MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 485: 75–89, 2013doi: 10.3354/meps10329

Published June 27

INTRODUCTION

Marine biogenic habitats alter both environmentalconditions (Fonseca et al. 1982, Jackson & Winant1983, Lowe et al. 2005) and biotic interactions (Irlandiet al. 1995, Arkema et al. 2009), and thus play animportant role in shaping population structure andcommunity dynamics (Bégin et al. 2004, Arkema etal. 2009). Although the presence and type of biogenichabitat influences diversity and community structure(Graham 2004, Pérez-Matus & Shima 2010), there isalso the potential for species distributions and eco-logical processes to vary spatially within hab itat

patches. For example, epifaunal abundances in sea-grass beds are often higher near edges despitegreater structural complexity in the interior, with dis-tributions varying by taxa (Bologna & Heck 2002,Moore & Hovel 2010). There are also uncertaintiesconcerning the sources of this variability, as adultdistributions are influenced by a suite of processesthat may vary with location within a habitat, diffe -rentially reducing the abundance of organisms. Asexamples, juvenile blue crabs have higher survivalrates in smaller fragmented patches of seagrassbecause predatory adult blue crabs are less abun-dant in patches with more edge area (Hovel & Lip-

© Inter-Research 2013 · www.int-res.com*Email: dana.morton@lifesci.ucsb.edu

Spatial patterns of invertebrate settlementin giant kelp forests

Dana N. Morton1,2,*, Todd W. Anderson1

1Department of Biology and Coastal & Marine Institute, San Diego State University, San Diego, California 92182-4614, USA

2Present address: Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, California 93106, USA

ABSTRACT: Settlement of kelp-associated organisms may vary as they are delivered to (andthrough) giant kelp (Macrocystis pyrifera) forests, with implications for local population dynamicsand community structure. Previous work suggests that settlement of invertebrates with longpelagic durations would be reduced as they move from an offshore environment toward the inte-rior of kelp forests due to dampened current flow and reduced larval delivery. We evaluated spa-tial variation in settlement across giant kelp forests in an extensive field study conducted over 2 yr.We collected and sorted >36000 settling organisms and had sufficient data to explore patterns indetail for 8 taxa. Orthogastropods (snails) were the most common invertebrates and exhibited apattern of declining settlement from the outer (seaward) to inshore edge of kelp forests. Inversepatterns were observed for Crepidula spp. and carideans, and other abundant taxa (non-sessilepolychaetes and pectinids) showed spatial structure that differed regionally and between years.Other taxa failed to exhibit significant spatial variation in settlement. In general, settlement waslower near the sea floor than in the upper water column, and similar across locations for mostgroups. For some taxa, spatial variation was more apparent when the magnitude of settlement wasrelatively low, which may suggest that kelp forests become ‘saturated’ with larvae during pulsesof high settlement. Our results are in contrast to previous predictions, as we observed high settle-ment in the interior for several species with long pelagic durations. For taxa that settled evenlyacross kelp-forested reefs, differential distributions of adults may be attributed to post-settlementprocesses. The patterns we observed here warrant additional study to address potential mecha-nisms for differential settlement.

KEY WORDS: Settlement · Invertebrates · Giant kelp forests · Larval filtering · Macrocystispyrifera · Biogenic structure

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Mar Ecol Prog Ser 485: 75–89, 2013

cius 2001, 2002), whereas bivalves have higher set-tlement (Bologna & Heck 2000) coupled with greaterpredation-induced mortality at the edges of seagrasspatches (Irlandi et al. 1995, Bologna 1999).

Recruitment (the addition of new individuals to apopulation) replenishes local populations but is high -ly variable (Caley et al. 1996) and is influenced byprocesses acting at multiple spatial and temporalscales (Keough & Downes 1982, Raimondi 1990,Pineda 1994). In particular, as larvae approach settle-ment, habitat structure may contribute to spatial vari-ation in settlement by altering current flow (Eckman1983, Jackson 1986), creating differential complexityand availability of suitable substrata (Foster & Schiel1985, Bégin et al. 2004), and also providing livingspace for resident organisms that may decrease settlement through predation (Keough 1984, Gaines& Roughgarden 1987). In turn, this may influencethe distribution and age structure of adults (Rough -garden et al. 1985, Reed et al. 2000).

On temperate rocky reefs along the Californiacoast and elsewhere, the giant kelp, Macrocystispyrifera, provides tremendous structural habitatcomplexity, extending from the sea floor to the watersurface in forming extensive forests on rocky reefs,supporting a diverse assemblage of organisms (re -viewed by Graham et al. 2007, Graham et al. 2008).The complex structure of giant kelp modifies thephysical environment significantly through greatlyincreased drag and reduced current flow (Jackson &Winant 1983, Jackson 1998, Gaylord et al. 2007) aswell as decreased light, with direct and indirecteffects on benthic communities (Reed & Foster 1984,Arkema et al. 2009). Specifically, the interior of largegiant kelp forests is characterized by greatly reducedflow relative to outer edges, and the delivery andsett lement of organisms to or through a giant kelpforest may differ depending on the location in or nearthe forest (Jackson 1986), with potential effects onlocal populations and communities. Furthur, kelpforests may act as a filter for larvae (Bernstein & Jung1979, Jackson 1986, Schroeter et al. 1996) via passiveprocesses (reduced delivery to the kelp forest interiordue to reduced flow), active processes (e.g. predationon larvae) (Gaines & Roughgarden 1987), or settle-ment as larvae encounter suitable substrata (Jackson1986, Carr 1994). Variation in larval traits (e.g.pelagic larval duration (PLD), swimming ability) andsettlement cues (Bernstein & Jung 1979, Keough &Downes 1982, Jackson 1986) may also play a role.

Although spatial patterns of invertebrate settle-ment (‘settlement shadows’) have been observed inseagrass beds (Orth 1992, Bologna & Heck 2000),

clear patterns of settlement in kelp forests have onlybeen detected for common encrusting epiphytes(Membranipora membranacea, Celleporella hyalina,Lichenopora huskiana, and Circeis spirillum; Bern-stein & Jung 1979). Overall, relatively few tests of alarval filtering hypothesis have been conducted inkelp forests, and results thus far have been inconsis-tent. For example, settlement of purple and red seaurchins (Strongylocentrotus purpuratus and Meso -centrotus franciscanus, respectively) was found to bespatially homogenous between inshore and seawardedges of giant kelp forests (Schroeter et al. 1996), andsettlement of multiple echinoderm species was notinfluenced predictably by stands of brown kelpSaccha rina longicruris (Balch & Scheibling 2000).Given that spatial patterns of settlement in biogenicstructure have been observed in some epiphytes, butnot in echinoderms, it is possible that settlement mayvary spatially within kelp forests for other speciesdue to the diversity of marine taxa and variation intheir life histories, especially the highly diverseorganisms that occur within kelp forests of southernCalifornia (Coyer 1984, Strathmann 1985, Graham etal. 2008).

Our objective was to determine whether settlementof multiple marine invertebrate taxa differed spa-tially within giant kelp forests and whether patternswere maintained between years. Therefore, wedeveloped an array of artificial substrata as settle-ment collectors for a variety of invertebrate taxaand addressed 3 questions: (1) Does the settlementof invertebrates differ among locations withinkelp forests, and if so, do taxa exhibit differential patterns? (2) Are spatial patterns of invertebrate settlement consistent between years? (3) Does themagnitude of settlement influence spatial patternsof settlement?

MATERIALS AND METHODS

Study system and design

Expansive subtidal rocky reefs off Point Loma inSan Diego, California, USA support large stands ofgiant kelp that extend nearly 7 km alongshore andapproximately 1 km perpendicular to shore at thewidest point. These kelp forests are located on a widerocky shelf of very low relief, and the dense stands ofgiant kelp attenuate currents to such a degree thatthe interior of the forests receives relatively low flowfrom alongshore or offshore currents, and is cha -racterized by reduced bidirectional oscillatory flow

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Morton & Anderson: Patterns of invertebrate settlement in kelp forests

(Jackson & Winant 1983, Jackson 1986, 1998). PointLoma is an ideal study area because stands of giantkelp are sufficiently large to test a larval filteringhypothesis while variation in bottom topography islow and thus unlikely to be confoun ded with bio-genic structure.

To detect potential cross-shelf (perpendicular toshore) and along-shore variation in settlement ofinvertebrates, a complete randomized block designwas used in which northern and southern regionsalong Point Loma were established, with regions sep-arated by approximately 1.5 km. Within each region,3 cross-shelf transects were established randomly,spaced between 100 and 500 m apart. Three siteswere then established haphazardly along each tran-sect, with one in each of the following along-shorestrata: (1) the ‘outer edge’, 10 m west of the outeredge of contiguous kelp forest, (2) the ‘interior’,approximately in the middle of kelp-forested reefsand at least 100 m east of the outer edge (this mini-mum distance was selected to account for narrowerregions of the kelp forest), and (3), the ‘inner edge’,10 m east of the inner edge of contiguous kelp forest(Fig. 1). Thus, this sampling design consisted of 2regions, 3 cross-shelf transects within each region,and 3 sites positioned along each transect for a totalof 18 sites.

At each site, 2 moorings were deployed to accountfor potentially high variation in invertebrate settle-ment within sites. The first mooring was placed

haphazardly, with the second placed 10 m south. Allgiant kelp within a 10 m radius of each mooring wascleared to prevent entanglement of kelp with moor-ings and to maintain a standardized amount of struc-ture immediately surrounding settlement collectors.All clearings were maintained throughout samplingperiods in 2009 and 2010.

Estimating invertebrate settlement

We were interested in the relative differencesamong locations in kelp forests and did not wish totarget a specific species, so dish-scrubbing pads(S.O.S. Tuffy, Clorox; hereafter Tuffys) were selectedas indices of invertebrate settlement as they are awell-established method of sampling a wide varietyof phyla (Leonard et al. 1998, Menge et al. 1999,Mace & Morgan 2006). Although settlement to Tuffysmay differ quantitatively from natural substrates, relative differences in settlement among sites shouldbe consistent regardless of the substrate used. Samp -ling of settlers was conducted every 2 wk during2 consecutive summer–fall periods, July to October2009 and 2010. During 2009, 1 Tuffy was placed at~7 m depth on each of the 2 moorings per site. Thisdepth was selected to determine spatial patterns insettlement while avoiding potential confoundingeffects of the kelp canopy. In 2010, 1 additional Tuffywas deployed ~2 m above the sea floor at each site to

determine any depth-associated spatialpatterns in settlement. The mooring usedfor monitoring settlement near the seafloor was randomly selected at each 2 wksampling period. Tuffys were collectedby divers every ~2 wk (Lagos et al. 2007)using a plastic bag that was sealed andthen stored at –20°C until processing. Allsamples were passed through a 500 µmsieve in the laboratory, and any echino-derms were identified and removed forpreservation in 75% ethanol while allother organisms were fixed in 10% for-malin and then preserved in 75% etha -nol. After preservation, samples weresorted to the lowest practical taxonomiclevel possible using conspicuous mor-phological traits. Thus the level of taxo-nomic re solution varied among phyla.Taxa present in very few samples andtaxa that do not possess a pelagic larvalstage (i.e. ‘brooding’ taxa) were ex -cluded from analyses.

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Fig. 1. Diagram of site locations at Point Loma, California, USA. Gray over-lay indicates every point where giant kelp was observed at >0.13 density(via LandSat imagery) during 2009 and 2010. Invertebrate sampling sitesare represented as black dots. OE: Outer Edge; Int: Interior; IE: Inner Edge

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Statistical analyses

Mean settlement per 14 d for each sampling siteover a 1 yr period was determined by averaging set-tlement between the 2 Tuffys at 7 m depth at eachsite for each 2 wk sample and then averaging settle-ment among samples at that site over the course ofthe entire sampling period. This provided a singlepoint estimate of mean settlement per 14 d for 2009and 2010 at each of 18 sites at 7 m depth (hereafter‘mean settlement’). The same procedure was used toobtain a single estimate for invertebrate settlement2 m above the sea floor in 2010 at each of the 18 sites.Thus, our replication is at the level of sites (and notwithin sites) with a sample size of 6 for each location(outer edge, interior, and inner edge) and we furtherreduced potential within-site variability by integrat-ing settlement over time rather than deploying addi-tional collectors at each site.

Todetectdifferences inoverall settlementof inverte-brates spatially (at 7 m depth) and inter-annuallywithin kelp forests, a 4-factor permutational multivari-ate analysis of variance (PERMANOVA) was con-ducted based on Bray-Curtis similarities (PRIMER-Ev6), followed by pair-wise comparisons between loca-tions. PERMANOVA was used to test for simultaneousresponsesofall taxatotheindependentvariablesinthesampling design. A square-root trans formation wasemployed to reduce the contribution of highly abun-dant taxa in relation to less abundant taxa (Clarke &Gorely 2006). Region (north or south) and location(outer edge, interior, inner edge) were in clu ded asfixed factors, with transect (nested within re gion) andsampling year (2009 and 2010) as random factors. Sim-ilarity percentage analysis (SIMPER) was then used todetermine the relative contributions of taxa to differ-ences among locations and between years.

To determine whether individual taxa exhibitedspatial patterns of settlement at 7 m, mean settlementfor each taxon was analyzed using a 4-factor mixed-model nested ANOVA (region and location as fixedfactors, and transect (within region) and year as random factors) followed by planned comparisons(Bonferroni method with corrections for multiplecomparisons) to identify differences among locations(SYSTAT 12). Planned comparisons were used be -cause of the prediction of reduced larval settlementacross kelp forests according to a larval filteringhypothesis. Log transformations (log[x +1]) were ap -plied to mean settlement when necessary to im proveassumptions of the model.

Sampling at depth (2 m above the sea floor) wasconducted in 2010 only, with a single Tuffy deployed

per site during each 2 wk sampling period. The Tuffyat 7 m from the same mooring line as the deeper Tuffywas used in a comparison of mean settlement be -tween depths. Mean settlement per 14 d was ana -lyzed using a 4-factor PERMANOVA based on Bray-Curtis similarities (depth, region, and location as fixedfactors, and transect nested with region as a randomfactor, with square-root transformation) followed bySIMPER and pair-wise comparisons as appropriate.

To assess whether settlement patterns of individualtaxa might be influenced by depth, mean settlement2010 for each taxon was analyzed using a 4-factormixed-model nested ANOVA (region, location, anddepth as fixed, and transect (within region) as ran-dom) followed by planned comparisons (Bonferronimethod) of locations within each sampling depth.Rather than examining overall spatial structure, wefocused only on differences between locations withineach sampling depth. Log transformations (log[x +1])were applied to mean settlement when necessary toimprove assumptions of the model.

To address whether observed spatial patterns ofsettlement differed when the magnitude (density ofsettlers per Tuffy) of settlement was relatively lowversus high, we identified the sampling dates withthe lowest (non-zero) and highest settlement withineach year. We ensured that the assumptions ofANOVA were met, and that mean settlement wasstatistically different between these 2 dates. Spatialpatterns on specific dates were unknown prior to theselection of dates. Settlement was examined usinga 3-factor nested ANOVA, with region, location,and transect (region) as fixed factors, followed byplanned comparisons (Bonferroni method) betweenlocations.

RESULTS

Over 2 yr, 36189 settling invertebrates were col-lected and sorted into 12 taxa. Eight taxa were suit-able for detailed analyses after less abundant taxawere excluded. Snails (hereafter orthogastro pods)were most abundant in our sample, followed bynon-sessile polychaetes and scallops (pectinids)(Table S1 in the Supplement at www.int-res. com/articles/ suppl/ m485p075_supp.pdf).

There was a significant difference in the collectivesettlement of all taxa among locations and betweenyears (Table 1). However, pairwise comparisonswithin PERMANOVA failed to detect differences be -tween individual locations (p > 0.05), indicating highvariability in this system. The difference among loca-

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http://www.int-res.com/articles/suppl/m485p075_supp.pdfhttp://www.int-res.com/articles/suppl/m485p075_supp.pdf

Morton & Anderson: Patterns of invertebrate settlement in kelp forests

tions was primarily due to variation in the relativeabundance of orthogastropods, but non-sessile poly-chaetes and scallops were also important; the 3 taxacollectively contributed over 60% of the dissimilarityin each of the pairwise comparisons between loca-tions (Table 2). These 3 taxa also were the lar gestcontributors to the difference in settlement be tweenyears.

Each taxon was examined individually to deter-mine its concordance with overall trends, and indeedsome taxa exhibited cross-shelf patterns while manyothers did not (Table 3, Fig. 2). Moreover, each of the3 gastropod taxa demonstrated differential patternsof settlement among locations. Orthogastropodswere similar in settlement between the outer edgeand interior (p = 0.49), but decreased from the outeredge to the inner edge (p = 0.05) and the interior tothe inner edge (p < 0.01) (Fig. 2a). By contrast, slipperlimpets Crepidula spp. increased from the outer edgeto the interior (p < 0.01), and from the outer edge to

the inner edge (p < 0.01) (Fig. 2b).Opisthobranchs showed a more complex pattern of settlement, withinteractions between location andyear and between region and year(Fig. 2c). Comparisons within yearsand regions revealed that settlementdid not differ among locations in2010, but trends were detected in2009, with nominally lower settle-ment along the in ner edge (outeredge to inner edge, p = 0.06; interiorto inner edge, p = 0.07).

Other taxa exhibited some variabil-ity in time and space, including spa-tial patterns of settlement as well as

interactions between variables. Non-sessile poly-chaetes (the second most abundant group) did notdemonstrate a statistical difference overall amonglocations, and a high degree of variability was pre-sent in both years (Fig. 2d). It is worth noting thatin the northern region in 2010 only, settlement washigher at the outer edge than at the inner edge(p < 0.01); however, this was the only difference de -tected between locations. The overall effect of regionwas nonsignificant (p = 0.08), as was the interactionbetween year, location, and region (p = 0.10). Pecti -nids differed in settlement between years, and in2009 the interior experienced higher settlement thanthe inner edge (p = 0.05), but all locations were simi-lar in 2010 (Fig. 2e). Other bivalves exhibited a pos -sible trend towards higher settlement to the outeredge vs. the inner edge (p = 0.08), but did not exhibita significant location effect and high variability insettlement was evident (Fig. 2f). Interactions be -tween region and year and between transect (region)

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Source SS df MS Pseudo-F p(perm)

Year 3241.00 1 3241.00 27.34

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and year indicate differences in along-shore larvalsettlement between years within this group. Bra chy -urans did not exhibit any significant spatial patternsin settlement, although settlement was higher in2010 (Fig. 2g). Carideans also had higher settlementin 2010, but they demonstrated clear spatial struc-ture in settlement, with in creasing settlement to -wards the shore (Fig. 2h); sett le ment at the outeredge was lower than the interior (p < 0.01) and theinner edge (p < 0.01).

We observed temporal variation in that overall set-tlement of invertebrates was higher in 2010 (Table 1),but this was largely due to higher settlement of ortho -gastropods (Table 2). Brachyurans and cari de ans alsosettled in higher numbers in 2010, but pectinidsreached their peak settlement in 2009. The spatialstructure of settlement did not differ significantly be-tween years for orthogastropods, brachyurans, andcari de ans, but pectinids showed higher settlement atthe interior in 2009 only (Table 3). Opisthobranchsex hibi ted a nominal trend of cross-shelf differences insettlement in 2009, but not in 2010 (Fig. 2c), and otherbivalves showed different along-shore and cross shelfpatterns of settlement between years (Table 3).

The overall spatial structure of settlement amonglocations at 2 m above the sea floor was typically sim-ilar to that at 7 m depth (i.e. overall there was nointeraction between depth and other variables detec -ted by PERMANOVA, and pairwise comparisonsshowed similar structure between both depths)(Table 4). However, for all taxa, settlement was lowernear the sea floor than at 7 m depth (Table 5).Orthogastropods, non-sessile polychaetes, and otherbivalves (non-pectinids) were responsible for almost70% of the dissimilarity be tween depths, with ortho -gastropods and non-sessile polychaetes each con-tributing approximately 30%. Upon examination ofindividual taxa in planned comparisons of locationswithin each sampling depth, only 2 taxa, Crepidulaspp. and carideans, displayed spatial structure at 7 mdepth (Table 6, Fig. 3b,h). For both of these groups,settlement at 7 m was lower at the outer edge thanin the interior (Crepidula spp., p = 0.05; carideans,p = 0.01) and the inner edge (Crepidula spp., p <0.01; carideans, p = 0.02), and statistically similaracross locations sampled near the sea floor. Ortho -gastro pods retained the same spatial structure at 7 mand near the sea floor (Fig. 3a). We did not detect

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Source Orthogastropoda Crepidula spp.a Opisthobranchia Non-sessile Polychaetaa

F p F p F p F p

Year 98.85

Morton & Anderson: Patterns of invertebrate settlement in kelp forests 81

Fig. 2. Spatial and inter-annual patterns of settlement for individual taxa at 7 m depth. Bars depict mean settlement at eachsampling site; error bars are standard error; lines indicate significant differences among locations overall; letter groups denote

significant differences among locations within regions or years (α < 0.05). (See Table 3 for ANOVA results)

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cross-shelf spatial structure at either sampling depthfor any other taxa, although an interaction betweendepth and region was detected in opisthobranchs,non-sessile polychaetes, and other bivalves (Table 6).

Due to high variability in settlement among sitesand sampling periods, or relatively consistent settle-ment over time, only orthogastropods and non- sessile polychaetes were suitable for inclusion in ouranalysis for exploring the influence of the magnitudeof settlement on spatial patterns (Table 7). High andlow periods of settlement of orthogastropods wereobserved in both years (Fig. 4a,b), and during bothperiods, there were significant effects of location butthe specific patterns differed: differences in settle-ment between the outer and inner edges of the kelpstands were detected during low but not high settle-ment. During low settlement, non-sessile polychae -tes exhibited significant differences between regionsand among locations, with lower settlement at theinner edge vs. outer edge (p = 0.02) and interior (p =0.04) (Fig. 4c). However, no significant differences

were observed during high settle-ment periods (p > 0.30 for all compar-isons), although a trend of higher set-tlement along the outer edge wasnoticeable. Overall, for the 2 taxa inwhich this analysis was possible,there were more pronounced spatialpatterns observed during relativelylow versus high settlement.

DISCUSSION

We observed a difference in over-all settlement of invertebrates amonglocations within kelp forests and

between 2 consecutive years. Individual taxa, how-ever, exhibited differential patterns of settlementspatially and temporally, and several taxa showed nopatterns in settlement whatsoever. Our results standin contrast to the larval filtering hypothesis as proposed by Bernstein & Jung (1979) and Jackson(1986), as several of the taxa we ob served did notexhibit spatial patterns of settlement and all taxareached the interior as well as the edges of the kelpforests in appreciable numbers. Based on their studyof epiphytes on giant kelp, Bernstein & Jung (1979)suggested that species with PLDs of 2 to 4 wk wouldonly be delivered to outer edges, whereas specieswith PLDs of a few hours would be retained in theinterior of kelp forests. We did not detect any rela-tionships between PLD and pattern of settlement forany of the taxa collected in our study. Taxa with thelongest PLDs (>3 wk: pectinids, other bivalves, cari -deans, and brachyurans; Strathmann 1987), showeda mixture of similar settlement spatially as well ascross-shelf patterns, although it had been predicted

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Source SS df MS Pseudo-F p(perm)

Region 104.72 1 104.72 1.03 0.50Location 1863.10 2 931.57 7.76

Morton & Anderson: Patterns of invertebrate settlement in kelp forests

that species with long PLDs would not be deliveredto the kelp forest interior in significant numbers(Bernstein & Jung 1979, Jackson 1986). Similarly, oftaxa with PLDs ranging from 1 to 3 wk (Crepidulaspp., orthogastropods, and non-sessile polychetes,Strathmann 1987), the gastropods de monstratedcross-shelf patterns of settlement while polychaetesonly show ed a pattern in one region in one year.Within larger taxonomic groupings, variability in set-tlement patterns was observed: cari deans showed apattern of settlement but brachy urans did not, andscallops showed a pattern in one year but otherbivalves did not. These observations conflict withpredictions of spatial settlement in kelp forests basedon PLD alone, and indicates that more general char-acteristics of life history may not be a predictor of pat-terns of settlement observed in our study.

In support of some version of a larval filteringhypothesis, we did observe reduced settlement oforthogastropods along the inner edge, but settlementbe tween the outer edge and interior was similar. Thispattern was partially repeated in non-sessile poly-chaetes but not consistently between years or re -gions, and an inverse pattern was obser ved in

Crepidula spp. and carideans. It is evident that highnumbers of settlement-stage larvae are reaching theinterior of wide kelp forests despite strongly damp-ened flow in the interior of these forests (Jackson1986). The presence of spatial gradients in these taxaindicates that similar processes may be acting onthese species and that giant kelp exerts a slight filter-ing effect in some conditions.

The lack of spatial structure in several taxa, how-ever, and the variability in settlement observed with -in regions and between years indicate that othermechanisms influencing settlement should be con-sidered. Predators may prefer or avoid habitat edges(Connell & Kingsford 1998, Hovel & Lipcius 2001,2002), and predation on settlement-stage larvaewhile in the water column could result in spatial pat-terns of settlement that reflect differential predatorabundance within kelp forests (Gaines & Rough -garden 1987), rather than a passive filtering effect.Spatial patterns of settlement could also result fromvariation in settlement cues, including changes inunderstory algae (Birrell et al. 2008, Arkema et al.2009, Matson et al. 2010) and conspecifics (Schel-tema et al. 1981, Toonen & Pawlik 2001, Donahue

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Source Orthogastropoda Crepidula spp.a Opisthobranchia Non-sessile Polychaetaa

F p F p F p F p

Depth 38.05

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2006), or to changes in light levels (Olson 1985,McFarland 1986).

The variation in spatial patterns of settlement ob -served among the 3 gastropod taxa in this study is no-table. Settlement of snails reflected a pattern consis-tent with larval filtering, with the exception thatsignificant numbers of larvae were delivered to theinterior, so the effectiveness of giant kelp as a filtermay be limited. We now know larvae can behave inresponse to settlement cues (Kingsford et al. 2002,Matson et al. 2010) and the patterns of settlement ob-served here may reflect delivery of larvae from off-shore, passive transport through kelp forests, andevenly dispersed settlement cues throughout the for-

est. Indeed, most of the snails observed(family Risso idae) are micrograzerson macroalgae (McLean 2007) andthus may respond to cues from thekelp itself. By contrast, slipper limpetsCrepidula spp. ex hibited an oppositegradient, with de creasing settlementto wards the outer edge of giant kelpstands. The adult distribution of thisspecies may provide an explanation:the species sampled is likely to beCrepidula nivea, which occurs inter-tidally (McLean 2007). If the majorityof larvae were spawned in the inter-tidal, settlement-stage larvae could bemost abundant inshore of the kelp for-est with reduced delivery to the outeredge. In addition, settlement-stagelar vae of this species and congenersare attracted to adult females (dueto protandrous hermaphroditism; Coe1953, Collin 2000), so the observedpatterns of settlement may reflect thedistribution of adult conspecifics. Sett -lement of opisthobranchs was variablein space and time, which may reflectthe variety of habitat types and life his-tories within this diverse group (Strath-mann 1987, Botello & Krug 2006) andthe interaction of species-specific be-haviors and phy sical processes. Tar-geted sampling of individual species ofopisthobranchs might be beneficial inresolving some of the variability ob-served in this group.

Variation in spatial patterns of settlement was also observed withindecapods, with different patternsobserved between carideans and

brachyurans. Cari deans were the only group outsideof gastropods to show consistent differences in settle-ment among locations. Most of these shrimp werehippolytids, which have intertidal to subtidal distrib-utions and are abundant on kelps (Kuris et al. 2007).Their patterns of settlement suggest stronger deliv-ery from inshore of kelp forests (if larval filtering isoccurring). The stands of kelp along Point Loma areseparated from shore by a wide area, so larval deliv-ery via along shore currents is possible. Brachyurancrabs were uncommon in our samples and did notshow strong evidence for spatial patterns in settle-ment. Settlement of decapods can be ex treme ly vari-able through time (Lough 1976, Eggleston & Arm-

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Fig. 3. Spatial patterns of settlement between 7 m depth and 2 m above the seafloor for individual taxa in 2010. Bars depict mean settlement at each samplingsite; error bars are standard error; letter groups denote significant differencesamong locations within each depth (α < 0.05). (See Table 6 for ANOVA results)

Morton & Anderson: Patterns of invertebrate settlement in kelp forests

strong 1995), and focused sampling using species-specific collectors over longer time scales may help toresolve the cause of the discrepancy be tween thesetaxa.

Non-sessile polychaetes, the second most abun-dant group, only settled differentially among loca-tions in the northern region in 2010. The northernand southern regions were separated by approxi-mately 1.5 km, and along-shore flow from the northmay have been a stronger source of larvae thancross-shelf flow in 2010. Diversity in life histories(e.g. settlement habitat, gregarious settlement) couldbe responsible for some of the variability observed.These spatial differences emphasize the potential forvariation in settlement processes over a relativelysmall scale.

As with decapods, the 2 bivalve taxa did not exhibitsimilar patterns of settlement. Pectinids showedsome spatial structure in 2009, with peak settlementin the interior of the forest. Individuals large enoughto identify were entirely Leptopecten latiauratus(Coan & Valentich-Scott 2007). This abundant scal-lop settles opportunistically and gregariously onblades of giant kelp (Morton 1994), so patterns of set-tlement could reflect the density of conspecifics.Other bivalves settled in relatively low numbers andwere too small to positively identify to species, butthey did show an interaction between year and re -

gion and between year and transect, indicating thatsettlement along shore was variable between years.As with polychaetes, along-shore currents from thenorth may have resulted in variation in larval de -livery. These differences between taxa and regionshighlight the heterogeneous nature of large kelpforests and the potential for ecological processes todiffer within them.

Spatial patterns of settlement were consistent at2 m above the seafloor. There were no taxa that dis-played a pattern at depth that was not observed at7 m, and settlement was lower near the sea floor thanat 7 m (upper water column) for all taxa. Orthogas-tropods showed the same spatial structure at bothsampling depths, but for Crepi dula spp. and cari -deans, the differences between locations ob served at7 m depth were not present 2 m above the seafloor.Many of the species collected in our study are foundin the kelp forest canopy or settle to giant kelp, somany larvae may have already settled at this depth inthe water column, explaining the low settlement ob -served. This would be a form of vertical larval filter-ing, and additional sampling at multiple depths inthe water column would test this hypothesis. We cansay that the patterns observed at 7 m were likely dueto cross-shelf position rather than overall depth ateach site as most spatial patterns of settlement wereunchanged with depth.

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Taxon Low settlement High settlementSource SS df MS F p SS df MS F p

Orthogastropoda2009a

Region 0.17 1 0.17 0.37 0.56 1.04 1 1.04 1.99 0.20Location 10.87 2 5.44 11.90

Mar Ecol Prog Ser 485: 75–89, 2013

Greater spatial structure in settlement was obser vedduring low settlement as opposed to high settlementwithin years for the 2 taxa that were suitable foranalysis. Periods of low settlement were consistentwith a more pronounced gradient of decreasing set-tlement towards shore, whereas this trend was lessclear during relatively high settlement. Non-sessilepolychaetes showed significant differences amonglocations during low settlement, but trends were

non-significant during high settlement. For ortho -gastropods, the magnitude of the low settlementpulse was slightly larger in 2009, and the outer edgeand interior received similar settlement. In 2010,however, the interior received lower settlement thanthe outer edge. During both high settlement pulses ineach of these years, high abundances of settlers wereobserved in the interior. For this taxon, the magni-tude of settlement may determine whether the kelpforest becomes ‘saturated’ with settling larvae. Whenlarvae are at low densities, giant kelp may dampencurrents sufficiently to reduce delivery to the interioror inner edge of kelp forests. At higher densities,there is a greater probability that an individual set-tler will be carried through kelp without encounter-ing suitable habitat or being removed by a predator.In this way, kelp forests could be effectively ‘satu-rated’ in settlement-stage larvae when larval densi-ties are high, creating high concentrations of settlersin the interior of kelp forests. This considers larvae aspassive particles, but larval behavior and navigationin response to settlement cues should be consideredas well. It is also important to note that several taxathat had low abundances overall did not show spatialstructure in settlement, reinforcing the taxon-specificnature of these results.

This work is the first to our knowledge to directlyobserve cross-shelf patterns of settlement of gastro -pods, non-sessile polychaetes, scallops, and carideancrustaceans through kelp-forested reefs. Althoughwe did not find any evidence for a consistent larvalfiltering effect observed across invertebrate taxa, thisin itself is a significant finding, as previous work hassuggested that large kelp forests should have a filter-ing effect on larvae. Due to our level of taxonomicresolution (versus identification to species), the pat-terns of settlement observed for some groups may re-flect the patterns of settlement for only one or a fewspecies, and it is possible that settlement patternsof less abundant species were obscured. However,even with this caveat the patterns of settlement docu-mented here are ecologically relevant as they reflectthe most abundant taxa, and further study could ad-dress species-specific patterns within these groups.

There is a lack of basic information on spatial dis-tributions of invertebrate settlement in near shoreecosystems in general and kelp forests in particular,despite a high level of general interest in these areasand the importance of these invertebrates in kelp forest food webs. A paucity of data exists for less con-spicuous and non-commercially harvested species,and few studies have examined the settlement ofmany subtidal invertebrate taxa in detail, with the

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Fig. 4. Influence of the magnitude of settlement on patternsof settlement of invertebrates among locations. Bars depictmean settlement at each sampling site; error bars are stan-dard error; lines indicate significant differences amonglocations at low settlement; letter groups denote significantdifferences among locations at high settlement (α < 0.05).

(See Table 7 for ANOVA results)

Morton & Anderson: Patterns of invertebrate settlement in kelp forests

exception of work on echinoderms and other groupsin which species are easily identified. The lack ofspatial structure in settlement for multiple taxa isinteresting given the hypothesis that such patternsshould exist. We can rule out larval filtering for sometaxa, and the patterns we did observe deserve addi-tional study to determine the mechanisms responsi-ble. Given our findings, why did Bernstein & Jung(1979) observe such clear patterns of settlement? Onekey difference between their study and ours is thatthey focused on settlement of sessile epiphytic spe-cies, whereas our study examined taxa with variedlife histories and mobilities. For encrusting species(epiphytes), encounter with giant kelp is a criticalstage of settlement, and larvae may begin to settle assoon as kelp is detected. The kelp may not only act asa filter, but as an important cue for these epiphytes.For more mobile species (e.g. orthogastropods), lar-vae may be influenced by a suite of other factors inaddition to the presence of kelp habitat. In addition,giant kelp forests are highly dynamic (Dayton et al.1992, 1999, Edwards 2004), so differences in kelp forest structure could result in variation in spatialpatterns of settlement (e.g. muted patterns in yearsof low kelp density). There is little evidence that thestructure of the kelp forests differed substantiallybetween our study and that of Bernstein & Jung(1979).

Because Point Loma supports expansive, widestands of giant kelp, we hypothesized that if cross-shelf patterns of invertebrate settlement occurred,they would be detectable in this system. The kelpforests of Point Loma have been extensively studiedand have served as a model ecosystem for many stud-ies of kelp forest dynamics and processes (e.g. Daytonet al. 1984, 1992) and its currents have been well de-fined (Jackson & Winant 1983, Jackson 1986), allow-ing us to ask detailed ecological questions. The spatialextent of our sampling area is large enough to encom-pass multiple kelp forests, and indeed there are sandchannels and other features that separate stands ofkelp spatially. Recent work by Cavanaugh et al.(2013) has demonstrated that population synchrony ingiant kelp decreases exponentially with distance be-tween populations, indicating that northern andsouthern ends of kelp forests function relatively inde-pendently. The fact that spatial patterns were ob-served for some taxa in these wide kelp stands pro-vides impetus for further study in smaller forests, aswell as attention to the processes involved. Becausethis study examines settlement of several invertebratetaxa simultaneously, including groups in which theidentification of species is difficult, this study provides

a benchmark from which future studies could explorespecies-specific patterns. For taxa that settled evenlyacross kelp forests, it is highly probable that spatialgradients of settlement would also be absent insmaller stands of giant kelp. Based on this know ledge,we can make inferences concerning the relationshipbetween patterns of settlement and the rela tive im-portance of post-settlement processes in determiningadult distributions of specific invertebrate taxa andsubsequent community structure.

Acknowledgements. We thank M. Edwards, S. Schellen-berg, and J. Shima for reviewing the manuscript, M. Ed -wards for statistical advice, and B. Hentschel for thoughtfuldiscussion. We thank J. Barr, T. Bell, M. Brett, J. Brower, M.Colvin, C. Jones, D. Hondolero, and S. Wheeler for fieldassistance in support of this project. We also thank C. Gram-lich for assistance in invertebrate taxonomy, T. Bell for pro-viding a detailed figure of our study area, and SBC LTER forproviding the Landsat data used in the figure. We also thankmany undergraduate volunteers, especially A. Bernabe, A.Evans, S. Grenier, I. Llamas, J. Mart, C. Mireles, and S.Waltz, for laboratory assistance. This research was conduc -ted in partial fulfillment of a master’s degree by D.N.M. andwas funded in part by the San Diego State UniversityDepartment of Biology Ecology Program and the CaliforniaState University Council on Ocean Affairs, Science, andTechnology. This is Contribution No. 25 of the Coastal andMarine Institute Laboratory, San Diego State University.

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Editorial responsibility: Richard Osman, Edgewater, Maryland, USA

Submitted: July 17, 2012; Accepted: March 5, 2013Proofs received from author(s): June 9, 2013

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