Annual primary production and nutrient dynamics of the seagrasses Posidonia sinuosa and Posidonia australis in south-western Australia

Aquatic botany ELSEVIER

Aquatic Botany 59 (1997) 277-295

Annual primary production and nutrient dynamics of the seagrasses Posidonia sinuosa and Posidonia australis in south-western Australia Marion L. Cambridge a,c,*, Peter J. Hocking b,c Department of Plant Ecology and Eeolutionarv Biology Utrecht Unit,ersit3,, P.O. Box 800-84. 3508 TB Utrecht, Netherlands b CSIRO Division of Plant lndusto,. G.P.O. Box 1600, Canberra, ACT 2601. Australia c Department of Botany, Unieersi~ of Western Australia. Nedlands 6907, Australia

Accepted 13 June 1997

Abstract Above-ground primary production and nutrient fluxes (N and P) were investigated for two species of seagrass, Posidonia sinuosa Cambridge et Kuo and P. australis Hook. f. from Warnbro and Cockburn Sounds over an annual cycle, at sites ranging in depth from 0.5-10 m where P. sinuosa formed either single-species stands or co-occurred with P. australis. Annual leaf primary production ranged from 600 to 900 g m -2 yr i in P. sinuosa and 900-1100 g m -2 yr - t in P. australis, and epiphytes on the leaves produced 130-160 g m - 2 yr i. In some patches, flowering shoots and fruits also made a substantial contribution, up to 160 g m 2 y r - ~. Annual above-ground productivity (dry weight production per unit ground area) of Posidonia spp. (600-1300 g m 2 y r - i) is similar to that of Amphibolis antarctica (Labill.) Sonder et Aschers. ex Aschers. and A. griffithii (Black) den Hartog, two species from the other genus of large seagrasses in south-western Australia, but only 30 to 50% of that of the kelp Ecklonia radiata (C. Ag.) J. Agardh. (3500 g m -2 y r - i ) . Nitrogen and phosphorus incorporated annually into new leaf tissue ranged from 9-17 g N and 1.1-1.7 g P m -2 yr ~, respectively, depending on species and site. Estimates of annual nutrient losses via leaf detritus ranged from 5 - 9 g N and 0.4-0.7 g P m - 2 y r - i, compared to maximum losses of 1.2 g N and 0.4 g P m 2 y r - t via the fruits at the highest density of flowering shoots (223 m-2). Thus, annual nutrient losses via leaf detritus represent a considerable proportion of the nutrients incorporated annually into new growth, indicating a lower degree of

* Corresponding author. m.cambridge @boev.biol.ruu.nl

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0304-3770/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S 0 3 0 4 - 3 7 7 0 ( 9 7 ) 0 0 0 6 2 - 4

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M.L. Cambridge, P.J. Hocking~Aquatic Botany 59 (1997)277-295

nutrient conservation than might be expected in a low nutrient environment. © 1997 Elsevier Science B.V. Keywords: Nutrient incorporation; Nitrogen; Phosphorus

1. Introduction

Seagrass and macroalgal communities play a major role in the marine ecology of south-western Australia, where concentrations of nutrients are in the lower range reported for temperate coastal waters (Johannes et al., 1994). Because nutrient levels are so low, phytoplankton populations are also generally low. Higher trophic levels, which include important fisheries species such as rock lobster, depend directly on benthic primary production from seagrasses and algae via detrital food webs (Robertson and Lenanton, 1984). This contrasts with middle latitude waters off the west coasts of other continents which are characterized by upwelling, with high-nutrient waters and large phytoplankton-based food chains (e.g., Barber and Smith, 1981). An unusual combination of features results in the low nutrient regime. A warm current, the Leeuwin Current (Cresswell and Golding, 1980), carries low-nutrient tropical water southwards. Transport of dissolved nutrients into the coastal waters from surface runoff is also low, as the coastal region consists predominantly of calcareous and siliceous sands or rock, rivers are few and only flow briefly in winter, and evaporation rates exceed precipitation. However, despite the low nutrient levels, values reported for macrophyte biomasses and productivities are high (Kirkman, 1984). Seagrass meadows occupy extensive areas of sand substrata on the south-west Australian coast wherever there is some shelter from the force of ocean swell waves. Macroalgal communities dominated by large brown algae, particularly the kelp E. radiata (C. Ag.) J. Agardh., are found on adjacent limestone reefs. The seagrasses P. sinuosa Cambridge et Kuo and P. australis Hook. f. form broad sub-tidal meadows in two embayments, Cockburn and Warnbro Sounds (Cambridge and McComb, 1984) but there are no detailed production or nutrient data over an annual cycle published for the predominant embayment species, P. sinuosa. For the co-occurring P. australis, there are seasonal productivity data from regions with different climates, from eastern Australia (Kirkman and Reid, 1979; Larkum, 1976; West and Larkum, 1979; West, 1990) and tropical western Australia (Walker and McComb, 1988). Distribution and peak (summer) standing crops of seagrasses, which include P. sinuosa and P. australis, have been reported for three areas in Western Australia (Cockburn and Warnbro Sounds, Shark Bay and Princess Royal Harbour; Cambridge and McComb, 1984; Cambridge et al., 1986; Walker and McComb, 1988; Walker et al., 1991; Wells et al., 1991). The accumulation of dry matter and nutrients by seeds, and the growth and nutrition of seedlings have been analyzed for P. australis and P. sinuosa from Warnbro Sound (Hocking et al., 1980, 1981). Seagrasses are frequently claimed to be among the most productive of aquatic ecosystems (Hillman et al., 1989). In this paper, these claims are examined for P. sinuosa and P. australis from a warm temperate environment by measuring their annual above-ground biomass production and nutrient pools, at sites spanning the depth range

M.L. Cambridge, P,J. Hocking~Aquatic Botany 59 (1997) 277-295

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of the meadows, from 0.5 to 10 m. Leaf and epiphyte biomass, leaf productivity and losses were measured monthly over an annual cycle. With these data, the contributions of both species to above-ground primary production and nutrient flux were then compared to productivity data from other major primary producers in the nearshore region, the large seagrasses, Amphibolis spp. (Walker and McComb, 1988) and the kelp E. radiata (Kirkman, 1984).

2. Methods

2.1. The stu@ sites The study sites, Cockburn and Warnbro Sounds, are semi-enclosed bays on the West Australian coast near Perth (32°S, I15°E). Cockburn Sound underwent a period of industrial and port development during 1960-1970, with subsequent massive loss of seagrass communities (Cambridge and McComb, 1984; Cambridge et al., 1986). P. sinuosa formed extensive uniform meadows from 0.5-10 m depth, which have been largely lost from Cockburn Sound. P. australis was present in a few areas as single species stands, and more commonly as one of a mixture of species in wave-disturbed areas together with the larger seagrasses, A. antarctica (Labill.) Sonder et Aschers. ex Aschers. and A. griffithii (Black) den Hartog, or the smaller species, Heterozostera tasmanica (Martens ex Aschers.) den Hartog, Halophila oL'alis (R. Br.) Hook. and Syringodium isoetifolium (Aschers.) Dandy. Warnbro Sound has remained relatively undisturbed and the seagrass meadows are still intact, including those in the adjacent Shoalwater Bay. The seagrass meadows occur on sand platforms with the greatest area present on gentle slopes (sometimes several kilometers wide) from 0.5-5 m depth, bordered by a narrow steep slope to the basin floor of each Sound some 20 m deep. One site was selected for this study at the deepest limit of Posidonia at 10 m on the steep slope; all other sites were selected from various habitats on the sand platforms between 0.5 and 4 m depth. Sites have been identified for convenience by their depths but were the same sites as six of those in Cambridge and McComb (1984), as indicated in Table 1. These included pure stands of P. sinuosa in different habitats (sites at 1, 3.5 and 4 m), species mosaics of P. sinuosa and P. australis (0.5 and 2.5 m), and the shallowest (0.5 m) and deepest (10 m) limits of the Posidonia meadows in Warnbro Sound. The waters of the study areas are derived from continental shelf waters of tropical and subtropical origin, and have rather constant salinity (35.8 g 1-~), low levels of nutrients and chlorophyll, and subtropical temperatures (15-23°C) (Jeffrey, 1981; Johannes et al., 1994). The warm Leeuwin Current carries low nutrient tropical water south in a narrow stream some 30-100 km wide along the edge of the continental shelf, flowing most strongly from April to October, particularly in winter (Cresswell and Golding, 1980). Water movement is dominated by wave action from ocean swell and strong onshore winds. The tidal range is very small, ca. 30 cm and there is only one tide per day. Water levels are often more influenced by barometric pressure than by tides, and with the high pressure anticyclonic weather systems which predominate in summer, water levels in summer are about 1 m lower than in winter. The wind and wave-driven exchange of water between the bays and the ocean is restricted by islands and sandbanks

280

M.L. Cambridge, P.J. Hocking~Aquatic Botany 59 (1997) 277-295

Table 1 Characteristics of sampling sites, including species present and shoot densities of Posidonia species Depth Species sampled Shoot density Habitat characteristics (shoots m -2 ) 0.5 m P. sinuosa P. australis

1.0 m P. sinuosa

2.5 m P. sinuosa P. australis

1857 827

408

1124 604

3.5 m P. sinuosa

883

4.0 m P. sinuosa

956

10.0 m P. sinuosa

142

Shoaling sandbank in Warnbro Sound with species mosaic of Posidonia and Amphibolis, subject to scorching at low water in summer and to on-shore winds at all times. (Site 3a) Dense meadow in Cockburn Sound predominantly P. sinuosa, a few small patches of P. australia', fine detritus-rich sediment in contrast to the coarser calcareous sand at other sites, sheltered from all winds and waves except northerly gales. (Site 7 a) Species mosaic of Posidonia, Amphibolis, Heterozostera and Halophila in Warnbro Sound, protected from full force of westerly ocean waves but subject to moderate disturbance by refracted ocean swell and strong onshore summer winds. (Site 2 a) Monospecific meadow on narrow sloping sand bank in Cockburn Sound. Sheltered from prevailing onshore (SW) winds but exposed to northerly gales. (Site 5a) Dense, monospecific meadow in Shoalwater Bay, open to refracted ocean swell. (Site 4 a) Warnbro Sound, lower limit of Posidonia meadow, predominantly sparse P. sinuosa with occasional patches of P. australis, fine silty substrate. (Site 1a)

aCorresponding site numbers in the paper of Cambridge and McComb, 1984.

( S t e e d m a n and Craig, 1983), so that there is some modification of open ocean conditions and in the case o f C o c k b u r n Sound, the addition of industrial effluents has led to increased levels of nutrients and p h y t o p l a n k t o n (Chiffings and M c C o m b , 1981). The coastline consists of Pleistocene and H o l o c e n e limestones and sand-dunes, with very little freshwater influence in the form of river run-off, although inflow of nutrient-enriched g r o u n d water in the nearshore can be locally important (Johannes, 1980; Johannes and H e a m , 1985). The waters are usually unstratified but on shallow sand banks in calm weather, more extreme temperatures m a y occur, up to 30°C on a few s u m m e r days. Day lengths vary from ca. 10 to 15 h. The s u m m e r s have a very high n u m b e r of sunlight hours (an average of 13 h per day in January), in contrast to the winters w h e n the passage of low pressure systems and a c c o m p a n y i n g storms result in of a c o m b i n a t i o n of cloud cover and w a v e - i n d u c e d turbidity.

2.2. M e a s u r e m e n t o f standing crop a n d l e a f p r o d u c t i o n

Six p e r m a n e n t l y m a r k e d sites were harvested by S C U B A diving each m o n t h for 18 months. Shoot densities were estimated once at each site by excavating 0.1 m 2 quadrats

M.L. Cambridge, P.J. Hocking/Aquatic: Botany 59 (1997)277-295

28I

in the form of tufts with a diver hammering a sharpened tool through the fibrous rhizome mesh. All shoots were harvested within 15-30 contiguous 0.1 m 2 quadrats forming a transect adjacent to the site marker. When more than one species of Posidonia was present, shoot density was sampled by a line of adjoining quadrats running through a pure stand of each species. The number of samples required was estimated (after West, 1990) from the number of replicates at which the standard deviation of the cumulative mean stabilized (between 10 and 16 quadrats, depending on the site). Leaf production was measured by the method of Zieman (1974) as described by Cambridge and McComb (1984). All leaves on 20-40 shoots were marked at ground level and the complete shoots were harvested one month later, cleaned of epiphytes and separated into new growth (consisting of new leaves and the part of the older leaves below the mark), and older tissue (from the punched hole to the leaf tip), then dried to constant weight at 70°C. Leaf production (g dw m 2 day- ~) was calculated by dividing the amount of new growth per shoot by the number of days between marking and harvesting, times shoot density. Leaf biomass (g dw m -2) was calculated by combining the leaf growth plus the remainder (dry weight per shoot times shoot density). Leaf losses (g dw m 2 day ~) were calculated from the leaf growth each month minus the difference in above-ground biomass between the beginning and end of the same sampling interval. The turnover rate of the leaf canopy (% day-~ ) was calculated from the daily leaf production divided by the leaf biomass. This gives a measure of the relative efficiency of plants in producing new leaf material and its reciprocal gives the number of days for replacement of the leaf canopy biomass. Seagrasses were sampled from stable stands, so that annual leaf losses were assumed to be equal to annual leaf production. Although this study was directed primarily at above-ground production, observations were also made on rhizomes excavated during the sampling program. In addition, a random sample of 20-40 complete shoots was collected each month within a 3-m radius around the marked plot. Standing crop (here leaf biomass) was estimated from the mean dry weight of the leaves per shoot and the shoot density. Epiphytic algal biomass on the leaves was measured as described by Silberstein et al. (1986) and annual epiphyte production rates (g dw m-2 y r - i ) estimated from the epiphyte biomass divided by the specific growth rate of leaves each month. Nitrogen (N) and phosphorus (P) concentrations (mg g--~ dw) were determined separately for bulked samples of new growth and older leaf tissue from the growth measurements above, using the methods outlined by Hocking et al. (1981). The average nutrient content of the leaf canopy (N and P pools: g m 2 ground area) was calculated from the N and P concentrations of both fractions, multiplied by the dry weight of leaf tissue from the leaf growth estimates each month. The daily incorporation of N and P into new leaf tissue was calculated from N and P concentrations in newly-grown leaf tissue (less than 1 month old) multiplied by the leaf growth rate (g dw m 2 day ~). Annual nutrient losses were derived from the decrease in concentration of N and P in senesced vs. young leaf tissue (35% and 44%, respectively, after Hocking et al., 1981) and the annual leaf losses. Resorption via internal recycling was calculated from the balance between nutrients incorporated into new growth and nutrient losses, assuming leaching and loss of dry weight during senescence to be negligible.

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M.L. Cambridge, P.J. Hocking~Aquatic Botany 59 (1997) 277-295

The density of flowering shoots and fruits of P. sinuosa and P. australis was sampled once in late October just prior to fruit shedding across a sloping sand bank some 3 km wide in Warnbro Sound over a depth gradient from 0.5-8 m, traversing a mixture of seagrass communities. Five 1-m 2 quadrats were sampled every 75 m. Fruits and stems were separated, counted and dry weighed as above after briefly dipping the stems in 2% HCI to remove calcareous epibiota. The N and P cost of fruit production per unit area of seagrass meadow was calculated from dry weights of fruits, and nutrient concentrations from Hocking et al. (1980). The data were statistically analyzed using the General Linear Models procedure for analysis of variance (SAS, 1988) to test for differences in leaf biomass, leaf production, N and P pools and N and P incorporation between sites and season. If differences were found to be significant ( P < 0.05), the rank order was determined using Tukey's Studentized Range. For the two sites where both species were present, differences between species at the same site were tested using two-tailed t-tests.

3. Results 3.1. Biomass and nutrient content of the leaf canopy

Mean leaf biomass averaged over 1 year for P. sinuosa was similar at the sites 0.5-4 m, ranging from 140-190 g m -2 but at 10 m, the value was significantly lower (Fig. la). There was no significant difference in the biomass between the species at sites where both occurred, despite differences in the density of shoots (Table 1). The average nutrient contents of the leaf canopy (N and P pools: g m -2 ground area) were similar for sites 0.5-4 m, ranging from 2.2-3.0 g N m -2 and 0.2-0.3 g P m -2, but much lower at the 10-m site (Fig. lb and c). When the two species co-occurred, N and P values of P. australis were not significantly different from those of P. sinuosa. 3.2. Shoot densities

Shoot densities for P. sinuosa were about 1000 shoots m -2 at the mid-depth sites, 2.5-4 m (Table 1). At the shallowest site (0.5 m), densities were higher with about 2000 shoots m -2, but were very low at the deepest site (10 m) with 142 shoots m -2. Densities of P. australis were approximately half those of P. sinuosa at sites where the species co-occurred. Shoot densities were assumed to be constant over the 18 months sampling program, as a new shoot is only produced infrequently at intervals of up to several years at the apex of the rhizome (Kuo and Cambridge, 1978). Although this may not be the case for a rapidly expanding patch colonizing new substratum, these areas were not chosen and sampling was confined to established meadows. 3.3. Seasonal variation in above-ground biomass and nutrients

Both leaves and algal epiphytes contribute to the above-ground biomass in a seagrass meadow, with maxima usually occurring in summer (for example, P. sinuosa at 4 m and

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both species at 2.5 m), but there were considerable differences in the patterns between sites (Fig. 2). There was no significant difference between sites for either mean summer or winter leaf biomass of P. s i n u o s a (with the exception of the lO-m site), or between the two species where they co-occurred (Table 2). For P. s i n u o s a the mean s p r i n g summer leaf biomass was significantly higher than in winter (Table 2). Biomass of epiphytic algae was highest at the shallowest sites (0.5 and 1 m) and at most sites in summer when the leaf biomass was highest (Fig. 2). Values for individual months could be highly variable (e.g., 10-350 g m -2 at 1 m) in part due to the seasonality of the algal

284

M.L. Cambridge, P.J. Hocking/Aquatic Botany 59 (1997) 277-295

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300 200

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400

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and epiphyte biomass (light shading) of P. sinuosa at 0 . 5 - 1 0

species, which included encrusting calcareous algae, filamentous red, brown, green and blue-green algae, and colonial diatoms. At 1 m, an unusually high value of 350 g dw m -2 was recorded during a blue-green algal bloom, compared to maxima of 70-150 g m -2 at other sites. Concentrations of leaf nutrients were generally low and similar at all sites, ranging from 1-2% of dry weight for N and 0.15-0.3% for P (Fig. 3). There was no consistent seasonal pattern for N, whereas, P concentrations tended to be higher in winter and spring and lowest in summer at the time of peak growth (data not shown). Young leaf tissue which had grown during the sampling interval had 20-30% higher concentrations of P than older leaf material, whereas N concentrations were similar in the young and older leaf material. Nitrogen and phosphorus content of the leaf canopy (N and P pools: g N and P m -2 ground area) were significantly different between sites (Table 2). Phosphorus content followed the same seasonal trends as leaf biomass, being significantly higher in spring-early summer than in winter, whereas the N content showed no difference between summer and winter (Table 2).

M.L. Cambridge, P.J. Hocking/Aquatic Botany 59 (1997) 277-295

285

Table 2 Summary of two-way A N O V A results with productivity and nutrient economy parameters of P. sinuosa and P. australis as the dependent parameters, and site and season ( s p r i n g - s u m m e r vs. a u t u m n - w i n t e r ) as the independent parameters Site P P P P P P

Leaf productivity c ( FI5.37 = 12.9)" Leaf biomass ~ ( F I 5 , 3 6 = 6.37) Leaf N content d (FI~,~ o = 4.09) Leaf P content J (Fi5,47 = 6.31) N incorporated in new leaf growth d (FI5,36 = 5.76) P incorporated in new leaf growth d (FI5,2 s = 7.31)

< < < < < <

0.001 0.001 0.001 0.001 0.001 0.001

Season

Interaction

P < P < NS P < P < P <

P < 0.001 NS NS NS NS NS

0.001 0.002 0.001 0.001 0.001

"F values of the overall ANOVA. bNS = not significant. ~Summer vs. winter. d • Spring-early summer vs. a u t u m n - e a r l y winter.

3.4. Lec~f production Annual leaf production of P. sinuosa was similar for sites from 0.5-4 m but much lower at the deepest (10 m) site (Fig. 4a), resulting in significant differences between sites (Table 2). Leaf growth in both species continued throughout the year, with mean

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Depth (m) Fig. 4. (a) Annual leaf productivity+ s.e. of P. sinuosa at 0.5-10 m sites, P. australis at 0.5 and 2.5 m sites, (b) total nitrogen and (c) total phosphorus incorporated annually into new leaf tissue + s.e. This total is made up of two components, nutrients resorbed from senescing leaf tissue ( • ) , and nutrients lost as leaf detritus ([]), which must be replaced by uptake from the environment if the stand is in steady-state. Where overall differences were significant ( P < 0.05), significant differences between sites are indicated by different letters.

growth rates in summer being significantly higher than in winter (2-3 g dw m -2 day- 1 compared to ca. 1 g dw m -2 day-1, respectively). At 10 m, no growth was recorded from February onwards, as sea urchin grazing had removed all seagrass in late January and there was no regrowth in the remaining months of the study. When the two species co-occurred, productivity of P. australis was consistently higher than that of P. sinuosa in spring and summer (shown for 2.5-m site in Fig. 5a), leading to higher annual mean rates of leaf production. Despite the similarity in annual production, a strong interaction term for site * season, P < 0.001 (Table 2), indicates different effects of season on leaf productivity between sites. For example, P. australis at the 0.5-m site had exceptionally high growth rates (7.4 g m -2 d a y - 1) but they were of short duration and only occurred after the leaf canopy had been almost completely removed by scorching in summer. Turnover rates for the leaf canopy averaged over an annual cycle ranged from 1-1.5%

M.L. Cambridge, P.J. Hocking/Aquatic Botany 59 (1997) 277-295

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day -l (equivalent to 70-100 days for complete replacement of the canopy) for P. sinuosa and 1.5-1.9% day -1 (57-70 days) for P. australis (Table 3). The highest monthly rates were recorded at the shallowest site after defoliation by scorching had occurred (both species, 2.4% day-l). Leaf losses occurred throughout the year, but were usually lowest during spring and highest in late summer, when whole leaves were shed forming floating wracks. Losses were also high in winter at sites exposed to winter waves (e.g., 2.5 and 4 m). 3.5. Nutrients

Nitrogen and phosphorus incorporated annually into new leaf tissue ranged from 9-17gNm -2 yr ~ and 1 . 1 - 1 . 7 g P m -2 yr -I (Fig. 4 b a n d c ) . At 10re, rates were much lower (1 g N m -2 yr- l and 0.2 g P m - 2 yr- l) due to the sparse seagrass and low

M.L. Cambridge, P.J. Hocking~Aquatic Botany 59 (1997) 277-295

288

Table 3 Algal epiphyte production (g dw m -2 yr - t ) at various sites for P. sinuosa and P. australis, calculated from the mean turnover rate of the leaf canopy (% day-J ) and mean epiphyte biomass (g dw m - 2 ). (Means and s.d.) Parameters

Sites 0.5 m

1m

2.5 m

3.5 m

4m

l0 m

1.1(5:0.1) -

1.2(+0.1)

Leaf turnover per day P. sinuosa 1.5(5:0.1) P. australis 1.8(5:0.1)

1.5(5:0.1) -

1.0(5:0.1) 1.5(+0.1)

1.2(5:0.1) -

Mean epiphyte biomass P. s i n u o s a 51(-t-14) P. australis 25(+4)

78(-t-15)

44(+14) 41(+ 11)

35(_+6)

-

-

-

11(5:2) -

Epiphyte production P. sinuosa 255(5:22) P. australis 160( _+64)

401(_+75) -

132(5:23) -

133(+23) -

50(5:2) -

158(5: 14) 211 ( _+20)

34(+5)

-

production rates. At the 1-m site, with a finer, more detritus-rich substratum and blue-green algal blooms in summer, values for N incorporation were highest (17 g N m -2 yr-1). Nutrient losses via leaf detritus (excluding the 10-m site) ranged from 5-11 g N m -2 yr -1 and 0.6-1.0 g P m - 2 yr -~, and resorption of nutrients from older tissue 3 - 6 g N m -2 yr -1 and 0.5-0.8 g P m -2 yr - l (Fig. 4b and c). On a seasonal basis, daily rates of nutrient incorporation (excluding the 10-m site) varied from a maximum of 4 0 - 8 0 mg N m -2 day -1 and 6 - 1 0 mg P m -2 day -1 during the peak growing season of spring-early summer, to a minimum of 10-20 mg N m -2 day - t and 1 - 2 mg P m -2 d a y - ~ in autumn-early winter (data shown only for 2.5-m site, both species, Fig. 5b and c). 3.6. E p i p h y t e p r o d u c t i o n

Epiphyte production was similar for P. sinuosa at the 2 . 5 - 4 m sites ( 1 3 0 - 1 6 0 g dw m -2 y r - 1), but higher for P. australis at 2.5 m due the higher leaf turnover rates (Table Table 4 Density, dry weights and nutrients (means 5: s.d.) of flowering shoots and fruits, and N and P contents of mature fruits prior to shedding. N and P pools in fruits estimated from mean fruit densities measured in this study, and N and P concentrations of Posidonia spp. fruits from Hocking et al., 1980 Species and depth

P. sinuosa, 1 m (n = 4) P. sinuosa, 1.5 m (n = 6 ) P. australis, 1.5 m (n = 10) P. australis, 2 m (n = 1) P. sinuosa, 3 m ( n = 6 ) P. sinuosa, 8 m (n = 5) P. australis, 8 m (n = 4)

Flowering shoots

Fruits

Density (m -2 )

Stem dw (g m - 2 )

Density (m - 2 )

Dry wt. (g m - 2 )

N

P

(mg m - 2 )

(mg m - 2 )

223(5:41) 43(5:11) 56(5:11) 145 93(+14) 8( q- 4) 14(+2)

96(_+ 19) 16(5:4) 66(5:17) 56 40(-t-5) 3( -t- 1) 8 ( + 1)

678(5:74) 332(_+ 101) 434(+ 102) 333 326( _+37) 50(5:23) 65(5:11)

58(_+5) 31(5: 16) 65(5: 16) 27 18( 5: 2) 3 ( + 1) 6(+1)

1153 564 1172 899 554 91 108

291 143 435 193 140 23 38

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3). At the 0.5-m site, production rates for the two species differed due to consistently lower epiphyte biomasses on P. australis leaves (P. sinuosa with 225 g m 2 yr-L compared to 160 for P. australis). The highest production rate occurred at the 1-m site (400 g m-2 yr-~) where frequent algal blooms led to high epiphyte biomasses, although the algal biomasses may have been over-estimated because of the inclusion of filterfeeding animals (colonial ascidians and worms) in the samples. Epiphyte primary production was usually far lower than leaf production (600-1000 g dw m-2 yr-~; Table 3). 3.7. Flowering density, .fruit biomass and nutrient content The distribution of flowering shoots was very patchy, but their contribution to productivity and nutrient demand could be substantial (Table 4); for example, a maximum dry weight of 330 g m 2 (peduncle, flower remnants and mature fruits) was measured just prior to release of the fruits in one quadrat. Flower shoot densities ranged from 0-223 m - z , with a maximum of over 600 fruits recorded from one quadrat. The highest flower shoot densities occurred on shallow sand banks and areas of patchy seagrass and the lowest in extensive, pure stands of P. sinuosa. Estimates of the N and P incorporated in fruit ranged from 0.5-1.2 g N m -2 and 0.15-0.4 g P m -z, respectively. Development of the flowering shoots and fruits occurred over 7 months, with the first flower shoots emerging in April for P. australis and May for P. sinuosa. Anthesis began in July to early August (late winter) and continued over several weeks, followed by fruit and seed development, with the fruits being shed in November and early December (summer).

4. Discussion

4. I. Primary productit~ity The most extensive areas of seagrasses were present on gently sloping sand platforms edged by a steeper slope to a deep basin. In these circumstances, it is not so much depth as other habitat characteristics, such as exposure to wave action listed in Table 1, which could have affected parameters such as biomass and productivity. In fact, there were no significant differences in means except for one site (10 m) on the steep slope at the deepest extent of the seagrass (Figs. 1 and 4 and Table 2), despite habitat differences and the distances between sites (several kilometers). The mean values for leaf production and standing crop recorded here for Warnbro Sound (1-3 and 1-2 g m -2 day ~ for P. australis and for P. sinuosa, respectively) lie in the low to mid range for the larger temperate seagrasses, including those for P. australis from other sites in Australia, and P. oceanica (L.) Delile in the Mediterranean (see review in the paper of Hillman et al., 1989). However, shoot densities were considerably higher; ca. 1000 shoots per m 2 for P. sinuosa and ca. 600 for P. australis, compared to 80-400 for P. australis in south-eastern Australia (West and Larkum, 1979; West, 1990) and 400 for P. oceanica in the Mediterranean (Bay, 1984). The highest growth rates and standing crops in P.

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australis have been recorded by West and Larkum (1979) from Spencer Gulf (annual range of 2.7-5.5 g dw m -2 day -1, 444-616 g m-2), where seagrasses grew on terrigenous sediments and were very robust, with leaves almost twice the length and width of those from Warnbro Sound. Values for P. australis leaf production and standing crop at temperate sites in south-eastern Australia were generally lower (e.g., annual range of 1-5 g dw m -2 day -~ and 294-453 g m -2, respectively, at Jervis Bay; Kirkman and Reid, 1979 and 1-3 g dw m -2 day -~, 190-280 g m -2 at Botany Bay; West and Larkum, 1979). In our study, the highest daily rates for leaf production and turnover were found on a shoaling sandbank (0.5 m depth), where the leaf canopy had been scorched during a period of very low water levels combined with hot, sunny days. The duration of high growth rates and the area occupied by Posidonia in such conditions is very limited, so that it is misleading to use these temporary peaks induced by canopy removal for comparison with other studies. Seagrasses communities on southern Australian coasts form the dominant primary producers on sand substrata in areas which would otherwise be expanses of shifting sands; their counterparts on hard substrata are the large brown algae (mainly the kelp E. radiata) which dominate the adjacent reef systems in the region. Our study has shown that the net above-ground productivity of Posidonia spp. (500-1000 g dw m -2 yrfrom leaves and a further 130-250 g dw m -2 yr-~ from algal epiphytes) is moderate (30-50%) when compared to Ecklonia (Table 5). For example, Ecklonia at 5 m produced 3500 g dw m -2 yr-1 and 2000 at 10 m (Kirkman, 1984). Is the difference in above-ground productivity between Posidonia and Ecklonia due to the below-ground fraction in seagrasses? Seagrass meadows have a substantial underground biomass (e.g., above-ground to below-ground ratio 1:4 for P. australis; West and Larkum, 1979; Table 5 Annual above-ground productivity (g dw m -2 y r - ~) of seagrass species, and the brown alga, E. radiata

P. P. P. P. A.

sinuosa a australis a australis b australis c antarctica c

A. antarctica a A. griffithii d P. oceanica e Thalassia testudinum f Thalassia hemprichii g E. radiata h

Leaves

Fruits

Flower stems

Epiphytes

600-900 900-1100 930 940 3140 i 920-1580 850 840 1180 580-1022 3500

3-58 6-65

3-96 8-66

133-161 130

aThis study. bWest and Larkum, 1979. CWalker and McComb, 1988. d Walker (personal communication) Rottnest Is., W. Austr. eBay, 1984. fZieman, 1974. g Heijs, 1985. h Kirkman, 1984. iLeaves and stems included in estimate.

139-584

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Kirkman and Reid, 1979; 1:3 in the paper of Hocking et al., 1981) and underground productivity estimates range from 10-40% of leaf productivity (Hillman et al., 1989). However, the total productivity would still be less than that of Ecklonia suggesting some other limiting factor, the most likely being carbon (Beer and Koch, 1996), particularly in view of the 6C 13 values for leaf material from Warnbro Sound (approximately - 10%o, indicative of C limitation; Cambridge, unpublished data). In a system with a large detritus-based component, the timing of detritus input will be important. Periods of maximum growth and detritus losses in Posidonia are not synchronized, with growth continuing throughout the year but at a maximum in early summer. Detritus production is also continuous but peaks in late summer. Fruits are shed for a few weeks in early summer and the fleshy fruits break down in a few days as the seeds are released. Filamentous epiphytes also decompose rapidly, whereas Posidonia leaves break down slowly, requiring over 200 days to be reduced to particles < 2 mm (Walker and McComb, 1985), and entering a detrital cycle together with large brown algae in the nearshore and beach wrack deposits (Hansen, 1984; Robertson and Lenanton, 1984). In contrast to the leaves, the underground fraction of Posidonia appears to be largely stored after death, often forming layers of fibrous material, which may represent a long-term source of organic matter and nutrients (cf. Kenworthy and Thayer, 1984). 4.2. Nutrient losses

Nutrient losses via leaf shedding were considerable (5-11 g N and 0.6-1.0 g P m 2 yr-~), corresponding to 65% and 56% of the N and P, respectively, incorporated annually into new leaf growth. Although losses might be expected to be minimal in a low-nutrient environment, the rather short life span of the leaves (60-100 days) results instead in higher losses and will preclude rigorous nutrient conservation. However, a relatively high leaf turnover rate may be important in the maintenance of functional leaf tissue, because the leaves are continuously colonized by epiphytes which shade the distal portion of the leaf as they accumulate over time. Thus, leaves must always outgrow the epiphytes, with new tissue being produced fast enough from the base as the old, heavily colonized portion of the leaf breaks off or is shed in its entirety to make way for a new leaf. All nutrients are lost when the fruits are released but the amounts are minor in most areas where fruiting is often not very abundant compared to leaf losses. However, in areas with unusually high fruit densities such as the maxima recorded in Table 4, losses were estimated to be at most 1.2 g N and 0.4 g P m -2 yr -~, or approximately 10% and 40% of the maximum values for N and P, respectively, lost annually via leaf shedding. 4.3. Nutrient incorporation

Amounts of N and P incorporated annually into new leaf tissue from Cockburn and Wambro Sounds were similar to those reported for P. australis in Shark Bay (10 vs. 9 g N m -2 yr -1 and 1.5 vs. 1.3 g P m 2 yr ~, respectively, cf. Walker and McComb, 1988). The daily requirement of N for leaf growth (seasonal range 20-80 mg N m -2

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day- 1 ) is similar to measurements for a few tropical seagrasses but much lower than the summer maxima of 200-450 mg N m -2 day-1 recorded for Zostera marina (Moriarty and Boon, 1989). Nutrient incorporation into the fruits (up to 1.2 g N m -2 and 0.4 g P m -2) mainly occurred some 4 - 1 0 weeks after anthesis, in September and October (Hocking et al., 1980), which corresponded at some sites with low leaf growth rates, reduced N:P ratio, and leaf shedding followed by a flush of new leaves (Cambridge, unpublished data), suggesting a degree of nutrient redistribution. 4.4. Sources of nutrients incorporated into new growth

Since a substantial portion of the N and P pool in the leaves is lost annually, these losses must be replaced by uptake from the environment to maintain the same amount of N in the standing crop. The remaining balance of the nutrients incorporated into new growth is derived from nutrient retrieval in senescing tissue. Hocking et al. (1981) showed that senesced leaf tissue has approximately 35% less N and 44% less P than young leaf tissue in P. australis on a dry weight basis. This indicates a moderate resorption efficiency when compared to average values for over 200 species of 50% N and 52% P (Aerts, 1996), particularly as leaching may have contributed to the reduction in nutrient concentration during senescence. The proportions of the plant's N and P contained in the below-ground organs (roots, rhizomes and leaf bases) are also substantial (Hocking et al., 1981); for example, the below-ground living leaf bases in a 5-year old P. australis plant had over 25% of the plant's total P content. However, it is likely that considerable proportions of the below-ground stocks of N and P are not available for redistribution to above-ground organs, given the moderate differences in concentrations between mature and senescent organs (Hocking et al., 1981). Seagrasses have access to nutrients from both the water column and sediments (e.g., Hemminga et al., 1994; Erftemeijer and Middelburg, 1995). The Posidonia meadows in this study are established on calcareous sediments enriched with organic matter, rather than on terrigenous sediments. As the waters are oligotrophic, similar processes of nutrient cycling to those in tropical seagrasses could be expected (Short et al., 1990); i.e., major regenerative processes of nitrogen are similar to those in terrigenous sediments, but the P dynamics are very different due to sorption of phosphate ions by carbonates. Nutrient contents of a volume of substratum, corresponding to 1 m 2 sediment and 10 cm thick underlying a meadow, were estimated to be 60 g N (total acid digestible) and 2 g P (McComb et al., 1981). Thus, the total nutrients in the sediment are more than enough for growth over a year, but they will not necessarily be available, as much will be in the form of very slowly decaying organic matter. Nutrients in the water column are in the low range for temperate coastal waters. Johannes et al. (1994) found mean nitrate concentrations in winter (1.6 /zM) 3 times higher than in summer, whereas inorganic phosphate peaked in summer (1.0 /zM) at roughly twice the mean winter concentration. Pearce et al. (1985) found similar concentrations, with inorganic N averaging 20 /zg 1-~ (1.3 /zM). However, organic N is much higher, up to 95% of the total N (Paling, 1991), which probably accounts for the 20-fold higher values for total N quoted in Hocking et al. (1981), over seagrass in Warnbro Sound: 400 /xg N 1-1 and 25 /xg P 1-1 in spring, which dropped to 100 /zg N

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1 i and l 0 / x g P 1-1 in summer. In a 3-year study in waters over seagrass meadows and kelp stands off the coast of Perth, Johannes et al. (1994) found evidence for uptake of nutrients from the water column by seagrass and kelp stands. There was a trend of increasing nitrate concentration with depth: in a well mixed water column, the shallower the water the greater will be the reduction in nitrate concentration due to benthic uptake. Nitrate concentrations over seagrass were also higher than over kelp communities at comparable depth, suggesting that the seagrass communities removed less nitrate per unit area than the kelp communities. This would be expected if the seagrasses were not only less productive per unit area than the kelps, but also obtained a significant portion of their nutrients from the sediments through their roots.

5. Conclusions Posidonia meadows form a source of moderate above-ground primary production but maintain a substantial standing crop over the whole year. They produce less above-ground biomass per unit area than major macroalgal primary producers in the region but occupy extensive sand habitats unsuitable for macroalgat colonization. Despite habitat differences, there was little difference in mean biomass and productivity between the shallow and mid-depth sites (0.5-4 m), suggesting that factors associated with depth, density or substratum had limited influence on productivity. Only the deepest boundary of the meadow where the seagrass was growing at its lower limit showed consistent differences because of the low shoot density. The productivity (but not biomass) of P. australis was significantly higher than P. sinuosa when they co-occurred. Leaf detritus makes the largest contribution to nutrients entering the system from the Posidonia species on an annual basis, despite the low nutrient content of senescent leaves. The relatively high leaf turnover rates probably preclude highly efficient nutrient conservation. Shedding of large numbers of the fruits contributes to a brief peak of nutrients entering the system in early summer, but is minor compared to the leaf detritus on an annual timescale.

Acknowledgements We thank W. Aeschlimann, D.V. Koontz, M.J. Thompson and A.H. van der Wiele for help in field collections and sorting samples. R. Aerts, H. Lambers, M. van Oorschot and D.I. Walker made helpful comments on an earlier draft. D. Raaimakers assisted with the statistical analyses. Logistical support for field work was provided by the Western Australian Department of Conservation and Environment.

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McComb, A.J., Cambridge, M.L., Kirkman, H., Kuo, J., 1981. The biology of Australian seagrasses, in: Pate, J.S., McComb, A.J. (Eds.), The Biology of Australian Plants. University of Western Australia Press, Perth. Moriarty, D.J.W., Boon, P.I., 1989. Interactions of seagrasses with sediments and water, in: Larkum, W.D., McComb, A.J., Shepherd, S.A. (Eds.), Biology of Seagrasses. A Treatise on the Biology of Seagrasses with Special Reference to the Australian Region. Elsevier, Amsterdam, pp. 500-535. Paling, E., 1991. The relationship of nitrogen cycling and productivity in macroalgal stands and seagrass meadows. PhD Thesis (unpubl.), University of Western Australia, 314 pp. Pearce, A.F., Johannes, R.E., Manning, C.R., Rimmer, D.W., Smith, D.F., 1985. Hydrology and nutrient data off Marmion, Perth, 1979-1982. Report 167. CSIRO Marine Laboratories, Western Australia. Robertson, A.I., Lenanton, R.C.J., 1984. Fish community structure and food chain dynamics in the surf zone of sandy beaches: The role of detached macrophyte detritus. J. Exp. Mar. Biol. 84, 265-283. SAS, 1988. User's Guide: Statistics, 6.03 edn. SAS Institute, Cary, NC. Short, F.T., Dennison, W.C., Capone, D.G., 1990. Phosphorous limited growth of the tropical seagrass Syringodiumfiliforme in carbonate sediments. Mar. Ecol. Prog. Ser. 62, 169-174. Silberstein, K., Chiffings, A.W., McComb, A.J., 1986. The loss of seagrasses in Cockburn Sound, Western Australia: Ilk The effect of epiphytes on productivity of Posidonia a,stralis Hook. f. Aquat. Bot. 24. 355-371. Steedman, R.K., Craig, P.D., 1983. Wind driven circulation of Cockburn Sound. Aust. J. Mar. Fresh. Res. 34, 187-212. Walker, D.I., McComb, A.J., 1985. Decomposition of leaves from Amphibolis antarctica (Labill.) Sonder et Aschers. and Posidonia australis Hook. f., the major seagrass species in Shark Bay, Western Australia. Bot. Mar. 28, 407-413. Walker, D.I., McComb, A.J., 1988. Seasonal variation in the production, biomass and nutrient status of Amphibolis antarctica (Labill.) Sonder ex Aschers. and Posidonia australis Hook. f. in Shark Bay, Western Australia. Aquat. Bot. 31,259-275. Walker, D.I., Hutchings, P.A., Wells, F.E., 1991. Seagrass, sediment and infauna--a comparison of Posidonia australis, P. sinuosa and Arnphibolis antarctica in Princess Royal Harbour, south-western Australia: I. Seagrass biomass, productivity and contribution to sediments, in: Wells, F.E., Walker, D.I., Kirkman. H., Lethbridge, R. (Eds.), The Marine Flora and Fauna of Albany, Western Australia. Proc. Third Int. Marine Biological Workshop, Vol. 2. Western Australian Museum, Perth, pp. 597-610. Wells, F.E., Walker, D.I., Hutchings, P.A., 1991. Seagrass, sediment and inthuna--a comparison of Posidonia at~stralis, P. sinuosa and Amphibolis antarctica in Princess Royal Harbour, south-western Australia: III. Consequences of seagrass loss. in: Wells, F.E., Walker, D.I., Kirkman, H., Lethbridge, R. (Eds.), The Marine Flora and Fauna of Albany, Western Australia. Proc. Third Int. Marine Biological Workshop, Vol. 2. Western Australian Museum, Perth, pp. 635-640. West, R.J., 1990. Depth-related structural and morphological variations in an Australian Posidonia seagrass bed. Aquat. Bot. 36, 153-166. West, R.J., Larkum, A.W.D., 1979. Leaf productivity of the seagrass Posidonia australis in eastern Australian waters. Aquat. Bot. 5, 57-65. Zieman, J.C., 1974. Methods for the study of the growth and production of turtle grass, Thalassia testudinum. Aquaculture 4, 139-143.