Journal of Experimental Marine Biology and Ecology 438 (2012) 76–83

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Journal of Experimental Marine Biology and Ecology

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Extreme spatial variability in sessile assemblage development in subtidal habitats offsouthwest Australia (southeast Indian Ocean)

Dan A. Smale ⁎Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UKUWA Oceans Institute & School of Plant Biology, The University of Western Australia, Crawley 6009 WA, Australia

⁎ Corresponding author. Tel.: +44 1752633273; fax:E-mail address: dansma@mba.ac.uk.

0022-0981/$ – see front matter © 2012 Elsevier B.V. Alhttp://dx.doi.org/10.1016/j.jembe.2012.10.002

a b s t r a c t

a r t i c l e i n f o

Article history:Received 11 September 2012Received in revised form 1 October 2012Accepted 5 October 2012Available online 31 October 2012

Keywords:Marine benthic communitiesRecruitmentSettlement panelsSpatial variationTemperate reefsWestern Australia

The development of marine benthic communities is strongly influenced by patterns of settlement, recruit-ment and survival, which may vary across multiple spatial scales in concordance with the scale-dependentprocesses that drive them. The temperate subtidal reefs off southwest Australia support highly diverse as-semblages of macroalgae and sessile invertebrates, yet little is known about spatial variability in the structureof developing assemblages compared with established assemblages. Here, settlement panel arrays weredeployed adjacent to subtidal rocky reefs, in 13–15 m depth, at 3 locations spanning 400 km of temperatecoastline in Western Australia. Panel assemblages were allowed to develop for ~14 months before theywere harvested. Variability in ecological pattern was analyzed at 4 spatial scales, spanning centimeters to100 s of kilometers. The structure of sessile assemblages was vastly different between the 3 locations, inthat one location (Geographe Bay) supported an impoverished assemblage comprising a single macrofaunalspecies whereas assemblages at the other two locations (Jurien Bay and Marmion Lagoon) supported fairlyrich assemblages of macroalgae and sessile invertebrates. Multivariate assemblage structure, total richnessand total cover varied significantly between the locations, although variability at the smallest spatial scale(centimeters) was consistently pronounced. Variability patterns for key taxa were less consistent across spa-tial scales. While explanations for the extreme between-location variability remain unclear, there was someevidence to suggest that herbivory by demersal fish may inhibit assemblage development at Geographe Bay,although local hydrodynamic factors (i.e. relatively lower water movement and influence of the dominantregional-scale oceanic current) could also be important.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction

Sessile marine organisms that colonize newly-available hard sur-faces form tractable model assemblages for testing and developingecological theory (e.g. Stachowicz et al., 2002; Svensson et al.,2007). Artificial substrata, such as settlement panels, have long beenused to cultivate assemblages of sessile marine organisms, whichcan then be manipulated to provide novel insights on ecological pat-tern and process. For example, recent settlement panel experimentshave shed light on the effects of physical disturbance (Atalah et al.,2007; Valdivia et al., 2008), nutrient availability (Sugden et al.,2008; Valdivia et al., 2008), temperature (Smale et al., 2011a) andwave exposure (Smale et al., 2011b) on assemblage structure. Panelsrepresent useful tools for quantifying patterns of settlement(Connolly et al., 2001; Pineda, 1994), recruitment (Underwood andAnderson, 1994), and community succession (Bowden et al., 2006;Sutherland, 1974, 1981), as they standardize small-scale habitatstructure, the time available for colonization and ecological ‘history’,

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while having obvious practical advantages. On the other hand, artifi-cial substrata may be ‘favored’ by certain species, so that assemblagecomposition is not entirely representative of local assemblagesfound on the natural substrata which they are designed to mimic(see Glasby, 1998 and references therein). Even so, the first use ofsettlement panels to investigate community development datesback almost 90 years (Wilson, 1925), and panels have since proveduseful tools for marine ecologists studying polar (Bowden et al.,2006), temperate (Glasby and Connell, 2001) and tropical (Hugheset al., 2000) ecosystems.

The majority of subtidal settlement panel studies have beenconducted in marine habitats that are heavily influenced by humanactivity, such as marinas, embayments or estuaries that are inherentlyinfluenced by anthropogenic factors including sediment and nutrientinput, pollution, water movement, invasive species and the proximityof artificial habitats (e.g. Glasby and Connell, 2001; Sugden et al.,2008; Underwood and Anderson, 1994). As such, patterns of commu-nity development are likely influenced more by human-mediatedprocesses than natural processes that influence patterns of spatialand temporal variability (but see Hughes et al., 2000; Bowden et al.,2006 amongst others). Moreover, panel experiments that have

77D.A. Smale / Journal of Experimental Marine Biology and Ecology 438 (2012) 76–83

explicitly examined spatial variability patterns have more often beenconducted across scales of meters to tens of kilometers, with arelative paucity of experiments conducted over scales of hundredsof kilometers (see Fraschetti et al., 2005 for review, but seeConnolly et al., 2001 as an exception).

The coastal ecosystems off southwest Australia represent a globalhotspot of biodiversity and endemism for marine macroalgae(Kerswell, 2006; Phillips, 2001) and are also characterized by rich as-semblages of sessile invertebrates (Hatcher, 1989) and demersal fish(Fox and Beckley, 2005; Hutchins, 2001; Langlois et al., 2012).Hard-bottom habitat, in the form of subtidal limestone and granitereef, is widespread in this region and supports dense kelp beds inthe shallows and rich macroalgae and invertebrate assemblages indeeper water (Smale et al., 2010a,b). Mature reef assemblages arecharacterized by high species richness and turnover (Kendrick et al.,1999; Smale et al., 2011c), pronounced small-scale variability(Phillips et al., 1997; Smale et al., 2010a), and predictableregional-scale shifts in biodiversity associated with an oceanic tem-perature gradient (Smale et al., 2010a; Wernberg et al., 2003). It isalso clear that small to intermediate scale spatial variability ispromoted by the patchy removal of macroalgal canopies by wavedisturbance, which creates newly-available space for colonizationand subsequent community development (Toohey et al., 2007;Wernberg and Goldberg, 2008). However, patterns of community de-velopment onto newly available substrata are poorly known in thissystem compared with elsewhere (but see Toohey et al., 2007;Smale et al., 2011b), and have not been examined across a range ofspatial scales.

This study aimed to investigate patterns of community structureon settlement panels across 400 km of southwest Australian coast-line. The use of settlement panels removed habitat heterogeneity,which is elevated on subtidal reef structures in the region andpromotes small-scale variability in sessile assemblage structure,and standardized ecological disturbance ‘history’, which may also beimportant, especially for taxa with microscopic life histories(e.g. the kelp, Ecklonia radiata). The study adopted a multi-scaleapproach, spanning from centimeters to hundreds of kilometers, toprovide novel insights into patterns of sessile assemblage develop-ment in relatively pristine subtidal habitats, and to make inferencesabout the processes that drive such patterns.

Fig. 1. (A) Map of southwest Australia indicating the Jurien Bay (JB), Marmion Lagoon (ML)temperature gradient, represented here by average winter isotherms (in °C, 2005–07). (suspended ~2 m from the seabed (see methods).

2. Methods

2.1. Study area

Sessile assemblage structure was examined at 3 locations off south-west Australia; Jurien Bay (30°23′40″S, 115°1′20″E) , Marmion Lagoon(31°45′26″S, 115°41′49″E ) and Geographe Bay (33°34′16″S, 115°9′13″E). Adjacent locations were situated ~200 km apart (Fig. 1) andthe experiment encompassed ~400 km of southwest Australian coast-line (southeast Indian Ocean). At each location, 2 comparable studysites were selected 1.0 to 1.5 km apart from one another. All studysites were at 13–15 m depth, 3–5 km offshore and were characterizedby a conglomeration of rocky reef and sandy habitats. All locationswere moderately exposed to the considerable oceanic swell systemsthat influence the ecology and geomorphology of the region (Searleand Semeniuk, 1985). In 2010, the average wave height recorded atwave buoys offshore from the study locations was ~2 m (Table 1) andmaximum wave heights exceeded 6 m (Bosserelle et al., 2012). Studysites in Jurien Bay andMarmion Lagoonwere partially protected by off-shore islands and submerged limestone reefs which – to some extent –dissipate wave energy. Sites in Geographe Bay were partially protectedby Cape Naturaliste, which alleviates the influence of southwesterlyswells. These locations encompass a temperature gradient of ~1.5 °Cand fall within a larger regional-scale oceanic temperature gradientthat defines the west coast of Australia (Table 1, and see Smale andWernberg, 2009, for detailed climatology of the region). This coastlineis strongly influenced by the Leeuwin Current (LC), which originatesin the Indo-Pacific and flows polewards along the coast ofWestern Aus-tralia, before deviating eastwards into the Great Australian Bight(Pearce, 1991; Smith et al., 1991). The LC transports tropical (and sub-tropical) dispersal stages and warm, nutrient-poor water polewards,which enhances north to south mixing of species and effectively raiseswinter water temperatures (Ayvazian and Hyndes, 1995; Caputi et al.,1996; Smale and Wernberg, 2009). As such, the coastal system offWestern Australia is considered oligotrophic (Table 1). The southwestAustralian coastline experiences a low magnitude diurnal tidal regime(Table 1) and subtidal rocky reef habitats support a rich flora andfauna that exhibit high levels of diversity and endemism (seeWernberg et al., 2003; Smale et al., 2010a; Tuya et al., 2011; Langloiset al., 2012 for quantitative examinations of biodiversity patterns).

and Geographe Bay (GB) study locations. The region is characterized by a well-definedB) A diver inspects a settlement panel ring, which comprised of 6 individual panels

Table 1Broad-scale environmental conditions at the three study locations, Jurien Bay (JB),Marmion Lagoon (ML) and Geographe Bay (GB), in southwest Australia. SSTs (meanand range) and chlorophyll a values are for 2010 and were generated from monthlymeans obtained from the MODIS Aqua 4 km dataset (hosted by NOAA). Swell heightand tidal range data were obtained through the Department of Transport, WesternAustralia. Swell heights are estimated from the nearest wave buoys to the study loca-tions, which are up to 25 km further offshore, and as such are over-estimations of ac-tual wave heights experienced at the study locations (see Bosserelle et al., 2012, forfurther details).

Location Latitude(°S)

SST Mean(°C)

SST Range(°C)

Chlorophyll a(μg chla/L)

Swellheight(m)

Springtidalrange (m)

JB 30.39 20.78 3.26 1.25 2.08 0.6ML 31.75 20.12 4.47 0.70 1.92 0.7GB 33.58 19.19 3.89 0.41 2.37 0.5

78 D.A. Smale / Journal of Experimental Marine Biology and Ecology 438 (2012) 76–83

2.2. Experimental design

The development of sessile assemblages was examined bydeploying standardized artificial substrata (PVC settlement panels)at each site. Although assemblage composition on artificial substratais known to differ from that on natural substrata (e.g. Glasby, 2000),a previous study in Marmion Lagoon indicated that panel assem-blages are largely representative of those found on subtidal limestonereefs (Smale et al., 2011b). Settlement panels were deployed using amoored ring system, modified from Svensson et al. (2007). First, sixgrey settlement panels (200×200 mm, 3 mm thick) were attachedto an ‘upper’ ring and a ‘lower’ ring, using cable ties and stainlesssteel wire. Rings were 800 mm in diameter, constructed fromstrips of PVC (40×2400 mm, 6 mm thick). Panels were attached~200 mm apart from one another and were suspended ~150 mmfrom the rings. Panels were initially roughened with an industrialsandblaster; the duration and areal coverage of sandblasting werestandardized. Panels were cut from the same batch of PVC sheets,treated in exactly the same way and randomized across all locations.The upper ring was tied to a buoy, while the lower ring was tied to~20 kg iron weight, which in turn was tethered to a galvanized ironDanforth anchor with 5 m of chain. Thus, each ring comprised 6 inde-pendent, inward-facing, vertically orientated settlement panels(Fig. 1). At each site described above, 2 rings were haphazardlydeployed from a research vessel and then positioned ~8 m apart byscuba divers. Panels were suspended ~2 m from the seabed belowthe subsurface buoy, at depths of 11 to 13 m. Panel rings weredeployed in early January 2010 and were retrieved in late February/early March 2011, some 14 months after deployment.

2.3. Analysis

The percent cover of all flora and fauna (>5 mm in size) was esti-mated using a gridded overlay. A 25 mm perimeter was excludedfrom analysis (to account for ‘edge effects’, see Todd and Turner,1986 and references therein), thereby an analytical area of150×150 mm was obtained for each panel. Macro images of floraand fauna were collected, and voucher specimens of all discernibletaxa were taken and preserved accordingly. All sessile organismswere identified to the lowest taxonomic level possible (generallyspecies for macroalgae and family or genus for fauna). In this manner,32 distinct faunal groups (comprising principally of ascidians andbryozoans) and 11 floral groups (principally red algae) were used toquantify assemblage structure on the panels. At ‘Marmion Lagoon-site 2’, 2 panels were lost from one of the rings as a result of damageto the wire and cable ties, so only 4 replicates were available foranalysis.

Variability in panel assemblage structure was examined withPERMANOVA (Anderson 2001), with ‘location’ (fixed, 3 levels), ‘site’(random, 2 levels, nested within ‘location’) and ‘ring’ (random, 2

levels, nested within ‘site’) as the factors within the model. Permuta-tions were based on a Bray–Curtis similarity matrix generated fromsquare-root transformed percent cover data; the transformation wasused to down-weight the influence of large space occupiers. Multivar-iate patterns were also explored using a zero-adjusted Bray Curtismatrix, to account for low abundances at one study location (Clarkeet al., 2006); variability patterns and results of statistical tests werevery similar. Tests used 4999 permutations under a reduced modeland significance was accepted at Pb0.05. Where negative variancecomponents were generated, they were re-set to zero (as perBenedetti-Cecchi, 2001; Graham and Edwards, 2001). A PCO plotbased on the Bray–Curtis similarity matrix was used to visualize mul-tivariate partitioning between spatial scales. Where significant differ-ences between locations were detected, a posteriori pairwisecomparisons were conducted. The taxa that contributed most to anybetween-location differences in assemblage structure were deter-mined using SIMPER. Variability in univariate metrics, includingtotal cover, taxon richness and the cover of dominant taxa, was alsotested with PERMANOVA, using the model described above (butwith matrices based on Euclidean distances of untransformed data,which is analogous to traditional ANOVA). All tests were conductedwith PRIMER 6 (Clarke and Warwick, 2001), using the PERMANOVAadd-on (Anderson et al., 2008).

3. Results

Sessile assemblage structure on subtidal settlement panels after14 months immersion was vastly different between the study loca-tions. Assemblages at Geographe Bay were depauperate, comprisingonly serpulid worms, and were therefore markedly lower in richness,spatial coverage and complexity than assemblages at Jurien Bay andMarmion Lagoon (Fig. 2). Assemblages at Marmion Lagoon weregenerally dominated by macroalgae, in terms of areal coverage, andcomprised a variety of both floral and faunal species (Fig. 2). Assem-blages at Jurien Bay were generally dominated by sessile fauna,specifically the bryozoan Triphyllozoon moniliferum and the bivalvesOstrea angasi and Anomia trigonopsis (Fig. 2).

Multivariate sessile assemblage structure varied significantly at allspatial scales (Table 2). A PCO ordination indicated that moderatepartitioning between rings occured at both Jurien Bay and MarmionLagoon (Fig. 3) whereas site-level variability was principally causedby pronounced variability between the 2 study sites at Marmion La-goon (Fig. 3). At the largest spatial scale of location panel assemblagesat Geographe Bay were statistically distinct from those at the other lo-cations (Table 2, Fig. 3). Pseudo-variance components showed thatvariability at the scale of location was by far the greatest contributorto total variability, followed by variability at the scales of site andpanel (Table 3).

SIMPER analysis showed that assemblages at Jurien Bay andMarmion Lagoon were 90.6% and 93.4% dissimilar to those asGeographe Bay, respectively (Table 4). The bryozoan T. moniliferum,and the bivalves A. trigonopsis and O. angasi, were major contributorsto the observed difference between Jurien Bay and Geographe Bay,being completely absent from the latter (Table 3). Similarly, themajor contributors to the difference between Marmion Lagoon andGeographe Bay were all absent from Geographe Bay; the bryozoansT. moniliferum and Watersipora subtorquata, and a member of theDidemnum genus of colonial ascidians (Table 4).

Univariate analysis showed that total percent cover and taxonrichness varied significantly at the smallest spatial scale of ring, andat the largest spatial scale of location (Table 2). The total coverageof panels at Jurien Bay and Marmion Lagoon was significant higherthan at Geographe Bay, whereas taxon richness was greatest atMarmion Lagoon and lowest at Geographe Bay (Table 2). On average,spatial coverage was 40 times lower at Geographe Bay compared tothe other locations, while taxon richness was 15–25 times lower at

Fig. 2. Representative images of panel assemblages after 14 months at Jurien Bay (A), Marmion Lagoon (B) and Geographe Bay (C). Panels at Jurien were generally dominated bysessile fauna, including solitary ascidians, serpulid polychaetes and demosponges, whereas panels at Marmion were colonized by a greater diversity of macroalgae as well as faunaincluding bryozoans and colonial ascidians. In stark contrast, panels at Geographe were devoid of all macrofauna and flora except serpulid polychaetes. Images represent an area of~160×160 mm.

79D.A. Smale / Journal of Experimental Marine Biology and Ecology 438 (2012) 76–83

Geographe Bay (Fig. 4). For these assemblage-level metrics, variabili-ty at the largest (location) and smallest (panel) spatial scales werethe principal contributors to total variability, whereas variability atintermediate spatial scales (site) was minimal (Table 3, Fig. 4).

Abundance patterns for dominant sessile taxa were also examined(Table 2, Fig. 5). Spatial variability patterns were highly inconsistentbetween taxa, with very little generality in pattern. For example, thecover of the bryozoan T. moniliferum varied significantly betweenrings and sites but not locations, whereas the cover of the bryozoanW. subtorquata varied between locations but not at smaller spatialscales (Table 2). Similarly, the cover of bivalve O. angasi was highlyvariable between sites but not at other spatial scales, whereas thebivalve A. trigonopsis did not vary significantly at any spatial scaleexamined (Table 2, Fig. 5). In all cases, pseudo-variance componentsfrom the PERMANOVA model indicated that variability betweenpanels (i.e. residual variability) was the first or second most impor-tant contributor to total variability.

4. Discussion

The development of sessile assemblages exhibited pronouncedvariability between the study locations, with assemblages atGeographe Bay being depauperate and vastly different in structureto those at Jurien Bay and Marmion Lagoon. While the reasons forthis remain unclear (and ultimately careful experimental manipula-tions are required to determine mechanistic processes), it is possibleto draw on existing knowledge to suggest likely explanations for the

Table 2Results of multivariate and univariate PERMANOVA to test for differences between locatiosites). Permutations were based on a Bray–Curtis similarity matrix generated from square-rovariate analysis, matrices were based on Euclidean distance and generated from untransformvalues (at b0.05) are indicated with an asterisk. Where a significant difference between loc(ML) and Geographe Bay (GB) are also shown.

Response variable Loc Site (loc

F 2,3 P F 3,6

MV assemblage structure 5.83 0.007* 6.48Total cover 224.0 0.002* 0.12Taxon richness 76.88 0.002* 2.70Triphyllozoon moniliferum 0.76 0.536 11.48Hydroides sp. a 0.63 0.599 0.79Ostrea angasi 0.94 0.460 85.54Anomia trigonopsis 5.79 0.093 4.33Watersipora subtorquata 109.6 0.005* 0.41Spyridia dasyoides 0.80 0.586 1.57

observed variability. Clearly, a prerequisite for recruitment ontohard surfaces is availability of larvae or propagules from sourcepopulations on similar habitats (Hughes et al., 2000) and, in general,the closer such populations are to the newly-available surface themore chance of higher recruitment rates (e.g. Goldberg et al., 2004).Geographe Bay is a predominantly soft-sediment system, character-ized by extensive seagrass meadows (McMahon et al., 1997), butthere are extensive rocky reef platforms which support rich assem-blages of macroalgae and invertebrates (Westera et al., 2008). Theseassemblages include many species that are also abundant at theother study locations and that have considerable dispersal potential(e.g. the kelp E. radiata and the bryozoan T. moniliferum). Indeed, set-tlement panels at one of the sites within Geographe Bay were posi-tioned b5 m from rocky reef colonized by an array of benthic taxa,including macroalgae, sponges, ascidians and bryozoans. Moreover,a 112 m long military vessel, the HMAS Swan, was scuttled as a recre-ational scuba diving wreck in 1997 and now sits in 10–30 m of waterjust ~7 km from the current study sites. This artificial ‘reef’ has sincebeen colonized by a wealth of sessile species (Morrison, 2000),including many that can colonize PVC settlement panels (e.g. the co-lonial ascidian Didemnum sp., the brown algae Sporochnus comosusand the bivalve A. trigonopsis). As such, a lack of proximal sourcepopulations on suitable hard-bottom habitat is not a likely explana-tion for the observed disparity in assemblage development.

Another key ‘bottom up’ factor that influences recruitment and,ultimately, the structure of populations and communities is oceanog-raphy as a determinant of larvae and propagule supply (Broitman et

ns (fixed), sites (random, nested within locations) and rings (random, nested withinot transformed percent cover data for multivariate (MV) assemblage structure. For uni-ed data. All main tests used ~4999 permutations under a reduced model. Significant Pations was detected, pairwise comparisons between Jurien Bay (JB), Marmion Lagoon

) Ring (site) Pairwise

P F 6,58 P

0.001* 2.11 0.001* JB=ML≠GB0.943 2.61 0.035* JB=ML>GB0.147 3.03 0.009* ML>JB>GB0.009* 3.56 0.001* n.s.0.518 8.74 0.001* n.s.0.001* 0.13 0.999 n.s.0.661 0.35 0.915 n.s.0.752 0.87 0.511 ML>JB>GB0.221 1.24 0.238 n.s.

Table 4Percentage contributions of individual taxa to observed differences between locations,as determined by SIMPER. Overall dissimilarity between locations is shown in italics.The mean percent cover (‘Loc x Av.’, square-root transformed data) of each taxon isshown for each location. ‘Contr. (%)’ refers to the contribution of each taxon to theoverall dissimilarity between locations, while ‘Cum. (%)’ is a running total of the contri-bution to observed dissimilarity. The top 5 contributors to observed dissimilarity areshown.

Locations (% dissimilarity)

Taxon Loc 1 Av. Loc 2 Av. Contr. (%) Cum. (%)

Jurien vs. Geographe (90.6%)Triphyllozoon moniliferum 2.24 0.00 13.30 13.30Anomia trigonopsis 1.86 0.00 10.22 23.52Ostrea angasi 1.77 0.00 8.61 32.13Bugula sp. a 1.63 0.00 8.36 40.48Encrusting coralline algae 1.12 0.00 6.73 47.21

Marmion vs. Geographe (93.4%)Triphyllozoon moniliferum 2.32 0.00 8.82 8.82Watersipora subtorquata 2.21 0.00 8.42 17.24Didemnum sp. a 1.86 0.00 7.07 24.31Balanus trigonus 1.62 0.00 6.04 30.35Anomia trigonopsis 1.58 0.00 5.98 36.33

Fig. 3. PCO ordination of panel assemblages based on a Bray–Curtis similarity matrixgenerated from square-root transformed percent cover data. Centroids representeach ring (6 panels pooled), with 2 rings per site and 2 sites nested within each loca-tion. Centroid symbols represent locations while centroid labels denote the 2 sites.

80 D.A. Smale / Journal of Experimental Marine Biology and Ecology 438 (2012) 76–83

al., 2008; Connolly et al., 2001). The west coast of Australia is gener-ally well connected through both oceanography and coastal morphol-ogy. The Leeuwin Current transports dispersal stages poleward andenhances north to south mixing of species (Caputi et al., 1996;Pearce, 1991), while there are no major biogeographic breakpointsto impede connectivity along the coastline (Fox and Beckley, 2005).However, a recent study by Feng et al. (2010) modeled particle trans-port and found Geographe Bay to have the highest particle retentionrate of any location along the west coast of Australia. The LeeuwinCurrent is diverted offshore upstream of Geographe Bay, so thatcurrents within the bay are weak and particle retention rates maybe as high as 40% after 14 days of release (Feng et al., 2010). Thus,compared to the other two study locations, which have low particleretention rates and receive an influx of particles on the current, theimport of propagules and larvae into Geographe Bay from northernsource populations may be limited. Clearly, very low propaguleand larvae pressure would influence settlement, recruitment andsessile assemblage development rates to some degree, althoughlocal populations in Geographe Bay should, intuitively, providesome recruits. The influence of larval and propagule dispersal onbenthic communities in Geographe Bay clearly warrants furtherexperimental study.

In considering ‘top down’ factors that may influence benthic com-munities, it is important to note that grazing and predation pressurein temperate west Australian marine ecosystems is thought to becomparatively low compared to many other temperate marine eco-systems (Vanderklift et al., 2009). The abundance of invertebrate her-bivores on subtidal reefs is generally low and patchy (Vanderklift andKendrick, 2004; Wernberg et al., 2008) and, as such, the structure ofbenthic communities in the region are thought to be primarilyinfluenced by ‘bottom up’ processes, including wave disturbance,habitat heterogeneity temperature and oceanography (Smale et al.,

Table 3Pseudo-variance components (square-root) at each spatial scale, for multivariate as-semblage structure, total cover and taxon richness response variables.

Loc Site Ring Panel

Assemblage structure 45.7 27.1 11.8 27.0Total cover 22.8 0 6.7 12.7Taxon richness 6.6 0.8 0.7 1.3

2010a; Toohey et al., 2007; Wernberg et al., 2003, 2010). At all thecurrent study locations, no benthic grazers or predators were ob-served on the settlement panels at any time, presumably becausethe panels were suspended ~2 m above the seabed, so that any ‘topdown’ pressure would most likely have stemmed from demersalfish. While early research on the ichthyofauna of Geographe Baysuggested that fish assemblages were relatively impoverished(Scott, 1981), more recent surveys on both hard and soft bottom hab-itats indicated that assemblages were fairly rich, abundant and repre-sentative of the region (Westera et al., 2008). However, very few fishwere observed by scuba divers at Geographe Bay during the study,and the structure of macroalgae and fish assemblages at nearbyCape Naturaliste (~20 km southwest) is not particularly unusual ordistinct from other locations within the region (Hutchins, 2001;Langlois et al., 2012; Smale et al., 2010a). As such, there is no clear ev-idence to suggest that herbivory and predation pressure on sessile as-semblages at Geographe Bay should be greater than at the otherlocations, certainly not to the point of restricting assemblage develop-ment. Even so, panel assemblages at Geographe Bay comprised onlyserpulid polychaete worms and a film of ‘green microalgae’, whichwas notably scoured by grazing marks. This observation wouldsuggest that demersal fish do in fact graze developing biofilms, and

Fig. 4. Mean total cover and taxon richness (±SE) of panel assemblages at each sitewithin each location. Values are means of 2 panel rings within each site (6 panelspooled per ring).

Fig. 5. Mean percent cover (±SE) of dominant taxa at each site within each location. Values are means of 2 panel rings within each site (6 panels pooled per ring).

81D.A. Smale / Journal of Experimental Marine Biology and Ecology 438 (2012) 76–83

perhaps recruiting macroalgae and invertebrates, and thereby inhibitassemblage development on settlement panels in Geographe Bay.Again, manipulations of grazing pressure, through the use of cagesfor example, would shed light on the importance of localized ‘topdown’ processes in a system that is generally structured from the bot-tom up.

In addition to the extreme variability in sessile assemblage devel-opment between locations, variability at the smaller spatial scales ofsites (i.e. kilometers) and panels (i.e. centimeters), was observed.Pronounced variability in sessile assemblage development at thescale of kilometers been observed previously in relatively pristinecoastal systems (Bowden et al., 2006; Glasby, 1998), and may be at-tributed to variability in recruitment rates or proximity to sourcepopulations, acting across similar spatial scales. Here, the two studysites at Jurien Bay supported distinct assemblages, principally becauseone site was dominated by the bryozoan T. moniliferum and the otherby the bivalve O. angasi. Patterns of recruitment of subtidal inverte-brates have been found to vary across scales of kilometers manytimes before (Bowden et al., 2006; Butler, 1986; Glasby, 1998),while recruitment patterns at multiple spatial scales often vary be-tween taxa (Glasby, 1998). Here, differences in initial recruitment be-tween sites may have been due to variability in water movement(caused by swell-induced water movements and eddies of theLeeuwin Current, which both influence subtidal reefs at Jurien Bay)or proximity to source populations. Subsequently, variability inwater movement, food availability or predation pressure may haveinfluenced variability in survival or growth between the study sites.Finally, small-scale variability, at scales of centimeters to meters, is

a ubiquitous feature of spatial variability patterns of populationsand communities in coastal marine ecosystems (Fraschetti et al.,2005). Pronounced small-scale variability has been observed in thestructure of mature benthic communities on subtidal reefs in the re-gion (Hatcher, 1989; Smale et al., 2010a, 2011a), perhaps due to con-siderable habitat heterogeneity at similar spatial scales, whichinfluences both biological and physical factors. While habitat struc-ture was standardized with the use of settlement plates in the currentstudy, a wealth of other biological interactions and physical processesoperate over small spatial scales and are pervasive in marine ecosys-tems (Coleman, 2002; Underwood and Chapman, 1996).

In conclusion, rates and trajectories of assemblage development onhard surfaces in marine ecosystems off southwest Australia are poorlyknown, even though the provision of newly available space throughphysical disturbance and the co-existence of assemblages at differentsuccessional stages are thought to be key processes in maintaininghigh levels of species richness and turnover in the region (Toohey etal., 2007;Wernberg et al., 2003). This experiment has provided novel in-sights into sessile assemblage structure after 14 months of develop-ment, which was extremely variable between locations situated~200 km apart, despite similar environmental conditions and nearbyfauna and flora. Panels at Geographe Bay supported impoverished as-semblages, comprising a single macrofaunal species after 14 monthsof colonization time. Moreover, in a pilot study conducted at GeographeBay, where panels were deployed in early October 2009 and left in situfor ~4 months, zero recruitment of macrofauna and macroflora wasalso observed (Smale, unpublished data). The explanations for these ob-servations are unclear, but are likely to include intense (previously

82 D.A. Smale / Journal of Experimental Marine Biology and Ecology 438 (2012) 76–83

unrecognized) grazing and predation pressure, different hydrodynamicinfluences, and a low influx of propagules and larvae due to local to re-gional scale oceanographic processes. Temperate Western Australia hasbeen proposed as an excellent ‘natural laboratory’ for studying the ef-fects of temperature on populations and communities, because the re-gional scale oceanic temperature gradient is largely unconfounded byvariability in other key processes that drive ecological pattern (Smaleand Wernberg, 2009). While this is generally the case, care should betaken to ensure that localized anomalies in the importance of otherkey processes, such as grazing or predation pressure, do not complicatebroad-scale comparisons.

Acknowledgments

I thank Gary Kendrick, Renae Hovey and Anne Brearley fortaxonomic assistance and Thibaut de Bettignies, Alex Grochowski,Samantha Childs, Renae Hovey, John Statton, Ben Saunders, LauraFullwood, Scott Bennett, Jordan Goetze, Bryce MacLaren, AdamGartner, Kris Waddington and Anthony Payne for assistance in thefield. Cecile Rousseaux assisted with remote sensing data. Thisresearch was supported by a Research Development Award fromthe University of Western Australia and a Marie Curie InternationalIncoming Fellowship within the 7th European Community Frame-work Programme. [RH]

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