Vol. 514: 71–86, 2014 MARINE ECOLOGY PROGRESS SERIES Published November 6 doi: 10.3354/meps10961 Mar Ecol Prog Ser

Comparative study of sediment particle mixing in a meadow and a bare sediment mudflat

Guillaume Bernard1,*, Marie-Lise Delgard1, Olivier Maire1, Aurélie Ciutat2, Pascal Lecroart1, Bruno Deflandre1, Jean Claude Duchêne2, Antoine Grémare1

1UNIV. BORDEAUX, EPOC, UMR 5805, 33400 Talence, France 2CNRS, EPOC, UMR 5805, 33400 Talence, France

ABSTRACT: Seasonal changes in sediment particle mixing, surface sediment and seagrass charac teristics, and benthic infaunal composition were measured in Arcachon Bay (France), within both a well-developed Zostera noltei meadow and a bare sediment mudflat. Sediment par- N ticle mixing intensities (measured by the normal biodiffusion coefficient Db ) were obtained by fitting a continuous time random walk model to in situ measured vertical luminophore profiles. N 2 −1 Db values (mean ± SD) were between 2.99 ± 2.75 and 22.45 ± 43.73 cm yr within the bare mud- flat and between 0.39 ± 0.30 and 18.07 ± 18.14 cm2 yr−1 within the Zostera meadow. Spatiotempo- N ral changes in infauna and Db were lower within the Zostera meadow, which supports the buffer- ing effects of seagrass meadows on biological sedimentary processes. Within the Zostera meadow, root biomass declined during the survey, in correlation with increases in (1) the mean value and N the variability of Db and (2) the spatial variability of infaunal composition with a decrease in the N dominant Melinna palmata. At this station, similarity matrices of mean Db and abun- dances of a set of 3 infaunal species (including M. palmata) correlated significantly, which further supports the key role of this species in controlling sediment particle mixing through sediment stabilization. When considering the whole data set, the similarity matrices of the coefficients of N variation of Db and of the abundances of a set of 5 species (Abra segmentum, Glycera convoluta, Tubificoides benedii, Heteromastus filiformis, Ruditapes phillipinarum) correlated significantly, which supports the suspected role of these species in controlling sediment particle mixing.

KEY WORDS: Seagrass decline · Bioturbation · Infauna · Spatial heterogeneity · Community structure · Melinna palmata

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INTRODUCTION seca & Fisher 1986, Meadows et al. 2012) and oxy- genate bottom water and sediment, thereby shelter- Seagrass meadows occupy less than 0.2% of the ing abundant and highly diverse epi- and infauna world ocean but are among the most productive eco- (Boström & Bonsdorff 1997, Reise 2002). Seagrass systems worldwide (Duarte 2002). They store a large meadows are declining worldwide, and in temperate fraction of this production, making them responsible areas, major mechanisms responsible for this pheno - for about 15% of carbon storage in the world’s oceans menon include (1) eutrophication, which reduces (Duarte & Chiscano 1999). Seagrasses are ‘ecosystem light penetration and, combined with rising sea engineers,’ creating complex structures that enhance water temperature and sea level, inhibits seagrass the entrapment of suspended organic matter (Fon- growth; (2) wasting diseases inducing seagrass mor-

*Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 72 Mar Ecol Prog Ser 514: 71–86, 2014

tality; and to a lower extent (3) biological interactions the establishment of a more spatially heterogeneous such as herbivory or the introduction of species that infaunal community (Boström et al. 2006, Schückel et can physically affect seagrasses through bioturbation al. 2013), subsequently leading to a higher spatial (Orth et al. 2006). heterogeneity in sediment particle mixing intensity. Bioturbation is defined as ‘all transport processes Arcachon Bay, a macrotidal lagoon on the south- carried out by that directly or indirectly affect western coast of France, is colonized by a Zostera the sediment matrices’ (Kristensen et al. 2012, p. 285). noltei meadow, which used to cover most (70 out of It includes both sediment particle mixing and bio - 110 km2) of the intertidal flats (Auby & Labourg irrigation. Through bioturbation, benthic fauna 1996). In this bay, Z. noltei meadows protect inter- strongly affect the chemical, physical, and geotechni- tidal flats from sediment erosion (Ganthy et al. 2013). cal properties of marine sediments (Aller 1982, Lohrer They also structure macrozoobenthic communities et al. 2004). Sediment particle mixing mainly results (Blanchet et al. 2004), which present only limited sea- from locomotion, burrowing, defecation, and feeding sonal changes compared to adjacent bare sediment by benthic macrofauna (Meysman et al. 2006). It con- flats (Castel et al. 1989, Bachelet et al. 2000). The sur- trols the fate of sedimented particles and thereby af- face occupied by Z. noltei in Arcachon Bay has di - fects the remineralization (Kristensen 2000) and re- minished by a third between 1988 and 2008, and this suspension (Reise 2002) of particulate organic matter. decline has been more pronounced since 2005 (Plus Complex interactions occur between seagrasses et al. 2010), resulting in the replacement of large Z. and benthic infauna which most often result in nega- noltei meadows by bare mudflats. tive effects of bioturbating species on seagrass The present study focuses on sediment particle growth and colonization through increased (1) phys- mixing as a functional response of the whole infaunal ical alterations of shoots and rhizomes and (2) burial benthic community to both changes in its own struc- rates of seeds and seedlings (Philippart 1994, Dele- ture and in seagrass meadow characteristics. We fosse & Kristensen 2012, Suykerbuyk et al. 2012). aimed to (1) quantitatively assess seasonal changes Conversely, many studies have revealed a negative in vertical sediment particle mixing intensities within effect of the establishment of dense root/rhizome both a Z. noltei meadow and an adjacent bare sedi- networks on the density and burrowing activities of ment area, and (2) relate these intensities to infaunal large bioturbators (Hughes et al. 2000, Berkenbusch community composition and seagrass meadow dyna - et al. 2007). Nevertheless, these local negative inter- mics in order to (3) assess the impact of the decline of actions could result in an overall positive effect by intertidal seagrass meadows on biological sedimen- maintaining spatial heterogeneity and thereby en- tary processes. This was achieved through the com- hancing seedling recruitment (Townsend & Fonseca parisons, over a 1 yr survey, of sediment mixing 1998, Meadows et al. 2012). At the whole benthic intensity, sediment and seagrass population charac- infaunal community level, seagrass meadows clearly teristics, and macrozoobenthic community structures structure community patterns and stabilize sediment at 2 closely related intertidal stations: a well-devel- (Reise 2002). To our knowledge, vertical sediment oped Z. noltei meadow and a bare sediment mudflat. particle mixing intensity induced by the whole ben- thic infaunal community has never been quantita- tively assessed within seagrass meadows. However, MATERIALS AND METHODS studies focusing on individual bioturbator species have shown that both their densities and bioturbation Study area intensity tended to be higher in unvegetated areas than in seagrass meadows (Berkenbusch et al. 2007, The present study was conducted at a site named van Wesenbeeck et al. 2007). Overall, feedback ef- ‘Germanan,’ which is located in Arcachon Bay, fects (‘biomechanical warfare’) contribute to a dyna - France (44°42.73’ N, 1° 07.94’W; Fig. 1). This site con- mic equilibrium between seagrasses and infauna sisted of an intertidal flat characterized by the pres- (van Wesenbeeck et al. 2007). This suggests that sea- ence of 2 distinct habitats at the same hypsometric grass meadows already affected by another stressor level (ca. 2 m deep at high tide) only isolated by a will be more sensitive and threatened by biomechan- small channel. The first habitat corresponded to an ical disturbance induced by sediment particle mixing unvegetated mud flat (‘bare sediment’), whereas the (Orth et al. 2006, Berkenbusch et al. 2007, Meadows second one was colonized by a well-established et al. 2012). It also suggests that, at a local scale, sea- Zostera noltei meadow (‘Zostera meadow’). Based on grass degradation or disappearance would lead to measurements of currents performed at these sta- Bernard et al.: Comparative study of sediment particle mixing 73

dependence on experimental dura- tion of sediment particle mixing (Maire et al. 2007). These cores were frozen (−20°C) and sliced (0.5 cm thick sections down to 5 cm depth, 1 cm thick thereafter). After being freeze-dried, each slice was weighed and homo genized. Aliquots (2 g) of sediment were photo graphed under UV light using a digital camera fitted with a yellow filter. Luminophore pixels were counted after a binarization step (based on the Fig. 1. Study site (A) along the RGB level) for each image correspon- French Atlantic coast and (B) within ding to a single slice using image- Arcachon Bay analysis software (Maire et al. 2006). The relative concentrations of lumi no- tions, and despite slight differences between vege- phores in each slice were then used to compute corre- tated and bare sediment flats, Ganthy et al. (2013) sponding vertical depth profiles. concluded that both habitats were subject to similar Sediment particle mixing intensity was assessed hydrodynamic forcing. by fitting a continuous time random walk (CTRW) model (Meysman et al. 2008a) to luminophore verti- cal depth profiles. This model was chosen because it Field sampling and experiments proved more efficient than the biodiffusion model in describing the sediment particle mixing process over General strategy a short time scale (Maire et al. 2008, Meysman et al. 2010). The CTRW model assumes that sediment par- Experiments and samplings were performed sea- ticle mixing is controlled by 2 probability distribu- sonally between October 2010 and October 2011 tions. The jump-length distribution defines the ele- (5 campaigns during October 2010; February, April, mentary distance a particle travels during a given July, and October 2011) both at the bare sediment mixing event. The waiting-time distribution de- and the Zostera meadow stations. scribes the elementary time a particle waits in be - tween 2 consecutive mixing events. The jump-length and waiting-time distributions are most often as - Sediment particle mixing experiments sumed to follow a Poisson process and a Gaussian distribution, respectively (Meysman et al. 2008b, Sediment particle mixing was assessed through in 2010). For each replicate of each combination of Sea- situ incubations of sediment cores using lumino - son × Station × Experiment duration, a single normal N 2 −1 phores as sediment particle tracers (Mahaut & Graf biodiffusion coefficient (Db in cm yr ) value reflec - 1987) together with a mathematical model to fit ting sediment particle mixing intensity was obtained lumino phore vertical depth profiles (Maire et al. from fitted parameters according to Meysman et al. 2008). (2008b, 2010): σ2 One day prior to each experiment (i.e. each combi- D N = (1) b 2 nation of Station × Season), 6 cores (height = 30 cm, τc ∅ = 9.6 cm) were pushed ca. 25 cm into field sedi- where σ2 is the variance of the jump-length distribu- ments and left for 1 full tidal cycle. Cores were tion, and τc is the average of the waiting-time distri- placed within a ca. 3 m2 surface. At the beginning of bution. The fitting error (quality of the model adjust- the experiment, 6.9 g dry wt luminophores (green ment) was expressed via the root mean square error eco-trace®, environmental tracing systems, sediment (see Maire et al. 2007 for details). This was carried −3 median grain size, D50 = 35 μm, density = 2.5 g cm ) out using the TURBO package (‘functions for fitting were suspended in seawater and spread at the sedi- bioturbation models to tracer data’) within the open ment surface. Three cores were sampled after 7 and source R programming framework (v2.13.1., www. 14 d, respectively, in order to overcome the known R-project.org). 74 Mar Ecol Prog Ser 514: 71–86, 2014

For all Season × Station combinations, no signifi- Statistical analysis N cant differences in Db were detected between the 2 experimental durations (univariate permutational Univariate analyses ANOVA, PERMANOVA, p < 0.05). Consequently, N the 6 Db values measured for each combination Differences between stations and seasons in surface were considered as replicates for further statistical sediment POC and PON; total macrofaunal abun- analyses. dance, biomass, and species richness; infaunal abun- N dance, biomass, and species richness; and Db were assessed using univariate PERMANOVAs (Anderson Water and sediment characteristics 2001, McArdle & Anderson 2001) without data trans- formation. Euclidean distance was used, and the de- Water temperature and sediment characteristics sign consisted of 2 crossed factors, namely ‘Season’ (granulometry and organic carbon and nitrogen con- (fixed, 5 levels) and ‘Station’ (fixed, 2 levels). Because tent of the sediment surface) were assessed for each a strong decrease in the shoot density was observed Season × Station combination. The uppermost 1 cm within the Zostera meadow in October 2011, differ- N of sediment from 4 cores (∅ = 6 cm) were sampled for ences between stations and seasons in Db were first further analyses. One core was used for sediment tested in the same way (but with only 4 levels of the median grain size (D50) using a laser microgranulo - Season factor) on data obtained from October 2010 to N meter (MALVERN® Master Sizer S). For determina- July 2011. The seasonal dynamic in Db within the tion of surface sediment carbon (particulate organic Zostera meadow from October 2010 to October 2011 carbon, POC) and nitrogen (PON) content, the top was then analyzed using a single fixed factor (Season, 1 cm of the 3 other cores was sliced, freeze-dried, 5 levels) PERMANOVA. Pairwise tests were also per- homogenized, and later separately analyzed. Sam- formed to highlight differences among factor modali- ples for carbon analysis were decarbonated (HCl ties. The effects of factors on spatial variability (i.e. 0.3 N). Both POC and PON were assessed using a CN among-replicate variability) were tested using the auto-analyzer (Thermo Flash® EA112). PERMDISP procedure (Anderson 2006; same distance measure and same design as above).

Z. noltei population characteristics Infaunal community structure For each Season × Station combination, 6 cores (internal diameter = 9.6 cm) were sampled to assess Infaunal community structure was investigated Z. noltei population characteristics. Sediment was using non-metric multidimensional scaling (nMDS). sieved on 1 mm square mesh to retain leaves and This analysis was based on Bray-Curtis similarities roots. Shoots were first counted. Leaves and roots calculated on untransformed abundance and bio- were then separated before being dried (60°C for mass data. Differences in infaunal compositions be - 48 h) and weighed (precision: 0.1 mg). tween seasons and stations from October 2010 and July 2011, and among seasons within the Zostera meadow from October 2010 to October 2011, were Infauna tested using multivariate PERMANOVAs with Bray- Curtis similarities and using 1- and 2-way crossed For each Season × Station combination, 5 replicates designs described above, respectively. Correspon- of sediment were sampled using a 0.04 m2 square ding pairwise tests and dispersion analyses were per- corer (Castel et al. 1989) and sieved on a 1 mm formed as well (using Bray-Curtis similarities). For square mesh. Macrofauna was then fixed (4% both abundance and biomass data, species contribut- buffered formaldehyde) and colored with Rose Ben- ing most to differences were identified using the gal. Each organism was identified to the species SIMPER procedure (Clarke & Warwick 2001). level, counted, and its biomass assessed. Infaunal species were separated from other macrofauna, and −2 N their species richness, abundance (ind. m ), and bio- Linking Db and species distribution patterns mass (in ash-free dry weight, g AFDW m−2) were N assessed. Db values were linked to species distribution pat- terns using an inverse BIO-ENV procedure (ENV- Bernard et al.: Comparative study of sediment particle mixing 75

Luminophores (%) BIO; Clarke & Warwick 2001). The aim 0201030 40 50 60 70 80 90 100 02030401050 60 70 80 was to identify infaunal species poten- 0 0 tially responsible for spatiotemporal 2 2 changes (both in mean values and vari- N ability) in Db . Coefficients of variation 4 4 (CVs) were used as indicators of va- 6 riability (i.e. spatial hetero geneity) 6 RMS = 4.49 ± 8.91% RMS = 9.47 ± 7.02% N N patterns of both Db (varDb ) and spe- 8 8 cies abundance/biomass because they A B have proven more useful in comparing 10 10 variability among biological characteris- 02030401050 60 70 80 90 100 0105 90 95 100 0 0 tics than standard deviations (Fraterrigo & Rusak 2008, Hewitt & Thrush 2009). 2 2 ENV-BIO procedures were performed 4 separately on abundance and biomass 4 data and carried out on 3 distinct data - 6 6 sets. The first one corresponded to all RMS = 6.18 ± 8.52% RMS = 0.09 ± 0.11% 8 Season × Station combinations, whereas C 8 D the 2 others corresponded to only bare 10 10 sediment and Zostera meadow stations, 0201030 40 50 60 70 80 90 100 02010 70 80 90 100 respectively. For each dataset, only the 0 0 species that represented at least 3% of 2 2 the total abundance or 3% of the total biomass within at least 1 replicate were 4 4 selected. ENV-BIO analyses were run 6 6 separately to identify (1) species whose RMS = 3.97 ± 6.42% RMS = 0.71 ± 0.79% average abundance/biomass patterns Depth (cm) 8 8 correlated best (BEST procedure; Clar - E F N 10 10 ke & Warwick 2001) with Db patterns, and (2) species whose CVs of their 0203010 60 70 80 90 100 010 20304050 60 70 80 90 100 0 0 abundance/biomass patterns correlated N best with varDb patterns. Correlations 2 2 were assessed using Spearman coeffi- 4 4 cients, and corresponding significances were tested with permutation tests 6 6 involving 999 random permutations. All RMS = 3.52 ± 8.51% RMS = 5.21 ± 7.08% of the above described statistical analy- 8 G 8 H ses were performed using the PRIMER® 10 10 v6 package with the PERMANOVA+ 0203010 60 70 80 90 100 010 20304050 60 70 80 90 100 0 0 add-on software (Clarke & Warwick 2001, Anderson et al. 2008). 2 2

4 4

RESULTS 6 6 RMS = 0.75 ± 7.37% RMS = 12.63 ± 12.53% N 8 8 Db I J 10 10 Mean depth profiles of luminophores obtained in both bare sediment and the Fig. 2. Depth distribution (mean ± SD, n = 6) of luminophores, together Zostera meadow, together with corre- with corresponding model fits (mean ± SD in solid and dotted lines, re- spectively) and fitting error (root mean square expressed in percentage, sponding fitting errors of the model to mean ± SD, n = 6) obtained both within bare sediment (open symbols) these profiles, are shown in Fig. 2. Fit- and Zostera meadow (black symbols) during (A,B) October 2010, (C,D) ting errors were low, indicating a good February 2011, (E,F) April 2011, (G,H) July 2011, and (I,J) October 2011 76 Mar Ecol Prog Ser 514: 71–86, 2014

adjustment of the CTRW model to our data. Corre- 60 N Bare sediment sponding means and standard deviations of Db are 50 N Zostera meadow shown in Fig. 3. Mean Db was maximal during Octo- 2 −1 ber 2010 (22.45 ± 43.73 cm yr ) and minimal during 40

October 2011 (2.99 ± 2.75 cm2 yr−1) in bare sediment, ) –1 whereas it was maximal during October 2011 (18.07 yr 30 ± 18.14 cm2 yr−1) and minimal during February 2011 2 2 −1 (0.39 ± 0.30 cm yr ) in the Zostera meadow. Overall, (cm N 20 N b Db values were characterized by a high spatial vari- D ability as indicated by high standard deviations. Due to this variability, we detected no global effect, using 10 PERMANOVA main tests, of season and station fac- tors, and no significant interaction between these 2 0 Oct. 10 Feb. 11 Apr. 11 Jul. 11 Oct. 11 factors from October 2010 to July 2011. However, a Sampling season significant effect of station on the dispersion of data Fig. 3. Mean (± SD) particle mixing intensities (measured by through PERMDISP was detected, indicating that N N the normal biodiffusion coefficient Db ) recorded within Db was more spatially variable in bare sediment both bare sediment (open bars) and Zostera meadow (black during these seasons (Fig. 3). bars) during the 5 sampling seasons Within the Zostera meadow, the effect of Season on N Db was significant (1-way PERMANOVA, pseudo- N F = 3.8803, p(perm) = 0.0144). Db recorded in Feb- shown in Table 2. There was a significant decrease in ruary 2011 was significantly lower and less variable both shoot density and root biomass between Octo- than those recorded in October 2010, April 2011, and ber 2010 and October 2011 (Table 2). July 2011, and only significantly less variable than in N Ocotber 2011. Db was also significantly more vari- able during October 2011 than during the 4 other Benthic infaunal characteristics sampled seasons (Table 1). Occasionally, fewer tracers were found at the end Univariate parameters of the incubations within bare sediment than within the Zostera meadow. Means and standard deviations of species richness, abundance, and biomass of benthic infauna are shown in Table 2. Species richness only significantly Water, sediment, and Zostera population varied with Season (pseudo-F = 9.7705, p(perm) = characteristics 0.0001). It was minimal during July 2011 within both bare sediment and the Zostera meadow. Species Water temperature and main surface sediment richness was maximal during October 2011 within characteristics (D50, POC, PON) are listed in Table 2. bare sediment and during October 2010 within the Water temperature presented typical seasonal varia- Zostera meadow. tions, and differences in D50 were not well marked (Table 2). Both surface sediment POC and PON were Table 1. Seasonal dynamics of the normal biodiffusion co - minimal during April 2011 within bare sediment as N efficient (Db ) within a Zostera meadow: p-values obtained well as within the Zostera meadow. Maximal values by pairwise permutational ANOVAs between all possible of both surface sediment POC and PON contents seasons within the Zostera meadow. Values in bold indicate D were recorded during October 2011 within bare sed- seasons that significantly differ (p < 0.05), and indicates combinations that present significantly different dispersions iment and during July 2011 within the Zostera (PERMDISP analysis, p < 0.05) meadow. Both POC and PON were also significantly affected by the interactions between Season and Sta- October February April July tion (PERMANOVA main test, p < 0.05). POC and 2010 2011 2011 2011 PON were significantly higher within bare sediment than within the Zostera meadow only during October February 2011 0.002D D 2011 (Table 2). April 2011 0.193 0.012 July 2011 0.102 0.003D 0.662 Means and standard deviations of Zostera shoot October 2011 0.186D 0.053D 0.147D 0.134D densities, leaf biomasses, and root biomasses are Bernard et al.: Comparative study of sediment particle mixing 77

Infaunal abundance varied significantly with cd c a b c c Season × Station (pseudo-F = 5.3252, p(perm) =

ab 0.0020). Within bare sediment, infaunal abun- biomass) dance was significantly lower during July 2011 Zostera 11 ± 2 than during the 4 other sampling seasons 2.08 ± 0.07 0.23 ± 0.02 14.27 ± 9.31 3285 ± 1814 ht a b b (Table 2). Conversely, it was maximal during bc

c October 2010. This last value was significantly

00 6052 ± 1317 0 38.10 ± 7.28 54.55 ± 18.38 higher than the one recorded during October Bare 14 ± 2 2011 (Table 2). A similar trend toward a signifi- 0.29 ± 0.04 2595 ± 681 d by the same letter do not 2.68 ± 0.35 cantly lower infaunal abundance during October ab c a ac ab 2011 than during October 2010 was found within abc

b the Zostera meadow (Table 2). Infaunal abun- dances were always significantly higher in the 8 ± 2 Zostera Zostera meadow than in bare sediment, except 11.83 ± 5.81 5.47 ± 2.57 2.86 ± 0.47 6962 ± 755 0.31 ± 0.06 during October 2011 (Table 2). b b b c

b Infaunal biomass only significantly varied with

00 ± 5929 10029 0 40.27 ± 4.92 47.58 ± 8.04 Station (pseudo-F = 17.786, p(perm) = 0.0002). Bare 5 ± 2 Lowest biomasses were recorded during July 494 ± 350 2.63 ± 0.19 0.25 ± 0.01 1.98 ± 1.24 2011 within both bare sediment and the Zostera a indicate significant differences among stations for the given bd c ab b b meadow. Highest biomasses were recorded dur-

ab ing April 2011 and October 2010 within bare sed- bold iment and the Zostera meadow, respectively. 9 ± 3 Zostera Infaunal biomass was significantly higher within 1.03 ± 0.04 0.14 ± 0.02 15.47 ± 4.07 8175 ± 2803 the Zostera meadow than within bare sediment ab a a a

a during October 2010 and July and October 2011. 00 14362 ± 3902 0 22.14± 6.29 72.25 ± 18.57 Bare 10 ± 1 1.64 ± 0.31 0.17 ± 0.03

2895 ± 1298 Community structure (multivariate) a b bc a a b

ab The results of the nMDS suggested that the compositions of benthic infauna differed between 9 ± 3 Zostera bare sediment and the Zostera meadow (Fig. 4). 2.32 ± 0.47 0.17 ± 0.02 15.52 ± 15.57 8.54 ± 6.52 5440 ± 1463 This was confirmed by PERMANOVA and a a b ac

), and means ± SD of surface sediment organic contents (percent particulate organic carbon and nitrogen, PERMDISP results, which showed that from ac 50 October 2010 to July 2011, both the mean com- 00 12560 ± 2644 0 9.84 ± 1.89 95.69 ± 18.93 Bare

12 ± 2 position and the variability of benthic infaunal 6.12 ± 3.14 2490 ± 438 composition were significantly affected by Sea- a a a a son × Station interactions (pseudo-F = 6.4634,

a p(perm) = 0.0001 and significant PERMDISP). Overall, there were clearly stronger seasonal 12 ± 1 Zostera changes in benthic infaunal composition within 7960 ± 1455 16.82 ± 11.62 bare sediment than within the Zostera meadow a ab (Fig. 4, Table 3). An exception to this general pat- population characteristics (shoot density, leaf and root biomasses), and infaunal characteristics (species richness, abundance, population characteristics (shoot density, ac

October 2010 February 2011 April 2011 July 2011tern was October October 2011 2011, with (1) different benthic Bare meadow and bare sediment stations during 5 sampling seasons. Values in meadow and bare sediment stations during 5 sampling seasons. Values infaunal composition within bare sediment and sediment meadow sediment meadow sediment meadow sediment meadow sediment meadow Zostera 4.11 ± 3.50 5405 ± 1807 Zostera meadow, and also (2) a more variable benthic infaunal composition within the Zostera Zostera

) ) ) meadow than in October 2010 (Fig. 4, Table 4). significantly differ among the considered seasons (univariate PERMANOVA pairwise comparison, p < 0.05). AFDW: ash-free pairwisesignificantly differ dry among the considered comparison, p < 0.05). AFDW: weig seasons (univariate PERMANOVA −2 −2 −2

) Infaunal biomasses showed the same general ) −2

−2 pattern, but with less marked differences in mean compositions and especially in variability. (μm) 27.2 43.9 37.8 61.4 26.2 46.5 32.5 32.2 29.8 25.0

50 SIMPER analysis carried out on abundance (shoot m (g AFDW m (g AFDW m richness (no. of species) (ind. m (g AFDW m Infaunal abundance Leaf biomass 0 36.18 ± 7.84 % PONShoot density 0 – 10339 ± 987 – 0.19 ± 0.02 % POC – – 2.23 ± 0.61 Infaunal biomass Water temp. (°C)Water D 14.5 14.5 6 6 16.5 16.5 21.5 21.5 14.5 14.5 Root biomass Infaunal species 12 ± 3 0 123.10 ± 10.09 Table 2. Water temperature, 2. Water median sediment grain size (D Table measured within % POC and PON), sampling season (univariate permutational ANOVA, PERMANOVA pairwise a given station, values linke comparison, p < 0.05). Within PERMANOVA sampling season (univariate permutational ANOVA, data showed that Zostera meadow assemblages 78 Mar Ecol Prog Ser 514: 71–86, 2014

Fig. 4. Non-metric multi- dimensional scaling or- dination of infaunal as- semblage compositions. Data are based on non- transformed abundances

Table 3. Pairwise comparisons of average dissimilarity percentages among infaunal abundance assemblages given by SIM- PER analyses from October 2010 to July 2011. Values in bold indicate assemblages that significantly differ (permutational ANOVA pairwise tests, p < 0.05), and D indicates assemblages that present significantly different multivariate dispersions (PERMDISP analysis, p < 0.05)

October 2010 February 2011 April 2011 July 2011 Bare Zostera Bare Zostera Bare Zostera Bare sediment meadow sediment meadow sediment meadow sediment

October 2010 Bare sediment Zostera meadow 54.4 February 2011 Bare sediment 49.1 60.8 Zostera meadow 51.8 32.1 53.0 April 2011 Bare sediment 61.1 68.5 44.2 59.0 Zostera meadow 62.5 24.1 67.5 35.6 70.4 July 2011 Bare sediment 89.8 93.1D 77.0D 91.7D 76.8 94.5 Zostera meadow 61.0D 20.3 65.6D 33.6D 66.6D 20.9D 91.9D had an overall similarity of 61.9% mostly due to the chaetes M. palmata, H. filiformis, Aphelochaeta mar- Melinna palmata and Heteromastus fili- ioni, and Nephtys hombergii, the bivalve Abra seg- formis, whereas bare sediment assemblages had an mentum, and the oligochaete Tubificoides benedii. overall similarity of 44.0% mostly due to the poly- Within-station similarities changed with Season from 51.1% in October 2011 to 87.7% in July 2011 within the Zostera meadow, and from 50.7% in July 2011 to Table 4. Pairwise comparisons of average dissimilarity per- 70.8% in February 2011 within bare sediment. They centages among infaunal abundance assemblages given by SIMPER within a Zostera meadow. All assemblages signifi- were always higher within the Zostera meadow than cantly differed (permutational ANOVA pairwise tests, p < within the bare sediment, except in October 2011. 0.05), and all presented significantly different multivariate SIMPER analysis also showed that both between- dispersions (PERMDISP analysis, p < 0.05) station and seasonal differences in infaunal composi- tions were mostly driven by differences in the abun- October February April July dances of the 5 above-mentioned species (Table 5). 2010 2011 2011 2011 The 2 dominant polychaetes H. filiformis and M. pal- October 2011 57.6 47.2 62.9 62.5 mata contributed to all between-station dissimilari- ties because of their higher abundances within the Bernard et al.: Comparative study of sediment particle mixing 79 Zostera meadow stations Bare 40 ± 45 85 ± 78 25 ± 43 40 ± 76 105 ± 76 10 ± 22 250 ± 97 380 ± 159 100 ± 50 10 ± 22 505 ± 255 125 ± 88 125 ± 115 120 ± 54 Zostera Zostera meadow) letters indicate species that 10 and July 2011 (c/C), October 2010 y 2011 (h/H), April and October (i/I), Zostera Bare together with results of SIMPER analysis. Spe- 19 ± 38 206 ± 139 125 ± 122 181 ± 90 meadow assemblages. Letters in the Seasons SIMPER Zostera Zostera Bare 5 ± 11 35 ± 55 19 ± 24 156 ± 55 15 ± 22 0 775 ± 318 15 ± 14 Zostera Bare 10 ± 14 0 10 ± 22 0 0 0 20 ± 27 170 ± 132 100 ± 92 355 ± 276 80 ± 82 395 ± 355 310 ± 167 10 ± 14 30 ± 67 10 ± 22 56 ± 113 19 ± 24 during the given season 35 ± 22 Zostera indicate species that contributed to 90% of dissimilarity between bare sediment and 0 15 ± 22 15 ± 22 35 ± 65 0 ± 97 55 0 ± 13 6 5 ± 11 45 ± 27 005 ± 1135 ± 4245 ± 4520 ± 210000 ± 4520 ± 4245 ± 1135 ± 005 0 00000000015 ± 33 ± 00000000015 bold 5 ± 11 0 0 0 10 ± 13 0 0 0 20 ± 32 0 45 ± 62 160 ± 104 30 ± 33020 ± 320000025 ± 250 ± 320000025 ± 33020 ± 30 15 ± 14 60 ± 42 15 ± 22 40 ± 42 30 ± 21 10 ± 14 19 ± 24 13 ± 14 15 ± 22 40 ± 38 30 ± 41 15 ± 14 65 ± 14 40 ± 38 sediment meadow sediment meadow sediment meadow sediment meadow sediment meadow 175 ± 229 0 h-i ± 22 15 40 ± 52 5 ± 11 0 70 ± 84 20 ± 21 0 0 g-G-h-H-i-I-j-J f-F-g-G-h-H-i-I-j-J - f-F-g-G-h-H-i-I-j-J e -f- g-G- h-i-I-j-J G-H-i-j-J a-A-B-C-d-D-e-E-f-F- g-Ja-b-B-e-H-f-g-h-i-ja-b-c-d-g-i-j 0 ± 89 40 0 0 120 ± 82 0 0 ± 201 180 20 ± 45 110 ± 232 19 ± 38 0 0 ± 11 5 40 ± 55 0 15 ± 14 31 ± 63 e-g-i-j-J 25 ± 18 30 ± 41 60 ± 38 0 20 ± 21 5 ± 11 75 ± 35 0 a-A-b-B-c-C-d-D-e-E- 2000 ± 884 6115 ± 1661 1170 ± 434 3535 ± 928 1165 ± 624 6745 ± 2013 156 ± 52 6050 ± 805 1015 ± 477 1475 ± 1688 A-C-E-G-H e a-c-d-f-Jga-A-b-B-c-C-d-D-e-E- 405 ± 160 855 ± 368 425 ± 165 1065 ± 455 185 ± 76 ± 177 370 680 ± 705 65 ± 29 55 ± 27 0 0 80 ± 57 256 ± 149 190 ± 117 45 ± 27 830 ± 409 5 ± 11 50 ± 40 35 ± 29 6 ± 13 13 ± 14 0 35 ± 29 20 ± 27 70 ± 27 0 0 6 ± 13 0 0 a-A-b-B-c-C-d-D- 2310 ± 1827 460 ± 373 b-C-d-e-f-F-h-g- SeasonsSIMPER October 2010 Bare February 2011 April 2011 July 2011 2011 October indicate those that contributed to 90% of dissimilarity between overall bare sediment and bold Tubificoides benedii Tubificoides Notomastus latericeus Pseudopolydora pulchra Pygospio elegans Ruditapes philippinarum Streblospio shrubsolii Nephtys hombergii Nemertea Melinna palmata Mediomastus fragilis Cerastoderma edule Clymenura clypeata Galathowenia oculata Glycera convoluta diversicolor Heteromastus filiformis Ampelisca brevicornis Aphelochaeta marioni Abra segmentum cies names in Table 5. Abundance means ± SD of infaunal species that representedTable at least 3% of the total abundance in at least 1 replicate, column relate to a pairwise comparison of species between seasons: lowercase (within bare sediment) and uppercase (within contributed to 90% of dissimilarity between October 2010 and February 2011 (a/A), October 2010 and April (b/B), 20 October 2011 (d/D), February and April 2011 (e/E), February and July 2011 (f/F), February and October 2011 (g/G), April Jul and between July and October 2011 (j/J). Values in and between July October 2011 (j/J). Values 80 Mar Ecol Prog Ser 514: 71–86, 2014

Table 6. Best results of the ENV-BIO analysis within (A) the entire data set, (B) bare sediment, and (C) Zostera meadow. Text in N bold indicates significant results (p < 0.05), i.e. best correlations found. Db : normal biodiffusion coefficient

N N N N Db vs. abundance Db variability Db vs. biomass Db variability vs. abundance variability vs. biomass variability

(A) ρ (Spearman) 0.368 0.728 0.425 0.686 p 0.569 0.046 0.607 0.09 Species Mediomastus fragilis Abra segmentum; Abra segmentum; Heteromastus filiformis; Glycera convoluta; Diopatra biscayensis; Mediomastus fragilis; Heteromastus filiformis; Mediomastus fragilis Ruditapes phillipinarum; Tubificoides benedii; Streblospio shrubsolii; Ruditapes phillipinarum Tubificoides benedii (B) ρ (Spearman) 0.491 0.83 0.491 0.5 p 0.854 0.329 0.984 0.835 Species Abra segmentum; Melinna palmata; Cerastoderma edule; Streblospio shrubsolii; Mediomastus fragilis; Tubificoides benedii Glycera convoluta; Tubificoides benedii Nephtys hombergii Heteromastus filiformis; Nephtys hombergii; Pygospio elegans (C) ρ (Spearman) 0.964 0.842 0.879 0.503 p 0.024 0.187 0.448 0.855 Species Aphelochaeta marioni; Abra segmentum; Aphelochaeta marioni; Cerastoderma edule; Mediomastus fragilis; Cerastoderma edule Mediomastus fragilis Tubificoides benedii Melinna palmata

Zostera meadow than within bare sediment. These 2 significant results were found within bare sediment species also contributed to seasonal differences in (Table 6B). both bare sediment and the Zostera meadow, with lower abundances in July 2011 within bare sediment and a strong decrease of M. palmata in October 2011 DISCUSSION within the Zostera meadow (Table 5). N Sediment particle mixing intensity (Db )

N N Linking Db and infaunal species distributions The Db values obtained during the present study patterns (Fig. 3) are in the same order of magnitude as litera- ture data regarding sediment particle mixing intensi- The results of the ENV-BIO procedure are shown ties measured in coastal environments using a large N N in Table 6 for correlations between Db (varDb ) and variety of methods (Josefson et al. 2002, Gilbert et al. infaunal species compositions within the whole data 2003, Wheatcroft 2006, Duport et al. 2007, Teal et al. N set (Table 6A), bare sediment stations (Table 6B), and 2008). Db measured within bare sediment (Fig. 3) Zostera meadow stations (Table 6C). are largely consistent with Db reported in intertidal When considering the whole data set, the ENV-BIO mudflats, from 1.8 to 108 cm2 yr−1 (Clifton et al. 1995), procedure highlighted a significant correlation (ρ = from 4 to 5 cm2 yr−1 (Herman et al. 2001), and from 6 0.728, p = 0.046) between the similarity matrices to 52 cm2 yr−1 (Widdows et al. 2004). Measuring sed- N based on varDb , and the abundances of 5 species iment particle mixing through core incubation clear - (A. segmentum, Glycera convoluta, H. filiformis, ly limits the (hydrodynamical or biological) lateral T. be ne dii, and Ruditapes phillipinarum; Table 6A). movements of particles to a maximal length defined Another significant correlation (ρ = 0.964; p = 0.024) by the core diameter. Although the reduction of bio- was detected within the Zostera meadow between logically driven lateral transport was limited here N the similarity matrices based on Db and the abun- because of the small size of the present infauna (see dances of 3 species, namely A. marioni, Medio mastus below) compared to the diameter of the used cores, fragilis, and M. palmata (Table 6C). In contrast, no hydrodynamical lateral transport was clearly limited Bernard et al.: Comparative study of sediment particle mixing 81

by the use of cores projecting ca. 5 cm above the sed- of dense root/rhizome networks, which provide pro- iment surface. tection for many prey species (Summerson & Peter- N Overall, our Db measurements were characterized son 1984), and (2) the accumulation of organic matter by high among-replicate variability (Fig. 3). Previous through both enhanced sedimentation (Fonseca & studies have also shown high variability in vertical Fisher 1986, Wilkie et al. 2012) and the decay of plant luminophore profiles within replicated sediment materials (Castel et al. 1989, Rossi & Underwood cores during in situ sediment particle mixing experi- 2002). ments (Wheatcroft 2006, Duport et al. 2007, Gilbert et Species richness never differed between the al. 2007). This mostly explains why we failed to de - Zostera meadow and bare sediment (Table 2). The tect any significant effect of both Season and Station composition of infauna in the Zostera meadow was using PERMANOVAs. More generally, within-treat- characterized by high abundances of the deposit- ment variability reflects the degree of small-scale feeding polychaetes Melinna palmata, Heteromastus spatial heterogeneity in sediment particle mixing filiformis, and Aphelochaeta marioni and the oligo - processes, closely linked to those of infaunal species chaete Tubificoides benedii (Table 5), as already distribution and activities. reported (Bachelet et al. 2000, Blanchet et al. 2004, Do et al. 2013). Interestingly, these species were also present, albeit in lower abundances, in bare sedi- Overall comparison of the Zostera meadow and ment (Table 5). Differences between the Zostera bare sediment meadow and bare sediment thus mostly resulted from (1) higher abundances of M. palmata, H. fili- N Sediment particle mixing (Db ) formis, T. benedii and Abra segmentum, and (2) lower abundances of A. marioni within the Zostera N From October 2010 to July 2011, Db was signifi- meadow (Table 5). This suggests that the bare sedi- cantly less variable and tended to be lower within the ment infaunal community corresponds to an impov- Zostera meadow than within bare sediment (Fig. 3). erished Z. noltei meadow sub-community. A similar This suggests that sediment particle mixing was less pattern (i.e. higher infaunal abundance in a seagrass intense and particularly more spatially homogeneous meadow but similar species richness and composi- within the Zostera meadow, which is consistent with tion as within bare sediment) was reported by the consideration of seagrasses as sediment stabil- Fredriksen et al. (2010) along the Norwegian coast. izers (Orth 1977, Townsend & Fonseca 1998, Reise This was attributed to the fact that the corresponding 2002, Meadows et al. 2012) through the creation of Z. marina meadow and bare sediment stations were dense root/rhizome networks (Reise 2002). The pres- directly adjacent, which was also the case during the ence of seagrasses should result in lower sediment present study. Interestingly, this phenomenon has particle mixing due to (1) sediment compaction also been observed in tidal flats structured by (Hughes et al. 2000, Berkenbusch et al. 2007) and (2) other engineers such as tube-building polychaetes the exclusion and/or inhibition of the activity of large (Volkenborn et al. 2009). bioturbators (Berkenbusch et al. 2007, van Wesen- For all given Seasons except October 2011, the beeck et al. 2007). The fact that more particles compositions of infauna were also much more (spa- seemed to occasionally have been washed away tially) homogeneous within the Zostera meadow than within bare sediment tends to confirm this stabilizing within bare sediment, as indicated by (1) the higher effect, but is difficult to assess because it was not among-replicate Bray-Curtis similarity within the linked with any experimental factor. Zostera meadow than within bare sediment, and (2) the corresponding dispersion of replicates in the nMDS based on infaunal compositions (Fig. 4). A Infauna similar effect was suggested by Blanchet et al. (2004), who showed that benthic faunal compositions at sta- Infaunal compositions clearly differed between the tions with low above- and below-ground Zostera bio- Zostera meadow and bare sediment (Fig. 4). Similar mass were highly heterogeneous. Such differences in differences have already been observed both in variability within the Zostera meadow and bare sed- Arcachon Bay (Blanchet et al. 2004, Do et al. 2013) iment can be related to differences in spatial homo- and in other seagrass meadows (Boström & Bonsdorff geneity between the 2 habitats. This may refer to (1) 1997, Fredriksen et al. 2010). These differences re - food availability and (2) the occurrence of Z. noltei sult from several processes, including (1) the crea tion root/rhizome networks. Within the Zostera meadow, 82 Mar Ecol Prog Ser 514: 71–86, 2014

buried leaf debris and enhanced sedimentation pro- organic content of the sediment in this particular sea- vide an abundant and homogeneous food source for son (Table 2), which again is in good agreement with benthic infauna. Conversely, infaunal abundance the positive effect of food availability on sediment and composition within bare sediment are mostly particle mixing (Maire et al. 2006, 2007, Wheatcroft conditioned by the heterogeneous distribution of (1) 2006). spots of buried leaf debris and (2) deposition in pits/ Second, there was a clear decline in root biomass hollows. This hypothesis is supported by (1) the within the Zostera meadow (Table 2) between Octo- more variable surface sediment POC contents rec - ber 2010 and October 2011. The infaunal abundance orded within bare sediment than within the Zostera during October 2011 did not significantly differ with - meadow during the present study (except in July in the Zostera meadow and bare sediment (Table 2). 2011; Table 2) and (2) the higher variability in abun- Infaunal composition within the Zostera meadow was dance within bare sediment of the oligochaete T. also significantly more heterogeneous during Octo- benedii and the polychaete M. palmata (Table 5), ber 2011 than October 2010 (Fig. 4, Table 4). This which are associated with high concentrations of mainly resulted from a decrease in the polychaete M. sedimentary organics (Rossi & Underwood 2002). palmata between October 2010 and 2011, and to a Higher spatial heterogeneity within bare sediment lower extent from (1) a decrease in the opportunistic compared to the Zostera meadow may also result polychaete A. marioni and, (2) an increase in the from the sole effect of the distribution pattern of oligochaete T. benedii. Such enhanced abundances any spatial structures within the sediment column of T. benedii following a seagrass mortality event (hetero geneous distribution of buried debris versus have already been reported and attributed to organic homogeneous dense root/rhizome networks). Inert enrichment through the decay of buried plant mate- buried debris can enhance local abundance of oligo - rial (Rossi & Underwood 2002). Since the variability N chaetes (Rossi & Underwood 2002), and dense Zoste - in the composition of infauna and Db were higher in ra root/rhizome networks are known to provide shel- bare sediment than in the Zostera meadow, we ter from for small species (Summerson & attribute differences (both in absolute values and N Peterson 1984). According to Brenchley (1982), poly- variability) in infaunal composition and in Db rec - chaete tube mats, such as the dense mats created by orded in October 2011 to a degradation of the Zostera M. palmata at our study stations, induce similar and meadow and thus to a convergence to bare sediment additional structuring effects as Zostera root/rhizome conditions. Blanchet et al. (2004) reported a sig - networks. nificant effect of Z. noltei meadow on the composi- tion of benthic infauna in Arcachon Bay for shoot densities higher than ca. 6000 shoots m−2. This Spatio-temporal changes within the Zostera threshold value corresponded to the shoot density meadow and bare sediment recorded within the Zostera meadow during October 2011 (Table 2), supporting the occurrence of a posi- Within the Zostera meadow, all sampled Seasons tive effect of a decline of the Zostera meadow on sed- except October 2011 were characterized by (1) rela- iment particle mixing. In contrast, the facts that (1) N N N N tively low Db associated with low varDb and (2) both Db and varDb were low during October 2010 similar and low among-replicate variability in the and April and July 2011 and (2) infaunal composition composition of benthic infauna. Low variability in did not significantly differ among these 3 seasons infaunal composition should therefore result in low (Fig. 4, Tables 2 & 3) support the importance of this N variability in Db , thereby facilitating the assessment threshold and are therefore in accordance with the of the effect of environmental factors on sediment postulated role of Zostera meadows in buffering sea- particle mixing. Two lines of evidence suggest that sonal environmental changes (De Wit et al. 2001, this is indeed the case. Bachelet et al. 2000). N First, Db measured within the Zostera meadow The analysis of temporal changes in bare sediment during February 2011 was lower and significantly was more complex due to higher among-replicate N less variable than during all other sampled seasons variability both in Db and infaunal composition. The N (Fig. 3, Table 1), which is in good agreement with the low Db (with low associated variability, Fig. 3) re - negative effect of low temperature on sediment corded in April 2011 could nevertheless be related to pa rticle mixing (Grémare et al. 2004, Maire et al. a lower organic content of the sediment in this partic- N 2006, 2007). Along the same line, the low Db rec - ular season, as was also the case for the Zostera orded in April 2011 could be related to a lower meadow (Table 2). Bernard et al.: Comparative study of sediment particle mixing 83

N Control of sediment particle mixing intensity (Db ) surface to a few centimeters deep, leading to a sedi- by infaunal composition ment compaction effect, which is superimposed on the one induced by Zostera root/rhizome networks During the present study, we looked at a possible (Brenchley 1982). M. palmata is consequently con- effect of infaunal composition by using an ENV-BIO sidered to be a sediment stabilizer, which is in accor- procedure carried out through 12 modalities (3 data dance with the correlation between its low abun- N sets, 2 modalities corresponding to mean values and dance and the high Db measured during October CVs, and 2 modalities corresponding to the use of 2011. Given its often (very) high abundances, M. N abundance and biomass as the basis for the computa- palmata is a key species in contributing to low Db tion of similarity between infaunal compositions). within the Zostera meadow. No significant results were obtained when using As stated above, macrobenthic species abun- biomass as a basis for the computation of similarity in dance, species richness, and species composition infaunal compositions (Table 6). This was surprising, increase in variability when communities are subject since biological processes are more often cued by to increasing levels of disturbance (Warwick & biomass rather than by abundance (Rice et al. 1986, Clarke 1993, Hewitt & Thrush 2009). Variability in Wheatcroft et al. 1990). A possible explanation is that ecological patterns and processes is also more sensi- during the present study, sediment particle mixing tive to disturbance than their mean values (Frater- was mostly cued by small organisms (see below), rigo & Rusak 2008), explaining that a significant N exhibiting no major spatio-temporal changes in their correlation be tween Db and species abundances individual biomass. patterns was obtained for the whole data set when The only significant result when using mean abun- using the CV as an index of variability, whereas it dance values was obtained for the Zostera meadow was not the case when using mean values (Table 6). data set (Table 6), where the combined abundances The combined CV of A. segmentum, Glycera convo - of the 3 polychaetes A. marioni, M. palmata, and luta, H. filiformis, T. benedii, and Ruditapes philli- Mediomastus fragilis correlated best with spatio- pinarum correlated best with spatio-temporal chan - N N temporal changes in Db . Interestingly, the analysis ges in varDb . In most cases (i.e. 4 out of 5), changes of (1) temporal changes in the abundances of these in the abundances of these species together with organisms and (2) their sediment particle mixing their sediment particle mixing modes agreed with modes are coherent with their postulated role in the the available literature regarding their potential control of sediment particle mixing. role in the control of sediment particle mixing. The The cirratulid A. marioni was abundant when small deposit-feeding biodiffusor bivalve A. seg- mean sediment particle mixing intensity was high mentum reworks sediment down to a few centime- (i.e. during October 2010 and 2011) and was scarcer ters (Maire et al. 2006, 2007, Garcia 2010). The high during the other sampling seasons (Table 5), which is variability in its abundances recorded within bare not unexpected since this species is a downward con- sediment during October 2010 and July 2011 could veyor (Bouchet et al. 2009, Garcia 2010). Conversely, therefore partly explain the high corresponding N the capitellid M. fragilis was absent in October 2011 varDb . G. convoluta is a gallery-diffusor (Fran çois N N when mean Db was the highest (Table 5, Fig. 3), et al. 1997). It locally in creases Db by extending its which concurs with the fact that this species is a semi-permanent burrow while pros pecting the sedi- head-down upward conveyor (Quintana et al. 2007, ment (Garcia 2010). The capitellid polychaete H. fil- Garcia 2010). The ampharetid M. palmata was al - iformis and the oligo chaete T. bene dii are both ways the dominant species within Zostera. Its abun- upward conveyors (Quintana et al. 2007, Garcia N dance dramatically decreased in October 2011 when 2010), which therefore contribute to decrease Db N Db was the highest, which here again is consistent when present. with its sediment mixing mode. This gregarious (Oyenekan 1988) tube-building polychaete develops dense populations, particularly when sediment orga - CONCLUSIONS nic matter concentrations are high (Cacabelos et al. 2011) such as within Zostera meadows (Dauvin et al. Sediment particle mixing processes and infaunal 2007, Table 5). M. palmata constructs mucus-lined community structure were less intense and hetero- tubes covered with sediment particles (Fauchald & geneous and also less subject to seasonal variations Jumars 1979) forming dense tube mats that impact within the Zostera noltei meadow than within adja- sediment structure (Cacabelos et al. 2011) from the cent bare sediments. This tends to confirm the struc- 84 Mar Ecol Prog Ser 514: 71–86, 2014

turing and buffering effects of seagrass meadows on spatial variation of benthic invertebrates associated with biological sedimentary processes. Zostera marina (L.) beds in the northern . J Sea Res 37:153−166 The observed decline in meadow structure down to Boström C, Jackson EL, Simenstad CA (2006) Seagrass land- a structuring shoot-density threshold previously re - scapes and their effects on associated fauna: a review. ported in the literature was accompanied by in - Estuar Coast Shelf Sci 68: 383−403 creases in both the amplitude and the spatial vari- Bouchet VMP, Sauriau PG, Debenay JP, Mermillod-Blondin F, Schmidt S, Amiard JC, Dupas B (2009) Influence of the ability of sediment particle mixing intensity and mode of macrofauna-mediated bioturbation on the verti- changes in infaunal composition. cal distribution of living foraminifera: first insight from Showing a significant correlation between mean axial tomodensitometry. 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Editorial responsibility: Erik Kristensen, Submitted: September 20, 2013; Accepted: July 19, 2014 Odense, Denmark Proofs received from author(s): September 29, 2014