Zostera muelleri as a structuring agent of benthic communities in a large intertidal sandflat in New Zealand

Journal of Sea Research 65 (2011) 19–27

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Journal of Sea Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e a r e s

Zostera muelleri as a structuring agent of benthic communities in a large intertidal sandflat in New Zealand P.F. Battley a,⁎, D.S. Melville b, R. Schuckard c, P.F. Ballance d,1 a

Ecology Group, Massey University, Private Bag 11-222, Palmerston North 4442, New Zealand Dovedale, RD2, Wakefield, Nelson 7096, New Zealand 4351 Croisilles French Pass Road, RD3, French Pass 7193, New Zealand d Department of Geology, University of Auckland, Private Bag 92019, Auckland, New Zealand b c

a r t i c l e

i n f o

Article history: Received 6 July 2009 Received in revised form 25 June 2010 Accepted 25 June 2010 Available online 30 June 2010 Keywords: Zostera Muelleri Seagrass Intertidal Benthos New Zealand

a b s t r a c t The influence of seagrass beds on intertidal infaunal communities has been widely studied, with vegetated areas typically having higher diversity and abundances than adjacent bare sand patches. Such “seagrass– sand” comparisons, however, do not reflect the gradient of seagrass cover that may exist across large landscapes. We studied the large-scale distribution of intertidal macrozoobenthos over approximately 10,000 ha of sandflat on Farewell Spit, New Zealand. The benthic fauna, sediment composition and surface cover of the seagrass Zostera muelleri were studied at 192 sites evenly spaced along 30 transects covering the length of the 30 km spit. Most sites had Zostera present, generally at low densities (1–25% surface cover). Overall, invertebrate taxon diversity increased with Zostera cover, from a median of 4 taxa at sites with no Zostera to 23 at sites with high Zostera cover. Multivariate analyses of 37 frequently occurring taxa (of the 91 recognised) indicated that there was a site gradient of taxon abundances that reflected seagrass cover, with 23 taxa increasing as Zostera cover increased. Only three taxa tended to be found more where Zostera was scarce. Seventeen taxa were identified as being significant indicators of Zostera cover; in all cases abundances peaked with high Zostera scores. Cluster analysis revealed a number of major groupings. One group was associated with low Zostera; two were strongly associated with high Zostera cover; a fourth was probably distinguished by low tidal elevation and proximity to channels. On the Farewell Spit tidal flats, large-scale patterns of abundance seem to be largely structured by the presence and density of Zostera. © 2010 Elsevier B.V. All rights reserved.

1. Introduction Invertebrate assemblages on intertidal flats have been well documented to vary with the presence or absence of intertidal seagrasses such as Zostera spp (reviewed in for example Boström et al., 2006). Most studies, however, treat seagrass beds as a singular entity: samples are either within or outside a seagrass patch (e.g. Honkoop et al., 2008; van Houte-Howes et al., 2004). Seagrass may, however, occur across intertidal landscapes in varying densities ranging from sparse to complete cover. This variation may be partly captured by studies that measure seagrass biomass at sampling sites, but the number of sites (and hence number of patches included) is often limited and patches may be categorised as simply “high” or “low” biomass Zostera. Studies focussing on edge effects in invertebrate numbers or diversity will, for practical reasons, focus on well defined seagrass beds (e.g. Bologna and Heck, 2002; Tanner, 2005) and where seagrass beds have become fragmented or comprise very ⁎ Corresponding author. Tel.: +64 6 356 9099; fax: +64 6 350 5623. E-mail address: [email protected] (P.F. Battley). 1 Deceased, October 2009. 1385-1101/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2010.06.005

small patches (Hirst and Attrill, 2008), that approach may be appropriate. But not all Zostera beds are well defined and highdensity — large areas can be covered by quite ‘light’, otherwise continuous, seagrass cover. Analysing benthic invertebrate occurrence in relation to a gradient in seagrass densities or cover may give much stronger insights into the role that seagrass beds play in structuring intertidal communities than simply comparing high-density beds with bare sand. Such patchbare sand comparisons often find that dissimilarities in the benthic assemblages are due to a few common taxa; these analyses are often restricted to a small subset of the commoner taxa present (e.g. van Houte-Howes et al., 2004). This does not reveal much about how communities as a whole are influenced by the presence and density of seagrass. A key issue is whether the invertebrates associated with Zostera beds are part of a wider tidal flat community and respond favourably to the presence of Zostera, or whether there are specialist Zostera taxa found largely or exclusively in the seagrass. Conversely, whether there are species that truly favour non-vegetated habitats is seldom established, due in part to limited spatial sampling and limited sample sizes. In this study we present data from a study of the

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intertidal fauna of one of New Zealand's largest tidal flats, the c. 9500–10,000 ha sandflats of Farewell Spit, Northwest Nelson (Fig. 1). Farewell Spit extends approximately 30 km eastwards from the northernmost point of the South Island, and has tidal flats extending up to 6–7 km into Golden Bay on the spit's southern side. These tidal flats contain extensive beds of the seagrass Zostera muelleri (Jacobs et al., 2006) that are readily evident in satellite images (e.g. http://earthobservatory.nasa.gov/IOTD/view.php?id=5754); many areas, however, are devoid of vegetation and the total area of seagrass present has not been estimated. We used a transect survey across the flats to sample 192 regularly spaced sites across the entire flats. The coarse level of spatial resolution required to cover the entire tidal flats (transects every 1 km, samples every 500 m) cannot address finescale variability in seagrass and non-seagrass faunas. It does, however, enable us to determine whether large-scale patterns in macrozoobenthos abundance and diversity exist and whether these reflect differences in Zostera coverage. 2. Materials and methods The Farewell Spit Nature Reserve is situated at the northwest corner of the South Island of New Zealand (40°31′S, 172°45′E to 40°35′S 173°04′E). Extensive Z. muelleri beds occur on the sandflats on the southern side of the spit, especially at lower tidal elevations and adjacent to major channels. 2.1. Sample collection and processing Using a large team of volunteers, we sampled macrozoobenthos, sediments and Zostera at 192 sites in a grid survey over 10 days in March 2003 (Fig. 1) (see Battley et al., 2005). Transects were run in a north–south direction every km along the spit, with samples taken every 500 m. At each site, three 100 mm-diameter benthos cores were taken to a depth of 250 mm, sieved in the field through a 1 mm sieve (earlier work found that large amounts of sand were retained in a smaller sieve: Battley, 1996), stored in plastic bags and sorted that

Fig. 2. Zostera fresh (squeeze-dried) mass in relation to surface cover on the Farewell Spit tidal flats. Numbers above the boxes give the sample size per category.

night. All invertebrates were retained and stored in 5% formalin in seawater. They were later identified to the lowest practicable taxonomic level given the available equipment and expertise, which varied amongst groups. In general molluscs were identified to species or genus, polychaetes and small Crustacea to family. Some reference specimens of groups that we only coarsely identified were identified to higher levels (by Rod Asher, Cawthron Institute, New Zealand; see Table 1). For analyses, the three cores were combined. Any live Zostera (both above- and below-ground) taken with the benthos cores was sorted in the laboratory, squeeze-dried by hand and weighed to the nearest gram to give an index of Zostera biomass (there were only trivial amounts of algae or epiphytes on leaves). To estimate seagrass surface cover at each sampling station, percent cover of Zostera in a 50 cm × 50 cm quadrat was estimated with reference to a standard set of photographs, this being the

Fig. 1. Map and location of Farewell Spit, New Zealand. The thick line marks the approximate spring low-tide edge of the tidal flats (as judged from water cover during fieldwork) and the thin line shows the ‘dry’ land part of the spit. The compass arrow points north.

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recommended method of the SeagrassNet project (Short et al., 2001). A six-category scale was used, based on the Braun–Blanquet scale (Mueller-Dombois and Ellenberg, 1974). The 1–6 scale recorded in the field corresponded roughly with Zostera cover of 0%, 1–5%, 6–25%, 26–50%, 51–75%, and 75–100%. Observations were made at low tide, when the plants were lying flat. A 25 mm diameter×100 mm deep core was also taken for sediment grain size analysis. A wet-washing sieving method suitable for field conditions was devised (see Ballance et al., 2006 for details and discussion of accuracy). For analyses here, sediments have been grouped into three categories: fine sand (over 0.25 mm), medium sand (0.25–0.5 mm) and coarse sand (over 0.5 mm). As initial field-sieving suggested there was little variation between samples, and the processing proved to be relatively time-consuming (0.5 h per sample), not all samples were analysed at the time. On some transects only every second sample was analysed, so that 145 samples were analysed fully. The coarse sand fraction was subsequently measured on 42 of the remaining sites. 2.2. Analysis We used four main techniques to explore structure in the species and habitat data: Principal Components Analysis (PCA), Indicator Species Analysis, Cluster Analysis and Detrended Correspondence Analysis (DCA). All analyses were performed in PC-Ord, version 4.0 (McCune and Mefford, 1999). Analyses used two matrices. The first was the site × taxon matrix, in which the densities were log10(n + 1) transformed to reduce the scale of the differences in abundances. The second was a habitat matrix, which contained the Zostera surface cover score, Zostera mass, and the percent coarse sand in the substrate, for each sample site. Four taxa were split into subclasses for analysis: the bivalve Austrovenus stutchburyi into five size-classes (1–10 mm, 11–20 mm, 21–30 mm, 31–40 mm, and greater than 40 mm); the bivalve Paphies australis into two size-classes (1–13 mm, greater than 13 mm); the limpet Notoacmea helmsi into two subspecies (helmsi and scapha); and polychaetes of the family Maldanidae into ‘lower’ and ‘upper’ flat taxa (‘Maldanidae 1’ and ‘Maldanidae 2’ respectively: see Battley et al., 2005). Because many taxa were recorded rarely, the dataset was trimmed of uncommon taxa. Initially, all taxa that occurred in only one site were removed, as was the one site that had no animals present, and any sites that were lacking sediment data. The dataset was further reduced by removing taxa that totalled five individuals or fewer, and then those totalling 10 or fewer. Trial analyses were done with all three datasets; results were very similar

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for the three datasets, but the smallest one had fewer taxa that were seemingly significant mainly because of their rarity. Analyses discussed here were done on the dataset containing all taxa in which more than 10 individuals were recorded (187 sites and 45 taxa, including size classes). 3. Results 3.1. Seagrass cover and sediments Z. muelleri was present at 120 of the 192 sample sites on the tidal flats. Fifty-five sites had visual cover scores of 2 (equating to about 1– 5% cover), 33 a score of 3 (6–25% cover), 14 a score of 4 (26–50% cover), 13 a score of 5 (51–75% cover), and five with a score of 6 (over 76% cover). Surface seagrass cover was therefore mostly light, with few sites having dense beds. Squeeze-dried Zostera mass from the core samples was well correlated with the surface cover estimate (Fig. 2; ANOVA, F5,184 = 80.721, P b 0.0001, R2 = 0.685), with all but categories 5 and 6 having significantly different Zostera masses (Bonferroni post-hoc test). The areas of moderate to high seagrass biomass occurred across a 15 km stretch of the central tidal flats of the spit, particularly in the mid- to lower-level flats (Fig. 3). For the 189 sites for which we had coarse sand (particle size 0.5 mm and above) data, there was a tendency for few sites to have a substantial biomass of Zostera and also high coarse sand proportions (Fig. 4). As the data were largely concentrated along both zero axes, we categorised sites as high or low coarse sediment (cut-off of 5%) and high or low Zostera mass (cut-off of 10 g fresh mass). A contingency table analysis confirmed that frequencies differed significantly from expected, with the coarse sand/high Zostera combination occurring 43% less frequently than expected (Chi-square test, χ2 = 18.12, P b 0.001). More detailed sediment data (proportion of fine, medium, and coarse grains) are available for 144 sites. There was no consistent pattern of variation between Zostera biomass and these sediment categories. Only a negative relationship between coarse sediment (arcsine-transformed proportion) and Zostera biomass (log transformed) approached significance (F143 = 2.775, P = 0.098). 3.2. Macrozoobenthos In total, 12,839 individuals of 91 taxa were recorded in samples (Table 1), but six taxa dominated the samples numerically (the

Fig. 3. Fresh mass of Zostera present in the three core samples per site on the Farewell Spit tidal flats.

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P.F. Battley et al. / Journal of Sea Research 65 (2011) 19–27 Table 1 Taxon list for those analysed in detail, with abbreviations used in figures. Phylum

Class

Order/family

Genus/species

Abbreviation

Cnidaria

Anthozoa

Actinaria

Anthopleura aureoradiata Edwardsia tricolor

antho

Nemertea Annelida

Polychaeta

Capitellidae

Cirratulidae Glyceridae Maldanidae Nephtyidae

Fig. 4. Coarse sediment (N 0.5 mm) in relation to Zostera fresh mass. Point sizes are proportional to the number of sites with that combination of values (range 1–14 sites).

bivalves A. stutchburyi and P. australis, spionid polychaete worms, amphipods, the barnacle Elminius modestus and isopods). These 6 accounted for almost 70% of the individuals recorded. Most sites had 2–14 taxa, with the mode of 7 being close to the median of 8 taxa. The most diverse site had 31 taxa. Spatially, the most diverse sites were those of the large central flats, with the least diverse areas being those on the fairly narrow tidal flats along the inner part of the spit and those on outer areas on the extreme eastward end of the spit (Fig. 5). This partly reflects the extent of Zostera on the central flats (Fig. 3), as the number of species at a site increased with Zostera biomass (linear regression of number of taxa against (log + 1) Zostera fresh mass, F191 = 140.32, P b 0.001, R2 = 0.43; Fig. 6). In terms of surface cover scores, diversity increased from a median of 4.6 (average 4) species at score 1 to 23 (average 20.6) at score 6. 3.3. Community analyses 3.3.1. Principal Components Analysis A PCA was performed on the variance–covariance matrix. The first three axes generated explained 40.9% of the variance in the data (22.9% by axis 1, 10.9% by axis 2, and 8.4% by axis 3). Eigenvalues for the first four axes were larger than the corresponding broken-stick eigenvalues, indicating that they were, in effect, significant axes. Although plots of the sampling sites in relation to Axes 1–3 indicated there were no discrete groups of sites, there was nevertheless a gradient of sites that reflected the presence of Zostera. This is most obvious in the plot of Axes 1 and 3 (Fig. 7), where Zostera biomass increased from the right-hand side (no or little seagrass) to the lower left corner (high seagrass biomass) of the main plot (Zostera mass was strongly negatively correlated with axis 1: r = −0.650), while the proportion of coarse sand grains was positively correlated to it (r = 0.191; sites with a high coarse sand component sit towards the right-hand end; Fig. 8). The third axis provided more separation, based on the proportion of coarse sand grains but not on Zostera mass (percent coarse sand, r = −0.192; Zostera mass, r = −0.099). Neither variable was strongly correlated with Axis 2 (Zostera mass, r = −0.108; percent coarse sand, r = −0.019). The main species data can also be correlated to the PCA axes (Table 2), and suggest that the distribution of some taxa reflects differences in Zostera and sediments. Of the 23 taxa with correlations of 0.33 or above (an arbitrary cut-off point), all correlations with Axis 1 were negative. This indicates that abundances of a substantial proportion of the fauna increase with the amount of Zostera present. Three taxa had positive, though lower, correlations with Axis 1: Amalda at 0.227, Maldanidae 1 at 0.256, and Nephtyidae at 0.244.

Capitella capitata Heteromastus filiformis Hemipodus sp. Clymenella sp. Macroclymene sp. Aglaophamus sp. Nephtys sp.

Nereididae Orbiniidae Orbinia papillosa Oweniidae Owenia fusiformis Scalibregmatidae unidentified species Spionidae Aonides sp. Laonice sp. Polydora/ Boccardia sp. Prionospio sp. Scolecolepides benhami Syllidae Mollusca Bivalvia Lasaeidae Arthritica bifurca Mesodesmatidae Paphies australis Mytilidae Xenostrobus pulex Nuculidae Nucula hartvigiana Tellinidae Macomona liliana Veneridae Austrovenus stutchburyi Gastropoda Batillariidae Zeacumantus lutulensis Zeacumantus subcarinatus Buccinidae Cominella glandiformis Eatoniellidae Eatoniella cf. lambata Lottiidae Notoacmea helmsi scapha Notoacmea helmsi helmsi Olividae Amalda sp. Trochidae Diloma bicanaliculata Diloma zeylandica Micrelenchus tenebrosus Polyplacophora Chitonidae Chiton glaucus Arthropoda Maxillopoda Cirripedia, Elminius modestus Balanidae Malacostraca Amphipoda Caprellidae Cumacea Isopoda Isocladus spicatus Flabellifera Stomatopoda Squilla armata Squillidae Decapoda Halicarcinus cookii Ocypodidae Halicarcinus whitei Pinotheridae Macrophthalmus hirtipes Echinodermata Holothuroidea Apodida Trochidota dendyi Stelleroidea Ophiuroidea Patiriella regularis

edward nemert capitel

cirrat glycer maldan 1 maldan 2 nephty nereid orbin owenii scali spionid

syllid arthrit paphies xenos nucula macomo austro zeacum

cominel eaton notoscap notohelm amalda diloma

micrelen chiton elimin amphi caprel cumac flabel squilla halicar macrop

holoth patirel

There was a mix of positive and negative correlations with Axes 2 and 3. 3.3.2. Indicator Species Analysis This tests whether any taxa are particularly good indicators of certain environmental conditions. Environmental variables were

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Fig. 5. Map of species diversity along Farewell Spit.

summarised as categories, and each taxon's occurrence at sites in those categories summarised. First, for each taxon the relative abundance in each category was calculated (i.e. what percentage of the total individuals occurred in each category). Secondly, the relative frequency in each group was calculated (what percentage of the sites in each category the taxon occurred in). Finally an indicator value was calculated, which summarises the relative abundance and relative frequency for each taxon across the categories. This is the ‘percentage of perfect indication’; a value of 100 would mean that all individuals occurred in that category, and all sites in that category contained that taxon. A Monte-Carlo simulation was also run (1000 times) to calculate the probability that the indicator scores could occur by chance (Dufrene and Legendre, 1997). Zostera surface cover score (1–6) was used as the environmental grouping. Seventeen taxa were statistically significant indicators (Table 3). All of these taxa increased with Zostera score (Anthopleura and Austrovenus 21–30 mm and 31–40 mm peaking at score 5). This may partly be a consequence of the unequal number of sites in each category – with only five sites with score 6, it is easier for a taxon to be recorded at a high proportion of these than it is in a group with large

Fig. 6. Number of taxa per site in relation to biomass of Zostera. Point sizes are proportional to the number of sites with that combination of values (range 1–11 sites).

numbers of sites – but most of these taxa clearly increase in occurrence and abundance as the density of Zostera increases. The only taxon to be recorded only at the highest Zostera level was the crab Macrophthalmus. As only 11 individuals were recorded, it is hard to know whether this apparent restriction to high-density seagrass is real or whether they hide in seagrass over low tide. Other taxa that seem to be especially strongly associated with high seagrass levels (and were never recorded without some Zostera present) were the limpet N. helmsi scapha (a known Zostera associate), the tube-building polychaetes Oweniidae, the nutshell Nucula hartvigiana, and the stout polychaetes Scalibregmatidae. No taxa were significantly indicative of bare sand, though two infrequently recorded taxa were recorded primarily in areas with little seagrass. The olive snails (Amalda sp., 10 individuals at eight sites), and the skeleton shrimps Caprellidae (11 individuals at four sites), occurred only at sites with Zostera scores of 1–3. Their infrequent occurrence, however, makes them statistically poor indicators of those habitats.

Fig. 7. Correlations of the mass of Zostera (“zostmass”) to Axes 1 and 3 of a Principal Component Analysis. Points in the main plot are proportional to Zostera mass; their symbols represent visual surface cover scores.

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P.F. Battley et al. / Journal of Sea Research 65 (2011) 19–27 Table 3 Significant indicator taxa, based on an Indicator Species Analysis. Only taxa with P b 0.05 are shown. Zostera group with the highest score is given in bold. For reference, the number of sites and total number of individuals recorded is given.

Fig. 8. Correlations of the percent of coarse sediment (“sedi05”) to Axes 1 and 3 of a Principal Component Analysis. Points in the main plot are proportional to the coarse sand proportion; their symbols represent visual surface cover scores.

3.3.3. Cluster Analysis Cluster analysis defines groupings of species based on their similarity of occurrence. This was performed on the main data matrix, which had been transposed so that taxa, rather than sites, were the items being grouped. Alternative dendrograms were generated using the Sorensen (Bray–Curtis) distance measure, and a variety of linkage methods (Nearest Neighbour, Farthest Neighbour, Group Average, and Centroid). Of these methods, the Farthest Neighbour linkage gave the lowest chaining (sequential addition of small groups, so that few groups are evident; 24.8% c.f. 28.6–84.7%) and is shown here.

Table 2 Correlations between individual taxa and the first three Principal Component axes of a PCA. Only correlations of 0.33 and above are shown. Taxon Amphipoda Anthopleura Arthritica Austrovenus 0–10 mm Austrovenus 11–20 mm Austrovenus 21–30 mm Austrovenus 31–40 mm Capitellidae Cominella Cumacea Diloma Eatoniella Elminius Flabellifera Glyceridae Halicarcinus Macomona Micrelenchus Nereididae Notoacmea subsp. scapha Nucula Oweniidae Paphies 1–13 mm Paphies N13 mm Scalibregmatidae Spionidae Zeacumantus

Axis 1 − 0.382 − 0.344 − 0.779 − 0.773 − 0.584 − 0.686 − 0.588 − 0.372 − 0.422 − 0.362 − 0.364 − 0.369 − 0.556 − 0.450 − 0.553 − 0.449 − 0.375 − 0.644

− 0.470 − 0.659 − 0.691

Axis 2 0.436

0.396

Axis 3 0.453 − 0.420

− 0.467 − 0.522

0.505

0.453 0.669 − 0.335

− 0.395 0.337

− 0.398 0.384 − 0.351 − 0.357 0.528 0.610 − 0.473 0.331

Taxon

P

Anthopleura Austrovenus 1–10 mm Austrovenus 21–30 mm Austrovenus 31–40 mm Capitellidae Cominella Diloma Glyceridae Halicarcinus Macrophthalmus Micrelenchus Notoacmea subsp. scapha Nucula Oweniidae Scalibregmatidae Spionidae Syllidae

0.001 0.036 0.007 0.038 0.003 0.015 0.018 0.008 0.006 0.001 0.002 0.001 0.001 0.001 0.001 0.003 0.031

Indicator scores per Zostera category

N

N

1

2

3

4

5

6

Sites

Indiv

0 0 1 1 0 0 0 6 0 0 0 0 0 0 0 1 0

3 6 5 2 3 4 0 2 2 0 0 0 0 0 0 3 1

3 15 5 2 13 5 1 2 10 0 3 1 7 1 4 9 0

9 16 17 12 4 4 3 2 1 0 4 0 6 0 4 9 3

36 18 30 24 13 20 13 6 12 0 24 1 6 4 13 16 0

2 25 9 0 39 27 25 32 33 55 33 58 51 69 50 35 22

45 87 73 32 65 54 20 50 42 6 34 13 42 15 30 80 14

210 532 514 125 357 106 32 96 82 11 229 19 630 270 155 1737 34

The resulting dendrogram (Fig. 9) revealed a number of groupings. (1) A quartet that was well separated from all others: Amalda, Nephtyidae, Glyceridae, and the ‘seaward’ Maldanidae 1. (2) A tight grouping of Amphipoda, Flabellifera, Nereididae, and Cumacea. (3) A slightly less-tightly bunched group of small A. stutchburyi (1–20 mm), Zeacumantus, Cominella glandiformis, Halicarcinus, and Macomona liliana, with Capitellidae, Spionidae, and N. hartvigiana closely linked nearby, while Eatoniella, Micrelenchus tenebrosus and Scalibregmatidae branched off the same stem. (4) A group in the lower half of the plot of Anthopleura aureoradiata and A. stutchburyi 21–40 mm, P. australis, E. modestus, and Xenostrobus pulex. 3.3.4. Detrended Correspondence Analysis (DCA) The dendrogram groupings were then used as identifiers in a DCA of the taxon data (Figs. 10 and 11). The two plots show Axes 1 and 2, and 1 and 3, respectively. Most taxa occurred in the same general ‘axis space’. Some exceptions were clear, though: Amalda, Nephtyidae, and Maldanidae 1 were well separated, with Caprellidae, Notoacmea h. helmsi, Squilla armata, Edwardsia tricolor, Holothuroidea, P. australis, and A. stutchburyi over 40 mm also peripheral to the main grouping via either Axis 2 or 3. These seem to be the ‘sandy’ taxa. 4. Discussion The large-scale survey of intertidal macrozoobenthos across the Farewell Spit tidal flats confirmed that there was extensive, often quite light, cover of Zostera on the tidal flats, and that the diversity and abundance of invertebrates was strongly related to the presence and density of Zostera. This in itself is not surprising — many studies have found higher invertebrate numbers and diversity in seagrass beds than in bare sand (e.g. Boström et al., 2006, and references therein). However, here we show that the influence of Zostera on invertebrates was a general increase in diversity and abundance of many taxa across a wide gradient of Zostera coverage and biomass. Forty-three percent of the variance in diversity across sites was explained simply by the biomass of Zostera present. Up to half of the taxa analysed in detail increased in number as Zostera increased (Tables 2 and 3), and the DCA plots showed that most taxa grouped in the same general area of the plots (Figs. 10 and 11). It is notable that these relationships are evident despite our not having accounted for many other factors that

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Fig. 9. Cluster dendrogram of groupings of common taxa on the Farewell Spit tidal flats, generated with the Sorensen distance and Farthest Neighbour linkage method. For taxon abbreviations see Table 1.

must influence the invertebrate communities, such as tidal elevation, emersion time, sediment temperatures and current speeds (e.g. Legendre et al., 1997; Turner et al., 1999). Most of the taxa that the Indicator Species Analysis recorded as significant occurred in four or more Zostera classes. These taxa seem to be Zostera ‘generalists’, occurring wherever Zostera is present but

Fig. 10. Ordination plot of Axes 1 and 2 of a Detrended Correspondence Analysis of the species data, with groupings from the Cluster Analysis shown. Abbreviations take the first four to six letters of the family or genus. Notoscap and notohelm refer to Notoacmea helmsi scapha and N. h. helmsi respectively. Numbers refer to size-classes (Paphies, 0=1–10 mm, 10=N 10 mm; Austrovenus, 0=1–10 mm, 10=11–20 mm, 20=21–30 mm, 30=31–40 mm, 40+= over 40 mm).

being most abundant in dense beds. Four taxa could be considered to be Zostera specialists (and are well known for this association: Morton and Miller, 1973) and were never recorded without some seagrass present: the Zostera limpet N. helmsi scapha, the nutshell Nucula, and polychaetes of the family Oweniidae and Scalibregmatidae (note that the taxon found during the survey was not Travisia olens, which had earlier been found in sandy sediments in the outer spit: Battley, 1996; Battley et al., 2005). Some taxa evidently did respond to factors other than Zostera, and these showed some separation from other taxa in the DCA plots.

Fig. 11. Ordination plot of Axes 1 and 3 of a Detrended Correspondence Analysis of the species data, with groupings from the Cluster Analysis shown.

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Group 1 taxa (of the Cluster Analysis: Amalda, Nephtyidae, Glyceridae, and the seaward Maldanidae 1) were distinctive largely because of their limited distribution on the flats and their occurrence primarily where there was little seagrass. Amalda, Nephtyidae, and Maldanidae 1 were found only near the spring low-tide waterline. Although all were found at sites with eelgrass present (maximum Zostera scores of 3, 5, 5 and 6 respectively), all were commonest where eelgrass was absent. Group 4 taxa (the anemone A. aureoradiata and A. stutchburyi 21– 30 mm and 31–40 mm, P. australis, the barnacle E. modestus, and the mussel Xenostrobus pulex) showed high correlations with Axis 2 of the PCA, and all but Paphies also had moderate to strong negative correlations with Axis 1 (Xenostrobus, not in Table 2, was –0.271). The similarity in response of these taxa is not surprising: Anthopleura lives predominantly on large Austrovenus shells, and Xenostrobus and Elminius both require firm substrates for attachment. Xenostrobus was generally found in localised hummocky areas of firm eelgrass. They all were found low on the tidal flat or near to major tidal channels (see maps in Battley et al., 2005). For Austrovenus 21–40 mm, this distribution was a consequence of a seaward shift with age (Battley et al., 2005). In contrast, Paphies spat were concentrated in a few extremely high-density sites at the extreme lower edge of the tidal flats. Seven of the eight sites with densities of more than 1000 small Paphies per square metre had no eelgrass present, and all but one site had high coarse sand content (average 37.6%, range 13.3–73.3%; the remaining site had 0.4% coarse sand). Many spat were present in three adjacent sites along a sand island in a channel near the spring low-tide mark; next to this was a dense patch of larger Paphies, and the presence of large numbers of eleven-armed seastars (Coscinasterias calamaria) and eagle rays (Myliobatis tenuicaudatus) suggest that substantial populations of large Paphies were also present nearby (and subtidally). Hence, although Axis 2 of the PCA was not well explained by Zostera mass or coarse sediment, features of Group 4 taxa suggest that low tidal elevation and proximity to channels may be reflected in it. Cole et al. (2000) likewise recorded high densities of Paphies spat subtidally near a major channel in Tauranga Harbour, New Zealand. There are several limitations to this study. The taxonomic resolution employed in this study was low in this study. Polychaetes, for example, are grouped by family, despite the diversity in life histories and ecologies that are probably present between species. No seasonal variation is accounted for, even though this must be present and could affect the strength of the Zostera–invertebrate relationships (e.g. Rueda and Salas, 2008; Turner et al., 1999). Tidal elevation was not measured for the sampling sites. The tidal flats have several large channels crossing them, and seagrass beds tend to occur along the edge of these channels and their branches. The intervening flats (up to 1.5 km wide) are often much higher in elevation, subject to a strong drying predominantly westerly wind, and may become desiccated over a daytime low-tide period. We have no data on whether samples were taken from within discrete patches, and if so, where they were situated relative to the edge. Dense patches certainly do occur, cover very large areas of tidal flat, and are highly stable over time in their location and surface cover (P.F. Battley, pers. obs, from 1993 to present). But much of the seagrass on the Farewell Spit tidal flats occurs in quite low densities and is not readily identifiable as patches (pers. obs). It is also possible to find areas of degrading Zostera (established beds eroding back), apparently colonising Zostera (light surface cover but without extensive build-up of subsurface root or other organic matter), and areas that presumably have been had seagrass present in the past (bare sand but with large volumes of brown organic material present in the sediment). Such variation in ‘history’ is present but unrecognised in the data. Finally, the sediment analysis method used in this study was not sensitive enough to accurately divide the sediments up into standard

fine-scale components. Consequently, we restricted our analyses to the most reliably measured component, the proportion of coarse sand grains (0.5 mm and above). Seagrass beds tend to accumulate fine-particle sediments because of decreased water velocities, production of organic matter, and different infauna to unvegetated areas (Heiss et al., 2000; Little, 2000). A corollary of this is that there should be a lower proportion of coarse sand grains with higher seagrass levels, and sites with high Zostera biomass on Farewell Spit tended to have little coarse sediment (Fig. 4). Despite these limitations, clear relationships between the benthic fauna and the biotic (seagrass) and physical (sediment) environment were detected. These would likely have been stronger had we measured sediments more sensitively and analysed seagrass structure in detail. As it is, the proportion of coarse sand grains was weakly related to the PCA axes, indicating that the gradient in invertebrate composition to a degree reflected sediment structure, in addition to the stronger effects of Zostera content. Given the absence of obvious west–east gradients in macrozoobenthos distribution (see maps in Battley et al., 2005) and the strength of the relationships between macrozoobenthos and Zostera, the distribution of Zostera is arguably the dominant structuring agent in the intertidal benthic communities across the 10,000 ha tidal flats of the spit. The distribution of high-density seagrass beds is decidedly non-random, being found mainly adjacent to large channels over about a 16-km stretch of the spit, as well as at the base. The sediments of the tidal flats are thought to be composed largely of sand grains brought up the West Coast of the South Island by longshore movement and blown south onto the flats, augmented by coarse sand grains possibly brought into the system by floating trees (Ballance et al., 2006). Fine sand grains are recirculated by waves and currents, but coarse grains are irregularly distributed on the flats (being mostly on the western and far eastern flats) and are probably transported less around the flats. Those few taxa that were associated with low or absent Zostera were found in sandy sediments, on areas of firmer substrate, or near the extreme lower edge of the tidal flats. Indirectly (for “Zostera taxa”) or directly (for others), then, the large-scale distribution of invertebrates must also be related to the local geomorphology, particularly the tidal drainage patterns across the flats. Our study addressed the seagrass–macrozoobenthos relationship differently to most others, which focus on edge effects or patch sizes of seagrass beds (e.g. Bowden et al., 2001; Connolly, 1997) and tend to cover small spatial scales (Hirst and Attrill, 2008) or concentrate sampling effort within sites (Turner et al., 1999; van Houte-Howes et al., 2004). Our finding that over a large spatial scale communities responded across a wide gradient of Zostera covers suggests that the dichotomous Zostera-bare sand comparisons prevalent in the literature are biased representations of seagrass beds — the choice of welldemarcated patches to study restricts our knowledge to a subset of what is present on tidal flats.

Acknowledgements This project was funded by the Ministry of Fisheries Project ZBD2002-18 scheme to the Ornithological Society of New Zealand. Thanks to the New Zealand Department of Conservation (DOC) for permission to work within the Farewell Spit Scientific Reserve, and to DOC and the Maritime Safety Authority for logistical assistance. The survey relied on a large amount of volunteer labour, especially from the Nelson-Marlborough Institute of Technology's Trainee Ranger programme. Thanks to Rod Asher, Cawthron Institute, Nelson, New Zealand, for taxonomic assistance, Ian Henderson, Massey University, Palmerston North, New Zealand, for statistical advice, Matt Irwin from Massey University for map-making and two anonymous referees for helpful comments on the manuscript.

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