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Low-Canopy Seagrass Beds Still Provide Important Coastal Protection ServicesMarjolijn J. A. Christianen1", Jim van Beizen2, Peter M. J. Herman2, Marieke M. van Katwijk1, Leon P. M. Lamers3, Peter J. M. van Leent1, Tjeerd J. Bouma21 D epartm en t o f Environm ental Science, Faculty o f Science, Institu te fo r W ater and W etland Research, R adboud University N ijm egen, N ijm egen, The N etherlands, 2 Spatial Ecology D epartm ent, Royal N etherlands Institu te fo r Sea Research, Yerseke, T he N etherlands, 3 D epartm en t o f A quatic Ecology and Environm ental Biology, Faculty o f Science, Institu te fo r W ater and W etland Research, R adboud University N ijm egen, N ijm egen, T he N etherlands

AbstractOne of the m ost frequently quoted ecosystem services of seagrass m eadow s is their value for coastal protection. Many studies em phasize the role of above-ground shoots In a ttenuating waves, enhancing sedim entation and preventing erosion. This raises the question If short-leaved, low density (grazed) seagrass m eadow s with m ost of their biomass In below ground tissues can also stabilize sedim ents. We examined this by combining manipulative field experim ents and wave m easurem ents along a typical tropical reef flat w here green turtles Intensively graze upon the seagrass canopy. We experimentally m anipulated wave energy and grazing Intensity along a transect perpendicular to the beach, and com pared sedim ent bed level change betw een vegeta ted and experimentally created bare plots at three distances from the beach. Our experim ents show ed tha t /') even the short-leaved, low-blomass and heavily-grazed seagrass vegetation reduced wave- induced sedim ent erosion up to threefold, and ii) th a t erosion was a function of location along the vegetated reef flat. Where o ther studies stress the Im portance of the seagrass canopy for shoreline protection, our study on open, low-blomass and heavily grazed seagrass beds strongly suggests tha t below ground biomass also has a major effect on the Immobilization of sedim ent. These results Imply that, com pared to shallow unvegetated nearshore reef flats, the presence of a short, low-blomass seagrass m eadow maintains a higher bed level, a ttenuating waves before reaching the beach and hence lowering beach erosion rates. We propose tha t the sole use of aboveground biomass as a proxy for valuing coastal protection services should be reconsidered.

C ita tio n : C hristianen MJA, van Beizen J, H erm an PMJ, van Katwijk MM, Lamers LPM, e t al. (2013) Low-Canopy Seagrass Beds Still Provide Im portan t Coastal P ro tec tion Services. PLoS ONE 8(5): e62413. doi:10.1371/journal.pone.0062413

E d ito r: Richard K.F. U nsw orth, Sw ansea University, U nited Kingdom

R eceived D ecem ber 28, 2012; A c cep ted March 21, 2013; P u b lish ed May 28, 2013

C o p y rig h t: © 2013 Christianen e t al. This is an open-access article d istribu ted u n d er th e te rm s o f th e Creative C om m ons A ttribution License, w hich perm its unrestricted use, distribution , and reproduction in any m edium , provided th e original au th o r and source are credited .

F u n d in g : Research by MJAC is fu n d ed by th e N etherlands O rganization fo r Scientific Research - Science for Global D evelopm ent (NWO-WOTRO), g ran t W84-645 (appo in ted to MJAC). The w ork o f JvB and TJB is su p p o rted by th e THESEUS pro jec t on innovative techno log ies for safer European coasts in a chang ing clim ate, which is fu n d ed by th e European Union w ithin FP7-THEME 6 - Environm ent, including clim ate (contract no. 244104). The funders had no role in s tudy design , da ta collection and analysis, decision to publish, o r p repara tion o f th e m anuscript.

C o m p e tin g In te rests : The au tho rs have declared th a t no com peting in terests exist.

* E-mail: marjolijn.christianen@ gmail.com

Introduction

Biological structures located in coastal sub- and intertidal ecosystems can attenuate waves and as a result directly contribute to coastal p ro tection [1—3]. Both reef form ing taxa such as corals [4], mussels [5] and oysters [6] an d m acroalgae and m acrophytes such as kelp [7], seagrass [8], m angrove [9] and salt-m arsh vegetation [10—12], are well know n for their capacity to a ttenuate waves (see [1] for a review). As a consequence o f the reduction o f hydrodynam ic energy, m acrophyte vegetation typically accum u­lates sedim ent causing the w ater above the fore- o r nearshore to becom e shallower [14,15] (but: see [16,17]). Such sediment accretion also contributes to coastal protection, because wave a ttenuation increases with decreasing relative w ater dep th [18], T h e bathym etric w ave-attenuating effect o f vegetation-induced sedim ent accretion becom es especially im portan t for those vegetation types that have a relatively small direct wave a ttenuating effect via their aboveground biomass. This applies for exam ple to m eadows o f relatively short and highly flexible seagrass plants, w hich have lim ited w ave-attenuating capacity by their canopy com pared to stiffer vegetation [12]. If the structural

complexity o f such short vegetation is degraded further, e.g. due to a high grazing intensity, it becom es unclear to w hich extent they can still contribute to coastal protection.

A lthough sediment stabilization is often acknowledged as an im portan t ecosystem service o f seagrasses [19,20] and anecdotic evidence points at increased erosion after a seagrass m eadow has been lost (e.g. [13,21]), experim ental evidence for the exact m echanism s involved in sedim ent stabilization rem ains scarce. Seagrass m eadows have been shown to a ttenuate hydrodynam ic energy from currents [22,23] an d waves [12,24,25] and thereby trap suspended sedim ent and cause sedim ent accretion [14,26— 30]. H ow ever, w ith respect to sedim ent stabilization, m ost studies only refer to the effect o f the canopy in the reduction o f the hydrodynam ic forces that m ay reach the sedim ent and impose a bed shear stress (xb) to the sedim ent [31]. It has been suggested that below ground biomass o f rhizom es and roots can stabilize sediments by altering the erodability as the critical bed shear stress (x crit) is increased [31]. How ever, the relative im portance o f this m echanism is generally h a rd to study w ithout d isturbing the seagrass m eadow an d is, therefore, generally not addressed when studying the role o f these m acrophytes for coastal protection.

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Grazed Seagrass Meadows Still Protect Shorelines

In the tropics, seagrass m eadows typically occur on shallow reef flats in subtidal nearshore areas. In general, seagrass grow th is often controlled by tem perature, light availability and freshwater input bu t also by physical disturbance from waves and associated sedim ent m ovem ent [32,33]. T op-dow n effects can also drive seagrass growth by the foraging of large herbivores. R ecent studies in B erm uda, Ind ia and Indonesia reported intense grazing of green turtles on seagrasses [34-36], w ith harvesting rates up to 100% o f the daily leaf p roduction [36], As a consequence, these heavily grazed m eadows can have an extrem ely sparse cover with a low aboveground biom ass (± 10 g D W m _ ~) and short (< 5 cm) canopy, while m aintain ing a high below ground biom ass (± 5 0 g D W m ~) [36], This is in strong contrast to ungrazed m eadows, w here the aboveground biomass can be at least 10 times higher (e.g. biomass 118 g D W m ", canopy height ± 2 5 cm, described in [37]. Such grazing-induced alteration o f the canopy structure makes these m eadows interesting m odels to study the contribution o f below ground tissues to coastal defense.

In this study, we therefore question i) if intensively grazed seagrass m eadows with a very low-biomass canopy contribute to coastal pro tection by stabilizing the sedim ent against wave induced erosion, ii) if the im portance o f the sedim ent stabilizing effect o f seagrass changes along a cross-shore profile and iii) if the sediment stabilization by seagrass m eadows depends on the height o f the canopy. T o answer these questions, we experim entally m anipu­lated seagrass above- and below -ground cover, wave forcing and grazing intensity along a transect betw een the reef and the beach.

Methods

Field siteT h e study was conducted on a subtidal seagrass m eadow that

covers the fringing reef flat o f D eraw an Island (Fig. la), Indonesia (2"17’19’N, 118"14’53’E; see [36] for a m ap and m ore details). T h e seagrass m eadows are dom inated by Halodule uninervis (Ehrenberg, Ascherson) growing on carbonate sediment. T he carbonate substrate had a m edian grain size o f 591 ± 3 0 pm (d5Q, m ean ± SE, M alvern Laser Particle Sizer) and did no t differ significantly betw een stations. T h e canopy was o f low structural complexity as a result o f intensive grazing by green sea turtles (Chelonia mydas, 20.6 individuals ± 2 .2 h a *, [38]). T he hair-like leaves were short (< 5 cm), narrow (<1 nini) and th in (< 0 .2 nini). Shoot density was 3 3 3 5 ± 2 2 4 shoots m ~ and shoots only hadI.8 ± 0 .1 leaves pe r shoot [36], A boveground biomass wasI I .4 ± 0 .7 g D W m ~, an d below ground biomass 5 2 .0 ± 4 .5 g D W m _ ~. D uring the experim ent (D ecem ber 2011 -F eb ru ary 2012) spring tidal range was 2.9 m.

Survey of reef flat d ep th profileW e m apped a cross-shore dep th profile during slack low tide

from the beach starting at the low w ater line, over the reef flat, to the coral reef. W ater dep th along the profile was m easured by dragging a pressure logger (Sensus ultra, R eefnet Inc., O ntario , C anada) over the seabed at a fixed speed and sim ultaneous logging o f tim e and position using a han d held G PS (GPSM A P 60CSx, G arm in, O lathe, USA). W e averaged dep th readings (obtained with a frequency o f 1 Hz), using a sliding w indow over a 60 second interval, to reduce noise as a result o f w ater level fluctuations caused by waves and m ethodological errors. Finally, the cross-shore dep th profile is recalculated, based on the average burst reading by the wave gauges (see below ‘W ave m easure­m ents’), to get the average w ater dep th over time.

Wave m e asu rem en tsW e m easured hydrodynam ic forcing along the reef flat as a

result o f waves at four stations along the dep th profile given in Fig. 1, using self-logging pressure sensors (Wave gauge: OSSI-10- 003C, O cean Sensor Systems, C oral Springs, ETSA). T he instrum ents w ere placed a t a height o f 0.1 m above the bed. T h ree pressure sensors were p laced in the seagrass m eadow on the reef flat, and one sensor m easured the waves com ing in from the ocean over the reef crest a t increasing distance from the shore (stations ‘A ’ 45 m, ‘B’ 262 m, ‘Cl’ 513 m ,‘C ora l’ 712 m from the shore; see Fig. lb). W ave heights were m easured under a range o f offshore wave conditions and tidal elevations during the whole experim ent. A total o f 3140 recording bursts were collected a t a sam pling ra te o f 10 H z for 4 m inutes, every 20-m inutes. R ecordings com prise a total o f 209 hours o f wave m easurem ents (over a 44 day period, during ra iny season). D uring the deploym ent o f the wave gauges we caught a storm event (January 27, 2012, bursts 2879 to 3074), w ith peak w ind speeds reaching 19 m s 1 from the n o rth - northw est (±335"). W e calculated wave a ttenuation values relative to the waves com ing in a t the reef station (Coral) for each station a t the vegetated reef flat.

T h e obtained high frequency wave records were processed according to the following sequence: (1) pressure readings were converted to w ater level fluctuations (f;), (2) erroneous spikes, shifts and corrup ted bursts w ere rem oved from the data, (3) low- frequency tidal com ponents were rem oved from each burst by detrend ing the w ater level fluctuations using a polynom ial fit (4) from the detrended da ta significant wave heights (77,) (cf. e.g. [10,39]) were calculated (c.f. [40]):

H s = 4S tf-

( 1)

in w hich n is the num ber o f w ater level records in each burst (h = 2400). In addition, we corrected the calculated significant wave height for the a ttenuation of the wave pressure field with dep th and wave period [39]. From the detrended data, peak wave periods (77) were com puted based on zero-upcrossings [41],

^ H s(StationCoral) — H s(Stationx) ^QQ0/ H s (StationCoral) (2)

Bottom shear stress calculation (xb)Because the influence o f waves on the sediment bed strongly

depends on w ater depth, we calculated the w ave-related bottom shear stress (ty) over tim e (c.f. [42,43]):

T6 = 0.5p/2,5Í7,„ (3)

w here p is the w ater density, J2 .5 is the grain roughness friction factor calculated as 2.5d50. T h e wave height related orbital velocity at the bed (Uzt>) was estim ated using [44]:

u * = §ft \/gh (4 )

in w hich g is the gravitational acceleration, and h is the m ean w ater depth.

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Grazed Seagrass Meadows Still Protect Shorelines

p1*3

•

■ j f i | y Q 1

B

CLa>■aa)*->re5crea)E

0CoralSandS eagrass meadow

A: 0.87 mB: 1.26 m Coral:

1.65 mC: 1.48 m2

3

200 400 600 8004

Cross-shore distance (m)

Figure 1. Location and depth-profile of the experim ental site. (A) Aerial pho to of th e field site show ing th e locations of th e stations, the seagrass bed on th e reef flat in th e subtidal nearshore area (light blue), and th e coral drop off (transition to dark blue). See [36] for a m ore elaborate map. Waves are com ing predom inantly from th e north (right). (B) Depth profile a t increasing distance from th e beach. Location of stations are indicated including their m ean w ater depths. doi:10.1371/journal.pone.0062413.g001

Experiments to te s t and clarify sed im en t stabilization by seagrass

T o test effects o f seagrass presence on sedim ent stabilization, we com pared the changes in sedim ent level inside bare sedim ent gaps {i.e., 6 0 x 3 0 cm) to those inside a grazed seagrass m eadow at T 0 (n = 5). These m easurem ents were repeated at 3 stations, station A, B and C (for description see section “wave m easurem ents”) to test for possible effects o f different hydrodynam ic forcing along the reef flat. Gaps were created a t day 1 o f the experim ent by cutting the roots and rhizom es a round a fram e (60x30 cm) and rem oving all p lan t biomass w ithin this fram e. T he size o f the gaps was scaled to p lan t size and to dimensions o f turtle gaps.

T o test if waves were driving the erosion, we m anipu lated wave action entering the plots. W ave reduction was achieved by constructing bunkers o f sandbags (50 kg) w hich were piled up (W:H; 5:3 bags; ±3 :0 .75 m) in a sem i-circular shape to protect plots th at were situated 30 cm beh ind the bunker (Fig. 2c). W e com pared plots w ith and w ithout this wave reduction treatm ent, by m easuring 5 replicate plots a t three stations [n = 15, in total).

T o study the effect o f canopy leaf surface area on sedim ent stabilization we com pared sedim ent bed level in grazed plots with ungrazed plots th at were p rotected from turtle grazing for 2 m onths (Fig. 3a). M easurem ents for bo th treatm ents were replicated 5 times for each station. Plots com prised seagrass strips (60x15 cm) bo rdered by 2 bare sedim ent gaps (60x30 cm). W e used exclosures (1 .2x i . 2 x 0 .3 m , 5 cm m esh, Fig. 3a) th a t were designed to m axim ize light passage and m inim ize wave a ttenua­tion while excluding grazing of green turtles. Exclosures consisted

of fishing net a ttached to the tops of four steel poles th at were connected to ropes [36], and were inspected and cleaned trice a week. W ave attenuation by exclosures was m inim al as weight loss o f plaster sticks placed in and outside cages exposed to waves did not differ significantly. T h e seagrass canopy height was deter­m ined by m easuring lengths of 28 shoots from cores ( 0 23 cm) in grazed {n = 35) and ungrazed seagrass plots {n = 15).

T h e experim ental plots were selected a t a location with hom ogeneous seagrass substrate, w ith m inim um distances of 15 m betw een them . T he plots o f each station were located in a zone w ith m inim al differences in w ater depth (20 cm) and were placed at a line parallel to the shore. T rea tm en ts were random ly assigned to the plots.

Evaluation of sed im en t changeQ uantitative m easurem ents o f changes in bed level were

obtained using a sedim ent elevation b a r m ethod (SEB, e.g. [45,46]) a t the start and the end of the experim ent. A long m etal pin (150 cm) was inserted into the sedim ent as a reference a t the start o f the experim ent. A horizontal b a r o f 150 cm, a ttached to a second vertical p in was p laced on top o f the vertical reference pin at each m easurem ent until the horizontal b a r touched the reference pin and was level. T h e distance betw een the horizontal ba r and the bed surface was m easured at 9 points, at a diagonal line over each experim ental plot, during each m easurem ent. T he relative erosion during the experim ent was determ ined as the difference betw een T 0 and T end values. This m ethod was estim ated to have an accuracy o f 5 m m .

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c 0)Ea> — -

« E 20) O> I- -5** CL « ■- CL) -t-12: t/>Q . </5re (/) o) «C 05

§ % -10 « .so Zo Sc .2cuE(D (A

Station A 0

Station A

-15 -

-20 J

STORM

A

Iab

• W a v e sO R educed w aves by bunker

Ba

* * *

?a 4 WK AFTER B STORM*

Figure 2. The effect of seagrass presence on sediment stabilization. Sedim ent levels in unvegeta ted gaps com pared to levels in th e seagrass m eadow at T0 for tw o treatm ents: gaps exposed to w aves (black circles) or exposed to w aves reduced by wave bunkers (white circles). Seagrass stabilizes sedim ent bo th (A) directly after a storm and (B) 4 w eeks after a storm . The inlay show s th e se tup of a bunker to reduce w ave energy to seagrass and unvegetated gaps behind (left of) th e bunkers. Significant differences betw een stations are indicated by different letters, and betw een wave exposed and w ave-reduced plots by stars. doi:10.1371/journal.pone.0062413.g002

D uring the experim ents the sedim ent erosion in the gaps was also scored visually in a sem i-quantitative way (unchanged: ‘ — m inim al erosion: ‘± ’, m edium erosion: ‘+ ’, strong erosion '++'). These estimates were perform ed every 3r day during m ain te­nance checks o f all experim ental plots, and da ta were converted to sedim ent erosion rates using a conversion factor th at we derived from plots with bo th quantitative and sem i-quantitative m easure­m ents for the same day.

Evaluation of th e w ave reduction t rea tm e n tT o evaluate the wave reducing effect o f the sandbag bunkers,

w ithout having m ore wave loggers available, we com pared weight loss o f plaster sticks deployed inside and outside a bunker, at 3 locations along the reef flat. Relative weight loss by dissolution of the plaster is considered a proxy for hydrodynam ic forcing and integrates effects from tidal currents and waves [47,48], Sticks were placed at seagrass canopy level at the seagrass - gap border {n — 5 for each seagrass station) on a day with a large tidal difference, w ith sticks staying subm erged continuously. Plaster sticks were m olded using 20 m l o f m odel p laster attached to the

1= T3 w ai N

S3 5 2 » 05 q re = a) c in —

B

o ü?I sc >05 + 3E JS ‘■5 £05in

a>in

Station A 0 r

B C

2

Figure 3. Effect of canopy length on sediment stabilization. (A) Turtle exclosure. (B) Difference In sedim ent bed level betw een grazed and ungrazed seagrass strips for th e th ree stations (A, B, C) after 2 m onths pro tection by th e turtle exclosure. The difference In leaf length of th e canopy In turtle exclosures was a factor 2.6 longer (117.8±16.6 mm) than In grazed m eadow s (45.8±11.6 mm). dol:10.1371/journal.pone.0062413.g003

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Grazed Seagrass Meadows Still Protect Shorelines

plungers o f 60 ml syringes o f w hich tips had been cut off. T he sticks were weighted before and after 24 hours o f placem ent at the plots, after drying until constant weight.

S tatis tica l an a ly sesA one-way A N O V A was used to analyze differences in wave

height betw een stations. T w o way A N O V A ’s w ere used to analyze the effect o f station an d wave reduction on sedim ent erosion and curren t velocity, and to analyze the effect o f canopy length on sedim ent bed level. D a ta were log-transform ed w hen necessary to m eet assum ptions for the AN O V A s. T o evaluate possible differences betw een stations, we used T ukey H SD post hoc tests and for all hydrodynam ic param eters we used D u n n e tt’s post hoc tests for w hich we report T-values. Differences at T < 0 .0 5 were considered significant. R (version 2.15.1, Ju n e 2012) was used for all analyses. Results are p resented as m eans ± their standard errors, unless stated otherwise.

Results

H y drodynam ic forcingM ean significant wave heights (Hs) differed significantly betw een

stations along the reef flat, except for stations A and Cl (Table 1). D uring norm al conditions (periods w ithout storms), significant wave height from waves com ing in from the sea onto the reef (at station Coral) was on average 0.19 m with an average peak period o f 6.06 s (Table 1). D uring the storm in Jan u a ry , incom ing significant wave height increased to an average o f 0.40 m, w ith a peak value o f 0.78 m (incom ing waves a t the station Coral, see T able 1). Typically, wave height decreased from the coral, over the vegetated reef flat, tow ards the beach as is shown by the lower average significant wave heights a t stations Cl to A an d the average relative wave a ttenuation (% in T able 1). Because there was very little standing canopy biom ass to attenuate wave energy, this m ust be m ainly the consequence of the decreasing w ater dep th (Fig. lb). How ever, a t certain configurations o f wave height and w ater depth, wave height started to increase, w hich is a typical consequence of shoaling or wave breaking. This increase in wave height was observed a t all three stations on the reef flat (stations A, B an d Cl T able 1; shoaling is wave a ttenuation < 0), bu t a t the station nearest to the beach (A) it occurred m ost frequently. H ere, significant wave height could increase up to 1.8 fold (wave a ttenuation o f -88.2% in T able 1) relative to the incom ing wave height. Such increase is m ost p robably due to wave breaking.

T h e im pact o f waves on the reef-flat bed, estim ated as the bottom shear stress (BSS), showed roughly the same trend as the

significant wave heights. T h a t is, BSS differed significantly betw een stations (/>< 0 .0 5 , T able 1). T h e relative wave height (the significant wave height relative to the w ater depth, HJK) at station A was exceptionally high com pared to the o ther stations, w hich m eans th a t the wave height was no t yet accom m odated to the local w ater depth. As a consequence, wave friction with the seabed m ight cause wave breaking, resulting in high turbulence and (swash an d rip) currents at station A.

T h e wave bunker trea tm en t (Fig. 2c) was effective in that it significantly reduced weight loss from the plaster sticks, indicatiOng that hydrodynam ic energy was significantly lower beh ind the sandbags com pared to plots fully exposed to waves (_P = 0.01).

S e d im e n t s tab iliza tio nSeagrasses significantly reduced sedim ent erosion by waves,

although the degree o f the erosion reduction strongly depended on the location along the reef flat (Fig. 2a and b). After a period of 2 m onths, stations A an d Cl showed significant erosive bed level change in artificially created bare plots (F>< 0 .0 1 , Fig. 2b). At station B the sedim ent was no t significantly eroded, w hich is in line with the low er hydrodynam ic forcing m easured at this station (Table 1). After a storm event, the sediment erosion was higher (Fig. 2a). T h e effect o f waves on sedim ent erosion was largest at the nearshore, ‘swash’, zone a round station A an d close to the reef crest, ‘b reaker’, zone a round station CI. T his was dem onstrated by the m arkedly lower sedim ent bed level at station A, than that at station B (_P = 0.02) and station Cl (_P<0.001)(Fig. 2b). W hen exposed to waves, sedim ent level in the unvegetated gaps was eroded with, on average, 5.1 cm at station A, 6.3 cm at station Cl and only 1.3 cm at station B in 66 days (Fig. 2b). R ight after the storm event, the sedim ent erosion in wave exposed plots at station A was a factor 2.5 h igher (—13.0 vs. —5 .1 c m , T<0.001) com pared to erosion four weeks after the storm (Fig. 2a and b), bu t erosion was no t significantly higher for station B an d Cl after the storm.

Interestingly, the turtle exclosures revealed that grazed and ungrazed seagrass vegetation stabilize the sedim ent equally well. T h a t is, excluding grazing d id no t cause any difference in sediment bed level com pared to the grazed treatm ent (Fig. 3b), even though leaf length of the canopy in grazing exclosures was a factor 2.6 longer (117.8 ± 16.6 nini) than in grazed m eadows (45.8± 11.6 nini).

T h e wave bunker treatm ent was effective in that it significantly reduced weight loss from the plaster balls, indicating that hydrodynam ic energy was lower beh ind the sandbags com pared to plots fully exposed to waves (P= 0.01,).

Table 1. Summary of the m easured significant wave height (Hs), peak wave period (Tz) and bed shear stress (BSS) along a cross­shore seagrass profile (Fig. 1).

S tatio n Hs M ean Hs M a x im u m T zW a v e a tte n u a tio n (n o rm a l) BSS M ean BSS M a x im u m

n o rm al(m)

storm(m)

n o rm a l(m )

storm(m ) (s) m ín n o rm a l m ax n o rm a l (Pa) s to rm (Pa)

n o rm a l(Pa) s to rm (Pa)

A 0.15a ± 0 .09 0.23as ± 0 .19 0.52 0.68 5.13C± 1.96 -88% 18% 100% 0.046a" 0.034 0 .111abs*0.101 0.22 0.40

B 0.13b± 0 .07 0.24abs ± 0 .17 0.45 0.72 5.27b± 1 .84 -45% 30% 100% 0.026b"0.020 0.083bs 0.077 0.14 0.36

C 0.16a± 0.07 0.30cs ± 0 .17 0.48 0.74 5.27b± 1 .53 -28% 11% 100% 0.034c" 0.026 0.113bs*0.086 0.19 0.38

Coral 0.19C± 0 .07 0.40ds±0.12 0.49 0.78 6.06 a±1.41 0.044a*0.034 0.207cs*0.115 0.23 0.66

M eans w ith the ir s tanda rd deviations and m axim um significant w ave heigh ts are g iven for norm al cond itions (n = 2945, "norm al" = periods w ith o u t storm s) and during th e storm (n = 195). W ave a tten u a tio n values less th a n 0 indicate w ave shoaling. doi:10.1371 /journal.pone.0062413.t001

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Grazed Seagrass Meadows Still Protect Shorelines

Discussion

C oastal p ro tection and sediment stabilization by seagrass is often valued as an im portan t ecosystem service, w hich generally has been a ttribu ted to seagrass canopy properties [12,24,25,29,30], T his raises the question to w hich extent seagrass m eadows that have very little canopy and have m ost o f their biomass in below ground tissue can still contribute to coastal defense by stabilizing sediments. Present results convincingly dem onstrate that even intensively grazed subtidal seagrass m eadows, w ith a very short canopy, can still stabilize sediments effectively. This effect could be due to the rem ainder o f the canopy, bu t although the seagrass has a relatively high density (± 3000 shoots m ~), the leaves are extrem ely short and narrow . T h e aboveground biom ass is m inim al (± 1 0 g m _ ~) and the percentage cover o f the sedim ent is very low (< 2 5 %). It is m uch m ore likely, therefore, that the difference in erosion betw een grazed vegetation and b are soil under high wave conditions is due to the role p layed by the relatively high below ground biomass. Roots and rhizom es can stabilize the sediment by reducing its erodability. This is an im portan t novel addition to the findings o f previous studies, w hich identified the hydrodynam ic effect o f the canopy as the only essential m echanism in sedim ent stabilization [12,22].

T h e sedim ent stabilizing effect o f grazed seagrass, w hich can even occur by low-biomass m eadows, is expected to have im portan t implications for bo th coastal p ro tection an d ecosystem functioning. W ith respect to coastal protection, by reducing sedim ent erodability, seagrass fields m ain tain a h igher bed elevation that will help to attenuate waves. W e have schem atized these results in a conceptual d iagram (Fig. 4). T h e sediment anchoring effect by short, grazed seagrass vegetation, w hich has m ost o f its biom ass in roots and rhizom es (Fig. 4c), increases the critical bed shear stress that is needed for bed erosion. W e speculate that the presence o f a dense m at o f rhizom es and roots can have similar effects a t the sedim ent-w ater interface as described for o ther b io ta that reduce erosion, such as biofilms of m icrophytobenthos [31]. Seagrass cover causes the sedim ent level to rem ain h igher com pared to eroded unvegetated gaps. In our study this was up to 13 cm, in others 18 cm [49^(Zostera marina). O ver longer tim e scales, this difference in erodability o f the sedim ent is expected to seriously affect the form o f the cross-shore height profile. T he shallower profile o f seagrass beds, com pared to situations w ithout seagrass, m ay imply that m ore wave energy is absorbed before waves reach the coastal strip (Fig. 4b), because dissipation o f wave energy is a direct function o f w ater dep th [1]. As a result, it is expected th a t less wave energy can propagate over the nearshore towards the beach (Fig. 4b). It should however be detailed how this picture is influenced by wave breaking. In our study we observed wave breaking at the station closest to the shore, at least during p a rt o f the tidal cycle. Preferential zones o f wave breaking could locally experience higher bo ttom shear stress and smaller-scale variations in the profile could arise, bu t this effect will decrease with the vegetation-induced stabilization o f the sediment.

W ith respect to ecosystem functioning, arm oring o f the sedim ent can have profound implications for the subtidal seagrass com m unity by the reduction o f the am ount o f sedim ent that is resuspended. Biotic com m unities are know n to suffer from sedim ent m ovem ent, due to processes such as direct sm othering [50] o r burial [51], and abrasion o f tissues [52,53]. T he prevention o f erosion by seagrass as a foundation species [54](Flughes et al. 2009) is further critical for burrow ing fauna like shrimps that need stable sedim ent environm ents to reinforce their burrow s [55]. A rm oring by seagrasses m ay also indirectly pro tect the adjacent

ClQ)

Û

seagrass present

03

Distance along the foreshore

/ Roots/ rhizomes

coc/)o

crit -newLU

Bed shear stress

Figure 4. Conceptual model showing how erosion is decreased along a nearshore seagrass bed with a minimal canopy due to the combination of increased critical shear stress and resulting shallowness. Sedim ent erosion occurs w hen bed shear stress (force per unit area of the flow acting on the bed) exceeds a critical bed shear stress ( ib > icrit). (A) A typical d ep th grad ien t of a nearshore habitat w here w aves break above th e coral reef, are then further reduced in the surf zone and "sw ash" on to th e beach. Sedim ent stabilization by seagrass (green line) increases sed im ent bed levels com pared to a situation with seagrass (yellow). (B) As a consequence o f th e reduction of the w ater dep th by sedim ent stabilization of seagrass (green line), m ore wave energy is a tten u a ted while travelling tow ards the shore com pared to unvegeta ted areas (yellow), and less wave energy can reach the shore in th e surf zone. This highlights th e im portance of seagrass with respect to coastal defense. (C) In the grazed seagrass m eadow with sho rt leaves and low-biomass, th e low structural com plexity of shoo ts in com bination with the relative high root and rhizom e biom ass increases th e critical bed shear stress th a t is needed for erosion (icrit.).doi:10.1371/journal.pone.0062413.g004

coral reef com m unity that can suffer critically from sedim entation, by lowering sedim ent concentrations in the w ater colum n [4,56].

M ore generally, our results show the stabilizing effects o f m acrophytes even w hen canopies are strongly reduced. T his could also have im portan t im plications for o ther vegetated coastal ecosystems, such as salt m arshes and dunes, as well. In our system, grazing by turtles was the m ain driver m inim izing the canopy, bu t m any o ther processes can have a similar effect, e.g. seasonal changes in aboveground biomass, shedding o f leaves in au tum n and w inter o r degradation due to high turbidity, epiphyte cover or eutrophication. W e show, however, that these changes in canopy m orphology do no t autom atically m ean that seagrass beds have com pletely lost their coastal p ro tection value. A lthough the relative

seagrass present coral reef

Swash Surf zone Breaker

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Grazed Seagrass Meadows Still Protect Shorelines

value o f seagrasses for coastal p ro tection is strongly species dependent, w ith e.g. clim ax species (e.g. Enhalus acoroides) generally having a h igher value th an m ore ephem eral species (e.g. Halodule uninervis) that can be highly variable in biomass and cover [57], even presence o f low-canopy sea grass beds is significant. Therefore, w hen valuating seagrass habitats for coastal defense purposes, the idea o f using aboveground biomass as a proxy for wave a ttenuation should be reconsidered. Such approach could greatly underestim ate the coastal p ro tection service o f seagrass with canopies o f low structural complexity. Seemingly insignificant low-biomass seagrass m eadows that cover wide reef flats, m ay still offer significant coastal pro tection services, and should be valued as such. This ecosystem service is expected to becom e even m ore im portan t in the n ear future, as storm frequencies are expected to increase and natural coastal pro tection structures like reefs are under on-going degradation [58],

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