spore supply and habitat availability as sources of recruitment limitation in the giant kelp...

SPORE SUPPLY AND HABITAT AVAILABILITY AS SOURCES OF RECRUITMENTLIMITATION IN THE GIANT KELP MACROCYSTIS PYRIFERA (PHAEOPHYCEAE)1

Daniel C. Reed,2 Stephen C. Schroeter

Marine Science Institute, University of California, Santa Barbara, California 93111, USA

and

Peter T. Raimondi

Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California 95060, USA

The causes of spatial variation in the recruitmentof benthic marine algae are frequently misunder-stood because of difficulties in distinguishingamong the many factors that influence the supplyand establishment of microscopic propagules. Weused the recently constructed San Clemente Artifi-cial Reef (SCAR) experiment to examine the roles ofdispersal distance, size of spore source, and habitatavailability as sources of variation in the recruitmentof the giant kelp Macrocystis pyrifera (L.) C. Ag., aspecies whose recruitment has often been consid-ered to be dispersal limited. Sparse colonization onSCAR by adult Macrocystis occurred within 6months after reef construction via drifters (i.e.individuals from neighboring kelp beds that becamedislodged and set adrift). The abundance of drifterson SCAR declined exponentially with distance fromthe nearest source population (San Mateo), suggest-ing that San Mateo was the likely source of drifters.Dense recruitment of smallMacrocystis sporophyteswas observed within 8 months of reef construction.The density of recruits on SCAR showed an initialincrease with distance from San Mateo beforedeclining exponentially. Nonetheless, substantialrecruitment was observed at the most distantlocations on SCAR located 3.5 km from San Mateo.In contrast to drifters, the density of recruits waspositively correlated to the bottom cover of artificialreef substrate. Importantly, no correlation wasfound between the local density or fecundity ofdrifters and the local density of kelp recruitssuggesting that recruitment on SCAR resulted fromwidespread spore dispersal rather than from thelocal dispersal of spores from drifters.

Key index words: artificial reef; colonization; dis-persal; establishment; fecundity; kelp; Macrocystispyrifera; recruitment limitation; spore

Abbreviation: SCAR, Scan Clemente Artificial Reef

Recruitment limitation occurs when the size of apopulation is constrained by the supply and/or estab-lishment of propagules. It has been invoked to explainspatial and temporal variability in the local abundanceof terrestrial plants (Tilman 1997, Hubbell et al. 1999,Connell and Green 2000) and benthic freshwater andmarine organisms (Underwood and Fairweather 1989,Downes 1995, Caley et al. 1996). Rates of supplydepend on the dispersal potential of propagules andon the size and fecundity of their source populations,whereas the availability of suitable habitat, favorableenvironmental conditions, and biotic interactions de-termine whether propagules survive long enough tobecome established once they have settled. Thesedifferent constraints on recruitment have been termeddispersal limitation, source density and source strengthlimitation, and establishment limitation (Clarke et al.1998).

Recruitment from propagules is the only means ofcolonization for sedentary marine organisms, and thedegree to which constraints on propagule supply andestablishment interact to limit recruitment is particu-larly important in systems subjected to frequentdisturbance. Shallow temperate reef communitiesdominated by large brown seaweeds known as kelps(order Laminariales) are one such system. The highproductivity, large size, and three-dimensional archi-tecture of kelps lead them to have an overwhelminginfluence on community structure and ecosystemfunction in areas where they occur (Mann 1982,Dayton 1985, Foster and Schiel 1985). The shallowreefs on which kelps live are subjected to a variety ofphysical and biological disturbances, causing theirpopulations in many areas to fluctuate greatly in spaceand time. Intensive grazing, large waves, and unfavor-able growing conditions such as those during El Nino-Southern Oscillation events have all been identified asthe cause of widespread kelp loss (Schiel and Foster1986, Harrold and Pearse 1987, Dayton and Tegner1989). Acting singly or collectively, these disturbancescan create bare patches that range in size from severalsquare meters to many square kilometers, which,depending on the size of a reef, can lead to thecomplete loss of a local kelp population (Mann 1977,Ebeling et al. 1985, Seymour et al. 1989, Camus 1994,

1Received 10 July 2003. Accepted 6 January 2004.2Author for correspondence: e-mail [email protected].

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J. Phycol. 40, 275–284 (2004)r 2004 Phycological Society of AmericaDOI: 10.1046/j.1529-8817.2004.03119.x

Reed et al. 1996). Kelp populations tend to be veryresilient, however, and recolonization typically ensuessoon after the disturbance has subsided (Harris et al.1984, Miller 1985, Tegner and Dayton 1987, Ladahet al. 1999). Indeed, the fact that species distributionshave changed little in recent times despite the highincidence of severe disturbance (Dayton and Tegner1989, Dayton et al. 1992, Edwards 2001) shows thehigh resilience of kelp populations.

The rapid recovery of kelp populations in theabsence of a local spore source presents an apparentparadox given the common perception that effectivespore dispersal in kelps is limited to a few meters of theparent plant (Dayton 1985, Schiel and Foster 1986,Santelices 1990, Murray and Bray 1993, Shanks et al.2003). The constraint on longer distance dispersalarises because fertilization in kelp occurs on the bottomafter spore dispersal. As spores disperse, they becomeprogressively diluted in the water column, therebyreducing the odds that male and female spores willsettle close enough for fertilization to occur. Because ofthis limitation, colonization by kelps at sites removedfrom extant populations has been explainedmost oftenby local spore dispersal from detached plants thatdrifted to the site (Dayton 1973, North et al. 1986,Paine 1988, Hay 1990) or by the growth of quiescentmicroscopic stages that survived the disturbance(Ladah et al. 1999). Findings from other studies,however, challenge the notion that effective sporedispersal in kelps is limited to a few meters. Thesynchronized release of spores from a population hasbeen shown to occur in some species (Amsler andNeushul 1989, Reed et al. 1997). Such phenomena canhelp compensate for dilution effects associated withlonger distance dispersal and extend the distance overwhich spore dispersal leads to successful colonization.Extended spore dispersal in kelps is possible becausespore photosynthesis and large internal lipid reservesserve to prolong spore competency in the plankton(Amsler and Neushul 1991, Reed et al. 1992, 1999).The idea of dense colonization in kelps via widespreadkilometer-scale spore dispersal is supported by ob-servations of significant spore settlement in the palmkelp Pterygophora californica 4km from the nearestpopulation (Reed et al. 1988) and by results ofhydrodynamic modeling that indicate a sizable fractionof Macrocystis pyrifera spores may routinely dispersehundreds to thousands of meters (Gaylord et al. 2002).

Patterns of kelp colonization depend not only on thenumber of colonists (i.e. spores, drifting plants,resident dormant stages), but also on the amount andquality of hard bottom habitat and on suitable abioticand biotic conditions for postsettlement recruitmentand growth. Substrate size and shape, surface rough-ness, and bottom topography have all been shown toinfluence patterns of algal colonization (Foster 1975,Sousa 1979, Kennelly 1983, Johnson 1994). Shallowtemperate reefs are extremely variable with respect tothese physical characteristics, and there are few studiesof the extent to which these features interact with the

supply of new colonists to influence patterns of kelprecruitment.

Newly created artificial reefs are ideal systems forstudying dispersal and colonization in kelps for thefollowing reasons: 1) They are usually built in areasdevoid of reefs, which makes it easier to determine thenearest source populations; 2) there is no possibilitythat colonization will result from dormant microscopicstages; and 3) they lack established populations ofpotential competitors and grazers that reduce theprobability of recruits becoming established. Here weuse data collected from a recently constructed artificialreef off San Clemente, California (USA) to investigatethe potential for different modes of dispersal and reefcharacteristics to influence patterns of colonization inthe giant kelp M. pyrifera. The San Clemente ArtificialReef (SCAR) was designed as a 5-year experiment totest the extent to which the type and amount ofartificial reef habitat and its proximity to natural reefsthat serve as source populations influence the devel-opment and persistence of giant kelp forest commu-nities. Results from the experiment will be used todesign a 61-ha artificial reef at the site whose purposewill be to compensate for the loss of kelp bed habitat ona nearby natural reef caused by the operation of acoastal power plant. Specifically, we used data collectedfrom the first year of the experiment at SCAR to testthe effects of the type and availability of reef substrateand distance from nearest kelp bed (a proxy forcolonist supply) on the colonization patterns of driftingplants and benthic recruits of M. pyrifera.

STUDY SITE AND METHODS

The SCAR is located approximately 1 km offshore of the cityof San Clemente, California (USA) (Fig. 1). It was constructedin August and September 1999 on a mostly sand bottom at 13to 16m depth. It consists of 56 modules clustered at sevenlocations (eight modules per location) spaced relatively evenlyalong 3.5km of coastline encompassing an area of approxi-mately 144ha. For convention, the locations of the moduleclusters are numbered 1 through 7 from south to north.During this study the nearest natural populations ofMacrocystisto SCAR were at San Mateo kelp bed located approximately500m south of location 1, Barn kelp bed located approximately14 km south of San Mateo, and Dana Point kelp bed located9.4km north of location 7. Longshore currents in the area arehighly variable, oscillating between upcoast and downcoast atspeeds ranging from near zero to more than 50 cm2 � s�1

(Elwany et al. 1990).Each artificial reef module was roughly 40 � 40m in area,

and the 56 modules collectively covered about 9ha of the seafloor. The modules at each location were built either fromquarry rock or concrete rubble and were constructed to formlow-lying reefs (i.e. o1m tall) that mimicked natural reefs inthe region. These two types of materials were chosen becausethey are the two materials most preferred by the CaliforniaDepartment of Fish and Game for building artificial reefs inCalifornia and little information exists on their relativeeffectiveness in supporting reef biota. Four modules at eachlocation were built from quarry rock and four were built fromconcrete rubble. These two constructionmaterials differed withrespect to their size and shape: The quarry rock was boulder-likein appearance, whereas the concrete rubble consisted primarily

DANIEL C. REED ET AL.276

of pieces of flat slabs that tended to be longer, wider, andslightly shorter than quarry rocks (Table 1). The different sizesand shapes of the two materials caused rock and concretemodules to differ somewhat with respect to small scaletopography. The slabs used to build concrete modules resultedin modules that had a greater proportion of horizontalsubstrate and a surface that was slightly more regular thanmodules constructed from quarry rock (Table 2). Surfaceirregularity was estimated by divers by draping four regularlyspaced chains across 12 regularly spaced 1-m2 quadrats onselected modules and measuring the surface slope at 10-cmintervals along each chain. Surface irregularity within quadratsis expressed as the mean proportion of observations where theslope category (Table 2) differed between contiguous 10-cm

intervals. Mean � SE surface irregularity of rock (n5228) andof concrete modules (n5204) were 0.449 � 0.054 and0.376 � 0.048, respectively. By design, the amount of quarryrock and concrete rubble used to build the modules wassystematically varied to produce a wide range in the bottomcoverage of hard substrate (approximately 30%–90%) onmodules of the two reef types within each location. This wasdone to evaluate the extent to which the bottom coverage ofreef substrate influenced the abundance and species richnessof colonizing biota.

The abundance and size of Macrocystis at SCAR, San Mateo,and Barn were sampled on two occasions (March–April 2000and July–August 2000, hereafter referred to as surveys 1 and 2,respectively) during the first year after completion of construc-tion on 29 September 1999. All Macrocystis greater than 5 cmtall were counted in a 2-m wide area centered along apermanent transect line that ran the length of each artificialreef module (approximately 40m). Four transects weresampled per module for a total sample area of about320m2 �module�1 (or approximately 20% of themodule area).Nine permanent 40 � 2–m transects were sampled at SanMateo and Barn. Because it was inefficient to count smallerMacrocystis in an area as large as that delineated by the transects,individuals less than 5 cm tall were counted in six 1-m2 quadratsthat were spaced evenly along each transect. These small plantsconsisted of a single blade attached by a stipe. Macrocystisgreater than about 2 cm tall can easily be distinguished fromother species of kelp by an undulation at the base of the blade.Smaller plants lacking this undulation could not be identified tospecies by divers and therefore were not included in ouranalyses. Such small plants were not abundant at the times ofour sampling.

Macrocystis is the world’s largest alga. An adult plant consistsof a bundle of vine-like fronds buoyed by small gas bladdersand anchored by a common holdfast. Upon reaching the seasurface, the fronds (sometimes exceeding 30m in length)spread out to form a dense canopy. Spores are produced in asorus on blades located near the base of the plant. Forconvention, we use the term ‘‘recruit’’ to mean individuals lessthan 1m tall and ‘‘adult’’ to mean individuals more than 1mtall. We measured plant size, fecundity (i.e. spore standingcrop), the size of the reef substrate to which the holdfast wasattached, and survivorship for all adults. Plant size wasdetermined in two ways: by the number of fronds more than1m tall and by the basal area of the holdfast. Holdfast area wascalculated from measurements of holdfast length and widthusing the equation for an ellipse (area5 length � width � p/4). Fecundity was estimated as the total area of all sori on anindividual following the methods of Reed et al. (1996). Thelength and width of the substrate to which each adult wasattached weremeasured and used to estimate substrate size (i.e.area) using the equation for a rectangle (length � width). Thismeasurement was made to help distinguish dislodged adult

FIG. 1. Map of San Clemente Artificial Reef (SCAR) and thenatural reefs at Dana Point, San Mateo, and Barn. Numbersshown in the inset represent the locations of the seven clusters ofeight modules. The distances between the northern edge of SanMateo and the center of each location are as follows: location 1,0.6km; location 2, 0.9km; location 3, 1.3km; location 4, 1.8 km;location 5, 2.1 km; location 6, 2.5 km; location 7, 3.4km.

TABLE 1. Physical characteristics of rock and concretemodules on SCAR.

Reef type Length Width Height n

Rock 60 � 1.50 42 � 1.10 30 � 0.83 145Concrete 90 � 1.30 62 � 0.95 25 � 0.34 864

Values are the mean � SE dimensions (cm) of quarry rockand concrete boulders used to build SCAR. Data are frombouldersmeasured in the construction yard before deploymentto the ocean.

TABLE 2. Frequency distribution of the surface slope ofquarry rock and concrete on the artificial reef modules.

Slope (degrees) Rock Concrete

0–15 25.3 35.516–45 25.8 20.046–75 18.7 14.276–90 25.7 25.5OV 4.4 4.8

OV, overhang. Surface slope was recorded by divers atuniformly distributed points within regularly spaced 1-m2

quadrats on each module. Data are percentages. N53816 and3104 points for rock and concrete, respectively.

COLONIZATION IN GIANT KELP 277

Macrocystis that drifted to SCAR (hereafter referred to as‘‘drifters’’) from resident adults derived from spores thatsettled on SCAR; drifters in the San Clemente region aretypically attached to smaller sized rocks, which are easily liftedoff the bottom by the added buoyancy that accompaniesincreased plant size. The holdfast of each adult Macrocystiscounted in survey 1 wasmarked with a uniquely numbered tag,and its position on the transect was measured. We determinedthe survivorship of these plants by recording their presence orabsence in survey 2. The number of untagged adults recordedin survey 2 provided us with a measure of the amount of adultrecruitment that occurred between surveys 1 and 2.

We took two approaches to determine the likely source ofspores for the high densities of recruits observed in survey 2(see results below). First, we compared estimates of the sizes ofthe spore sources at SCAR, San Mateo, and Barn during thewinter of 2000 using data collected during survey 1. Resultsfrom previous studies of recruitment inMacrocystis suggest thatthe vast majority of plants that recruit in spring are derivedfrom spores that are released and settle during the precedingwinter (Reed and Foster 1984, Deysher and Dean 1986, Reed1990, Reed et al. 1997). The size of the spore source on SCAR,San Mateo, and Barn was estimated as the product of adultdensity, mean per capita fecundity, and reef area at each site. Todetermine whether the density of recruits at SCAR was linkedto local spore production, we examined the relationshipbetween the number of recruits on a given module in survey2 (estimated as the density of recruits � area of the module)and the standing crop of spores on the module in survey 1(calculated as the density of adults � per capita fecundi-ty � area of the module).

Our second approach to assessing the contributions of localverses distant spore sources to local recruitment involvedmultiple linear regression analysis. Here we tested whetherrecruitment to SCAR in survey 2 was related to local sources(i.e. the abundance of drifters in survey 1) and/or distance fromSan Mateo using the 56 modules as replicates. Because sporesupply is expected to decline with distance from the sporesource in a geometric fashion (Gaylord et al. 2002), we used logof distance from San Mateo kelp bed for the distance variable.Multicollinearity of explanatory variables can often be aproblem when examining ecological data using multipleregression (Graham 2003). We tested for collinearity betweendrifter abundance and distance from SanMateo kelp bed usingtwo different methods: 1) by evaluating tolerance variables(Quinn and Keough 2002) and 2) by evaluating conditionindices (Belsley et al. 1980). Both approaches showed thatcollinearity between distance from San Mateo and drifterdensity was not a problem in our multiple regression model.Thus, a result in which only drifter abundance was significantwould be evidence for dispersal from a local source. A result inwhich only distance was significant would be evidence forwidespread dispersal from a distant source. A result in whichboth drifter abundance and distance were significant wouldsuggest that both local and distant dispersal contributedsignificantly to the colonization event observed on SCAR.

We examined the individual and combined influences ofhabitat availability (i.e. bottom cover of artificial reef substrate),reef type (i.e. quarry rock vs. concrete rubble), and distance tothe nearest source population (our surrogate for colonistsupply) on the density ofMacrocystis colonists on SCARusing ananalysis of covariance (ANCOVA) procedure in which distanceand reef type were considered fixed categorical factors and thepercentage cover of artificial substrate the covariate. Separateanalyses were done for drifters in survey 1 and benthic recruitsin survey 2. We treated distance as a categorical variable in thisanalysis (above it was treated as a continuous variable) becausewe were specifically interested in whether the relationshipbetween bottom cover and recruitment varied as a function of

distance from San Mateo kelp bed. This interaction betweenbottom cover and distance may be interpreted more clearlywhen distance is a categorical variable. In these analyses wefollowed the recommendation of Quinn and Keough (2002) byfirst testing the full ANCOVA model and then parsing termshaving an alpha 40.2 until a reduced model was attained. Tofurther investigate the role of habitat availability and sporesupply in determining the patterns of Macrocystis recruitmentobserved in survey 2, we expressed data on the density ofrecruits in two different ways: as the number of recruits �m�2

of artificial substrate and as the number of recruits �m�2 of thesea floor. Data used in all analyses were mean densitiescalculated for each module. All density data were transformedto log (xþ 1) to meet the assumption of homoscedasticity.

RESULTS

Relatively sparse colonization by Macrocystis oc-curred on SCAR during the first 6 months of theexperiment. At the time of survey 1, the mean densityof giant kelp on SCAR was 10% of that at San Mateoand 2% of that at Barn (mean numbers of Macro-cystis � 100m�2 � SE were 40.8 � 7.8, 10 � 2.6, and0.9 � 0.1 for Barn, San Mateo, and SCAR, respec-tively). All theMacrocystis observed on SCAR at this timeappeared to be intact adults that drifted to the artificialreef from nearby natural reefs. Most Macrocystis atSCAR were relatively small individuals (both in termsof frond number and holdfast area) that were attachedto cobbles and small boulders made of natural rock(Fig. 2). In contrast, adult Macrocystis growing in SanMateo and Barn were relatively evenly distributedamong a wide range of sizes and were attached mostlyto bedrock and large boulders, suggesting that most ofthese plants recruited directly to San Mateo and Barnfrom spores (as opposed to drifting in from other kelpbeds). Follow-up observations revealed that the fewdrifters on SCAR recorded as being attached to largeboulders were actually attached to smaller naturalrocks that became wedged among larger quarry rockor concrete boulders. No recruitment by Macrocystis toquarry rock or concrete rubble was observed at thistime. Patterns of drifter colonization on SCAR were notaffected by reef type nor were they related to thebottom coverage of artificial substrate (P40.35 for themain and interactive effects of reef type and bottomcoverage in the reduced ANCOVA model). Theabundance of drifters at SCAR, however, was signifi-cantly affected by location (F6, 41514.29, Po0.001) asdrifter density declined exponentially with distancefrom San Mateo kelp bed, the nearest source popula-tion (Fig. 3).

The mortality of drifters at SCAR was higher thanthat of adults at San Mateo and Barn. Sixty-six percentof the drifters tagged on SCAR in survey 1 were notfound in survey 2 (compared with 48% for San Mateoand 22% for Barn). Most of the mortality at SCARresulted from the loss of small plants (i.e. less than fivefronds), which tended to have low fecundity and beattached to small rocks (Fig. 4). The recruitment of newadult drifters on SCARwas not sufficient to compensatefor the mortality of drifters, and the overall density of


drifters on SCAR declined by 47% between survey 1and survey 2.

High densities of Macrocystis recruits were observedon SCAR during survey 2 (Fig. 5). Interestingly,relatively low numbers of recruits were found in thecluster of modules located closest to San Mateo. Asidefrom this, densities of Macrocystis recruits on SCARdropped off rapidly with distance from San Mateomuch in the same way that drifters did. Nevertheless,mean densities of giant kelp recruits still exceeded0.5perm2 of artificial substrate and 0.3perm2 of thesea floor on the most distant modules, which werelocated an average of 3.4 km from the nearest sourcepopulation. The density of recruits on quarry rock andconcrete rubble was generally similar regardless ofdistance (Table 3). The effects of reef type on thedensity of recruits per area of bottom, however, variedinconsistently with distance from San Mateo kelp bed(Fig. 5b; see significant distance � reef type interactionin Table 3).

The density of Macrocystis recruits on quarry rockand concrete substrates was unrelated to the amount of

quarry rock or concrete on a module (Table 3).Consequently, the number of kelp recruits on amoduletended to be higher on modules having a greater coverof rock and concrete (Fig. 6). However, the strength ofthis positive relationship varied inexplicably withdistance from San Mateo kelp bed (see distance �cover interaction in Table 3). Unlike that at otherdistances, recruitment of Macrocystis on moduleslocated 2.1 and 2.5km from SanMateo was consistentlylow and did not vary with the bottom cover of artificialreef habitat (Fig. 6).

The sparse density and reduced fecundity of drifterscoupled with a relatively small area of reef resulted in aspore source at SCAR during winter 2000 that wasapproximately 2.5 orders of magnitude smaller thanthat at San Mateo and Barn (Table 4). Also, we foundno relationship between the total fecundity on amodule in survey 1 and the number of Macrocystisrecruits observed on it in survey 2 (F1,5450.13,P50.7174). Finally, the results of the multiple regres-sion showed that recruitment to the artificial reefmodules was strongly and negatively related to theirdistance from San Mateo (Table 5). Importantly, thedensity of drifters was not a significant source variationin the model. Together these results indicate that thelocal dispersal of spores released from drifters con-tributed very little to the recruitment of giant kelpobserved on SCAR.

DISCUSSION

Partitioning out variation in recruitment due tolimitations on dispersal, source density, source strength,and establishment in a natural setting is logisticallychallenging for many species including kelps, whosetiny spores (approximately 10mm in length) are difficultto study in nature. Studies showing kelp recruitsrestricted to within a few meters of a single or smallgroup of isolated adults have led many to believe that

FIG. 2. Frequency distributions of (a) Macrocystis frondnumber, (b) Macrocystis holdfast area, and (c) the size of the rockto which Macrocystis was attached for B (Barn), SM (San Mateo),and SCAR. Data are from survey 1. n5294, 72, and 165 plantsfor B, SM, and SCAR, respectively, in Figure 4a and 4c, andn5290, 72, and 150 plants for B, SM, and SCAR, respectively, inFigure 4b.

FIG. 3. Mean ( � SE) density of Macrocystis drifters �m�2 ofbottom at SCAR during survey 1 at different distances from SanMateo kelp bed. n58 modules per distance.


dispersal limitation plays a prominent role in determin-ing local patterns of kelp abundance (Dayton 1985,Schiel and Foster 1986, Santelices 1990). Caution needsto be used when interpreting the results of such studies,which largely ignore other sources of recruitmentlimitation. The role of source limitation is of particularinterest in this case, because kelps typically occur inrelatively dense stands that can encompass hundreds ofhectares in area. The odds of detecting long-distancedispersal from a dense stand is much greater than it isfrom a few individuals because an increase in theconcentration of propagules at their point of release willresult in a proportional increase in their concentrationat a given distance from their source (Reed et al. 1997,Clarke et al. 1998). Thus, relying on results derivedfrom unnaturally small sources can lead to under-estimates of dispersal distance and overestimates of

dispersal limitation. Unfortunately, measuring coloni-zation to estimate spore dispersal from large popula-tions of kelp can be problematic because it requiresunoccupied reef habitat that is sufficiently isolated fromother sources of spores. Such conditions, which aretypically uncommon in nature, were provided after theconstruction of SCAR, thus allowing experiments ondispersal in Macrocystis to be done under more typicalconditions of source density and source strength.

As in earlier studies, we found that recruitment ofMacrocystis was generally limited by spore supply; afteran initial increase, the density of recruits rapidlydeclined with distance from the nearest source popula-tion. The rapid drop-off in recruitment to the northcoupled with the relatively large size, high fecundity,and close proximity of the kelp bed at San Mateo to thesouth implicate it as the most likely source for theobserved colonization event. However, unlike otherstudies where recruits were restricted to within a fewmeters of the parent plants, we observed relatively

FIG. 4. Macrocystis drifters at SCAR. (a) Percent of totalmortality that occurred between surveys 1 and 2 for plants ofdifferent sizes. (b) Relationship between size and fecundity forplants sampled during survey 1. (c) Mean ( � SE) size of rock towhich drifters were attached for different sized plants. Meansthat share the same letter are not significantly different from oneanother at P5 0.05 using Ryan-Einot-Gabriel-Welsh multiplerange test (SAS 2001).

FIG. 5. Abundance of Macrocystis recruits at SCAR duringsurvey 2 vs. distance from San Mateo kelp bed. (a) Mean numberof recruits (� SE) �m�2 of artificial substrate. n5 8modules (rockand concrete combined). (b) Mean number of recruits(� SE) �m�2 of bottom on rock (open symbols) and concrete(closed symbols) modules. n54 modules per reef type for eachdistance.


dense colonization by Macrocystis over distances of atleast several kilometers. The small size and lowfecundity of the drifter population on SCAR, coupledwith the lack of a relationship between the localfecundity of drifters and the local density of recruitsand the failure of drifter density to explain any of thevariation in recruitment in the multiple regression,argue against drifters being the primary source ofspores for the colonization ofMacrocystis on SCAR. Thisview is consistent with Graham’s (2003) finding thatspore concentrations were unrelated to the localfecundity of adult Macrocystis growing near the edgesof the Point Loma forest, where advective currents thattransport spores are much less impeded by the forestcanopy. One would expect a similar decoupling

between local fecundity and spore supply to haveoccurred for isolated drifters on SCAR.

When invoking drifters to explain patterns ofdistant colonization in kelp, it is important to recognizethat a drifting plant constitutes a relatively small sporesource and constraints on colonization distance due todilution effects are expected to be high (Anderson andNorth 1966, Reed et al. 1997). Such constraints arguethat any colonization originating from spores releasedby drifters would be localized and would occur onlyalong the path the drifter had taken. Consequently,large numbers of highly fecund drifters would havebeen needed to produce the dense recruitment of giantkelp that occurred on SCAR. Such large numbers ofdrifters were never observed. In addition to oursurveys, we conducted a substantial amount of divingon SCAR before survey 1 (38 days totaling 147hunderwater) and between surveys 1 and 2 (36 daystotaling 448h underwater). At no time during thesedives did the sizes and densities of drifters appeardifferent from that recorded in our surveys. Moreover,our data on the mortality and recruitment of drifterssuggest that episodes of transient influxes of largenumbers of drifters were unlikely. Because mostdrifters wash up on the beach soon after becoming

FIG. 6. Relationships between the density of Macrocystisrecruits and the bottom coverage of artificial reef substrate forthe seven locations at SCAR. The distance of each location isgiven to the right of each regression line. Data are from survey 2.n58 module means per location.

TABLE 3. Effects of distance from the nearest sourcepopulation and reef type (quarry rock vs. concrete rubble)on the relationship between the percentage cover ofartificial substrate and the number of Macrocystis re-cruits �m� 2 of artificial reef substrate and the number ofMacrocystis recruits �m� 2 of sea floor.

Source df MS F P

Artifical reef substrateDistance 6 4.45 � 10�4 17.75 o0.0001Reef type 1 0.06 � 10�4 0.00 0.9614Distance � reef type 6 4.10 � 10�4 1.64 0.1614Cover 1 3.79 � 10�4 1.51 0.2258Error 41 2.51 � 10�4

Sea floorDistance 6 0.01141 0.87 0.5274Reef type 1 0.00079 0.06 0.8081Distance � reef type 6 0.03349 2.55 0.0373Cover 1 0.31448 23.95 o0.0001Distance � cover 6 0.03699 2.82 0.0242Error 35 0.01313

Shown are the reduced ANCOVAmodels. Other interactionsinvolving the covariate ‘‘cover’’ were not significant (allP40.20), indicating the assumption for homogenous slopeswas met for those terms.

TABLE 4. Estimates of the size of the spore sources atSCAR, San Mateo, and Barn during March–April 2000.

SCAR San Mateo Barn

Sorus area(m2) �plant� 1

0.086 � 0.022 0.213 � 0.089 0.379 � 0.291

Plant density(no �m�2)

0.009 � 0.001 0.100 � 0.026 0.408 � 0.078

Reef area (m2) 85,099 1,662,147 704,204Sorus area of

reef (m2)117 48,578 58,108

Values for sorus area and plant density are means � SE.Estimates of reef area are from side scan sonar data provided byEcosystems Management, Encinitas, California. Sorus area ofreef was calculated as the product of sorus area �plant�1, plantdensity, and reef area.

TABLE 5. Effects of distance from San Mateo kelp bed andnumber of local adults (i.e. drifters) on a module on thedensity of Macrocystis recruits on a module.

Effect Coefficient t P

Intercept 0.837 7.202 0.000Distance � 1.121 � 4.140 0.000Drifter number 0.001 0.285 0.777

Source df MS F P

Analysis of varianceRegression 2 0.798 16.244 0.000Error 53 0.049

Distance was log transformed, because of the expectation of anegative exponential decline in spore density as a function ofdistance. Recruit density was log transformed to meet theassumptions of homoscedasticity.


dislodged (Zobell 1971, Harrold and Lisin 1989), anylarge influxes of transient drifters to SCAR would mostlikely have been accompanied by a sizable increase inthe amount of drift kelp on the beaches inshore ofSCAR. Such was not the case. Monthly surveys of the 5-km stretch of coast inshore of SCAR during November1999 through June 2000 showed that amount of driftMacrocystis on the beach was consistently below average(Grove 2002). Thus, it is improbable that largenumbers of drifters immigrated to SCARwithout beingnoticed. Rather, our collective observations suggest thatthe colonization of SCAR by Macrocystis resulted fromthe widespread dispersal of spores from a large sporesource to the south (most likely San Mateo). Thishypothesis is supported by model predictions of sporedispersal (Gaylord et al. 2002) and by field observa-tions of giant kelp recruitment at isolated sites (Daviset al. 1982, Ebeling et al. 1985), which suggest thatkilometer-scale spore dispersal inMacrocystismay occurroutinely.

We initially considered distance from the San Mateokelp bed to be a good proxy for spore supply. However,the relatively low recruitment observed at the cluster ofmodules located closest to San Mateo suggests that therelationship between spore supply and distance fromthe spore source may be more complex, particularlyclose to the spore source. Such seemingly anomalouspatterns may occur regularly. Anderson and North(1966) found that density ofMacrocystis recruits actuallyincreased with distance from the edge of a dense kelpforest out to 40m, which is the farthest distance theyexamined. Similarly, Reed et al. (1988) found germlingdensities of the kelp Pterygophora californica weresometimes lower adjacent to the source populationthan at distances located as much as 500m down-current. The cause for such patterns are not known butmay be related to the time it takes for newly releasedspores to settle to the bottom. Kelp spores are nearlyneutrally buoyant in seawater and, depending on theconditions of turbulent flow, take several hours to reachthe sea floor after their release (Gaylord et al. 2002).The pattern of a peak in settlement at some distanceaway from the point of propagule release is not uniqueto kelps; suspension times in air have been used toexplain similar patterns of seed and pollen depositionin many species of wind-dispersed trees (Greene andJohnson 1989, Clark et al. 1998, Nathan et al. 2001).

Postsettlement mortality resulting from limitationsin the availability of suitable reef habitat (i.e. establish-ment limitation) was also important in determiningpatterns of colonization by Macrocystis because theoverall abundance of recruits tended to increase withthe bottom cover of artificial reef substrate. Thispattern is not surprising because giant kelp is restrictedlargely to growing on hard substrata in all but thecalmest of locations (Schiel and Foster 1986). Interest-ingly, we found that the type of hard substrata (rock vs.concrete) had little effect on patterns of colonization.Small-scale studies of algal recruitment have shownthat spores of many species settle disproportionately on

the edges or ridges of benthic substrates as a result ofturbulent deposition (Foster 1975, Norton and Fetter1981, Johnson 1994). The boulder-like appearance ofthe quarry rock used in the construction of SCARtended to have more, albeit less well-defined, edgesthan the concrete rubble. Any small-scale differences inrecruitment between rock and concrete that mighthave arisen from disproportionate spore settlementcaused by differences in their topography were notevident at the scale of a module.

Propagule behavior has been implicated as animportant factor affecting the distribution of older lifestages at a variety of spatial scales (Raimondi 1991,Wellington 1992, Cassele and Warner 1996). Althoughlaboratory studies have shown that spore behavior caninfluence patterns of settlement in Macrocystis (Amslerand Neushul 1990), little is known about the extent towhich habitat selection by spores influences patterns ofkelp recruitment in nature. Under conditions ofdispersal limitation, preferential settlement by sporesfor either hard or soft substrata would have beenindicated by a significant relationship between thedensity of recruits on artificial reef substrate and theamount of artificial reef substrate (a negative relation-ship if hard substrata were preferred vs. a positiverelationship if soft substrata were preferred). We foundno such relationships, suggesting that selective beha-vior for substrate type by spores did not influencepatterns of kelp colonization on SCAR at the spatialscales that we sampled (m2 to tens of m2). Instead, ourresults suggest that recruitment on SCAR resultedfrom a rain of spores settling uniformly on the bottomand that the abundance and distribution of recruits wasdriven largely by the intensity of the spore rain and thebottom cover of artificial reef habitat.

It is becoming increasingly clear that recruitmentlimitation in a wide diversity of organisms arises fromconstraints on both propagule supply and establish-ment (Connell 1985, Clark et al. 1998, Schmitt andHolbrook 2000). Our findings are consistent in thisregard. Spatial variability in spore supply and bottomcover of hard substrata explainedmuch of the variationthat we observed in the recruitment ofMacrocystis. Ourobservations of substantial colonization on moduleslocated several kilometers from the nearest sourcepopulation provide the first compelling empiricalevidence that dispersal limitation in Macrocystis is notas severe as has been commonly perceived. The largesize and high fecundity typical of many Macrocystispopulations helps to promote the supply of spores atquantities sufficient for colonization to most reefs inregions where giant kelp occurs. As in most systems,adequate supply and habitat do not by themselvesensure successful colonization. Recruitment in giantkelp also depends on suitable levels of competitors andgrazers (Reed and Foster 1984, Ebeling et al. 1985,Harrold and Reed 1985, Reed 1990) and abioticconditions that are favorable for spore germinationand embryonic growth (Luning and Neushul 1978,Deysher and Dean 1986, Kinlan et al. 2003). Although


such favorable conditions do not always coincide withepisodes of elevated spore supply, they appear to co-occur frequently enough to allow for the rapidreplenishment of most Macrocystis populations thatare damaged or destroyed by disturbance (Foster 1982,Dayton et al. 1992, Graham et al. 1997, Edwards2001).

We gratefully acknowledge the assistance of D. Huang, D.Malone, J. Bunch, D. Gates, I. Huasig, C. Nelson, J. Schaffer,G. Snyder, D. Toole, D. Weisman, and G. Welch in collectingand assembling the data. M. Carr, J. Dixon, B. Gaylord, M.Graham, and M. Steele provided helpful comments forimproving themanuscript. Funding was provided by SouthernCalifornia Edison as required by the California CoastalCommission under SCE’s coastal development permit (No.6-81-330-A, formerly 183-73) for Units 2 and 3 of the SanOnofre Nuclear Generating Station and by the NationalScience Foundation under grant number OCE99-82105.

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