conducted separately for each height level.Also, the test of the null hypothesis of no differencesamong height levels was conducted separately for eachtransect.
When testing the height factor, significant differencescould be found among all height levels, the majorexceptions being obtained between the highest levels, asshown in Table 4. The R-statistic values given in Table 4,globally for each transect (global R) and separately foreach height at each transect, vary widely from transectto transect, again suggesting that height above chartdatum plays different roles in different transects.Similarly, when testing for the difference among trans-ects, separately for each height level, the values of theR-statistic were significant at all heights on the shore asshown in Table 5, with relatively similar values for eachlevel. Table 5 only presents the global R-values for theANOSIM test among transects, separately for eachheight level, given the large number of pairwisecomparisons among transects. Although both factorsappear significant, when including all transects in thesame analysis, the global R-values for the height factor(vertical axis) and for the transect factor (horizontalaxis) were, respectively, 0.38 and 0.17, indicating that
Table 3
Spearman rank correlations for six transects obtained between the
BrayeCurtis similarity matrix and a model seriation matrix in which
sites are displayed according to their height on the shore
Site r
Moledo 0.297
Apulia 0.191
Montedor 1 0.767
Vila Praia de Ancora 1 0.496
Vila Praia de Ancora 2 0.456
Amorosa 0.718
variability between the assemblages was larger acrossthe vertical gradient.
Exposure to wave action may be a possible explana-tion for the fact that the distribution of assemblagesalong the height factor was not similar across alltransects in the study area. Fig. 3 shows the distributionof the total number of species per height level, fortransects with different degrees of exposure to the waveaction, while Fig. 4 presents the vertical distribution of afew species in the same transects (see also Appendix A).The total number of species varies from transect totransect and seems to be higher in less exposed transects.Also the number of species at the lower levels on theshore seems to be higher on sheltered transects than onexposed ones (Fig. 3). In exposed shores, the low andmidlittoral zones are dominated by animal organisms such asMytilus sp. and incrustant algae such as Lithophyllumincrustans (Fig. 4), while the moderately exposed and thesheltered shores are dominated by macroalgae at the lowlittoral levels and by animals at mid levels. However, themacroalgae species composition and their abundance aredifferent in moderately exposed shores and in shelteredones, as show in Fig. 4 (see also Appendix A). Also, thereare differences in the vertical extent of the area colonizedin shores with different degrees of exposure to waveaction. In exposed transects, most probably due tosplash, organisms colonize higher levels on the shore (4e5 m) than in sheltered ones (Fig. 4). In spite of thesevariations, each species usually appears more abundantwithin a particular height interval on the shore in alltransects where it occurs, as shown in the ordinationdiagrams represented in Fig. 5.
Finally, the visually identified assemblages weresignificantly different within transects. The global R-values for six transects chosen at random were alwaysabove 0.96, as shown in Table 6. Of all the pairwisepossible comparisons between assemblages, only twopresented the R-value below 0.5 and the associatedprobability above 0.05. The far majority of the visually
Table 4
One-way ANOSIM for the test of the null hypothesis of no differences between assemblages located on the various heights on the shore at each
transect. The values of the R statistic are shown with the respective probability values. Notice that the associated significance depends on the number
of possible permutations (as an example, for transect 1, RZ 1 between (!1 m)e(O3 m) but r! 0.01, while RZ 0.39 between (!1 m)e(1e2 m) but
r! 0.001). *r! 0.05; **r! 0.01; ***r! 0.001; n.s., non-significant
Transects
1 2 3 4 5 6 7 8 9 10 11 12
Height (m)
(!1)e(1e2) 0.39*** 0.92*** 0.36*** 0.35*** 0.59*** 0.57*** 0.95*** 0.80*** 0.37** 0.44** 0.71*** 0.98**
(!1)e(2e3) 0.41*** 1.00*** 0.88*** 0.99*** 0.99*** 0.73*** 0.93*** 0.42*** 0.91*** 1.00* 0.68*** 0.03
(!1)e(O3) 1.00** 0.97*** 0.98*** 0.75*** 0.47*** 0.81*** 0.26***
(1e2)e(2e3) 0.35** 0.79*** 0.16* 0.57*** 0.09n.s. 0.72** 0.58* 0.01n.s. 0.22* 0.31* 0.38*** 0.13
(1e2)e(O3) 0.54*** 0.66*** 0.84*** 1.00*** 0.23* 1.00** 0.38***
(2e3)e(O3) 0.14n.s. 0.41*** 0.99*** 0.858** 0.23*** 0.19n.s. 0.01n.s.
Global R 0.40*** 0.90*** 0.46*** 0.68*** 0.56*** 0.61*** 0.88*** 0.27*** 0.47*** 0.45*** 0.62*** 0.10**
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identified assemblages are thus significantly differentfrom each other, including when the comparison wasmade between the same potential assemblages located indistinct transects. Only the assemblages dominated byanimal organisms (Mytilus sp., Patella sp. and Chtha-malus sp.) were consistently, significantly similar be-tween themselves. The majority of the assemblagesdominated by algae were significantly different betweenthemselves, even the ones dominated by the samespecies. This difference was due to the variation inspecies composition and cover percentage of the ac-companying species.
Table 5
One-way ANOSIM for the test of the null hypothesis of no differences
between assemblages located on the same height on the shore, on
different transects. Values of the global R and associated probability.
***r ! 0.001
Height (m) Global R
!1 0.303***
1e2 0.324***
2e3 0.356***
O3 0.376***
38 27 42 77 69 52
} } }
Fig. 3. Total number of species along the height on the shore and for
the whole transect, in 6 of the 12 transects studied. Two transects
correspond to exposed shores (E) (Moledo (ML) and Apulia (AP)),
two transects refer to moderately exposed shores (SE) (Montedor 1
(MT) and Vila Praia de Ancora 1 (VPA1)) and two transects refer to
sheltered shores (S) (Vila Praia de Ancora 2 (VPA2) and Amorosa
(AMO)).
4. Discussion
For the northern Portuguese intertidal rocky shorewe could not find consistent patterns of distribution oforganisms along the vertical axis across sites and nohomogeneity between assemblages located within thesame level on the shore, but on different transects. Theseresults are in agreement with those reported byBenedetti-Cecchi and Cinelli (1997) for the Strait ofMagellan and by Benedetti-Cecchi (2001) for Mediter-ranean rocky shores. Important horizontal variability ata scale of a few meters in species dominating assemb-lages was also referred by Underwood (1981), fora rocky intertidal community of New South Wales.
When analysing the individual distribution of organ-isms along transects, it was clear that the majority of thespecies appeared only at some levels on the shore. Theoccurrence of any given species at a particular height onthe shore is well documented (Underwood, 1981), beingthe patterns of distribution of organisms in intertidalhabitats attributable to physiological needs in relation tophysical stress and biological interactions (Schonbeckand Norton, 1978, 1980; Kastendiek, 1982; Benedetti-Cecchi et al., 2000a,b). However, it was not possible toidentify groups of species recurrently occurring withineach tidal level across sites. In fact, the various transectspresented large differences in specific composition.
Apart from the observed distribution patterns foreach species, it must be emphasized that withina particular level on the shore, different mosaics ofspecies coexist (assemblages). The dominance in each ofthese assemblages is usually attributable to particularspecies with high cover percentage. Within the sameheight level, large variability existed in the assemblages’composition across transects. For instance, in somesites, communities dominated by Chondrus crispuscoexist with assemblages with high cover percentage ofGelidium sesquipedale, while in other sites, at the sameheight level, assemblages of Gigartina pistillata appearedtogether with communities of Bifurcaria bifurcata.
Increasing evidence points to the importance ofsmall-scale variation in the species composition ofassemblages within large zones (low, mid and highlittoral), along the vertical gradient (Menge et al., 1993).This variability was a conspicuous feature of the systemstudied here. Thus, it is important to consider small-scale variability between assemblages; otherwise thehorizontal variability between assemblages in any givensite can be underestimated.
The processes that regulate the variability in speciescomposition at small spatial scales have been the subjectof recent studies. Recent findings show that small-scalesubstratum heterogeneity is important in determining theassemblages’ structure within any particular height.Archambault and Bourget (1996), studying the pro-portion of variability explained by large and small spatial
665R. Araujo et al. / Estuarine, Coastal and Shelf Science 64 (2005) 658e670
Chondracanthus teedii
} } } } } } } } }
} } } } } } } } }
} } } } } } } } }Chondracanthus acicularis Chondrus crispus
Rhodothamniella floridula Mytilus sp. Chthamalus sp.
Patella sp. Lithophyllum incrustans Lomentaria articulata
Fig. 4. Representation of the vertical distribution of some species, in 6 of the 12 transects studied. Two transects correspond to exposed shores (E)
(Moledo (ML) and Apulia (AP)), two transects refer to moderately exposed shores (SE) (Montedor 1 (MT) and Vila Praia de Ancora 1 (VPA1)) and
two transects refer to sheltered shores (S) (Vila Praia de Ancora 2 (VPA2) and Amorosa (AMO)).
666 R. Araujo et al. / Estuarine, Coastal and Shelf Science 64 (2005) 658e670
Stress: 0,13
Chondrus crispus
Stress: 0,13
Chondracanthus acicularis
Stress: 0,13
Mastocarpus stellatus
Stress: 0,13
Sacchorhiza polyschides
Stress: 0,13
Fucus spiralis
Stress: 0,13
Chthamalus sp.
Stress: 0,13
Mytilus sp.
Stress: 0,13
Porphyra linearis
Stress: 0,13
Verrucaria maura
Stress: 0,13
Pelvetia canaliculata
Fig. 5. Two-dimensional nMDS ordinations for all transects sampled. Each plot represents the distribution pattern of a single species, being the circle
area proportional to the mean percent cover of species at each site.
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scales, found that variability in species richness wasexplained by large scale variability while differences inabundances were attributable to small-scale spatialvariability (!20 cm). Lapointe and Bourget (1999) alsofound that the substratum heterogeneity was the mostimportant factor determining community structure.Also, Bourget et al. (1994) demonstrated that substratumheterogeneity and complexity strongly structured thesmall-scale distribution of species during the earlydevelopment phases of a marine epibenthic community.Structural complexity may reduce environmental stressexperienced by intertidal communities during low tide(Thompson et al., 1996), allowing the development ofa higher diversity of assemblages. Biological interactionsare also responsible for the development of mosaics ofcommunities at small-spatial scales (Kaehler and Wil-liams, 1997; Johnson et al., 1998; Leonard, 1999;Benedetti-Cecchi et al., 2000b; Williams et al., 2000).
In this study, the major source of variability was thecommunities’ species composition within transects. Thecolonization history, small-scale substratum heterogene-ity, biological interactions and organisms’ physiologicalneeds can, altogether, contribute to the heterogeneity inassemblage structure found within each site. Benedetti-Cecchi (2001) suggested that the relative importance ofphysical factors such as tidal height and of physicalattributes of the habitat, such as small-scale spatialvariability, could depend on the magnitude of each ofthese factors. In microtidal systems, like the Mediterra-nean Sea, where physical factors are not importantlimiting factors, variations in physical attributes of thehabitat may be important in determining communitystructure (Benedetti-Cecchi, 2001). The relative impor-tance of each of these factors remains unknown for thePortuguese coast.
In our study area, the distribution patterns oforganisms showed different relations with height onthe shore. The worst relationship was observed in veryexposed sites. In these sites, the number of macroalgaein the low littoral zone was much lower than the onefound in other transects, except for incrustant forms likeLithophyllum incrustans, while the number of sessilesuspension feeders (mainly Mytilus sp.) and invertebrate
Table 6
One-way ANOSIM. Values of global R and associated probability for
the comparison between the visually identified assemblages within six
transects randomly chosen. Values of the global R and associated
probability. ***r ! 0.001
Transect R
1 0.983***
2 0.993***
5 0.961***
8 0.979***
11 0.978***
12 0.967***
herbivores (mainly Patella sp.) was higher. The exposedsites present very harsh conditions for algae to settle,while mussels profit from these environments where theyfind great feeding opportunities due to high flow andenhanced ‘splash’ (Dahlhoff and Menge, 1996). In veryexposed systems, the degree of exposure may thus be themost important factor affecting communities, disablingthe identification of clear distribution patterns inrelation to shore height or to small-scale spatialvariability. In this study, the strongest relation betweenthe distribution patterns of organisms and height on theshore was encountered in moderately exposed andsheltered shores. Several authors mention the grade ofexposure as an important factor regulating the assemb-lages’ composition (Underwood, 1981; Hawkins, 1983;Menge et al., 1993). Menge et al. (1993) refer thatprocesses maintaining macrophyte mosaics in the lowlittoral zones differ from wave-exposed to wave-shel-tered sites. The exposure grade can also influence thespatial distribution patterns of organisms along theshore. A tendency for shifting upwards the distributionof organisms with increasing wave exposure is welldocumented (Underwood, 1981). This tendency was alsoobserved in the present study. Moreover, the grade ofexposure to waves can also explain the vertical patternsobserved in the sheltered places. In these habitats, waveaction is unable to reach high shore levels which maylimit the vertical extent of the colonized shore area.Thus, organisms occurring at mid and higher levelsoverlap their distribution due to limitations on verticalspace.
In the studied area, the global variability in theassemblages’ composition along the vertical axis wasmore pronounced than along the horizontal axis. Heightin relation to chart datum seems to be the mostimportant factor affecting globally the communities’structure. Moreover, horizontal variability between siteswas also significant. We suggest that in the northwestcoast of Portugal, with broad tidal amplitude and whereextremely exposed sites are scarce, height on the shore isthe major factor determining spatial variability in theassemblages’ species composition. However, horizontalvariability, namely related with grade of wave-exposureat larger spatial scales and small-scale spatial heteroge-neity, was also significant and must be considered instudies within this area.
Acknowledgments
This work was developed under the project ‘Distri-bution, use and conservation of the botanical heritageof the Northern Coast of Portugal: a sustainabledevelopment approach for a (future) ‘‘Natura 2000’’site’ (PNATBIA15204/99) funded by the Portuguese
668 R. Araujo et al. / Estuarine, Coastal and Shelf Science 64 (2005) 658e670
Foundation for Science and Technology (FCT). Thefirst author was the recipient of a fellowship from thisproject. The authors acknowledge the help of CristinaCorreia during the field work.
Appendix A.
Species composition in an exposed (E e Apulia), amoderatly-exposed (M e Vila Praia de Ancora 1) and asheltered (S e Vila Praia de Ancora 2) transect, atdifferent heights on the shore. Only species with morethan 1% of mean cover percentage were considered.
Species composition of transects with different degrees of wave
exposure
!1 m 1e2 m 2e3 m 3e4 m O4 m
S M E S M E S M E S M E S M E
Ahnfeltiopsis
devoniensis
C
Bifurcaria
bifurcata
D C D
Calliblepharis
jubata
C
Callithamnion
tetricum
C
Ceramium
botryocarpum
C
Ceramium
echionotum
C
Ceramium
pallidum
C
Chondracanthus
acicularis
D C D
Chondracanthus
teedii
D C
Chondria
coerulescens
D
Chondrus crispus D D D C
Cladostephus
spongiosus
C
Codium
tomentosum
C
Corallina
elongata
C C D D D
Cryptopleura
ramosa
C C
Cystoseira
tamariscifolia
C
Desmarestia
ligulata
C
Dictyopteris
membranaceae
C C
Dictyota
dichotoma
C C C
Dumontia
contorta
C C
Enteromorpha
sp.
C C C C C C C
Gastroclonium
ovatum
C
Appendix A (continued )
!1 m 1e2 m 2e3 m 3e4 m O4 m
S M E S M E S M E S M E S M E
Gelidium
pulchellum
C
Gelidium
sesquipedale
C
Gigartina
pistillata
C
Gymnogongrus
crenulatus
C C
Ahnfeltiopsis
devoniensis
C
Gymnogongrus
griffithsiae
C
Haliptilon
squamatum
C
Halurus
equisetifolius
C
Himanthalia
elongata
C
Jania longifurca C
Laminaria
hyperborea
C
Leathesia
difformis
C
Leptosiphonia
schousboei
C
Lithophyllum
incrustans
C C C C C
Lomentaria
articulata
C
Mastocarpus
stellatus
C C C C
Mesophyllum
lichenoides
C
Mytilus sp. C C C C C
Ophidocladus
simpliciusculus
C
Osmundea
pinnatifida
C C C C C C
Palmaria palmata C
Plocamium
cartilagineum
C
Porphyra leucosticta C
Porphyra umbilicalis C C C C C C
Pterocladiella
capilaceae
C
Pterosiphonia
ardreana
C
Pterosiphonia
complanata
C C C
Pterosiphonia
pennata
C
Rhodothamniella
floridula
C C
Sacchorhiza
polischides
C C C
Scinaia furcellata C
Streblocladia
collabens
C C C C
Ulva sp. C C C C C C CUlvaria obscura C
Blidingia minima D D D D D D
Chthamalus sp. D D D D D C C C
669R. Araujo et al. / Estuarine, Coastal and Shelf Science 64 (2005) 658e670
References
Archambault, P., Bourget, E., 1996. Scales of coastal heterogeneity
and benthic intertidal species richness, diversity and abundance.
Marine Ecology Progress Series 136, 111e121.
Ballesteros, E., 1995. Comunidades algales en el Mediterraneo. Aulas
del Mar, Universidad de Murcia, 9 pp.
Benedetti-Cecchi, L., Cinelli, F., 1997. Spatial distribution of algae and
invertebrates in the rocky intertidal zone of the Strait of Magellan:
are patterns general? Polar Biology 18, 337e343.
Benedetti-Cecchi, L., Bulleri, F., Cinelli, F., 2000a. The interplay of
physical and biological factors in maintaining mid-shore and low-
shore assemblages on rocky coasts in the north-west Mediterra-
nean. Oecologia 123, 406e417.Benedetti-Cecchi, L., Acunto, S., Bulleri, F., Cinelli, F., 2000b.
Population ecology of the barnacle Chthamalus stellatus in the northwest
Mediterranean. Marine Ecology Progress Series 198, 157e170.
Benedetti-Cecchi, L., 2001. Variability in abundance of algae and
invertebrates at different spatial scales on rocky sea shores. Marine
Ecology Progress Series 215, 79e92.
Boaventura, D., Re, P., Cancela da Fonseca, L., Hawkins, S.J.,
2002. Intertidal rocky shore communities of the continental
Portuguese coast: analysis of distribution patterns. Marine
Ecology 23, 69e90.
Bockelmann, A., Bakker, J.P., Neuhaus, R., Lage, J., 2002. The
relation between vegetation zonation, elevation and inundation
frequency in a Wadden Sea salt marsh. Aquatic Botany 73, 211e221.
Bourget, E., DeGuise, J., Daigle, G., 1994. Scales of substratum
heterogeneity, structural complexity, and the early establishment of
a marine epibenthic community. Journal of Experimental Marine
Biology and Ecology 181, 31e51.
Clarke, K.R., Gorley, R.N., 2001. User Manual/Tutorial. PRIMER-E
Ltd., 91 pp.
Clarke, K.R., Warwick, R.M., 2001. Change in Marine Communities:
an Approach to Statistical Analysis and Interpretation. PRIMER-
E Ltd., 172 pp.
Connell, J.H., 1985. The consequences of variation in initial settlement
vs. post-settlement mortality in rocky intertidal communities.
Journal of Experimental Marine Biology and Ecology 93, 11e45.
Dahlhoff, E.P., Menge, B.A., 1996. Influence of phytoplankton
concentration and wave exposure on the ecophysiology of Mytilus
californianus. Marine Ecology Progress Series 144, 97e107.
Dethier, M.N., Graham, E.S., Cohen, S., Tear, L.M., 1993. Visual
versus random-point percent cover estimations: ‘objective’ is not
always better. Marine Ecology Progress Series 96, 93e100.
Appendix A (continued )
!1 m 1e2 m 2e3 m 3e4 m O4 m
S M E S M E S M E S M E S M E
Fucus spiralis C C C C
Hildenbrandia rubra C C C C C C C
Lichina pygmaea C C C C C CLomentaria articulata C
Policipes sp. C C
Verrucaria maura C C C C C
Catenella caespitosa DCeramium gaditanum D
Chaetomorpha linum C
Gelidium pusillum C
Pelvetia canaliculata C C CPorphyra dioica C C C
Porphyra linearis C
Polysiphonia stricta C
Hawkins, S.J., 1983. Interactions of Patella and macroalgae with
settling Semibalanus balanoides (L.). Journal of Experimental
Marine Biology and Ecology 71, 55e72.
Jenkins, R.J., Norton, T.A., Hawkins, S.J., 1999a. Interactions
between canopy forming algae in the eulittoral zone of sheltered
rocky shores on the Isle of Man. Journal of the Marine Biological
Association of the United Kingdom 79, 341e349.
Jenkins, R.J., Hawkins, S.J., Norton, T.A., 1999b. Direct and indirect
effects of a macroalgal canopy and limpet grazing in structuring
a sheltered inter-tidal community. Marine Ecology Progress Series
188, 81e92.
Jenkins, R.J., Norton, T.A., Hawkins, S.J., 1999c. Settlement and
post-settlement interactions between Semibalanus balanoides (L.)
(Crustacea: Cirripedia) and three species of fucoid canopy algae.
Journal of Experimental Marine Biology and Ecology 236,
49e67.Jenkins, S.R., Aberg, P., Cervin, G., Coleman, R.A., Delany, J., Della
Santina, P., Hawkins, S.J., LaCroix, E., Myer, A.A.,
Lindegarth, M., Power, A.-M., Roberts, M.F., Hartnoll, R.G.,
2000. Spatial and temporal variation in settlement and recruitment
of the intertidal barnacle Semibalanus balanoides (L.) (Crustacea:
Cirripedia) over a European scale. Journal of Experimental Marine
Biology and Ecology 243, 209e225.Johnson, M.P., Burrows, M.T., Hawkins, S.J., 1998. Individual
based simulations of the direct and indirect effects of limpets on
a rocky shore Fucus mosaic. Marine Ecology Progress Series 169,
179e188.
Kaehler, S., Williams, G.A., 1997. Do factors influencing recruitment
ultimately determine the distribution and abundance of encrusting
algae on seasonal tropical shores? Marine Ecology Progress Series
156, 87e96.
Kastendiek, J., 1982. Competitor-mediated coexistence: interactions
among three species of benthic macroalgae. Journal of Experimen-
tal Marine Biology and Ecology 62, 201e210.Kelaher, B.P., Chapman, M.G., Underwood, A.J., 2001. Spatial
patterns of diverse macrofaunal assemblages in coralline turf and
their associations with environmental variables. Journal of the
Marine Biological Association of the United Kingdom 81, 917e930.Lapointe, L., Bourget, E., 1999. Influence of substratum heterogeneity
scales and complexity on a temperate epibenthic marine commu-
nity. Marine Ecology Progress Series 189, 159e170.
Leonard, G.H., 1999. Positive and negative effects of intertidal algal
canopies on recruitment and survival of barnacles. Marine Ecology
Progress Series 178, 241e249.
Lewis, J.R., 1964. The Ecology of Rocky Shores. English Universities
Press Ltd, London, 300 pp.
Menconi, M., Benedetti-Cecchi, L., Cinelli, F., 1999. Spatial and
temporal variability in the distribution of algae and invertebrates
on rocky shores in the northwest Mediterranean. Journal of
Experimental Marine Biology and Ecology 233, 1e23.
Menge, B.A., Farrel, T.M., Olson, A.N., van Tamelen, P., Turner, T.,
1993. Algal recruitment and the maintenance of a plant mosaic in
the low intertidal region of the Oregon coast. Journal of
Experimental Marine Biology and Ecology 170, 91e116.
Moreno, C.A., Jaramillo, E., 1983. The role of grazers in the zonation
of intertidal macroalgae of the Chilean coast. Oikos 41, 73e76.
Peres, J.M., Picard, J., 1964. Noveau manuel de bionomie benthique
de la mer Mediterranee. Recueill des Travaux de la Station Marine
d’Endoume 31, 1e137.
Thompson, R.C., Wilson, B.J., Tobin, M.L., Hill, A.S., Hawkins, S.J.,
1996. Biologically generated habitat provision and diversity of
rocky shore organisms at a hierarchy of spatial scales. Journal of
Experimental Marine Biology and Ecology 202, 73e84.
Thompson, R.C., Crowe, T.P., Hawkins, S.J., 2002. Rocky intertidal
communities: past environmental changes, present status and
predictions for the next 25 years. Environmental Conservation
29, 168e191.
670 R. Araujo et al. / Estuarine, Coastal and Shelf Science 64 (2005) 658e670
Turner, T., Lucas, J., 1985. Differences and similarities in the
community roles of three intertidal surfgrass. Journal of Experi-
mental Marine Biology and Ecology 89, 175e189.
Schils, T., Coppejans, E., 2003. Spatial variation in subtidal plant
communities around the Socotra Archipelago and their bio-
geographic affinities within the Indian Ocean. Marine Ecology
Progress Series 251, 103e114.
Schonbeck, M.W., Norton, T.A., 1978. Factors controlling the upper
limits of fucoid algae on the shore. Journal of Experimental Marine
Biology and Ecology 31, 301e313.
Schonbeck, M.W., Norton, T.A., 1980. Factors controlling the lower
limits of fucoid algae on the shore. Journal of Experimental Marine
Biology and Ecology 43, 131e150.
Seoane-Camba, J.A., 1969. Sobre la zonacion del sistema litoral y su
nomenclatura. Investigation Pesqueira 33, 261e267.Stephenson,T.A., Stephenson,A., 1949.Theuniversal featuresof zonation
between tidemarks on rocky coasts. Journal of Ecology 38, 289e305.
Underwood, A.J., 1978. A refutation of critical tidal levels as
determinants of the structure of intertidal communities on British
shores. Journal of Experimental Marine Biology and Ecology 33,
261e276.Underwood, A.J., 1981. Structure of a rocky intertidal community in
New South Wales: patterns of vertical distribution and seasonal
changes. Journal of Experimental Marine Biology and Ecology 51,
57e85.Underwood, A.J., 1998. Grazing and disturbance: an experimental
analysis of patchiness in recovery from a severe storm by the
intertidal alga Hormosira banksii on rocky shores in New South
Wales. Journal of Experimental Marine Biology and Ecology 231,
291e306.
Williams, G.A., Davies, M.S., Nagarkar, S., 2000. Primary succession
on a seasonal tropical rocky shore: the relative roles of spatial
heterogeneity and herbivory. Marine Ecology Progress Series 203,
81e94.