MARINE ECOLOGY PROGRESS SERIES Vol. 143: 187-200,1996 Published November 14 Mar Ecol Prog Ser

Filtering capacity of seagrass meadows and other habitats of Cockburn Sound, Western Australia

'CSIRO Marine Laboratories, PO Box 20. North Beach. Western Australia 6020, Australia 'Dept Environmental Management, Edith Cowan University. Joondalup, Western Australia 6027, Australia 3Dept Environmental Protection, Marine Impacts, Perth, Western Australia 6000, Australia

ABSTRACT: Macro-suspension-feeders (predominantly ascidians, , bivalves) and epifaunal suspension-feeders (hydroids, spirorbids, bryozoans, , amphipods) in Posidon~ameadows of Cockburn Sound, Western Australia, demonstrate a clear spatial distribution. Although this may be due to a number of environmental variables, this compares well with spatial patterns in lev- els, which are relatively high in Cockburn Sound (0.94 to 2.66 g chlorophyll a I-') and are generally highest at the southeastern boundary. Macro-suspension-feeder biomass was high in Posidonia mead- ows (28.6 to 41.3 g AFDW m-2at the southeastern boundary, 9.6 to 15.4 g AFDW m-' dt other sites) and generally lower in bare sed~ment(0.2 to 9.3 g AFDW m-2),although on bare sediment of the Southern Flats (a site in the southwest) the introduced spallanzan~~reaches considerable bio- mass (458.9 g AFDW m-'). Heterozostera (1.2 g AFDW m2)and Amphibolis meadows (2.3 g AFDW m-') were found at only 1 site each, but appear to support a low biomass of macro-suspension-feeders. Epifaunal suspension-feeders on Posidonia leaves (hydroids, bryozoans, spirorbids, barnacles, coro- phiid amphipods) reached a substantial biomass (2.3X 10b feedlng units m-' at the southeastern site; 0.6 to 0.7 x 106 units at other sites; 'feeding unlts' refers to ~ndividualpolyps, zooids, etc ). Amphibolis leaves supported similar numbers of epifaunal suspension-feeders (0.7 X 106 units m-') but Hetero- zostera supported far lower numbers (80 X 103 units m-'). Initial estimates indicate that the suspension- feeding assemblages associated with Posidonia and Amphibolis meadows in Cockburn Sound are potentially able to filter the overlying water column daily, and may partially control local densities of suspended organic matter. F~ltrationrates in unvegetated and Heterozostera habitats are orders of magnitude lower, so benthic invertebrate control of suspended particles In these habitats is unlikely. However, habitats dominated by the introduced polychaete S. spallanzanii, which has colonised large areas in Cockburn Sound where seagrass meadows have disappeared, have a filtering capacity of at least the same order of magnitude as that of the seagrass meadows they have replaced.

KEY WORDS Filtering capacity . Seagrass meadows . Posidonia sinuosa . Cockburn Sound . SW Australia . Suspension-feeders . Invertebrates . Sabella spallanzanii . Chlorophyll a levels

INTRODUCTION are not identical, although the groups largely overlap (e.g. Jerrgensen 1966). Hydroids, for instance, are not, Suspension-feeders are a large component of coastal strictly speaking, filter-feeders, but capture individual marine ecosystems, both in terms of biomass and num- particles directly from the water column. bers. The term 'suspension-feeder' refers to organisms A recent survey of Port Phillip Bay, near Melbourne, that feed opportunistically on particles suspended in the Australia, estimated that suspension-feeders com- water; 'filter-feeders' refers to organisms that gather food prised half of the benthic macro-invertebrate biomass, through filtering of the water column. These concepts and processed a volume of water equivalent to the Bay in about 16.5 d (Wilson et al. 1993). They were also 'E-mail: [email protected] estimated to ingest 15% of all organic matter ingested "Present address: CALM-Marine Conservation Branch, Fre- by benthic macro-invertebrates, but because they mantle, Western Australia 6160, Australia have a greater assimilation efficiency than deposit-

0 lnter-Research 1996 Resale of full article not permitted Mar Ecol Prog Ser 143: 187-200. 1996

feeders, may account for 42% of the total assimilation sites were chosen because they are widely dispersed of organic material by Port Phillip Bay benthic macro- along the rim of the Sound (Fig l),and because of the invertebrates (Wilson et al. 1993). close proximity of Sites 1, 2, 4 and 5 to sample sites With such a capacity for assimilating organic ma- used by the Western Australian Department of Envi- terial, suspension-feeders - when abundant - must ronmental Protection for monitoring recent chloro- have an important impact on phytoplankton communi- phyll a (chl a) levels. These largely unpublished chl a ties. Cloern (1982), who showed that suspension-feed- data, collected during summer (December to March) ing bivalves in south San Francisco Bay (USA) filtered between 1990/91 and 1993/94, were used to determine a volume equivalent to that of the Bay at least once the distribution of phytoplankton in Cockburn Sound, daily, suggested that grazing by benthos is the primary and describe the food availability to suspension-feed- mechanism controlling phytoplankton biomass in sum- ers within the Sound. Itshould, however, be noted that mer and autumn. Since the depth at which seagrasses other particulate organic material such as resuspended grow is largely determined by light, and phytoplank- organic material, including phytoplankton and other ton affect light penetration (e.g. Dennison & Alberte detritus, may form a large food component to suspen- 1982, Fitzpatrick & Kirkman 1995), a relationship sion-feeders (e.g. Stuart et al. 1982, Seiderer & Newel1 between the densities of phytoplankton, suspension- 1985, Judge et al. 1993). The present study did not feeders and seagrass is likely. attempt to determine the contribution of other sus- Cockburn Sound, a coastal embayment near Perth, pended organic materials to the spatial distribution of Western Australia (see Fig. l), has suffered greatly suspension-feeders in Cockburn Sound. Cary & Masini from the effects of eutrophication: 80 to 90% of its (1995) indicated that the chl a distribution in Cockburn 4000 ha of seagrass meadows rimming the Sound is Sound is similar in winter and summer. estimated to have declined (Cambridge 1979, Simpson Chl a concentrations were determined spectro- et al. 1993). Although seagrass now occupies only 10Y0 photometrically by the trichromatic method (Jeffrey & of the area of Cockburn Sound, its communities are Humphrey 1975). Approximately weekly data for sur- considered to provide an important habitat for a range face, middle and bottom waters were available for all of organisms (Chittleborough 1970, Wilson et al. 1978). sites except Site 3 (Fig. 1) for the 4 summers from High nutrient inputs to Cockburn Sound have been 1990/91 to 1993/94. Mean concentrations were deter- implicated in the loss of large areas of seagrass beds (Cambridge & McComb 1986). Excessive growth of phytoplankton has increased light attenuation, there- by causing stress to seagrass (e.g. Cambridge & McComb 1986), which is compounded by the exces- sive growth of epiphytes on the seagrass (Cambridge & McComb 1986, Silberstein et al. 1986). As seagrass beds may be an important habitat for invertebrates, including suspension-feeders (Chittleborough 1970, Wilson et al. 1978), a decline in the beds may also mean loss of habitat and a consequent decrease of invertebrate biomass. The aim of the present study is to quantify the sus- pension-feeder component of seagrass meadows in Cockburn Sound, determine spatial patterns in bio- mass and composition, and relate these pat- terns to - largely unpublished - chlorophyll a levels in the water column. Furthermore, the filtering capac- ity of these communities is estimated.

MATERIALS AND METHODS

Sampling method. Five sites with both Posidonia sinuosaCambridge et Kuo meadows and unvegetated ('bare' sediment) were between Fig, 1. Sampling sites within Cockburn Sound, Western *us- and 8 September 1994 in shallow waters of Cockburn tralia. Site 1: Woodman Point; Site 2: Luscombe Bay; Slte 3: Sound, Western Australia (32" 15' S, 115" 45' E).These Buchanan Bay; Site 4: Southern Flats; Site 5: Kwinana Lemmens et al.: Filtering capacity of seagrass meadows 189

mined by averaging the concentrations at the 3 water tions for parametric testing were violated (as tested by depths (+0.061-19 I-'). a Cochran's test), data were log(1+X) transformed Because the seagrasses Amphibolis antarctica before analysis (Fowler & Cohen 1990).All values are (Labill.) Sonder et Aschers. and Heterozostera tasman- expressed in means * SE. ica (Martens ex. Aschers.) only occurred at Luscombe Patterns in mean chl a values were analysed by a 1- Bay and Woodman Point respectively, they could only way ANOVA and a Tukey test (Fowler & Cohen 1990). be sampled at these sites. Sabella spallanzanii, an Observations were compared with spatial patterns in introduced polychaete suspension-feeder discovered suspension-feeders. in Cockburn Sound during the present study, was sam- Estimated clearance rates. The clearance rate (the pled at the Southern Flats only. The study component volume of water cleared of suspended particles per for suspension-feeders occurred during winter (Sep- unit of time) is equal to the filtration rate (thevolume of tember). water transported through the filters of the feeding At each site, 3 replicate samples of suspension-feed- organ per unit of time) when particles are so large that ers were collected by means of SCUBA, using a 0.25 m2 they cannot pass the pores of the filter (e.g. Jlargensen quadrate, randomly placed in the respective habitats. 1966). All macro-suspension-feeders (ascidians, sponges, Estimates of the clearance rates of suspension- crinoids, bivalves, bryozoans, etc.) were collected from feeding communities were obtained by combining the quadrate. In the laboratory the samples were their mean biomass densities with clearance rates as sieved over a 2 mm sieve and stored at --20°C. reported in the literature, although it is recognised that Macro-suspension-feeders were sorted to such values are dependent on a range of variables (see and, where possible, species level. Each item was 'Discussion'). An average water temperature of 20°C dried to constant weight at -80°C and ashed for 4 h at was used for these calculations. Cockburn Sound has a -550°C to determine ash free dry weight (AFDW). mean winter temperature of 17"C, and 22°C in summer A smaller quadrate (0.04m2) was used to sample the (e.g. Pearce 1986). epifaunal suspension-feeder component on seagrass Filtration rates of a number of ascidians are available leaves, as well as the infaunal and epibenthic com- within the literature (e.g. Holmes 1973, Fiala-Medioni ponents. All leaf and rhizome material, as well as 1974, Randl~v& Riisgard 1979, Robbins 1983, Klumpp substrate down to where the roots reached, was col- 1984, Petersen & RiisgArd 1992) and range between lected within this quadrate and later separated into leaf, 10.2 and 26.0 1 g-' AFDW d-' for Pyura stolonifera rhizome and epiphyte components. The dry weight of (Klumpp 1984) to 145.7 1 g-' AFDW d-' for Microcos- each was determined to provide a measure of habitat mus sabatieri (Fiala-Medioni 1974).We applied clear- density. A sub-sample of -10 leaves was used to estimate ance rates of Petersen & Riisgard (1992), based on the epifaunal suspension-feeder component.Its density Ciona intestjnalis from European waters: was then related to a 0.04 m2 seagrass surface area F,,, = 118 DW0.68+ 1.21(T- 15) through the dry weight ratio of sample and sub-sample. Infaunal and epibenthic suspension-feeders were col- where F,,,,, is the maximum filtration rate in m1 min-' lected by sieving the substrate over a 2 mm sieve. ind.-l, DW is dry weight in g and T is temperature. An Epifaunal suspension-feeders on seagrass leaves ascidian clearance rate of 96 1 g-' AFDW d-' was ap- (hydroids, bryozoans, spirorbids, barnacles, amphi- plied for ascidians in Cockburn Sound (mean ascidian pods, etc.) were counted under a dissecting micro- DW: 15 g ind.-l; AFDW: 75 % of DW). Initial estimates scope and identified to species level where possible. of the F,,, of some small ascidians (AFDW: 0.18 g for Spirorbids, barnacles and bryozoans were measured Polycarpa nipicans, 0.27 g for Pyura australia, 0.39 g with a graticule. Of the amphipods, their tubular hous- for Polycarpa clavata, 0.51 g for Polycarpa viridis) ings were counted, after ascertaining that the majority which dominate in the seagrass meadows are between of tubes were occupied. Of the colonial organisms 30 and 120 1 g-' AFDW d-' (Lemmens et al. 1996). (hydroids, bryozoans),the number of polyps and zooids However, further measurements (Petersen & Lemmens (n) was used as a measure of density. The weight of unpubl. data) demonstrate that their F,,,,, may be closer epifaunal suspension-feeders on seagrass leaves was to those of Ciona intestinalis, while clearance rates per not estimated. unit of total AFDW of larger ascidians (e.g. Herdmania Data analysis. A nested experimental design was fol- mornus, Phallusia obesa), which dominate on soft bot- lowed (habitats within sites). Spatial patterns in macro- tom substrate, may be substantially lower (25-30 1 g-' and epifaunal suspension-feeders were analysed with AFDW d-l), largely due to their relatively heavy theca. a balanced hierarchical ANOVA (Minitab Inc. 1993)on Clapin (1996) recently determined the filtering each of the phyla as well as on the total of all filter- capacity of Sabella spallanzanii under laboratory con- feeders. Where data were heterogeneous and assump- ditions and found that its filtration rate increases with 190 Mar Ecol Prog Ser 143: 187-200, 1996

temperature from 1.7 1 h-' g-' DWbodvat 17°C to almost 277.1 1 g-' AFDW d-l, when using an AFDW/DW ratio 4 1 h-' g-' DW,,,.,,., at 22°C (dry welghts expressed as of 2 (see Riisgird et al. 1993). We applied a clearance weight of organisms, after removal from their tubes). rate of 100 1 g-' AFDW d'for sponges. Body DW in S spallanzanii relates to total DW accord- The diet of the Mediterranean hydroid Campanula ing to DW ,,,,,, ,= 3.92 DW,,,, (Clapin unpubl. data; R' = ever-ta consists largely (88%) of particulate organic

0.67) and AFDW ,,,, = 0.66 DW ,,,, I (Clapin unpubl.; R* = matter between 30 and 80 pm in slze, of which, by 0.45). Thus, F,,,,, of 2.7 1 h-' g-' DWbodyat 20°C (Clapin weight, 54% consisted of zooplankton (Coma et al. 1996) relates to a filtration capacity of -1.04 1 h-' g.' 1995). C, everta consumed 1860 food items polyp1 d-', AFDW,,,,, or 25.0 1 g-' AFDW d-I at 20°C. This is con- of which 97% was particulate organic matter other siderably lower than that of Sabella penicillus, which than zooplankton (Coma et al. 1995). Thus, although reaches 7.44 1h-' for a 'standard' 65 mg DW S. penicil- hydroids are not - strictly speaking - filter-feeders, lus, or 114.5 1 h-' g.' DW at 17°C (RiisgArd & Ivarsson they do affect the densities of suspended organic mat- 1990). Adult S. spallanzanii in Cockburn Sound (1.0 to ter. Assuming a mean phytoplankton density of be- 2.5 g DW) have a conlparable filtering capacity of tween 160 and 260 cells ml-' for Cockburn Sound (S. between 3 and 7.5 1 ind.-' h-' at 22OC, despite their Helleren pers. comm.), these hydroids are estimated to much larger size (Clapin 1996). clear -10 m1 polyp ' d-l. However, at an estimated par- Infaunal have a clearance rate of ticle density of -10 X 10%ells I-' (1.8 yg chl a I-',Fig. 2; between 2.2 and 88.1 1 g-' AFDW d-' (e.g.Dales 1957, 180 fg chl a cell-'; Thompson et al. 1989), hydroids are 1961, Buhr 1976, Klockner 1978, Shumway et al. 1988, Riisgard 1989, 1991, RiisgArd et al. 1992).We applied a mean clearance rate of 23.8 1 g-' AFDW d-' for infaunal polychaetes. 3 -1 Summer '91-l92 I Measurements of the clearance rates of bivalves are (n = 6 all cases) numerous (e.g. Haranghy 1942, J~rgensen1943, 1990, Allen 1962, Coughlan 1964, Hughes 1969. Winter 1969, 1973, 1978, Ali 1970, Widdows & Bayne 1971, Bayne et 0 al. 1976, Ki~rboe& M~hlenberg1981, Harvey & Luoma 1984, Calahan et al. 1989, Vismann 1990, Cole et al. Summer '92-'93 1992, MacDonald & Ward 1994).We used a mean clear- (n= 5 all cases) ance rate of 45.7 1g' AFDW d-' (see Wilson et al. 1993). rii 2 T Although a number of echinoderms are considered suspension-feeders (e.g. Rutman & Fishelson 1969, Warner & Woodley 1975, Labarbera 1978),we did not at- tempt to quantify their clearance rate per unit of AFDW. 3 Best & Thorpe (1986) estimated epifaunal bryozoan T Summer '93-'94 1 zooids to filter 3.6 to 220.8 m1 zooid-' d-'. Bullivant " (1968) calculated a feeding rate of 3.6 to 25.2 m1 zooid-' d-', or 333.6 to 2308.8 m1 g-' DW d-l at phytoplankton densities between 0.9 and 6.8 X 10hcells I-'. We applied a mean value of 24 m1 zooid-' d-' for bryozoans, and l0 l g-' AFDW d-' (assuming AFDW is 10% of DW). All Summers '90-'94 The clearance rate of sponges was based on mea- i I surements by Rilsgdrd et al. (1993) on 2 European sponges from the genus Halichondria (mean clearance rate: 80.4 1 g-' AFDW d-I for H. panicea and similar values for H. urceolr~sat 12°C) However, mean tem- peratures in Cockburn Sound are between 16 and 24°C (Pearce 1986) so that clearance rates may be sub- stantially hlgher for sponges in Cockburn Sound. Few other data are available on the filtration rate of marine Fig 2 Mean and standard error of summer chl a concentra- sponges (Reiswig 1971, 1974, 1975, Frost 1978, J0r- t~onsat the study s~tesbetween 1990 and 1994 S~gn~f~cant gensen 1983, Stuart & Klumpp 1984, Thomassen & d~ffercdnces br~tween means are represented by different charactcrs t 4'~0\ \ and Tukey test, u = 0 05) In all but one RilsgArd 1995); clearance rates of between 40.9 and year, the western slte (2) had s~qn~f~cantlylower concentra- 134.5 1 g-' DW d-l were measured for sponges (see tlons than the eastern sltes (1, 4 and 5) For s~telocdt~ons Thomassen & Riisg6rd 1995), or approximately 84.3 to see Fig. I. 'Miss~ngdata Lemmens et al.: Filtering capacity of seagrass meadows 191

estimated to clear only -0.2 m1 polyp-' d-l: Table 1. Analysis of variance for macro-filter-feeder biomass (g AFDW clearance rate estimates of these organisms m-2)for 5 sites and 3 replicates from 2 habitats (Posidon~ameadows; bare are heavily dependent on particle densities sediment) for each of the 6 phyla as well as the total number of filter- feeders. All data were log(x+ 1) transformed.The variance between repli- and digestion rates. On the other hand, cates over all invertebrate groups was relatively low and has been Barange & Gili (1988) estimated that the om~ttedfrom the table. Replicate(Site):df = 10; SS = 1.25; F= 0.23; Repli- hydroid Eudendrium racemosum consumes cate(1-labitat):df = 4, SS = 0.46; F = 0.54) only 4.3 zooplankton items polyp-' d-l Our calculations assume a clearance rate of 1 in1 Source of Site Habitat(Site) Error polyp-' d-' for hydroids. varlance df SS F df SS F Spirorbid clearance rates are based on Ascidlans 4 2.61 5.48" 5 5.44 9.13"' 20 2.38 Dales (1957), who estimated the clearance Sponges 4 0.73 1.64 5 2.06 3.69' 20 2.24 rate of S~irorbisborealis (mean wet wt: Bivalves 4 0.30 0.71 5 0.65 1.23 20 2.12 0.24 mg ind.-l) to be 0.23 m1 id-'h-', or 4 0.97 5.62" 5 017 0.77 20 0.87 55 m1 spirorbid-' d-', but did not provide a Echinoderms 4 0.54 4.29' 5 0.95 6.00" 20 0.63 Bryozoans 4 0.11 1.34 5 0.16 1.65 20 0.39 correction for size differences or water tem- All 4 1.08 1.84 5 6 47 8 84"' 20 2.93 peratures. Estimates of clearance rates 'p < 0.05. "p < 0.005, "'p < 0.0005 were based on Anderson (1981), who re- I ported a rate of 0.4 1 h-' for per- foratus at temperatures between 15 and 23°C. How- 1990-94 (Fig. 2). It corresponds to a simple differentia- ever, Anderson's (1981) specimens were of adult slze tion between northwestern (Site 2; Luscombe Bay) and (-37 mm diameter, -16 mm height), while epifaunal southeastern sites (Sites 1, 4 and 5; Woodman Point, barnacles from Cockburn Sound are -1 mm in height. Southern Flats and Kwinana respectively) and is likely Since the clearance rate is dependent on the volume of to be related to nutrient releases in the southeast of the the body cavity (Anderson 1981), the clearance rate of Sound. No significant differences were apparent epifaunal Elrninius covertus was estimated to be ap- among the southeastern sites in any of the years. proximately 0.1 m1 h-' or 2.4 m1 d-l (estimated volumes On the basis of all 4 summers' data, the mean con- of body cavities: 3 m1 for B. perforatus; 0.75 p1 for E. centration at Site 2 (Luscombe Bay) was 0.85 pg l-' and covertus). was significantly (ANOVA, p < 0.0001, n = 32) lower Blinn & Johnson (1982) reported a filtration rate of than the concentrations at the other sites (1.82, 1.89 15.6 m1 d-' for the freshwater amphipod Hyalella mon- and 2.22 pg 1-' at Sites 5, 4 and 1, respectively; Fig. 2). tezuma. Forster-Smith & Shillaker (1977) estimated pumping rates of the tubulous amphipod Corophium bonelli (body length -3.5 mm) to be between 6.0 and 7.4 m1 h-' and of Lembos websteri (body length -4.3 mm) between 0.7 and 1.3 m1 h-', while pumping The mean biomass of macro-filter-feeders in the between 51 and 86% of the total time, at water tem- Posidonia meadows was 21.9 g AFDW m-2, which is peratures of 9.5 to 11°C (no conversion for water tem- significantly (Table 1, Fig. 3) higher than that for bare perature is given). These rates are, surprisingly, com- sediment (3.0 g AFDW m-2; Fig. 4). Although overall parable to those of the much smaller cladocerans and differences among sites were not significant, differ- copepods (see J~lrgensen1966). A mean clearance rate ences in the biomass of ascidians (p = 0.004), annelids of -39.4 m1 d-' was applied for amphipods. (p = 0.003), and echinoderms (p = 0.011) were signifi- cant (Table 1). Furthermore, Posidonia meadows were significantly different from 'bare' sediment in ascidian RESULTS (p < 0.0005), sponge (p < 0.02) and echinoderm (p < 0.005) biomass; among-habitat differences were not Chl a levels significant for bivalves, annelids and bryozoans (p > 0.05) (Table 1). A consistent trend was evident in summer chl a con- Ascidians dominated in Posidonia meadows at Site 1 centrations throughout Cockburn Sound between 1990 (Woodman Point), Site 3 (Buchanan Bay) and Site 5 and 1994 (Fig. 2). Between 1990 and 1994, Site 2 had (Kwinana); ascidian biomass was at least twice as high consistently lower concentrations than the other sites at Kwinana (Site 5: 35.8 +3.3 g AFDW m-') than at the measured in that year (no data are available for Site 3, other sites (Fig. 3). Herdmania rnomus was the domi- Buchanan Bay). This difference was significant in nant ascidian at Woodman Point (Site l), Buchanan 1990/91 and 1993/94, and in pooled dates over Bay (Site 3) and Kwinana (Site 5). The ascidian genera 192 Mar Ecol Prog Ser 143: 187-200, 1996

1 Ascidians E3 Echinoderms Annelids Bryozoans m B~valves m Bivalves B Annelids

- -

- - T 1 2 3 4 5 1 2 3 4 5 Site Site Fig. 3. Mean AFDW m-? of macro-filter-feeders in Posidonia Fig. 4. Mean AFDW m-2 of macro-filter-feeders in bare sedi- meadows of Cockburn Sound (with SE). For site locations see ment of Cockburn Sound (with SE). For site locations see Fig. 1 Fig. 1

Phallusia (Sites 4 and 5), Botrylloides (Sites 1, 3 and 5) with the polychaete Sabella spallanzanii, a species and Polycarpa (Sites 1 and 5) (see Kott 1985 for des- introduced from European waters (see Clapin & Evans criptions) were represented at some of the southeast- 1995). Within this area the species reached a biomass ern sites. The poriferan genus Tethya (see Hooper & of 458.9 + 72.5 g AFDW m-'. Although the sabellid Weidenmayer 1994) was the dominant at polychaete dominated, both in numbers and in bio- Buchanan Bay (Site 3: 5.3 * 4.7 g AFDW m-') and mass, ascidians (predominantly the large Herdmania Kwinana (Site 5: 1.1 + 0.6 g AFDW m-*); a range of momus and Phallusia obesa; 79.2 + 41.8 g AFDW m-2) other sponge species were found in Posidonia mead- and bivalves (predominantly Pina bicolor.; 34.5 * 34.3 g ows at Woodnian Point (Site 1) and the Southern Flats AFDW m-2) were also abundant within this habitat - (Site 4). Infaunal species (see Wells 1978, far more abundant than in the nearby Posidon~a Hutchings 1982 for species) were common at the meadows (Fig. 3). Southern Flats (Site 4) but less common in Posidonia Well-developed Amphibolis and Heterozostera beds meadows at other sites (Fig. 3). The bivalves Pinna were found only at Site 2 (Luscombe Bay) and Site 1 bicolor, Cardita incrassata and Paphies elongata made (Woodman Point) respectively. Heterozostera at Wood- up a considerable biomass at Luscombe Bay (Site 2) man Point (Site 1) supported a substantially lower bio- and Kwinana (Site 5; Fig 3). Epibenthic bryozoans mass of large suspension-feeders than the Posidonia were only important at Woodman Point (Site 1). A meadows at this site (1.2 and 28.6 g AFDW m-' respec- range of infaunal annelids (predominantly Neireida, tively; see Fig. 3 and Table 51, while both Amphibohs Nephytidae) dominated in most bare sediments, and Posidonia at Luscombe Bay (Site 2) supported low although bivalves (l? bicolor, C. incrassata, P. elongata) numbers of macro-suspension-feeders (2.3 and 9.7 g and ascidians (e.g. Polycarpa viridis) were common at AFDW m-2 respectively; see Fig. 3 and Table 5). Small Sites 3 (Buchanan Bay) and 5 (Kwinana) (Fig 4) Vari- annelids were dominant in Heterozostera at Woodman ance between replicates was relatively low (~5%of Point (Site l. 0.9 * 0.9 g AFDW m-') and Amphibolis at total variance; Table 1).There was a weak linear cor- Luscombe Bay (Site 2: 1.2 2 0.8 g AFDW m-2). relation between seagrass biomass and macro-filter- feeder biomass (r2 = 0.46), and between rhizome bio- mass and macro-filter-feeder biomass (r2= 0.33). Epifaunal filter-feeders During the present study it was discovered that at the Southern Flats (Site 4) a large area previously The numbers of epifaunal filter-feeders on Posidonia occupied by seagrass meadows was densely covered leaves was high, compared with the number of macro- Lemrnens et a1 Filtenng capacity of seagrass meadows 193

Table 2. D~versity~nd~ces for suspens~on-feedingmacro-invertebrates ~~~thin5 marlne habltats of Cockburn Sound, based on 3 replicate samples S species count (infaunal polychaetes counted as 1 species);n m-'- mean number of macro-suspens~on-feeders per m2 over 3 ~repl~cates

Pos~donja Bare sedlment Amp111hol1s Heterozost~ra Sa bella meadows meadows n~eadours spallanzan~i n m-' (S) n n1rL (S) n m : (S) n m-' (S) n m ' (S) - P 1 (Woodman Polnt) 47 (11) 6 (1) - 8 (4) - 2 (Luscombe Bay) 4 (6) 2 (11 12 15) - 3 (Buchanan Bay) 16 (7) 4 (4) - - - 4 (Southern Flats) 11 (8) 1994 (4) - - 70 (91 5 (Kwinana) 11 (11) 3 (4) - - - filter-feeders (Tables 2 & 3). Five invertebrate groups moderately abundant at the other 3 sites (Sites 3, 4 and were found on these leaves: hydroids, bryozoans, 5: mean density of 4.5 X 103 + 2.6 X 103 ind. m-2; Fig. 5). spirorbids, amphipods and barnacles. Of these, over Differences in epifaunal densities on Posidonia 75% were hydroids (Fig. 5). The hydroid species leaves were highly significant between sites for barna- Monotheca australis and Pynotheca producta were the cles (predominately Eln~iniussp.; p i 0.0005), spiror- most common; Orthopyxis tincta, Plumularia filicaulis bids (p < 0.005) and amphipods (p < 0.0005; Table 4), and Diphasia tubatheca were less common (cf. Watson although there were fewer spirorbids and barnacles 1992). Tube-dwelling corophiid amhipods (predomi- than hydroids. Hydroid densities were higher at nantly Ericthonius sp.; see Barnard & Karaman 1991) Kwinana (Site 5: 2.27 X 106 + 0.52 X 10' polyps m-') were numerous at Woodman Point (Site 1: 1.4 X 105 + than at the other sites (mean: 0.45 X 106 + 0.06 X 106 0.5 X 105 ind. m-') and the Southern Flats (Site 4: 2.3 X polyps m-2; Fig. 5), but the level of significance of dif- 10' k 0.9 X 10' ind. m-'), but far less numerous on Posi- ferences between sites was low (p = 0.055; Table 3). donia leaves from other sites (Sites 2, 3 and 5: 105 + Bryozoans did not demonstrate significant between- 147 ind. m-2; Fig. 5). Similarly, the barnacle Elminius site differences (p >0.05; Table 4). sp. was common on Posidonia leaves at Woodman Spirorbids, barnacles and amphipods were abun- Point (Site 1: 1.3 X 104 + 0.6 X 104 ind. m-'), almost dant on tubes of Sabella spallanzanii from the South- absent at Luscombe Bay (Site 2: 52 + 26 ind. m-') and ern Flats (Site 4: 4.1 X 105 + 1.1 X 105 ind. m-'). At Luscombe Bay (Site 2) the Arnphibolis meadows sup- ported a variety of epiphytes, with numbers reaching EYI Barnacles similar densities (7.1 X 105 2.1 X 105 ind. m-') to those m Spirorb~ds on Posidonia meadows at this site (Table 3). However, Hydroids Heterozostera meadows from Woodman Point (Site 1) supported considerably lower densities of epifaunal suspension-feeders (total n m-2: 0.78 X 105 +- 0.62 X 105) than Posidonia leaves (total n m-2: 7.6 X 105 & 1.5 X 105). Here, hydroids were most important, but samples demonstrated considerable fluctuations between repli- cates (range: 1.2 X 103 to 1.9 X 10"olyps m-2).

Table 3 Divers~tyindices for epifaunal suspension-feeders on Pos~donialeaves from Cockburn Sound, based on 3 repl~cate san~plesS mean species count, n m mean number of sus- penslon-feeding units (polyps, zooids. ~ndlvlduals) with~n 1 mZover 3 repl~cates

S~te n m+ S (df = 4, F= 2 58) (df = 4; F= 3.36) P P l (Woodman Polnt) 7 6 X 103 + 1 5 X 105 8 0 Site 2 (Luscombe Bay) 5 9 X 105 t 1 8 X 105 12 0 3 (Buchanan Bay) 5 8 X 105 + 2 4 X 10' 7 7 Fig. 5 Mean number of epifaunal filter-feeder units (individ- 4 (Southern Flats) 7 4 X 105 t 4 3 X 105 9 3 uals. polyps, zoo~ds)per m2 Posldonla seagrass in Cockburn 5 (Kw~nana) 23 4 X 105+52x lo5 9 3 Sound (with SE) 194 Mar Ecol Prog Ser

Table 4. Analysis of variance for the dens~ty[n m-') of ep~fau- Garden Island) is undeveloped. Together the data 1nd1- nal suspension-feeders on Posidonid leav~sfrom 5 sites and 3 cate that the observed summer chlorophyll gradient is replicates for each of the 6 phyla as well as the total number a persistent environmental variable that could influ- of filter-feeders Data were log(1 +X) transformed ence the distribution of biota In the Sound.

Source of Site Error variance df SS F d f SS Spatial patterns in suspension-feeder densities Hydro~ds 4 1.782 3.35 10 1332 Bryozoans 4 12.670 2.69 10 11.780 Clear spatial patterns were observed in suspension- Spirorbids 4 8.207 13.29" 10 1.543 feeding communities. In Posidonia meadows the high- Barnacles 4 18.743 13.41 "' 10 3.494 Amph~pods 4 58.076 14.70"' 10 9.878 est densities of macro-suspension-feeders were ob- served at the eastern sites (Woodman Point and near All animals 4 0.924 2.58 10 0893 Kwinana; Sites 1 and 5), while the highest densities of 'p c 0.05, "p c 0.005, "'p c 0.0005 epifaunal suspension-feeders were near Kwinana. This spatial pattern positively corresponds to a large extent with levels of nutrient enrichment (expressed in chl a Species diversity concentrations) in the water and a high epiphyte bio- mass on the seagrass leaves (Silberstein et al. 1986, The abundance and diversity of macro-suspension- Borowitzka & Lethbndge 1989).Nutrient enrichment is feeders was relatively high in the Posjdonia meadows generally highest in the southeastern section of Cock- (Table 2). Only at the Southern Flats did the mean burn Sound (e.g. Cary et al. 1991). number of organisms in 'bare' sediment exceed that of It seems plausible that the spatial patterns in nutrient Posidonia meadows, mainly due to the numbers of inputs, phytopla.nkton, epiphyte biomass and suspen- infaunal polychaetes. sion-feeding communities are related; a significant The species diversity (S) of macro-suspension-feed- relationship between nutrient loads and chl a levels ers in Amphibolis meadows in Luscombe Bay (S = 5) in Cockburn Sound has already been demonstrated a.nd the Sabella patch on the Sou.thern Flats (S= 9) was (Cary et al. 1991; also see Chiffings 1979). Further- comparable to that in Posidonia meadows (range 6 to more, an increase in suspended organic material, in- 11; Table 2), but was low in the Heterozostera tasman- cluding phytoplankton, would be able to support a ica meadows at Woodman Point (S = 4). The species higher biomass of suspension-feeders. They, in turn, diversity of epifaunal suspension-feeders in Posidonia would affect the densities of suspended organic mate- meadows was relatively constant among the sites rial, as in San Francisco Bay (Cloern 1982). (Table 3), although hydroids dominated at Woodman However, since the western and eastern parts of Point, while at Luscombe Bay all phyla were more Cockburn Sound dlffer in a wide range of variables, evenly represented (Fig. 5). including wave exposure and invertebrate recruitment rates, and suspension-feeders also feed on other par- ticulate organic matter (e.g. Stuart et al. 1982, Seiderer DISCUSSION & Newell 1985, Judge et al. 1993), suspension-feeder biomass cannot simply be linked to one particular vari- Chl a levels in Cockburn Sound able such as chl a levels. Furthermore, such a relation- ship would be difficult to establish in the field. The chl a concentration displayed a consistent gradi- ent, from low in the west to high in the east of Cock- burn Sound. The east-west chl a gradient was a consis- Filtering capacity of suspension-feeding tent feature over the 4 summers for whlch data were communities collected. An almost ident~calchl a gradient was ob- served in the Sound as far back as 1977 (Chiffings & Ecological data on the biomass of the main suspen- McComb 1981). Several reports (e.g Cary et al. 1991, sion-feeders in a marine habitat can be combined with Lavery 1994a, b) attributed this distribution pattern to physiological data on the filtrat~oncapacity of the ani- the location of the nutrient sources in the southeast mals to estimate the filtering capacity of the habitat corner of the Sound and a wind driven counter-clock- (e.g. Petersen & Riisgdrd 1992). However, the filtering wise water current within the Sound under typical capacity of suspension-feeding communities is depen- summer sea breeze conditions (e.g.Steedman & Craig dent on such factors as species-specific differences, 1983) Industrial waste is discharged on the eastern water temperature, size, food concentrations, side of the Sound, while the western side (bordered by environmental conditions, flow rates, the boundary Leminens et al.:Filtering capaclty of seagrass meado\vs

effect (where flow rates decrease near the substrate), bottom substrate ('bare' sediment). This is only to a stratification, etc. (see Bayne et al. 1976 and Riisgard & small extent due to macro- and infaunal suspension- Larsen 1995 for overviews) and seasonal changes in feeders (24 '%) of the total filtering capacity; Table 5);the the biomass of suspension-feeders. Other sources of more numerous epifauna (hydroids, bryozoans, barna- error in estimating the filtration capacity of marine cles and amphipods) are far more important (76%; habitats may result from particle size selection (e.g. Table 5).Epifauna are uncommon on bare sediment. sponges generally ingest smaller particles than other Ascidians and sponges are the main rnacro-suspen- suspension-feeders; Reiswig 1975, Stuart & Klumpp sion-feeders in Posidonia meadows (Table 5), whlle 1984). Most measurements of filtration rates in the lit- bivalves and small, burrowing annelids provide most erature are of temperate organisms from the northern of the filtering capacity of bare sediment (Table 5). hemisphere, although a number of studies on ascidi- However, when dense communities of the large poly- ans, sponges and bivalves from southern Africa (which chaete Sabella spallanzanii invade the bare sediment, has similar environmental conditions) are available they substantially enhance the filtering capacity. (e.g. Griffiths 1980, Stuart 1982, Stuart et al. 1982, Sabellid polychaetes at the Southern Flats have a Klumpp 1984, Stuart & Klumpp 1984, Seiderer & similar filtering capacity to the macro-filter-feeders in Newel1 1985, 1988, Matthews et al. 1989).Few data are Posidonia meadows, although the epifauna on the available on the - often endemic - suspension-feed- polychaete tubes provides a substantial part of this fil- ers from southwest Australia, which may find an opti- tering capacity (Table 5).Our estimates of the filtering mum under substantially different environmental con- capacity of S. spallanzanii (11.5 kl d-' m-2 at 20°C) ditions (e.g. Lemmens et al. 1996),so that extrapolation compare well with more detailed recent estimates by of the available data is necessary. Clapin (1996), who estimated these polychaete com- The time to achieve a 50% decrease in phytoplank- munities on the Southern Flats of Cockburn Sound to ton densities is a more correct way of presenting the fil- represent a filtering capacity of 23 kl d-' m-2 in sum- terlng capacity of suspension-feeding communities mer (22°C) and 10 kl d-' m-%n winter (17OC). How- than the volume processed per unit of time, since levels ever, other organisms wlthin these communities more of suspended material do decrease linearly with time. than double the total filtering capacity to about 26 kl At a given clearance rate (C) and a known water vol- d-' m-2 (Table 5). 0u.r estimates indicate that S. spal- ume (V,,,), the time (t)to achieve a 50 O/odecrease in food lanzanii communities at the Southern Flats possibly density (where the final concentration, C,, is 0.5 times turn over the water column above them (-5 m) several the concentration at t = 0, C,,) can be calculated from times daily and constitute a considerably higher filter- the formula: C = (V,/t) In(Co/C,)(see Petersen & Riis- ing capacity than the Posidonia meadows they have gdrd 1992, RiisgArd et al. 1993).However, in this calcu- replaced. lation it is assumed that there is no replacement of Ampl~ibolis and Heterozostera meadows were found water and complete mixing of the water column; this is at only 1 site each. The Amphibolis meadows at Lus- rarely the case, as generally a current is present, and combe Bay constitute a s~milarfiltering capacity to that both stratification and the existence of a boundary layer of Posidonia meadows (Table 5) and will turn over the demonstrate incomplete mixing of the water column. water column above them (-5 m) in about a day. How- The biomass of the invertebrate suspension-feeding ever, due to n~orphologicaldifferences between Posi- groups and their filtering capacities (drawn from the lit- donia and Amphibolis, there are differences in the erature; see 'Materials and methods') provide an esti- ratios of the various epifaunal suspension-feeders: at mate of the filtering capacity of the community (Table 5). Luscombe Bay bryozoans and hydroids are more com- However, clearance rates are dependent on a range of mon on Amphibolis leaves (Table 5, Fig. S), possibly variables (see above), so must be used cautiously. because they tend to be more common near the leaf Nonetheless, such calculations may demonstrate the sheaths (J Lemmens pers, obs.), which are more relative importance of the various communities in clear- favourably placed in the water current than in Posido- ing the water column of organic material. nia (see remarks by Keough 1986). However, this is Posidonia meadows can, on average, turn over the surprising in view of the relatively high turnover times equivalent of the water column above them (-5 m water of Amphibolis leaves (between 28 and 40 d for Amphi- depth or -5000 1 seawater m-* habitat) approximately bolis antarctica compared with 65 and 125 d for Posi- daily, while communities on bare sediment (-5 m donia australis and 73.7 d for Heterozostera tasmanica; depth) will turn over the water column above them Halophila ovalis has a mean life-span of 11 to 24 d; e.g. approxin~ately once a month. Suspension-feeding Borowitzka & Lethbridge 1989), which would allow communities in Posidonia meadows have a substan- little time for the development of epifaunal suspen- tially higher filtering capacity (possibly over 25 times sion-feeders. It should, however, be noted that at Lus- higher; Table 5) than those on non-vegetated soft- combe Bay sponge and ascidian biomass is relatively Table 5. Estimated filtration capacity of 5 shallow-water habitats in Cockburn Sound (in bold; expressed in kl d.' m-2 habitat). Based on mean suspension feeding densi- ties of macro- and epifaunal suspension-feeders, combined with the estimated filtration rates of invertebrate goups as published in the literature (see 'Materials and methods' [or lurther details). Mean biomass (*SE) is given in parentheses

Suspension- Bare sediment Posidonia meadows Amphibolis meadows Heterozostera meadows Sabella spallanzanii feeding group (means of all sites) (means of all sites) (Luscombe Bay only) (Woodman Point only) (Southern Flats only)

Publ~shedclearance rate Estimated filtering capacity of macro- and infaunal suspension-feeders (kl d-' m-') Macro- (I cl' g-' AFDW) (mean biomass * SE, g AFDW m-')

Ascidians 96.0" 0 (0.2* 0.1) 1.3 (13.5* 6.3) - 0 (0.03* 0.03) 7.6 (79 5 + 41 .a) S. spallanzanii 25.0" - - - - 11.5 (458.9 + 72 5) Other polychaeles 23.8' 0 (1.3* 0.7) 0 (0.7 * 0.5) 0 (1.2 * 0.8) 0 (0.9 i 0.9) - Bivalves 45.7'l 0.1 (1.5 * 1.4) 0.1 (1.4 * 0.6) 0 (0.003 * 0.003) - 1.6 (34 5 t 34.3) e Echinoderms - - -'(1,s * 1,l) - -'(0.7 r 0.7) -" (3.3t 3.3) Bryozoans 10.0' 0 (0.4 * 0.3) - 0 (0.6i 0.1) - Sponges 100.0!J - 0.4 (4.4 i 2.1) 0 (0.009* 0.009) - - Totals 0.1 (3 0 * 1.81 1.8 (21.9 * 5.7) 0 (1.2* 0.8) 0 (2.3* 1.6) 20.7 (575.9+ 121.3)

Published clearance rate Estimaled filtering capacity of epifaunal suspension-feeders (kl d.' m-') Epifaunal (m1 unit-' (I-') (mean biomass i SE, 103 units m-')

Hydroids l.Oh 0.8 (816.0 * 366.3) 0.5 (529.2 * 149.7) 0 (72.1 * 62.0) 0 (1.1 * 1.1)

Bryozoans 24.0' p 2.0 (85.5 * 39.0) 5.0 (208.1 * 27.0) - - Spirorbids 5.5' 0.1 (13.9 k 9.8) 0 (0.8 * 0.4) - 0 (0.9 2 0.5) Barnacles 2.4k - 0 (13.0 i 9.7) 0 (0.7 * 0.2) 0 (0.05 i 0.05) 0.7 (297.9 * 36.4) Amphipods 39.4' - 2.9 (73.2 i 46.8) 0 (0.7 * 0.4) 0.3 (6.4 i 4.0) 4.3 (108.8 + 27.7) Totals - 5.8 (1016.8 + 336.3) 5.5 (739.5 * 122.8) 0.3 (78.5 i 61.9) 5.0 (408.7 * 64.4)

Overall filtratio~l 0.1 7.6 5.5 0.3 25.7

'Petersen & RusgArd (1992); see 'hlaterials dnd methods' "lapin (1996);see 'Materials and methods' 'Compilation of data from range of publications: Dales (1957, 1961), Buhr (1976),Klockner (1978),Shumway et al. (1988), RiisgArd (1989, 1991) "Compilation of data from wide range of publications; see 'Materials and methods' 'No quantitative data on clearance rate available (e.g. Rutman & Fishelson 1969. Warner & Woodley 1975, Labarbera 1978) ' Bullivant (1968) Wejswig (1971, 1974, 1975). Frost (1978),Jargensen (1983). Stuart & Klumpp (1984),Riisghrd et al. (1993) hBarange & Gili (1987). Coma et al. (1995); hydroids are not strictly speaking filter-feeders; thls group feeds on individual particles of suspended particulale organlc matter and zooplankton. See remarks in 'Materials and methods' ' Best & Thorpe (1986) I Dales (1957) 'Anderson (1981); see 'Materials and methods' ' Forster-Smith & Shillaker (1977). Blinn & Johnson (1982) I Lernrnens et al.: Filtering ca pacity of seagrass meadows

low in both A~nphibolis and Posidonia meadows mass in suspension-feeders than unvegetated soft-bot- (Table 5, Fig. 3),and also contributes relatively little to tom substrates: sufficient to turn over the water column the filtering capacity of Posldonia meadows here. above them in less than a day (at least potentially), Heterozostera meadows at Woodman Point support which would have a considerable impact on local con- low densities of suspension-feeding infauna. Hydroids centrations of suspended organic matter (Table 5).Sus- and amphipods are few, as are macro-filter-feeders, pension-feeders associated with unvegetated soft-bot- while infaunal polychaetes are relatively rare within tom substrate, on the other hand, are unlikely to have a these meadows. If complete mixing of the water col- significant impact on local concentrations of suspended umn occurs, these communities are estimated to turn organic matter, except where they have been invaded over the water column above them (-5 m) approxi- by the introduced polychaete Sabella spallanzanii mately twice a month, slightly more than unvegetated (Table 5).These observations correspond with other re- substrate (Table 5). ports. In Princess Royal Harbour, Albany, Western Aus- Although our biomass data, especially on epifaunal tralia, for example, the loss of seagrass meadows has re- organisms, are based on small samples, were collected sulted in a decline in the benthic marine invertebrate on 1 occasion only (September 1994),and have relatively biomass by 82 %, from 1937 to 340 t, although most of high error margins (seeTable 5), they give an indication these were gastropod molluscs and (Kirk- of the contribution of the various components to the total man et al. 1991, Wells et al. 1991). filtering capacity of the communities in Cockburn Limited data on Amphibolis and Heterozostera Sound. In the Posidonia meadows, for instance, the meadows indicate that the former may have a similar epifauna (-1 X 106 ind. m-') are estimated to provide filtering capacity to Posidonia meadows, although about 76% of the total filtering capacity of these largely through the high densities in bryozoans and meadows (-6 kl m-2 d-l; Table 5).The other epifauna: macro-suspension-feeder biomass is epifaunal suspension-feeders make an unexpectedly relatively low in both Posidonia and Amphibolis mead- high contlibution to the total filtering capacity. ows at Luscombe Bay (Table 5, Fig. 3) Heterozostera Although hydroids are not, strictly speaking, filter- meadows have a far lower filtration capacity than both feeders, and our estimates of their filtering capacity Posidonia and Amphibolis meadows - similar to un- (Table 5) are disputable (see 'Materials and methods'), vegetated substrate (Table 5) - due to their lower bio- they may have a substantial impact on densities of sus- mass of suspension-feeders. This may be due to the pended organic material. Coma et al. (1995)noted that, relatively small leaf area of Heterozostera, resulting in for example, the hydroid Carnpanularia everta - on less substrate for epifa.una1 suspension-feeders. In the algae Halimeda tuna in the western Mediter- addition, Heterozostera occurs in Cockburn Sound - ranean Sea - may ingest approximately 4 X 10"rey where it is often associated with Halophila - in rela- m-2 d-' in summer and 8 X 105prey m-2 d-' in winter or tively coarse and unstable substrates where epifauna 1528 mg C m-2 yr-', 88% of which may be detritus may be subject to abrasion. rather than zooplankton. The biomass of suspension-feeders is generally not The biomass of the deep basin (>l0 m) of Cockburn constant over time. Highest hydroid densities in south- Sound is dominated by molluscs (89.6% of individuals; west Australia are reached during August, when water 72.2% of biomass), of which 95.7% are infaunal sus- temperature is beginning to rise from a winter low of pension-feeders (Wells & Threlfall 1980). Polychaetes -16°C (Watson 1992). The present data set only pro- and crustaceans together make up a further 20.3 % of vides an estimate of suspension-feeder biomass in win- the biomass (Wells 1978). These organisms have a bio- ter. These may be quite different from the biomass in mass of between 336 and 2027 g wet wt m-' (Wells & summer. Threlfall1980)and may thus add considerably to the to- The importance of suspension-feeding communities tal filtering capacity of Cockburn Sound. Jetties and py- in controlling phytoplankton levels in shallow, semi- lons also support a considerable suspension-feeder bio- enclosed environments has been suggested by a num- mass - with a substantial filtering capacity -which ber of studies (e.g. Buss & Jackson 1981, Cloern 1982, thus far has largely been overlooked (e.g. Clapin 1996). Frechette & Bourget 1985, Dame et al. 1989, Asmus & Asmus 1991, Hily 1991, Alpine & Cloern 1992). How- ever, our study suggests that epifaunal suspension- Differences between habitats in density of feeders may have a far greater filtering capacity than suspension-feeder communities generally accepted (Table 5). The vertical distribution of seagrass is to a consider- The shallow-water soft-bottom communities in Cock- able extent determined by light penetration (e.g.Back- burn Sound have different suspension-feeder commu- man & Barilotti 1976),so factors affecting light penetra- nities. Posidonia communities support a far higher bio- tion (depth, concentration of suspended organic and Mar Ecol Prog Ser

inorganic material, epiphytic growth) play a large part Barnard JL, Katarnan G (1991) The families and genera of in determining the distribution of these seagrasses marine gammaridean (except marine gam- Seagrass meadows (Posidonia and Amphibolis) support maroids). Rec Aust Mus 13:209-241 Bayne BL, Thompson RJ, Widdows J (1976) Physiology I. In: high densities of suspension-feeders which - by feed- Bayne BL (ed) Marine , thtlir ecology and physiol- ing on phytoplankton and other suspended particulate ogy. Cambridge University Press, Cambridge, p 121-206 organic matter such as detritus (e.g.Stuart et al. 1982, Best MA, Thorpe JP (1986) Effects of food particle concentra- Judge et al. 1993) -could improve light penetration, tion on feeding current velocity in six species of marine . Mar B101 93:255-262 thereby partly counteracting the negative effects of eu- Blinn D W, Johnson D B (1982) Filter-feeding ~l~.dlellamon- trophication on the vertical distribution of seagrasses tezuma, an unusual behaviour for a freshwater amphipod. (although excessive epifauna itself can reduce light Freshwat Invertebr Biol 1:48-52 penetration to the leaves). It is uncertain if suspension- Borowitzka MA, Lethbridge RC (1989). Seagrass epiphytes. feeders are also capable of controlling settlement of In: Larkum AWD. McComb AJ, Shepherd SA (eds) Sea- grasses: a treatise on the biology of seagrasses with spe- epiphytes on seagrasses, by reducing the densities of cial reference to the Australasian region, Chap 14. Else- algal spores in the water column. However, loss of Posi- vier, Amsterdam, p 458-499 doniaand Amphibolismeadows leads to a consider- Buhr KJ (1976) Suspension-feeding and assimilation effi- able loss of suspension-feeder communities, thereby ciency in Lanlce conchilega (Polychaete) Mar Biol 38: 373-383 compounding the negative effects of eutrophication Bullivant JS (1968) The rate of feeding of the bryozoan and further complicating revegetation by seagrasses. Zoobotryon vertlc~llatum. NZ J Mar Freshwat Res 2: Pioneer species such as Heterozostera and Halophila 111-134 support a fraction of the invertebrate suspension- Buss LW, Jackson JBC (1981) Planktonic food availability and feeders in Posidonia and Amphibolis meadows. suspension-feeder abundance: evidence of in situ deple- tion. J Exp marBiol Ecol49:151-161 Calahan JA, Siddall SE, Luckenbach MW (1989) Effects of Acknowledgements. This study is part of the CSIRO Coastal flow velocity, food concentration and particle flux on Zone Program Filter-feeder Project, and was undertaken in growth rates of juvenile bay scallops Argopecten irradi- collaboration with the Edith Cowan University (ECU) and the ans. J Exp Mar B101 Ecol 129:45-60 Western Australian Department of Environm.enta1 Protc!ctlon Cambridge ML (1979) Technical Report on Seagrass, Cock- (DEP). CSIRO Marine Laboratories provi.ded logistical sup- burn Sound Study Report No. 7, Department of Conserva- port and laboratory space; DEP collected the chl a data and tion & Environment, Perth provided additional boat time. We thank Ed Greenway (ECU) Cambridge ML, McComb AJ (1986) The loss of seagrass from for collecting data on epifaunal filter-feeders; Dr Hugh Kirk- Cockburn Sound. Western Australia. 11. Possible causes of man (CSIRO) for sharing his ideas which formed the basis for seagrass decline. Aquat Bot 24:269-285 this study, and for his constructive comments; Dr Jeanette Cary JL, Masini RJ (1995) Water quality survey in Cockburn Watson (Marine Science & Ecology Environmental Consul- Sound, Warnbro Sound and Sepia Depression between tants, Victoria, Australia) for Identifying representative January 1991 and February 1992. Data Report SMCWS hydrolds, Drs Graham Edgar, Alan Butler, Vivienne Mawson ECOL-10, Department of Environmental Protection, Perth and a number of anonymous referees for their constructive Cary JL, Simpson CJ, Chase S (1991) Water quality in Cock- comments. burn Sound. Technical Series No. 47, Environmental Pro- tection Author~ty.Perth LITERATURE CITED Chiffings AW (1979) Cockburn Sound environmental study. Technical report on nutrient enrichment and phytoplank- Ali RM (1970) The influence of suspension, density and tem- ton, Report No. 3. Department of Conservation and Envi- perature on the filtration rate of Hiatella arctica. Mar Biol ronment. Perth 6:291-302 Chiffings AW, ~McCombAJ (1981) Boundaries in phytoplank- Allen JA (1962) Preliminary experiments on the feeding and ton populations. Proc Ecol Soc Aust 11:27-38 cxcret~onof blvdlves using Phaeodactylum labelled with Chittleborough RC (1970) Conservation of Cockburn Sound, P - J Mar Biol Ass UK42,609-623 a case study. Australian Conservation Foundation, Park- Alp~neAE, Cloern JE (1992) Trophic interactions and direct ville, Victoria physical effects control phytoplankton biomass and pro- Clapin G (1996) The i~ltrationrdte, oxygen consumption and duction in an estuary. Lirnnol Oceanogr 37:946-955 biomass of the introduced polchaete Sabella spallanzanii Anderson DT (1981) Cirral activity and feeding in the bar- Gmelln within Cockburn Sound. Honours thesis, Edith nacle Balanus perforatus Bruguiere (), with Cowan University. Joondalup comments on the evolution of feeding mechanisms in Clapin G, Evans DR (1995) The status of the Introduced thoracican cirripldes. Phi1 Trans R Soc Lond Ser B Biol Sci marine fan worm. Sabella cf. spallanzanii (Gmelin. 1791) 291:411-449 in Western Australia: a preliminary investigation. Techni- Asmus RM. Asmus H (1991) beds: limiting or promot- cal Report No. 2, CSIRO Centre for Research on Intro- Lng phytoplankton? J Exp Mar B101 Ecol 148:215-232 duced Marine Pests, Hobart Backman TW.Barilotti DC (1976)Irrad~ance reduction: effects Cloern JE (1982)Does the benthos control phytoplankton bio- on standing crops of the eelgrass, Zostera marina, In a mass in South San Franc~scoBay? Mar Ecol Prog Ser 9. coastal lagoon. Mar Biol34:351-353 191-202 Barange M, Gili JM (1988)Feeding cycles and prey capture in Cole BE, Thompson JK. Cloern JE (1992) Measurement of fil- Eudendrium racernosum (Cavolini. 1785). J Exp Mar Biol tration rates by infaunal bivalves in a recirculating flume. Ecol 115:281-293 Mar Biol 113(2):219-225 Lelnmens et al.: Filtering capaclty of seagrass meadows

Coma R, Gili JM. Zabala M (1995) Trophic ecology of a ben- Jergensen CB (1943) On the water transport through the gills thic marine hydroid, Campanularia everta. Mar Ecol Prog of bivalves. Acta Physiol Scand 5:297-304 Ser 119:211-220 Jsrgensen CB (1966) Biology of suspension-feeding. Perga- Coughlan JAA (1964) A direct method for determining the mon Press, Oxford pumping rates of siphonate bivalves J Cons Perm Int Jorgensen CB (1983) Fluid mechanical aspects of suspension Explor Mer 29:205-213 feeding. Mar Ecol Prog Ser 11:89-103 Dales RP (1957) Some quantitative aspects of feeding in Jsrgensen CB (1990) Bivalve filter feeding: hydrodynamics, sabellid and sepulid fan worms. J Mar Biol Ass UK 36: bioenergetics, physiology and ecology. Olsen & Olsen, 309-316 Fredensborg Dales RP (1961) Observations on the respiration of the sabel- Judge ML, Coen LD, Heck KL (1993) Does Mercenaria mer- lid polychaete Schizobranchia insignis. Biol Bull Mar Biol cenaria encounter elevated food levels In seagrass beds? Lab, Woods Hole 121:82-91 Results from a novel technique to collect suspended food Dame RP, Spurner JD, Wolaver TG (1989) Carbon, nitrogen resources. Mar %col Prog Ser 92:141-150 and phosphorus processing by an reef. Mar Ecol Keough M (1986) The distribution of a bryozoan on seagrass Prog Ser 54:249-256 blades: settlement, growth and mortality. Ecology 67(4): Dennison WC, Alberte RS (1982) Photosynthetic responses of 846-857 Zostera manna L. (eelgrass) to in situ manipulations of Kierboe T, Mehlenberg F (1981) Particle selection in suspen- light intensity. Oecologia 55137-144 sion-feeding bivalves. Mar Ecol Prog Ser 5:291-296 Fiala-Medioni A (1974) Ethologie alimentaire d'invertebres Kirkman H, Humphries P, Manning R (1991) The epibenthic benthiques filtreurs (ascidies). 11. Variations des taux de fauna of seagrass beds and bare sand in Princess Royal filtration et de digestion en fonction de l'espece. Mar Biol Harbour and hng George Sound. Albany, southwest Aus- 28:199-206 tralia. In: Wells FE, Walker DI, Kirkman H, Lethbridge R Fitzpatrick J, IOrkman H (1995) The effects of prolonged (eds) The marine flora and fauna of Albany, Western Aus- shading stress on the growth and surv~valof the seagrass tralia, Vol 2. Proc 3rd Int Mar Biol Workshop. Western Posidonia australis in Jervis Bay, NSW. Mar Ecol Prog Ser Australian Museum. Perth, p 553-564 127:279-289 Klockner K (1978) Zur Okologie von Pomatoceros triqueter Forster-Smith RL. Shillaker R0 (1977) Tube irrigation by Lem- (, Polychaeta). Helgolander Wiss Meeresunters bos weberi Bate and Corophium bonelli Milne Edwards 31:219-223 (Crustacea: Amphipoda). J Exp Mar Biol Ecol 26:289-296 Klumpp DW (1984) Nutritional ecology of the ascidian Pyura Fowler J, Cohen L (1990) Practical statistics for field biology. stolonifera: influence of body-size, food quantity and qual- John Wiley & Sons, New York ~tyon filter-feeding, respiration, assimilation efficiency Frechette M, Bourget E (1985) Energy flow between the and energy balance. Mar Ecol Prog Ser 19:269-284 pelagic and benthic zones: factors controlling particulate Kott P (1985) The Australian . Part I, Phlebobranchia organic matter available to an intertidal mussel bed. Can J and Stolidobranchia. Mem Queens1 Mus 23:l-440 Fish Aquat Sci 42:1158-1165 Labarbera M (1978) Particle capture by a Pacific brittle star: Frost TM (1978) In situ measurements of the clearance rates experimental test of the aerosol suspension feeding for the freshwater sponge Spongilla lacustris. Limnol model. Science 201:1147-1149 Oceanogr 23:1034-1039 Lavery P (1994a) Changes in seagrass cover. Commissioned Griffiths RJ (1980) Filtration, respiration, and assimilation in Report 1994-05. Department of Environmental Manage- the black mussel Chorornytilus rner~dlonalis. Mar Ecol ment, Edith Cowan University, Perth Prog Ser 3:63-70 Lavery P (199413) The current state of seagrass health in the Haranghy L (1942) Die Muschelvergiftung als biologisches Success Bank to Warnbro Sound region. Commissioned Problem auf Grund der neueren diesbezuglichen Ur- Report 1994-06. Department of Environmental Manage- sachenforschung. Helgolander Wiss Meeresunters 2: ment, Edith Cowan University, Perth 279-352 Lemmens JWTJ, Kirkpatrick D, Thompson P (1996) The clear- Harvey RW, Luoma SN (1984) The role of bacterial exopoly- ance rates of four ascidians from Marmion Lagoon. West- mer and suspended in the nutrition of the deposit- ern Australia. In: Kuo J, Phillips RC, Walker D1. Kirkman H feeding clam Macorna balthica. J Mar Res 42:957-968 (eds) Seagrass biology: Proceedings of an lnternational Hily C (1991) Is the activity of benthic suspension-feeders a Workshop. Rottnest Island, WA, 25-29 Jan '96. Faculty factor controlling water quality in the Bay of B.rest? Mar of Sciences, Un~versity of Western Australia, Perth, Ecol Prog Ser 69:1?9-188 p 277-282 Holmes N (1973) Water transport in the ascidians Styela clava MacDonald BA, Ward JE (1994) Variation in food quality and and Ascidiella aspera (Miiller). J Exp Mar Biol Ecol 11: particle selectivity in the sea scallop Placopecten magel- 1-13 lanjcus (: ). Mar Ecol Prog Ser 108: Hooper JNA, Wiedenmayer F (1994) Porifera. In: Wells A (ed) 251-264 Zoological catalogue of Australia, Vol 12. CSIRO Aus- Matthews S. Lucas MI. Stenton-Dozey JME, Brown AC (1989) tralia, Melbourne Clearance and yield of bacterioplankton and particulates Hughes RN (1969) A study of feeding in plana. for two suspension-feeding infaunal bivalves, Donax serra J Mar Biol Ass UK 49:805-823 Roding and Mactra lilacea. J Exp Mar Biol Ecol 125: Hutchings P (1982) Bristleworms (Phylum Annelida). In: 219-234 Shepherd SA, Thomas IM (eds) Marine invertebrates of Minitab Inc (1993) Minitab reference manual release 9 for southern Australia, Part 1. DJ Woolman, Government Windows. Sowers Printing CO, Lebanon, PA Printer, South Australia, p 228-298 Pearce A (1986) Sea temperatures of Western Australia. FINS Jeffrey SW, Humprey GF (1975) New spectrophotometric Fish News 19(2):6-9 equations for determining chlorophylls - a, b, cand c2 in Petersen JK, Riisgird HU (1992) Filtration capacity of the higher plants, algae and natural phytoplankton. Biochem ascidian Ciona intestinalis and its grazing impact in a shal- Physiol Pflanz 16?:191-194 low fjord. Mar Ecol Prog Ser 88:9-l? Mar Ecol Prog Ser 143: 187-200, 1996

Randlov A, RiisgArd HU (1979)Efficiency of particle retention (Molina) fed on a dlet of kelp detritus of different ages. and filtration rate in four specles of ascidians. Mar Ecol Mar Blol Lett 3(4-5):289-306 Prog Ser 1:55-59 Stuart V. Fleld JG, Newel1 RC (1982)Evldence for absorpt~on Reisivig HM (1971) Part~clefeedlng In natural populations of of kelp detritus by the ribbed mussel Aulacomya ater three marine demosponges. Blol Bull Mar Blol Lab, Woods using a new "Cr-labelled microsphere technique. Mar HoIe 141:568-591 Ecol Prog Ser 9:263-27 1 Reiswig HM (1974) Water transport, respiration and energet- Stuart V, Klumpp DW (1984) Evldence for food-resource par- ics of three tropical marine sponges. J Exp Mar Biol Ecol titioning by kelp-bed fllter feeders lMar Ecol Prog Ser 16: 14:231-249 27-37 Reiswig HM (1975) Bacteria as food for temperate-water Thomassen S, Riisgard HU (1995) Growth and energetics of marine sponges. Can J Zoo1 53582-589 the sponge Halichondria panicea Mar Ecol Prog Ser 128: Riisgard HU (1989) Properties and energy cost of the muscu- 239-246 lar piston pump in the suspension-feeding polychaete Thompson PA, Levasseur ME, Harrison PJ (1989) Light-lim- Chaetopterus variopedatus. Mar Ecol Prog Ser 56: 157-168 ited growth on ammonium vs nitrate: what is the advan- Riisgdrd HU (1991) Suspension feeding in the polychaete tage for marine phytoplankton? Limnol Oceanogr 34(6): Nereis diversicolor. Mar Ecol Prog Ser 70:29%37 1014-1024 Riisgard HU, Ivarsson NM (1990) The crown-filament pump Vismann B (1990) Field measurements of filtration and respi- of the suspension-feeding polychaete Sabella penicillus: ration rates in Mytilus edulisL. An assessment of methods. filtration, effects of temperature, and energy cost. Mar Sarsia 75:213-216 Ecol Prog Ser 62:249-257 Warner GF, Woodley JD (1975).Suspension feeding in the brit- RiisgArd HU, Larsen PS (1995) Fllter-feeding in marine tle-star Ophiothriv fragilis. J Mar Biol Ass UK 55:199-210 macroinvertebrates: pump characteristics, modelling, and Watson JE (1992) The hydroid community of Amphibolissea- energy cost. Biol Rev 70:67-106 grasses in southeastern and southwestern Australia. Sci Riisgdrd HU, Thomassen S, Jakobsen H, Meeks JM, Larsen Mar 56:217-227 PS (1993) Suspension-feeding in marine sponges HaB- Wells FE (1978) A quantitative examination of the benthic chondria panicea and Halichondria urceolis: effects of molluscs of Cockburn Sound, Western Australia. Western ttmperature on filtration rate and energy cost of pumping. Australian Museum, Perth Mar Ecol Prog Ser 96:177-188 Wells FE, Threlfall TJ (1980) A survey of the softbottom mol- Riisg6rd HU, Vedel A, Boyle H, Larsen PS (1992) Filter-net luscs of Cockburn Sound, Western Australia. Veliger 23: structure and pumping activity in the polychaete Nereis 131-140 diversicolor effects of temperature and pump-modelling. Wells FE, Walker DI, Hutchings PA (1991) Seagrass, sediment Mar Ecol Prog Ser 83:79-89 and infauna - a comparison of Posidonia australis, Posi- Robbins IJ (1983) The effects of body size, temperature, and donia sinuosa, and Amphibobs anfarctica. 111. Conse- suspension density on the filtration and ingestion of inor- quences of seagrass loss. In: Wells FE. Walker DI, Kirkman ganic particulate suspensions by ascidians. J Exp Mar Biol H, Lethbridge R (eds) The marine flora and fauna of Al- Ec01 70:65-78 bany, Vol2. Proc 3rd Int Mar Biol Workshop. Western Aus- Rutman J. Fishelson L (1969) Food composition and feeding tralian Museum, Perth, p 635-640 behavior of shallow-water crinoids at Eilat (Red Sea). Mar Widdows J. Bayne BL (1971) Temperature acclimation of My- Biol 3:46-57 tilus edulis with reference to its energy budget. J Mar Biol Seiderer W, Newel1 RC (1985) Relative significance of phyto- ASS UK 51:827-843 , bacteria and plant detritus as carbon and nitro- Wilson BR, Kendrick GW, Brearley A (1978) The benthjc flora gen resources for the kelp bed filter-feeder Choromytilus of Cockburn Sound, Western Australia. Part 1 Proso- meridionalis. Mar Ecol Prog Ser 223127-139 branch gastropods and bivalve molluscs. Report to the Seiderer LJ, Newel1 RC (1988) Exploitation of phytoplankton Department of Conservation and Environment by the as a food resource by the kelp bed ascid~anPyura stolo- Western Australian Museum, Perth nifera. Mar Ecol Prog Ser 50:107-115 Wilson RS, Cohen BF, Poore GCB (1993) The role of suspen- Shumway SE, Bogdanowicz C, Dean D (1988) Oxygen con- sion-feedi.ng and deposit-feeding benthic macroinverte- sumption and feeding rates of the sabellid polychaete, brates 1.n nutrient cycling in Port Ph~llipBay. Technical Myxicola jnfundibulum (Renier). Comp Biochem Physiol Report No. 10. CSIRO Institute of Natural Resources and 9OA(3):425-428 Environment, Port Phillip Bay Environment Study, Mel- Sllberstein K, Chiffings AW, McComb AJ (1986) The loss of bourne seagrass in Cockburn Sound, Western Australia. IIJ. The Winter JE (1969) On the influence of food concentration and effects ot epiphytes on productivity of Posidonla australis other factors on filtration fates and food utilization in the Hook. F. Aquat Bot 24:355-371 mussels Arctica lslandica and Modiolus modlolus. Mar Simpson CJ, Butt JS, Cary JL, D'Adamo ND, Masini RJ. Mllls Biol 437-135 DA (1993) Southern Metropolitan Coastal Waters Study Winter JE (1973) The filtrat~onrate of Mytilus edulis and its de- 1991-94. Environmental Protection Authority, Perth pendence on algal concentration, measured by a continu- Steedman RK, Craig PD (1983) Wind-driven circulation of ous automatic recording apparatus. Mar Biol22:317-328 Cockburn Sound. Aust J Mar Freshwat Res 34:187-212 Winter JE (1978) A review on the knowledge of suspension- Stuart V (1982) Absorbed ration, respiratory costs and resul- feeding IJI lamelhbranchate bivalves, with special reference tant scope for growth in the mussel Aulacomya ater to artificial aquaculture systems. Aquaculture 13:1-33

This article was submitted to the edltor Manuscript first received: January 23, 1996 Revised verslon accepted: August 16, 1996