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Estuarine, Coastal and Shelf Science 85 (2009) 472–478

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Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier .com/locate/ecss

Welcome mats? The role of seagrass meadow structure in controllingpost-settlement survival in a keystone sea-urchin species

Patricia Prado a,b,*, Javier Romero c, Teresa Alcoverro b

a Dauphin Island Sea Lab., 101, Bienville Boulevard, Dauphin Island, AL 36528, USAb Centro de Estudios Avanzados de Blanes, c/Acces a la Cala St., Francesc, 14, 17300 – Blanes, Girona, Spainc Departamento de Ecologıa, Facultad de Biologıa, Universidad de Barcelona, Avda, Diagonal 645, 08028 – Barcelona, Spain

a r t i c l e i n f o

Article history:Received 20 July 2009Accepted 18 September 2009Available online 24 September 2009

Keywords:sea urchinspopulation structurePosidonia oceanicapost-settlementrecruitmentrhizome mat structure

* Corresponding author. Dauphin Island Sea LaDauphin Island, AL 36528, USA.

E-mail address: pprado@disl.org (P. Prado).

0272-7714/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.ecss.2009.09.012

a b s t r a c t

Processes acting on the early-life histories of marine organisms can have important consequences for thestructuring of benthic communities. In particular, the degree of coupling between larval supply and adultabundances can wield considerable influence on the strength of trophic interactions in the ecosystem.These processes have been relatively well described in rocky systems and soft-sediment communities, andit is clear that they are governed by very different bottlenecks. Seagrass meadows make interesting studysystems because they bear structural affinities to both soft sediments as well as rocky substrates. Weexamined the early-life history of Paracentrotus lividus, one of the dominant herbivores in Mediterraneanseagrass meadows, to identify the drivers of population dynamics in this species. We measured spatial andtemporal variability in sea urchin post-settlement in 10 Posidonia oceanica meadows in the North-WesternMediterranean over a period of two years, and compared the numbers with the one-year old cohort a yearlater (i.e. the new population recruitment) as well as between successive size–age groups. Urchin post-settlers differed substantially between meadows but were present in both years in all meadows surveyed,suggesting that larval supply was not limiting for any of the studied sites. However, in six of the studiedmeadows, the one-year cohort of urchins was absent in both years, indicating that post-settlementprocesses strongly affected urchins in these meadows. In contrast, in four of the studied meadows, therewas a strong coupling between post-settlers and one-year cohort individuals. These meadows werestructurally different from the others in that they were characterised by an exposed matrix of rhizomesforming a dense seagrass mat. This mat apparently strongly mediates post-settlement mortality, and itspresence or absence dictates the successful establishment of urchin populations in seagrass meadows. Asthe population aged, the relationship between size–age groups decreased evidencing the action of otherprocesses. Yet, these results indicate that differences in physical structure are a vital bottleneck for seaurchin populations in seagrass meadows. Exploring the interaction between ecosystem structure andearly-life history may provide a broader and more unified framework to understand the dynamics ofa range of benthic habitats, including rocky substrates, soft sediments and seagrass meadows.

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1. Introduction

In exploring the centrality of early-life history to the structuringof marine benthic ecosystems, research has identified a complexsequence of processes, from larval production to eventual settlementand growth, which can each play a limiting role in influencing theabundance of key species and, hence, in shaping the benthiccommunity. Determining which of these processes (larval avail-ability, settlement and metamorphosis success, post-settlement and

b., 101, Bienville Boulevard,

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juvenile survival, including predation and competition etc) is thebottleneck for populations of benthic marine invertebrates is stilla matter of considerable debate, but it appears to be highly contin-gent on the species and ecosystems concerned (Morgan, 2001). Thematter has received most attention in hard-bottom ecosystems suchas coral reefs and rocky shore, both intertidal and subtidal. In suchhabitats, post-settlement processes (predation and both inter andintraspecific competition) have been identified to be the maindrivers, although larval supply can become important when ocean-ographic conditions are appropriate and transport occurs towardsfavourable habitats (Underwood and Denley, 1984; Roughgardenet al., 1988; Gaines and Bertness, 1992; Broitman et al., 2008).Although soft bottom communities have not received the same levelof attention, the emerging consensus is that populations inhabiting

P. Prado et al. / Estuarine, Coastal and Shelf Science 85 (2009) 472–478 473

marine sediments are rarely limited by propagule supply (Olafssonet al., 1994), particularly where adult abundance is locally very high(Highsmith, 1982; Pearce and Scheibling, 1990). Instead, the sedi-ment characteristics and stability seem to be of prime importance forsettlement and post-settlement stages whereas juvenile recruitmentand migration processes often help to determine community struc-ture (Woodin,1978; Morgan, 2001). The degree of coupling betweenearly-life history processes and adult distributions appears thus to becontingent on the physical properties of benthic substrate. In fact,these physical differences make difficult to extrapolate processesfrom one to another type of substrate (Wilson, 1991). The solidrugosity of rocky substrates, creating refuges, increasing space andproviding relative protection from environmental disturbances,makes stability and complexity their main attributes. In contrast,structurally simpler and relatively unstable soft bottoms are highlydynamic, and are governed by the interplay between environmentaldisturbance, grain size, sediment movements and burial (Morgan,2001). Seagrass meadows could be considered to lie somewherebetween this the two extreme cases, with structural attributes ofboth soft sediments and hard bottoms. The majority of seagrassecosystems thrive in soft sediment substrates, growing on sands andsilts, but meadow structural complexity both above (leave canopyand decaying leaves) and below (roots and rhizomes) the sedimentalso provides a firm, stable surface analogous to hard-bottom habi-tats. This duality makes them interesting models in which toexamine how structural characteristics influence the early-lifehistory of functionally important species within the ecosystem.

It is becoming increasingly evident that herbivory, a previouslyunderappreciated process plays a significant functional role inseagrass meadows (see review by Heck and Valentine, 2006 andreferences therein). Variations in herbivore populations can causelandscape level differences in seagrass meadow dynamics, and it isvital to understand what drives these differences in their pop-ulations. Sea urchins are perhaps the most important herbivores inseagrass ecosystems today, and their abundance can, under somecircumstances, reach explosion levels, causing serious overgrazingevents and urchin barrens (review by Eklof et al., 2008). Amongfactors controlling sea urchin populations, larval availability andpost-settlement mortality are perhaps the most important bottle-necks for the abundance of adult echinoids (Rumrill, 1990; Lozanoet al., 1995; Lopez et al., 1998). Predation seems to play a major role,as it has been demonstrated that it can reduce the densities ofrecently metamorphosed individuals from hundreds to only a fewindividuals per square meter (Turon et al., 1995; Lopez et al., 1998).Numerous species of fishes, gastropods and crustaceans seems tocontrol the abundance and size distribution of sea urchin throughdirect consumption (Tegner and Dayton, 1981; McClanahan, 1999;Guidetti, 2004). In seagrass habitats, however, the importance ofpredation in shaping sea urchin populations may be lower due tothe efficient sheltering effect exerted by the leaf canopy (Farinaet al., 2009). However, while the relative importance of theseprocesses have been well described in soft and rocky substrates(Morgan, 2001; Menge and Branch, 2001; Lenihan and Micheli,2001 and Hereu et al., 2005) very few attempts have been made tounderstand their importance in seagrass ecosystems.

This study was conducted on the sea urchin Parcentrotus lividus(Lamarck), one of the most important consumers of Posidoniaoceanica seagrass meadows in the Mediterranean. This species hasbeen estimated to remove, from 6% to 36% of annual leaf produc-tion, depending on sea urchin abundance (Prado et al., 2007). Thespecies spends around one month in its larval stage (Lopez et al.,1998), and it settles to both rocky and seagrass habitats betweenspring and early summer (Lopez et al., 1998; Hereu et al., 2004;Tomas et al., 2004). In this study we explored the importance ofearly-life history in determining juvenile sea urchin populations in

seagrass meadows. We monitored sea urchin post-settlers as wellas the size distribution and abundance of the juvenile and adultpopulation for two years at ten seagrass meadows along theSpanish Mediterranean coast. In particular, we focused on spatialand temporal variability in the abundance of post-settlers, and inthe degree of coupling with 1) the population cohort one year later(i.e. new recruitment in the population) as well as 2) between thisnew cohort and successive population sizes older than one year.

2. Materials and methods

2.1. Study sites and sampling design

Post-settlers, one-year cohort and adult sea urchin distributionwas assessed in ten shallow (5–8 m depth) Posidonia oceanica bedsalong the Catalan Coast (Fig. 1). These were largely representative ofshallow seagrass meadows within the region, which are extremelyscarce in the southern part, and encompassed a wide range ofstructural properties (see below). Artificial substrates were used tosample post-settlement rates in the seagrass canopy (Tomas et al.,2004). Post-settlement mortality was evaluated as the differencebetween the abundance of new post-settlers and one-year cohortwithin the seagrass beds one year later. Finally the abundance ofadults and subadults (i.e. all the cohorts older than one year) wasmeasured to establish its association to the abundance of post-settlers and one-year old cohort classes. We decided to estimatepost-settlement instead of settlement (as a proxy of larval supply),recognising full well that they do not equate to the same thingprimarily because effective quantification of settlement needs high-frequency sampling, which was logistically unfeasible across thelarge spatial and temporal scales considered here. As other authorshave noted (see the recent paper of Broitman et al., 2008) estimatesof post-settlers in collectors that mimic the settling substrate are thenet result of a number of transport, settlement, and post-settlementevents that occur at sub-monthly scales, and, as a result theseprocesses cannot be completely separated.

Post-settlement, the one-year old cohort (i.e. the new recruit-ment) and adult sea urchins were evaluated in summer 2003 (allsites except Montroig, see below), and re-evaluated in summer 2004(all sites). Additionally, in 2003 we characterised meadow substrate,determining whether the meadow had a buried or unburiedrhizome-root layer (see Fig. 2).

2.2. Post-settlement

Post-settlement rates in all study sites were evaluated byhaphazardly deploying nine collectors within the shallow seagrassmeadow. The collectors consisted of scrub brushes (16� 5 cm) withvegetal bristles; these brushes have been shown to be very effectivesettlement devices for collecting sea urchin larvae and are useful asa comparative recruitment assay (Tomas et al., 2004; Hereu et al.,2004). Collectors were fastened to a rope and attached to a smallbuoy at the canopy height at one end and hammered into the sedi-ment with a picket at the other (Tomas et al., 2004). The collectorswere left in the field for two consecutive 15 day periods from the15th May to the 15th June 2003 and 2004 to capture the entire larvaland settlement peak period, which has been reported to occurbetween spring and early summer for this species (Lopez et al.,1998;Hereu et al., 2004). Consequently, recovered post-settlers were �15days old. By replacing the collectors we also aimed to prevent theaccumulation of detritus and benthic algae and to minimise possiblepredation effects (Broitman et al., 2008). We removed collectors bycutting the rope to which they were attached and placing themcarefully into individual plastic bags. Special care was taken tominimise re-suspension and loss of attached organisms. Bags

Fig. 1. Map of the NW Mediterranean showing position of each study site.

P. Prado et al. / Estuarine, Coastal and Shelf Science 85 (2009) 472–478474

containing the collectors were placed into an icebox and transportedto the laboratory where they were thoroughly rinsed with fresh-water through a 250 mm mesh. Filtered contents were preserved inglass containers for further sorting and counting of post-settlersunder the microscope (Hereu et al., 2004). The size of the post-settlers was additionally measured with a microscope integratedmicrometer to verify that individuals had all a similar benthic age(407� 3.7 mm; ca. 15 days of benthic life).

2.3. One-year old cohort and adult and subadult populations

At each study site, Paracentrotus lividus abundance of one-yearold individuals (between 0.5 and 1.5 cm diameter, Crapp and Willis,1975) and the remaining age size distribution (individuals> 1.5 cm)was obtained by counting individuals in fifteen haphazardly placed50� 50 cm quadrats within each shallow meadow in both 2003 and

Fig. 2. a) Three-dimensional mat structure of Posidonia oceanica showing the availability of haccessible.

2004. For juvenile recruits (i.e. one-year old cohort), densities wereassessed by exhaustive visual inspection and careful, repeatedintroduction of bare hands among the rhizomes to allow sensing ofhidden individuals (always found in the first 10 cm of rhizomelawyer). Sea urchin test diameter was measured in situ usinga calliper to the nearest mm but for simplification sizes larger than1.5 cm were further grouped in subadult (1.5–4 cm) and adult(4–8 cm) individuals.

2.4. Substrate type

Substrate type (buried or unburied mat) was evaluated in eachmeadow. The mat is a three-dimensional net formed by overlappedvertical and horizontal rhizome axes of Posidonia oceanica (seeFig. 2). Depending on the local hydrodynamic conditions, thespaces between rhizomes can be filled with sediment to a greater or

oles and crevices; and b) mat buried with sediment where only the top rhizome layer is

Table 1Two-way ANOVA results for differences in the abundance sea urchin post-settlers incollectors between years (2003–2004) and among sites. Cochran’s test C¼ 0.36.

Paracentrotus lividus post-settlers

Source of variation ANOVAdf MS F p-level

Year¼ Y 1 0.62 0.016 0.9000Site¼ S 9 571.42 14.73 0.0000Y� S 9 186.75 4.81 0.0000

C¼ 0.36Transformation: None

P. Prado et al. / Estuarine, Coastal and Shelf Science 85 (2009) 472–478 475

to a lesser extent. When not filled with sediment, holes and crevicesamong intermingling rhizomes may provide a stable substrate forsettlement and refuge from predators. The presence of this type ofsubstrate was determined by inserting a centimetre-scaled stick(60 cm long by 2.5 cm width) into the rhizomes bed (Boudouresqueand Meinesz, 1982). Given that small-scale hydrodynamicprocesses also occur locally, we considered that an unburied matexisted when the meter stick could penetrate 30–40 cm in at least 7out of 10 haphazard assays.

2.5. Data analyses

Differences between Sites (fixed factor, 10 levels) and Years(fixed factor, 2 levels) in the number of post-settlers, one-yearcohort and adult and subadult individuals (>1 year old) wereinvestigated with a 2-way orthogonal ANOVA. For all the ANOVAs,data were first tested for normality (Chi-square) and homogeneityof variances (Cochran’s test) and transformed when necessary tosatisfy the ANOVA assumptions, as indicated in the results section.The existence of significant differences among site groups wasinvestigated by Student–Newman–Keuls (SNK) post hoc compari-sons. To investigate the early dynamics of the population wecompared the numbers of individuals within collectors at oneparticular year and the presence of one-year old cohort one yearafter by correlation analysis. This relationship was tested usingabundance of post-settlers in 2003 and that of juvenile recruitmentin 2004 (i.e. the one-year cohort was expected to result from post-settlement success during the previous year). Additionally, wechecked for correlations between successive size–age groups (i.e.the one-year old cohort and subadults and between subadults andadult densities) as well as between size–age classes older than oneyear (i.e. sizes 1.5–8 cm) and post-settlers.

3. Results

Although there was considerable local variability in abundanceof sea urchin post-settlers, individuals were observed in thedeployed collectors in all studied meadows and in both years (2003and 2004). The density of post-settlers ranged from 1.7� 0.4 percollector in Montroig to 25� 2.5 [S.E] in Giverola (Fig. 3). Differencesbetween years were not homogeneous across sites (significant

P. l

ivid

us

post

-set

tler

s (N

o. in

d./ c

olle

ctor

)

Site

Mr T F G M Mg Mj P J B0

5

10

15

20

25

30

3520032004

*

**

*

*

*

* *

*

* *

Fig. 3. Abundance of post-settlers at each study site in 2003 and 2004. Mr¼Montroig;T¼ Torredembarra; F¼ Fenals; G¼Giverola; M*¼Medes; Mg¼Montgo; Mj¼Mont-joi; P¼ Port Lligat; J¼ Jugadora and B*¼ Banyuls. In SNK, significant differencesbetween years at each site are indicated. Analysis was conducted on untransformeddata. Error bars are SE.

year� site interaction; see Table 1). The abundance of individualsdecreased from 2003 to 2004 at some sites (e.g. Montroig, Torre-dembarra and Montgo) and increased in others (e.g. Port Lligat,Jugadora and Banyuls).

These differences in urchin post-settlers were correlated withthe cohort one year later (r¼ 0.864, df¼ 9, P< 0.01, n¼ 10) as wellas to the abundance of urchin sizes older than one year (i.e.sizes> 1.5 cm; r¼ 0.736, df¼ 9, P< 0.05, n¼ 10). However, in 6 ofthe 10 studied meadows the one-year old cohort was completelyabsent from the meadow. The four meadows where one-year oldcohort individuals (between 0.5 and 1.5 cm diameter) were recor-ded (Torredembarra, Giverola, Fenals and Banyuls) consistentlyduring the two years (Fig. 4) were characterised by possessing anunburied rhizome mat, unlike the other meadows where the matstructure was buried under sand. These four sites alone, wereresponsible for the strong positive coupling between numbers ofpost-settlers and the number of individuals in the cohort one yearlater as indicated by increased correlation coefficient when siteswithout the one-year old cohort were removed (r¼ 0.964, df¼ 3,P< 0.05, n¼ 4). Even where present, the densities of juvenilerecruits did not exceed 4 ind m�2, suggesting that post-settlementmortality was very high (>99% of ind m�2). However, in the absenceof the mat structure, 100% of post-settlers in the meadow did notsurvive the first year.

Adult and subadult individuals of Paracentrotus lividus wererecorded in abundance in all seagrass meadows. The total numberof adult and subadult individuals (i.e. sizes from 1.5 to 8 cm) rangedfrom 14� 2.8 [SE] ind m�2 in Giverola to 1.7� 0.8 in Banyuls(Fig. 5a) and displayed significant differences among study sites but

Mr T F G M Mg Mj P J B0

2

4

6

8

10

P. l

ivid

us

(No.

ind

./ m

2 )

a

bbc

Site

One year old cohort: (0.5-1.5) cm

20032004

* *

Fig. 4. Abundance of the one-year old cohort (i.e. 0.5–1.5 cm individuals) at each studysite (data from 2003 and 2004 pooled, see text). Site labels as in Fig. 3. In SNK,significant differences in juvenile abundance among site groups are indicated withletters. Error bars are SE.

Mr T F G M Mg Mj P J B0

5

10

15

20

Subadults: (1.5-4) cm

P.

livi

dus

(No.

ind

. / m

2 )

b

Mr T F G M Mg Mj P J B0

5

10

15

20

P.

livid

us (

No.

ind

. / m

2 )

c

Site

Adults: (4-8) cm

Mr T F G M Mg Mj P J B0

5

10

15

20

ab

b

c c

a

de e e

d

P.

livi

dus

(No.

ind.

/ m

2 )

a

Adults and Subadults

* *

* *

* *

Fig. 5. Total abundance of adult and subadult Paracentrotus lividus (i.e. sizes 1.5–8 cm)at each study site (data from 2003 and 2004 pooled, see text). Site labels as in Fig. 3. InSNK significant differences in abundance of individuals among site groups are indi-cated with letters. Error bars are SE.

Table 2Two-way ANOVA results for differences in, a) juvenile recruits of Paracentrotus liv-idus (i.e. the one-year old cohort) and; b) adult and subadult populations (i.e.sizes> 1.5 cm; for further details see text) between the two study years and amongsites.

a) Juvenile recruits b) Adult and subadults

Source ofvariation

ANOVA

df MS F p-level MS F p-levelYear¼ Y 1 0.0646 1.8225 0.2100 25.81 0.976 0.3489Site¼ S 9 0.6269 2.6522 0.0164 935.35 22.682 0.0000Y� S 9 0.0355 0.1500 0.9976 90.41 0.725 0.6856

C¼ 0.339Transformation: OOx

C¼ 0.079Transformation: Ox

P. Prado et al. / Estuarine, Coastal and Shelf Science 85 (2009) 472–478476

not between years or among years and sites (Table 2). In particular,large adult sizes (i.e. >4 cm) were the dominant age class withinthe studied seagrass meadows (see Fig. 5b and c).

The one-year cohort showed to be associated to the subadultpopulation (i.e. sizes 1.5–4 cm; r¼ 0.885, df¼ 9, P< 0.001, n¼ 10)and the latter to adult individuals (i.e. >4 cm; r¼ 0.724, df¼ 9,P< 0.05, n¼ 10). Nonetheless, since the one-year old cohort wasonly observed at the four sites mentioned above they could notexplain the presence of adult and subadult individuals in mostmeadows.

4. Discussion

The processes that determine the survival of the sea urchinParacentrotus lividus between larval supply and early growth appearto be clearly dependent on the structural characteristics of theseagrass meadow. Being among the dominant herbivores of Pos-idonia oceanica meadows, this bottleneck in the early-life history ofP. lividus plays a vital role in determining meadow function. Verybroadly, for P. lividus populations, seagrass systems function eitherlike rocky systems or sandy substrates contingent largely onmeadow structure. Our results indicate that post-settlers’ supplywas not limiting in any of the studied meadows for the entire studyperiod of two years, and there were no large differences in larvalarrival between study sites and years, possibly because adult pop-ulations were largely stable. In contrast though, there were cleardifferences between meadows in post-arrival processes, mostly asfunction of the physical structure of the meadow. Specifically, inmeadows with an exposed rhizome mat, there was a strong rela-tionship between post-settlement rates and one-year old individ-uals, whereas, where the mat was absent, no juvenile recruits werefound. The presence of the mat in seagrass meadows appears tostrongly mediate early-life history mortality, although it is difficultwith the present study to precisely determine the mechanism of thismortality, or whether it acts most strongly at the recruitment stage,or is predominantly a post-recruitment process. What is clear is thatthis structural difference is significant enough to completely alterthe population dynamics of P. lividus in the meadow. In the absenceof this structure, urchins essentially do not recruit into juvenilepopulations, and the only satisfactory explanation for adult abun-dance is migration from neighbouring areas.

However, where bare mat exists, post-settlement success can bea relevant process in supplying individuals to local populations as therelationship between juvenile recruitment and post-settlers fromthe previous year is important. Although this evidence is weak due tothe low number of sites where the one-year old cohort was present(4 out of 10 study meadows), our results suggest that in contrast withother rocky benthic habitats where regular recruitment is the maindriver of sea urchin population structure (Rowley, 1989; Lopez et al.,1998) other factors are needed to account for the structure of seaurchin populations in Mediterranean seagrass meadows.

This limited distribution of one old year juveniles suggests thatlarge mortality occurs among early-life-history stages from otherwiseconspicuous availability of larval supply (as reflected by abundancesof post-settlers in collectors). As a benthic habitat, mat structure canplay multiple roles, providing at once, refuges from predation (i.e.crevice behaviour described in rocky substrates: Sala, 1997; McCla-nahan, 1999; Guidetti, 2004), a stable surface for settlement, or food,by enhancing the availability of rhizome algae (see Fig. 2). Theabundance of the labrid fish Coris julis, the main predator of juvenilesea urchins (Sala and Zabala, 1996; Sala, 1997), within the study

P. Prado et al. / Estuarine, Coastal and Shelf Science 85 (2009) 472–478 477

seagrass meadows was found to be low (Prado et al., unpubl data)compared to other sites where predation on small sizes (�1 cm) hasbeen shown to be a relevant process (Hereu et al., 2005). Yet, thepossible influence of other undetected benthic predators such aslarge gastropods, crustaceans and starfishes (Savy, 1987; Guidetti,2004) cannot be discarded. Early mortality may be also connected toturbulent hydrodynamic conditions and availability of food (e.g.Ebert, 1968; Himmelman, 1986; Turon et al., 1995). Spine breakageand test abrasion (Ebert, 1968) may occur during important sandmovements in exposed seagrass meadows (Patriquin, 1975) thusrising mortality rates on early life-stages when mat structure is notavailable. This hypothesis is also consistent with seawater flumeexperiments conducted by Eckman (1983) showing the existenceof negative effects of sediment particles on the rates of benthicinvertebrate recruitment near the stress boundary that causeserosion (i.e. death) of animals. Additionally, the presence of matstructure may also increase the availability of encrusting and endo-lithic rhizome algae, the food preferred by early stages of ca. 1 mmdiameter (Verlaque,1984), thus exerting a positive mediating effect inthe persistence of well-nourished individuals (Beddingfield andMcClinntock, 1998).

The presence of individuals older than one-year old was generaland independent of the existence of unburied mat, suggesting thatprocess other than annual inputs of recruitment in seagrass meadowsitself can contribute to the persistence of populations, among whichmigration from adjacent habitats appear to be the most likely, as hasbeen already proposed (Fernandez et al., 2001; Tomas et al., 2004;Ceccherelli et al., 2009). In fact, while well-nourished individualsoften display relatively limited foraging movements of ca. 0.5–5 m(Dance, 1987), substantial foraging trips occur under demographicexplosions (e.g. Rose et al., 1999; Peterson et al., 2002) and seem tosupport the likelihood of individual’s exchanges across habitats. Yet,the influence of landscape features in the migratory capacity of seaurchins is still poorly understood and requires further investigation.Given that individuals of Paracentrotus lividus do not normally moveacross unvegetated patches (Dance,1987), the degree of connectivitybetween distinctive types of habitats may also be a relevant medi-ating factor influencing the supply of individuals from neighbouringhard substrates (for a review see Fagan et al., 1999; Ries and Sisk,2004). During the study, densities of juvenile and adult individuals(0–4 ind m�2 and 2–20 ind m�2, respectively) were consistentlylower than in those reported commonly in rocky habitats (juveniles:20–40 ind m�2, Sala et al., 1998; adults: 10–80 ind m�2, Boudou-resque and Verlaque, 2001), suggesting that a spillover or mass effect(i.e. density-mediated migration; Shimida and Wilson, 1985) may bethe main source of individuals in the investigated seagrass beds.Preliminary measurements of habitat edge (degree of contactbetween seagrass meadows and rocky substrate) and populationnumbers in adjacent seagrass (ca. 3 m from the edge) indicatea strong relationship between these two variables, providing strongsupport for the role that migration played in driving urchin dynamicswithin study meadows (Prado, unpublished data). Other processessuch as predation may also have an additional impact on migrantsizes smaller than 3 cm (Sala and Zabala, 1996; Guidetti, 2004) andaccount for the dominance of large adult sizes (>4 cm) in most sea-grass meadows. Further research is needed to advance in ourunderstanding of the control of adult populations that includelandscape, habitat and predator–prey interactions, particularly whenthose species are living in the transition zone between habitats.

Taken together, these conclusions hint at a more general insightabout the control of herbivory in seagrass systems as a whole. If thepresence of rhizome structures is apparently so important in drivingherbivore populations in the meadow, it may help explain differencesseen in herbivore pressure between meadows of different plantcomposition. Short-lived or low structurally complex seagrass

species, however, are often highly preferred by herbivores (e.g. Trib-ble, 1981; Mariani and Alcoverro, 1999; Armitage and Fourqurean,2006). In fact, examples of urchin overgrazing of meadows dominatedby short-lived species (Halophila spp., Halodule spp., Cymodocea spp.,etc) are rare among the literature (reviewed by Eklof et al., 2008).Overgrazing events by the sea urchin Lytechinus variegatus have beenreported for somewhat longer living Syringodium spp (leaf age of ca.45 days; Duarte, 1991) in several occasions (Macia and Lirman, 1999;Rose et al., 1999; Peterson et al., 2002) but common populationnumbers and recruitment are still lower compared to neighbouringsites dominated by more structurally complex species of Thalassia(Beddingfield and McClintok, 2000; Prado, unpublished data). Theseshort-lived seagrass species never form complex rhizome structures,and potentially, sea urchins rarely successfully recruit to thesemeadows. Urchin herbivory in these meadows is likely to be confinedto migration events from other ecosystems and/or adjacent seagrasshabitats where urchins can successfully recruit. In contrast, mosturchin overgrazing events have been described from meadows oflong-lived species such as Thalassia testudinum, Thalassodendron cil-iatum, Posidonia oceanica and Posidonia sinuosa (Eklof et al., 2008). Inthe light of our present results, it is intriguing to note that all thesespecies, like many other long-lived species of seagrass, create denserhizome mats, making them ideal recruitment habitats for urchins,and potentially susceptible to occasional population explosions andovergrazing events.

As noted earlier, seagrass communities have structural affinitiesto both rocky systems as well as soft-sediment communities. Ourwork indicates that these structural properties have far-reachingconsequences for the early-life history of benthic species and theecosystem itself. The seagrass meadow is potentially an idealsystem to develop a unifying paradigm to understand the couplingbetween early-life history and benthic community structure. Whilewe do not yet fully understand all the underlying mechanisms, ourresults suggest that habitat structure will likely play a central role indefining this unified view.

Acknowledgements

This work was supported by a FI scholarship from the Depar-tament d’Universitats, Recerca i Societat de la Informacio (DURSI,Generalitat de Catalunya) and the CGL2009-12562, CGL2007-66771and CGL2009-12562 projects from the Spanish Ministry of Scienceand Technology. We are very grateful to S. Mariani for extensivefieldwork assistance and further advice during the elaboration ofthe manuscript. We would also like to thank R. Arthur for hishelpful comments and editing review that greatly improved thelatest version of the manuscript.

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