Canning Estuary, Western Australia

Aquatic botany ELSEVIER

Aquatic Botany51 (1995) 1-54

The distribution, biomass and primary production of the seagrass Halophila ovalis in the Swan/Canning Estuary, Western Australia K. Hillman 1 A.J. McComb 1, D.I. Walker * Department of Botany, Universityof WesternAustralia, Perth, W.A. 6009. Australia Accepted 15 February 1995

Abstract The seagrass Halophila ovalis (R.Br.) Hook f. is the dominant benthic plant of the Swan/Canning Estuary, southwestern Australia. This paper describes the biomass, distribution and primary production of this plant in relation to environmental factors. Halophila ovalis occupied 550-600 ha in the lower reaches of the estuary, approximately 20% of the area of the main estuarine basin. Over 99% of the seagrass was in water less than 2 m deep (relative to "datum", an extreme low water reference mark set in 1892). Distribution in the main estuarine basin differed little between 1976 and 1982, although the species was more ephemeral in the Canning Estuary. Uniform stands of Halophila ovalis reached a biomass of up to 120 g dry weight (DW) m -2 in late summer/early autumn, and maximum productivities of up to 40 g DW m - 2 day- t in summer. At peak biomass, the area of Halophila ovalis in the estuary represented approximately 350 t DW of plant material, 4200 kg of nitrogen and 630 kg of phosphorus. Average productivity was 500 g C m -2 year- ~, although uniform stands in shallow waters attained up to 1200 g C m -2 year- ]. The biomass, productivity and biometry of Halophila ovalis were strongly influenced by salinity, temperature and light supply. The main growing period was summer, when marine salinities prevailed, and light supply and temperature were highest. Salinity, temperature and light were lowest during winter. Field and laboratory studies indicated that during years of average river discharge ( 1980, 1982), Halophila oualis was little affected by the salinity range experienced (15-35%o). However, during 1981, a year of high discharge, conditions of low salinity and poor light supply caused severe declines in biomass, particularly in the Canning Estuary. Light was considered the more important factor controlling growth, since the waters of the estuary are generally turbid, and subject to sudden increases in turbidity. The effects of salinity, temperature and light were investigated by growing sprigs in artificial seawater culture and measuring growth increments. Each factor was investigated separately; salinity values ranged from 5 to 45%0, temperature from 10 to 25°C and light from 0 to * Correspondingauthor. Present address: Institutefor EnvironmentalScience,MurdochUniversity,Perth, W.A. 6150, Australia. 0304-3770/95/$09.50 © 1995 ElsevierScienceB.V. All rights reserved

SSDI0304-3770(95)00466-1

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K. Hillman et al./Aquatic Botany 51 (1995) 1-54

400 /zE m -2 s -~. Halophila ovalis grew actively at salinities from approximately 10 to 40%0. Saturating irradiance was approximately 200/.rE m-2 s- 1 ( 10% of surface PAR) and compensation point was approximately 40/zE m-2 s- 1 (2% of full sunlight PAR). Temperatures lower than 15°C severely limited productivity, and at 10°C no growth occurred, although plants did not die. Productivity increased from 15 to 20°C by a factor of seven, and a further 30% from 20 to 25°C. The highest observed growth rate, approximately 2.1 mg DW per apex day- 1, was reached at 25°C. These results were incorporated into a model to determine how much of the variance in productivity could be accounted for by these three factors, assuming independent action. The model was relatively successful at predicting seasonal growth responses, but underestimated spring productivity, probably because the unpredictable light climate in spring in the Swan River was not fully simulated. Keywords: Halophila ot,alis; Biomass; Distribution; Primaryproductivity;Nutrients; Modelling

1. Introduction The considerable amount of work carried out on seagrasses in the last 20 years reflects their importance as primary producers in shallow coastal areas and estuaries. There have, however, been few studies involving estuaries in mediterranean climates, which typically undergo marked seasonal changes in hydrology that might be expected to exclude seagrasses. The Swan/Canning Estuary, southwestern Australia (Fig. 1) is a typical example: freshwater discharge occurs only during the winter months, and the volume of discharge is largely determined by the time of onset, duration and intensity of the winter rainfall, which differ greatly from year to year. In terms ofphysico-chemical parameters the Swan/Canning

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biomass and productivityof Halophila ovalis.

K. Hillmanet al. /Aquatic Botany51 (1995)1-54

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Estuary has two distinct phases: a "winter" phase (June-August inclusive), with low temperatures (12-14°C) and salinities (less than 10%o), high turbidity and low light and a "summer" period (September-May inclusive), with high temperatures (22-24°C) and salinities (over 40%o), low turbidity and high light. The transition from summer to winter conditions often occurs rapidly, sometimes in less than 2 weeks (Spencer, 1956). Despite these abrupt and marked seasonal changes, the most prominent primary producer in the estuarine basin is the seagrass Halophila ovalis (R.Br.) Hook. f. Den Hartog (1970) notes that Halophila ovalis is capable of forming dense stands in very sheltered places, but rarely does so because when Halodule uninervis (Forssk.) Aschers. or Halodule pinifolia (Miki) den Hartog are present, they dominate the community. In the estuaries of southwestern Australia this competition does not arise because Halodule only extends as far south as latitude 29°S, whilst the characteristic extremes of local estuarine hydrology exclude the larger, more stenohaline species (Cambridge, 1980). At the commencement of this study Halophila ovalis was known to cover extensive areas of the shallow margins of the estuary, but its distribution had not been mapped nor its significance as a nutrient pool determined. The work described here began with the task of providing such information. In addition, seasonal and other than long-term changes in seagrass biomass were documented, and related to changes in physico-chemical parameters, so as to develop hypotheses about factors likely to be important in controlling distribution and biomass. 1.1. Productivity

Attention was next directed to measuring productivity. Seagrass meadows are amongst the most productive of submerged aquatic ecosystems and research in the last decade has extended the range of species for which primary production data are available (Hillman et al., 1989 and references cited therein). Most studies have been carried out on larger seagrasses, but some work has been published on small-leaved species of seagrasses (Pulich, 1982; Wahbeh, 1984; Herbert, 1986; Josselyn et al., 1986). The marking techniques used for measuring the primary production of large-leaved seagrasses (Zieman, 1975; Kirkman and Reid, 1979; Walker, 1985) are unsuitable for small, fragile species, Instead, techniques have been based on time-lapse photography (Virnstein, 1982), or the measurement ofplastochrone intervals (Herbert, 1986) or rhizome elongation (Josselyn et al., 1986). In this paper, details are given of a technique used successfully to measure the above- and below-ground primary production of Halophila ovalis. It was based on a combination of tagging, detailed morphometric measurements and destructive harvesting. These data have been related to seasonal changes in physico-chemical parameters to determine factors affecting growth. 1.2. Factors controlling growth

The interaction of environmental factors on aquatic plant growth makes it difficult to evaluate the relative importance of each factor using field data alone. Separating the effects of light and temperature is particularly difficult, since in most aquatic systems seasonal wtriations in insolation cause corresponding variations in water temperature.

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K. Hillmanet al./Aquatic Botany51 (1995)1-54

The response of seagrass productivity to light (Buesa, 1975; Drysdale and Barbour, 1975; Drew, 1979; McMillan and Phillips, 1979; Beer and Waisel, 1982; Williams and McRoy, 1982; Wahbeh, 1984) is similar to the generalised pattern described for other aquatic plants (Steemann Nielsen, 1975). At low light levels there is a linear response, productivity increasing proportionally with light to an apparent saturation irradiance, where light is no longer limiting and productivity reaches a maximum. Further increases in light beyond saturation irradiance cause only minor changes in productivity, unless very high irradiances cause photoinhibition (e.g. Drew, 1979; Williams and McRoy, 1982). Most studies have indicated that seagrasses become saturated at relatively low light levels (less than 40% of surface irradiance). Once saturation irradiances are reached, other environmental conditions can become controlling factors. The effect of temperature on seagrass productivity and/or morphology has been examined in the laboratory by Biebl and McRoy (1971), Drysdale and Barbour (1975), McMillan (1978, 1983), Drew (1979) and McMillan and Phillips (1979). In these studies most seagrass photosynthesis (not growth) had an optimum temperature between 28 and 32°C, with sharp declines above this range. Laboratory experiments on the effect of salinity on seagrass show that most species tolerate a broad range of salinities for at least short periods, with optimum productivity at around oceanic salinity (Ogata and Matsui, 1965; McMillan and Moseley, 1967; Biebl and McRoy, 1971; McMillan, 1974; Drysdale and Barbour, 1975). Tolerance to non-saline conditions was not demonstrated for any species in the above studies, and most could not tolerate salinities in excess of 45%o, except for Amphibolis antarctica (Labill.) Sonder ex Aschers., which grew in culture to over 55%o (Walker and McComb, 1990). Salinity, temperature and light are important factors controlling the distribution, growth and morphology of Halophila ovalis in the Swan/Canning Estuary. The characteristic hydrology of the Swan/Canning Estuary also results in seasonal trends in salinity closely following those of light and temperature. To separate these effects, laboratory experiments were carried out in which each of these three factors were investigated to determine their independent effects on the growth and morphology of Halophila ovalis. This paper presents the results of these experiments, which are used to interpret the behaviour of Halophila ovalis in the field. A simple model was developed to interrelate these data and to simulate seasonal changes in growth in response to environmental conditions.

2. Methods 2.1. Distribution

Maps of the distribution of Halophila ovalis were drawn from two series of aerial photographs: March 1976 (1:5000 scale) and March 1982 (1:10 000 Scale). Both were taken when the angle of the sun was less than 40° using infrared-sensitive colour film. Density of seagrass cover was categorised as light (5-40%), medium (45-80%) and heavy (85-100%), and the area of each cover category was measured using a digitiser (2000 Series, Summagraphics Corp., CT). As the photographs were taken in March, the seagrass areas measured maximum seasonal distribution (Allender, 1970; this study).

K. Hillman et al./ Aquatic Botany 51 (1995) 1-54

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2.2. Biomass Estimates of biomass were obtained by diving at seven sites (Fig. 1) on an approximately monthly basis from February 1981 to October 1982. The data set for site 5A was larger, extending from September 1980 to October 1982. Ten replicate samples were taken at each site in pure stands using a cylindrical "perspex" corer (64 cm 2 area), although in winter as few as six replicates were sometimes taken. Sites were chosen to cover the range in sediment type, water depth and exposure to wave action where Halophila ovalis was present. The depth of core sampled, 6-12 cm, was determined by depth of root material at particular sites. Root and rhizome material was recovered from cores by rinsing in a small sieve. Samples were decalcified in dilute hydrochloric acid (0.1 M), and washed in deionised water. Epiphytes were scraped off with a razor blade, but were not routinely weighed, as preliminary measurements gave weights of only 1-5% of that of the seagrass. Seagrass material was sorted into roots, rhizomes and leaves, and the number of growing apices recorded. Sorted material was dried to constant weight at 100°C, cooled in a desiccator, and dr), weight determined.

2.3. Seagrass nutrient concentrations For nutrient analyses, plant material for each site was bulked and ground in either a micro hammer mill with a 1 mm screen (Glen Creston model C580, Stanmore, UK), or a mortar and pestle when sample size was small. Total phosphorus content was determined colorimetrically using the single solution method (Major et al., 1972) following acid digestion (concentrated nitric acid followed by concentrated perchloric acid) of 0.1-0.2 g subsamples. Total nitrogen content was measured colorimetrically (Technicon Industrial Method 33474 w/b, Technicon Industrial Systems, Tarrytown, NY) following acid digestion of 0.10.2 g subsamples in concentrated sulphuric acid with a mercury catalyst (BDH, Poole, UK). Digestions were carried out using a programmable block digester (Windrift Instruments, Welshpool, W.A., Australia). Organic matter content was estimated by loss on ignition after heating 1 g subsamples for 1 h at 650°C in a muffle oven. Carbon content of leaves and rhizomes was calculated as 49% of ash free dry weight (AFDW), based on manometric measurements of carbon dioxide produced following combustion of 10 mg subsamples at 800°C for 30 min in an atmosphere of pure oxygen.

2.4. Estimation of total biomass and nutrient pools Total biomass in the estuary was calculated using the midpoints of the ranges of each percent cover category (i.e. 5-40%, 45-80% and 85-100%). Biomass data obtained for pure stands of seagrass were taken as an estimate o f " 100% cover", and used to calculate biomass per unit area for the midpoint of each range. Each of these values was multiplied by the total area covered, and the totals summed. For the calculation of total biomass for 1976, biomass per unit area values were assumed to be similar to those obtained during the study period.

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K. Hillmanetal./AquaticBOtany51 (1995)1-54

Estimations of total nutrients bound in Halophila ovalis were obtained by converting total biomass for the estuary to amounts of carbon, nitrogen and phosphorus using typical carbon, nitrogen and phosphorus concentrations.

2.5. Biomass and environmental conditions Significant linear correlations between biomass and environmental variables were sought using SPSS. Factors investigated were the average daily rate of photosynthetically active radiation (PAR) reaching the water surface, attenuation coefficient, PAR reaching the seagrass beds, water temperature, salinity, dissolved oxygen (% saturation), "organic" phosphorus, orthophosphate, "organic" nitrogen, ammonia-nitrogen and nitrate-plusnitrite nitrogen. Monthly measurements of these parameters were carded out at the same time as the biomass measurements (Hillman, 1985). PAR reaching the seagrass beds was calculated from the average daily rate of PAR reaching the water surface, corrected for 15% surface reflectance and scatter (this figure has been suggested as an average loss for use in field estimates; Strickland cited in Goldman, 1979), and attenuated to the average daily water depth over the plants using the attenuation coefficients obtained for each site, following Kirk (1977).

2.6. Primary production and morphology At each of six sites, sediment was gently fanned away to expose rhizomes and growing apices (generally 1-2 cm below the sediment surface). Ten shoots were tagged at the third node from the growing apex by inserting a labelled skewer into the sediment alongside the node. Lengths of internodes and stage of leaf development from the marker to the growing apex were recorded. Leaf development was recorded as one of four classes: (1) leaf less than 10 mm in length, no petiole; (2) leaf 10-20 mm in length, no petiole; (3) mature leaf, petiole less than 50 mm in length; (4) mature leaf, petiole greater than 50 mm in length. Sediment was then fanned back into place, and 4-14 days later the measurements were repeated. At the same time, 30 similar shoots were harvested with careful recovery of the roots. This material was sorted into the four leaf classes, rhizomes and roots, and used to measure dry weight per leaf class, dry weight per unit rhizome length, dry weight per unit root length and average length of root associated with each leaf class. Production rates were then calculated by relating the data from the harvested shoots to the measured increases in length of the tagged shoots. The harvested material was also used to record average leaf length, leaf breadth and petiole length of mature leaves, average mature rhizome internode length, and average mature root length. Shoots were harvested of similar size to those that were tagged (a growing apex with four to six internodes), and the measurement of only newly matured organs ensured that morphological measurements were representative of the environmental conditions that prevailed during the tagging interval. Measurements were carried out at monthly intervals, except during the winter months, when underwater visibility was poor.

2. 7. Estimation of total primary production in the estuary Production rates per growing apex for shallow sites (0-1 m relative to "datum", an extreme low water reference mark set in 1892: the tidal range relative to datum means that

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

7

the shallow seagrass meadows, given as occurring in the depth range 0-1 m, were typically covered by 0.4-1.6 m of water during the day) and deep sites ( 1-2 m) were converted to production per unit area using previously determined data on the number of growing apices per unit area. The resultant production rates per unit area for "100% cover" were used in combination with previously established areas of three categories of percent cover of Halophila oualis (5--40%, 45-80%, 85-100%) in the estuary to calculate the total primary production in the estuary. Data for 100% cover were multiplied by the midpoints of each category of percent cover. This calculation involved the assumption that there was a linear relationship between biomass and percent cover, and was therefore a slight underestimation since preliminary checks indicated that biomass in stands of higher cover was proportionately higher than in stands of lower cover.

2.8. Primary production and environmental parameters Production "per apex" at each site was compared with environmental data to determine the factors controlling productivity. Correlations between productivity and environmental parameters were determined using SPSS (Nie et al., 1975). Photosynthetically active radiation (PAR) reaching the tagged plants was calculated from PAR at the water surface, averaged over the tagging period, corrected for surface reflectance, and attenuated to the average daily depth of water over the plants using attenuation coefficients for each site and average daily tidal data for the estuary.

2.9. Culture techniques Plant material was collected from a site in the Swan River in April 1982. Each rhizome was severed at the internode behind the third node below the apical bud, and the growing shoot carefully removed from the sediment, so that the roots remained intact. Samples were transferred to the laboratory within 30 min, shaken in artificial seawater to reduce the number of epiphytes (mainly diatoms), and placed in controlled temperature and photoperiod growth cabinets. Light was supplied by a bank of 12 40-W Philips "warm white" fluorescent tubes, and eight 60-W Philips incandescent bulbs. Photoperiod was controlled by time clocks (Warburton Franki, model WF 60/0) linked independently to the fluorescent and incandescent lights. Intensity of photosynthetically active radiation (as measured by a Licor LI-185 Quantum/Radiometer/ Photometer, Lambda Instruments Corp., Lincoln, NB) was not uniform over the growth cabinet working area, and so random rearrangement of pots in the aquaria was required to minimise any effect of different light intensities. The growing shoots were planted in 1 1 plastic pots (one shoot per pot) in sterile sand 12 cm deep overlying a 2-cm-deep layer of gravel, and placed in 30 1 glass aquaria (five pots per aquarium), each containing 20 1 of artificial medium. An artificial medium was also used to avoid problems with the variable quality of coastal waters, and to enable easy manipulation of salinity levels (McMillan, 1980). The artificial medium was a modified ASP12 recipe (Provasoli, 1964). The main modifications to the original recipe were (i) the addition of an inorganic carbon source (NaHCO3) to give allkalinities similar to those of the estuary; (ii) the addition of inorganic nitrogen as NH4NO4 since both N species are present in the estuary; (iii) the addition of inorganic phosphorus as K2HPO4; (iv) the

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K. Hillmanet aL/Aquatic Botany51 (1995) 1-54

deletion of glycerophosphate, nitrilotriacetic acid buffer and Tris buffer. Medium pH was constantly monitored, and adjusted when necessary by the addition of NaaCO3; pH was maintained at 8.1 + 0.4 throughout the experiments. The water surface was 8 cm above the sediment, and evaporation was compensated for every 2 days by the addition of deionised, distilled water. The water in each aquarium was continuously aerated by aquarium air pumps (Epoch Model EIII), with flow rate controlled by T-taps. 2.10. Experimental design Three experiments examined the separate effects of temperature, salinity and light intensity on productivity. Temperature, salinity and light levels were chosen to cover the range of conditions experienced in the field. (i) Temperatures of 10-25°C were used. Salinity was held at 35%o (marine salinity), and light intensity at an average of 120/zE m -2 s - i with a 12 h photoperiod. (ii) Salinities were in the range 5-45%o. Average light intensity was 120/zE m -z s-1 with a 12 h photoperiod, and temperature was held at 25°C. (iii) Irradiances were in the range 20--400/zE m -z s -~, each with a 12 h photoperiod. To achieve light intensities in excess of 150/zE m -z s-~, the growth cabinet light supply was replaced by 400 W Metalarc mercury vapour lamps (Atkins Carlyle Ltd., Perth, W.A., Australia). Low light intensities were achieved using the original growth cabinet light source and layers of "50% shade" Sarlon mesh (F.R. Beaver, Sailmaker, Claremont, W.A., Australia). The temperature was held at 25°C and the salinity at 35%0. Each experiment was run for 6 weeks; 15 growing shoots were planted in each treatment, and five shoots were harvested from each treatment every 2 weeks. After harvesting, mature leaf length and breadth, mature petiole length, mature rhizome internode length and mature root length were measured. Material was then sorted into roots, rhizomes and leaves, rinsed in deionised, distilled water, decalcified in dilute HC1, and dry weight determined. 2.11. Computer simulation of growth A simple program was developed in Basic to relate laboratory-derived responses to conditions observed in the field. The program accepts specified environmental parameters for a given time of year, and estimates a daily growth rate on the basis of a percentage of maximum growth rates observed in culture. The model is based on Blackrnan's 1905 concept of "limiting factors", which can be summarised as follows. When photosynthesis or growth is affected by a number of independent factors, then at any particular time only one of the factors will limit the overall rate. For instance, if light and temperature are adequate, salinity may limit growth; if salinity is raised, light may become limiting. This fails to take into account any synergistic or antagonistic interactions between envir0nmental variables in affecting plant growth. However, it remains a useful way of interpreting the effects of different variables, and was considered the most suitable approach for the purposes of this exercise, since experimental design analysed responses to each of light, salinity and temperature when the other two variables were adequate for growth. A similar

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Fig. 2. Seasonalchangesin averagedallyPARjust belowthe watersurfaceofthe Swan/CanningEstuary(allowing for 15% surfacescatterand reflection),shown with the mathematicalfunctiondescribingthe fittedcurve.Day 1 equals 1 July. approach has been used by Gordon and McComb (1989) in interpreting the growth of an estuarine alga, Cladophora montagneana Kiitz. An important input in the program is light, because in addition to being a vital factor affecting aquatic plant growth, it is also the most variable of environmental parameters. The model, therefore, allows for seasonal changes in light intensity and daylength, and changes in light intensity during the day. The monthly means of average daily PAR reaching the water surface were plotted against day number, and a function derived which describes the shape of the curve (Fig. 2). A function was also derived to calculate daylength from day number. These two functions enabled the program to take into account seasonal changes in insolation and daylength. To take into account changes in light intensity during the day, the literature-derived curve of Gordon and McComb (1989) was used. The intensity of PAR at each 20th of daylength was expressed as a percentage of maximum intensity, and then converted to percentage of average light intensity for the day. The model assumes that the shape of the curve is the same for any day in the year. That is, whilst there are seasonal changes in light intensity and daylength, the percentage distribution of light intensity about mid-day is assumed to be constant. During program operation, the average intensity of PAR reaching the water surface for any nominated day is calculated using the function from Fig. 2. For each 20th of daylength, the intensity of PAR is then calculated, and reduced by a factor which accounts for the nominated water depth and attenuation coefficient, to arrive at light intensity reaching the seagrass bed. For each interval the growth rate is determined from the calculated light level. Independently, the growth rate is determined for the nominated temperature and then for

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K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

the nominated salinity in each case assuming that other factors were not limiting. The rates were calculated from laboratory responses percent of the maximum growth rates observed in cultures rather than absolute growth rates for reasons that are discussed below. The minimum of the three computed growth rates for each interval is selected as the rate achieved at that particular interval. This exercise is carried out for each interval from dawn till midday (ten intervals), and the mean of the growth rates of these ten intervals taken as the average growth rate for the day, as the curve of light intensity is symmetrical about midday. This average growth rate, still expressed as a percentage of maximum growth, is converted to milligrams DW per apex per hour using the maximum hourly growth rate measured in the field during the study period, then multiplied by the daylength to give an output of the growth rate as milligrams DW per apex per day. Since the program also prints out the percentage of maximum growth rate achieved under the nominated conditions of salinity and temperature, and for each of the calculated light intensities for the ten intervals from dawn till mid-day, the variable(s) responsible for limiting growth could be determined.

3. Results

3.1. Distribution The distribution of Halophila ovalis was similar in March 1976 and March 1982 (Fig. 3). Approximately 25% of the estuarine basin was occupied by Halophila ovalis in both years. The only major difference was the disappearance of Halophila ovalis from the Canning River by 1982. Nonetheless, the total area occupied by Halophila ovaIis increased from 568 ha in 1976 to 598 ha in 1982, largely because of the occupation of new areas of the estuarine basin by low-density seagrass beds (Fig. 4). Most of the seagrass was found in shallow waters; in both years more than 75% of the total area of seagrass was in water less than 1 m deep, and over 99% in waters less than 2 m deep. Halophila ovalis was only found in waters deeper than 2 m (relative to datum) in small areas near the estuarine mouth, where it extended down to 4 m. The extent of Halophila ovalis upstream corresponded to the changeover point from the salinity regime of the estuarine basin to that of the upper estuary (Fig. 5).

3.2. Biomass There were seasonal differences in biomass (Fig. 6), and there was also a marked difference in seasonal trends between 1980 and 1981. In 1980, the biomass increased rapidly during spring, and reached a peak by January 1981. High biomass was maintained until mid-autumn, but with the onset of winter fell sharply, and remained at a low level until late spring, 1981. During the summer of 1981/1982 biomass increased slowly, and in contrast to the previous year did not reach a maximum until mid-autumn. However, during the winter of 1982 high biomass was maintained, and had only declined slightly by mid-spring. Partitioning of biomass into roots, rhizomes and leaves remained reasonably constant from spring 1980 to autumn 1981, and in 1982; roots and rhizomes constituted approximately 50% of total biomass, and leaves the remainder. During winter and spring 1981 the

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proportion of leaf biomass fell to less than 30%, owing to a ten-fold decrease in leaf biomass while roots and rhizomes only decreased five-fold. Seasonal changes in leaf biomass were also more pronounced than those of root and rhizome biomass in 1982. Generally, seasonal trends in biomass for all sites were similar, as were the proportions of biomass in roots, rhizomes and leaves. Differences between sites were apparent in two areas: (i) the biomass decline in winter and spring of 1981 was least abrupt at the two deepest sites ( 3 and 5B), and most abrupt at the shallowest site (8), and (ii) the maximum seasonal biomass attained. Sites 2 and 8 both reached a maximum biomass of 60-80 g DW m - 2 , sites 3, 5B and 6 attained 80--100 g DW m - 2 , and site 5A attained 120 g DW m - 2 Although statistical variation was relatively high, the data indicate that maximum biomass increased with increasing depth up to 0.8 m (relative to datum), and thereafter declined (Fig. 7). There was little effect of depth on biomass during the winter/spring of 1981.

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There were marked seasonal differences in primary production per apex at site 5A in 1981 and 1982 (Fig. 8). Maximum production was reached in summer, and there was a marked decrease during early- to mid-spring and mid- to late autumn. No values could be obtained for winter, but since little light was available for photosynthesis (Hillman, 1985) it was assumed that primary production was very low or that respiratory losses occurred, as suggested by seasonal changes in biomass. There was a marked difference in the maximum production rate reached in the summer months of each year. In summer 1980/1981 a maximum of 12 mg DW per apex day- ~ was reached in December, whilst in 1981/1982 a maximum of 32 mg DW per apex day- 1 was attained in February. Primary production from October to December inclusive was comparable between the 2 years, but for January-May inclusive, 1982 values were more than double those of 1981. Sites 2, 6 and 8 had the same marked seasonal trends in primary production as site 5A, although there were differences in the maximum production rate reached at each site. Sites 2 and 8 reached a maximum of approximately 40 mg DW per apex day- ~, site 5A attained

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Distance uostream ( km )

Fig. 5. Typical changes in salinity with distance upstreamin the Swan/Canning Estuary during the months of maximumsalinity (May) and minimumsalinity (July) in 1981.Extent of Halophila ovalis also shown. 30 mg DW per apex d a y - ~, and site 6 attained 50 mg DW per apex day - ~. At the deepest sites (3 and 5B) primary production was low and not detectable within acceptable statistical limits for 8 months of the year. Above-ground productivity constituted approximately 50% of total productivity at sites 5A and 8 during the period measured, approximately 40% of site 2, and up to 60% at site 6. These differences in the proportions of above-ground to total production were largely due to the size of leaves produced at each site; those at site 6 were considerably larger than at other sites, whereas leaves produced at site 2 were considerably smaller. Seasonal changes in primary production, expressed per unit area, are presented in Fig. 9. Seasonal trends generally followed those of rates per apex, although rates per unit area in spring 1981 were relatively less compared with the seasonal maximum owing to low shoot densities, and relatively higher in the autumn and spring of 1982 owing to high shoot densities. Sites 2 and 8 reached a summer maximum of approximately 28 g DW m - 2 d a y - ~, site 5A reached 20 g DW m - 2 d a y - l, and site 6 reached 40 g DW m - 2 d a y - 1. Mean annual primary production for each site was calculated by taking the mean of monthly data, whilst assuming zero primary production during the winter months. These data are presented in Table 1, which includes rough estimates for the deeper sites calculated by assuming a production per apex of approximately 30% of that at site 5A (an assumption based on the few data that were collected for these sites during the summer months). The data emphasise the effect on growth of depth, and therefore presumably of light supply. The three shallowest sites had a mean annual production of 9-10 g DW m -2 day-~, site 5A averaged approximately 5 g DW m - 2 d a y - l, and the deepest sites averaged 1.5 g DW m - 2 d a y - ~. These data were used in turn to calculate the mean annual primary production of Halophila ovalis for the whole estuary. A rate of 8 g DW m -2 d a y - ~ was used for a pure stand (i.e. 100% cover) in the 0-1 m depth interval, and 1.5 g DW m - 2 d a y - 1 for the 1-2 m depth interval. An annual mean production rate of approximately 4 g DW m -2 d a y - ~was obtained for the

14

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

801 4O

120t

site 58

4O

i

0t 40

120t site3 40

120q site2 4O

F'M'A'M'j'J'A'S'O~N'D'J'F'M'A'M'J'J'A'S'O' 1981

I

1982

Fig. 6. Changes in the biomass of Halophila ovalis at six sites in the Swan/Canning Estuary, February 1981 to October 1982. Data are shown as cumulativeplots of the contributionsof roots, rhizomesand leaves. whole area of Halophila ovalis in the estuary, or approximately 1500 g D W m -2 y e a r (500 g C m -2 y e a r - 1). 3.4. Phenology

There were differences in phenology between 1981 and 1982 (Fig. 10). Flowering commenced in late November/early December 1980, and fruiting in January 1981. Flowers

15

K. Hilhnan et al. /Aquatic Botany 51 (1995) 1-54 : April 1981 (.sea s. max. ) AAugust 1982 (seas. max. • Sept. 1981 (seas. min. ) 20-

'E

90-

"o

o

0.5

1.0

115

Depth (m) Fig. 7. The biomass ofHalophila ovalis in the Swan/Canning Estuary plotted against depth for periods of maximum biomass in 1981 and 1982, and minimum biomass in 1981. Depths relative to datum.

30/

25-

/

/

;

IL

i

,

20-

!

//leaves I /

E v

15,

#.

//

10rhizomes~ 'x

5,~,J j /

OI N ' D 1980

' j ' F~ M' A~ M' j ' I

1981

j ~ A~ S ~ O '

N

D' j' I

FIM'

A'M'

j~ j T A'S'

1982

Fig. 8. Changes in productivity (per growing apex) ofHalophila ovalis at site 5A in the Swan/Canning Estuary, October 1980 to October 1982. Data are shown as cumulative plots of the productivity of roots, rhizomes and leaves, and standard error bars are included.

O

K, Hillman et al. /Aquatic Botany 51 (1995) 1-54

16

20

/

10 30. 20. 10

I

40- "

s

t-..[

~

3020-

/

10-

1°l

O N D J F M A M J J A' S'O ~ 1981 [ 1982

Fig. 9. Changes in productivity per unit area of uniform stands of Halophila ovalis at four sites in the Swan/ Canning Estuary, October 1981 to October 1982.

and fruits were still abundant in March, but by June only an occasional fruit was present. In the next summer, flowers were not found until late December 1981, and fruits until late January 1982. Fruits and flowers were abundant in March 1982, and continued to be found Table 1 Mean annual productivities of Halophila for six sites in the Swan/Canning Estuary, 1981/1982 Site

8 2 6 5A 3 5B

Depth a

0.0 0.1 0.3 0.8 1.2 1.3

"Depth relative to datum.

Productivity (g DW m - 2 d a y - 1) Above-ground

Below-ground

Total

4.9 4.1 4.6 2.6 0.8 0.7

4.1 5~6 4.3 2.8 1.0 0.8

9.0 9.7 8.9 5.4 1.8 1.5

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

150-

flowering f;ultlng

17

flowering fruiting

120-

90v

<

60-

30"

$'O'N'D 1980

IJ ' F'M'A'M

•

summer

.

J'J 'A'S'O'N' 1961 i

winter

t

DI J ' F ' M '

i

summer

.

A'M' J'J 1982 t

w~ter

'A'

S ' O'

,

Fig, 10. Changes in the biomass of Halophila ovalis at site 5A in the Swan/Canning Estuary, September 1980 to October 1982. Data are shown as cumulative plots of the contributions of roots, rhizomes and leaves, and the standard error bars are included.

well into July 1982. No differences were observed between sites in either flower or fruit abundance, or the timing of phenological changes.

3.5. Morphology 3.5.1. Apices Seasonal changes in the density of growing shoots (number of apices per unit area) closely followed changes in biomass (Fig. 11 ). At all sites the number fell below 300 m - 2 in the winter and spring of 1981, whilst in the same period in 1982 more than 600 m -2 were recorded. The two deepest sites (3 and 5B) generally had lower densities of apices throughout the year, but there was no significant difference between the remaining four sites. However, when expressed as number of apices per gram DW of rhizome, some differences emerged (Table 2). Although data interpretation was difficult owing to high statistical variation, it appeared that for the four deepest sites, differences in densities were largely related to differences in rhizome biomass, with no real difference between the number of apices per gram dry weight of rhizome. However the two shallowest sites had much higher numbers of apices per gram DW of rhizome, with site 2 having 30% more than the deeper sites, and site 8 almost 45% more. The effect of depth on number of apices per gram DW of rhizome was therefore much more marked in shallow water than was observed for biomass, but for depths in excess of 0.2 m (relative to datum), increasing depth appeared to have little effect. 3.5.2. Rhizomes and roots Seasonal trends in rhizome internode lengths were similar at all sites (Fig. 12). Lengths were lowest during early spring and late autumn, but approximately doubled from spring to a maximum in summer. This was true for all sites except site 5B (the deepest site), for

18

K. Hillman et al./ Aquatic Botany 51 (1995) 1-54

1800 -]

site 8

,,oo 1, 1800

~e6

1zoo

600

1800 1200

600

18oo]

site 58

~

~a

1211111

18001

"

1200 1

F'M,A'M'j. j ,A, S,O.N.DI j ' F,M.A,M'j, j 'A'S'O! 1981 1982 Fig. I 1. Changes in the density o f growing shoots (apices) in uniform stands o f Halophila oualis at six sites in the Swan/Canning Estuary, February 1981 to October 1982.

Table 2 Mean number of apices (growing shoots) per unit dry weight of rhizomes of Halophila in the Swan/Canning Estuary, February 1981 to October 1982 Site

8 2 6 5A 3 5B

Depth a (m) 0 0.1 0.3 0.8 1.2 1.3

Depth relative to datum,

Apices (no. g - 1 DW rhizome) x

SE

n

Range

64 56 41 44 41 41

4 5 4 4 4 4

20 21 21 26 19 21

36--100 18-100 22-59 10-83 20-88 21-87

K. Hillman et al. / Aquatic Botany 51 (1995) 1-54

19

100 t site 2 60

i/

"I.~

20

roots 1- -I" rhizomes

Site 5 8

•ot site 6

. -I.... I- - "t- - -I- _ E-

I

60 40 20

%-I

i-

site 8

80 1001 60 40 20 O'N'D'J t981 I

' F'M'A'M'J

' J ' A'S'O' 1982

Fig. 12. Changes in the lengths of mature roots and rhizome internodes of Halophila ovalis at five sites in the Swan/Canning Estuary, October 1981 to October 1982. which only a 50% increase was recorded from spring to summer. No significant difference was found in maximum rhizome internode lengths attained at the four shallower sites, but at the deepest site (5B), the maximum length was 25% less. Mature root lengths (Fig. 12) followed similar trends, although the seasonal changes were less pronounced than for the rhizome internodes. Changes in the weight of rhizome internodes and roots closely reflected changes in length, since weights per unit length of these tissues were relatively constant (Table 3). In addition, there were only slight differences between sites in seasonal maximum and minimum rhizome internode weight per unit length. For root weight per unit length, site differences were also slight with the exception of site 5B, which had slightly heavier root tissue. 3.:5.3. L e a v e s

In contrast to root and rhizome morphology, there were marked differences in leaf morphology between sites of similar depth and seasonal trends between the three leaf parameters measured varied considerably (Fig. 13). In deeper waters (sites 5A and 5B),

K. Hillman et aL /Aquatic Botany 51 (1995) 1-54

20

Table 3 Mean ( + SE) weights per unit length ofHalophila rhizomes and roots at five sites in the Swan/Canning Estuary, 1982. Seasonal maxima and minima depicted Site

8 2 6 5A 5B

Depth a (m)

April 1982 (rag m m - l )

0 0.1 0.3 0.8 1.3

June 1982 (mg m m - l)

Rhizome

Root

Rhizome

Root

0.31 + 0.3 0.33 +0.03 0.33 + 0.03 0.30 + 0.02 0.3 i + 0.03

0.16 ::k0.01 0.21 -I-0.02 0.18 + 0.02 0.20 + 0.02 0.24 + 0.02

28 + 0.02 32 ::t:0.01 28 + 0.001 25 + 0.03 28 + 0.02

14 + 0.01 18 ::t:0.01 16 + 0.01 17 + 0.01 21 + 0.01

a Depth relative to datum.

larger-bladed, shorter stalked leaves were produced in summer than in spring or autumn. In shallower waters (sites, 2, 6 and 8), shorter, broader leaves were produced in summer, and

30] 20.

401 10,

f

t

z

t

=

;

t ~ leaf breadth1

z

,

=

:

30

20

•

10

=

l

3O

~ 20

'°1 i '°

j

x

•

=

=

t

i

lO

5°1

p.4 ~

3O 20

t

I

t

"

i

z

= !

10

40

30 20

10 ,

0

,

N lg61

,

0

,

J I

,

F

,

M

,

A

M

.

J

.

.

J

.

A

S

0

1962

Fig. 13. Changes in the biometry of mature leaves of Halophila ovalis at five sites in the Swan/Canning Estuary, October 1981 to October 1982.

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

21

Table4 Seasonal maximumand minimumleaf weights (mean + SE) of Halophila at five sites in the Swan/Canning Estuary, 1982 Site

8 2 6 5A 5B a

Depth (m)

a

0.0 0.1 0.3 0.8 1.3

Seasonal minimum

Seasonal maximum

Weight (mg per leaf)

Month

Weight (mg per leaf)

Month

10.8 4-0.8 8.2 + 0.6 10.3 + 0.5 7.3 + 0.5 7.7 + 0.6

February January February May April

13.7+ 1.1 9.9 + 0.8 14.2 + 1.3 9.8 + 0.7 10.6 + 0.9

May April April February January

Depthrelativeto datum.

longer, narrower leaves in spring and autumn. There was a marked difference in leaf size between sites 2 and 8, which were at essentially the same depth; this was reflected in leaf weights (Table 4). This may have been related to differences in sediment type and/or degree of wave action, since these were the only factors in which the two sites appeared to differ. In view of the similar root and rhizome morphology and weight at these two sites, the difference in leaf weight may explain differences in the ratios of above-ground production to total production noted previously. 3.6. Statistical correlations with environmental factors

3. 6.1. Biomass With the exception of site 5B, biomass at all sites showed significant positive correlations with salinity, and significant negative correlations with factors affecting the amount of light reaching the seagrass bed (Table 5). Biomass at site 5B was correlated with light, but not with salinity.Variance in biomass accounted for by environmental variables at each site was also assessed using multiple linear regression analysis, but this technique was less useful than linear regression analysis due to complications caused by internal correlations between the variables used. The limitations of multiple regression analysis were partly overcome by analysing only the factors affecting light supply to the seagrass bed; 36-75% of the variance at all sites was accounted for by the combined influence of global radiation, attenuation coefficient, daylength and water depth. Selective analyses of the effect of physical factors emphasized the importance of salinity. At least 42% of the variance at all sites was accounted for by light and salinity. 3.6.2. Primary production The relationships between seasonal changes in primary production and environmental conditions for four sites are presented in Table 6, which ranks independent correlations in order of decreasing significance. All four sites showed a significant correlation with temperature, and site 5A (the deepest site) also showed a significant correlation with average

22

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

e~ o

~}.~ oo} ~

~o ~

o

<

$~

e~

~ ~

~' :~

, ,

zz

.~.~ ~

.=

>

>

~.~

?

~

~

0

>

~o >

~°° ,q

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

23

Table 6 The amount of variance in productivity of Halophila at four sites accounted for by different environmental variables. Data calculated by multiple linear regression analysis Site 2 (depth a 0.1 m) Variable

Site 5A (depth 0.8 m) % variance Variable (cumul.)

Temperature 70 P-organic 78 N-ammonia 81 Diss. oxygen (% sat.) 84 Atten. coeff. 86 Chlorophyll a 89 P-inorganic 91 Seagrass PAR 94 Incoming PAR 100

Site 6 (depth 0.3 m) % variance Variable (cumul.)

Temperature 38 P-inorganic 44 Salinity 49 Atten. coeff. 61 Seagrass PAR 70 Daylength 80 N-ammonia 83 N-organic 84 N-nitrate 92 Incoming PAR 95 Diss. oxygen (% sat.)96 Chlorophyll a 97

Site 8 (depth 0.0 m)

% variance Variable (cumul.)

Temperature 39 P-organic 93 N-organic 96 N-nitrate 99 N-ammonia 100

% variance (cumul.)

Temperature 54 P-inorganic 76 N-nitrate 86 Atten. coeff. 100

a Depth relative to datum.

daily PAR reaching the seagrass. The data in Table 6 plus the clearly demonstrated effect of depth in Table 5 indicated that water temperature and PAR reaching the seagrass beds were the factors most strongly related to observed seasonal fluctuations in primary production. Only site 2 showed a significant correlation between primary production and salinity, and between primary production and organic phosphorus levels. Correlations with salinity, nutrient concentrations in the water column, and dissolved oxygen levels were otherwise generally poor. Variance in primary production accounted for by environmental variables was also assessed using multiple linear regression analyses: the limitations of this technique (caused by internal correlations between variables) were overcome to some extent by analyses of the effects on primary production of only physical factors (salinity, temperature, light and dissolved oxygen). At least 60% of the variance was accounted for by these factors at all sites. Analysis of the combined effect of only those factors affecting light supply to the seagrass beds accounted for 49% of the variance at site 2, 30% at site 5A, 46% at site 6 and 44% at site 8.

3.6.3. Morphology Statistical relationships were only sought between biometry and salinity, temperature and average daily PAR' since these three variables consistently emerged as the important ones in linear correlations with biomass and primary production. With the exception of leaf length, all morphological parameters were significantly correlated with water temperature. Significant correlations between average daily PAR and rhizome internode length, root lengths and leaf widths were also obtained for most sites. To a lesser extent, salinity appeared to be a significant factor affecting leaf width and rhizome internode length, although generally correlations between salinity and biometry were less conclusive. Leaf length was the

K. HiUman et al. /Aquatic Botany 51 (1995) 1-54

24 a]

30-

E 20.J 10-

oaf

110

20

Ioroadth

30

410

Sellnity (~,)

b)

50

30-

E ~

~

l

.

+

-

-....... 1

20-

-J

10-

1dO

'26o

360

460

Light (~uEIn . m - ! . I r 1) c) 30-

E s "

20-

10-

Temperature ( * C )

Fig. 14. Effects of salinity (a), light (b) and temperature (c) on the biometry of mature leaves of Halophila ot,alis grown in culture.

least correlated with environmental changes, which was not surprising in view of the inconsistent seasonal trends illustrated in Fig. 14.

3. 7. Responses in culture 3. 7.1. Salinity Halophila ovalis tolerated a broad range of salinities, with severe limitation of growth at salinities less that 10%o or greater than 40%0 (Fig. 15). Optimum growth rates of approximately 2.5 mg DW per apex day- 1 were obtained in the salinity range 25-35%0, with growth rates of over 60% of the optimum still recorded at salinities as low as 15%o. In contrast, a 10%0 increase in salinity above the range for optimum productivity had a marked deleterious effect on productivity, although the data in Fig. 16---which depict changes in biomass per shoot for the duration of the experiment--indicate that the seagrass was capable of tolerating short periods of hypersalinity. Some new growth was produced at 45%0 in the first 2 weeks of the experiment, and losses were only recorded in the latter stages. A similar short term

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

A

25

//

°

i

/

x

//

:

/

2

"7.

t' '

X /

W tt

i~

II

D

t

E

¢ t

m>

0

i

1"6

I

Q

24

3'2

Salinity

40 (%o)

tl I

"0

El,

I

-1

-2

Y = -x/3.2+16.9x-129.3 Fig. 15. The effect of salinity on productivity of Halophila ovalis in culture. Productivity was calculated as the average increase in dry weight per day for the duration of the experiment.

tolerance was also apparent for essentially fresh water. At 5%o there was little loss ofbiomass during the first 4 weeks, but prolonged exposure to this salinity eventually killed the seagrass; decomposition in the final 2 weeks of the experiment was extremely rapid, such that the final harvest consisted only of a small amount of amorphous brown material. Within the salinity range 15-35%o, little variation occurred in root length, rhizome internode length and leaf length and width (Figs. 14a and 17a). Petiole length varied slightly 180-

,,25~. ~

~

12o-

| E .o ,~

~

J J

35~oo

~2o~.

15~o

10 N .

60-

i

Time (weeks) Fig. 16. Changes in the biomass ofHalophila ovalis plants grown at various salinities in culture.

26

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

a) iO080vE 3: 6 0 z ~

40-

20-

tb

2b

35

45

s~

Salinity ( % )

°, I 40-

r

o

o

t

s

~

~

30z

~ ~--~--~

2 0 - hizomes

°t 10-

1do

260

3do

4do

Light ~.Ein . m - = . i r t ) c)

~

30 2O

rhizomea

10

115

2'0

215

Temperature (o C)

Fig. 17. The effect of environmentalfactorson the lengths of matureroots and rhizomeinternodes of Halophila ovalis grown in culture: (a) salinity; (b) light; (c) temperature. more than the other morphological parameters, with maximum values between 20 and 35%o, and a 70% increase from 15 to 20%o. At 10 and 45%0 the size of all morphological parameters measured decreased considerably. This was particularly pronounced at 45%0; new leaves and rhizomes were only half the size of those produced at 15-35%o, and roots were a quarter the size. 3. 7.2. Temperature

Over the temperature range 10-25°C, the response of seagrass productivity to temperature is best described by a simple linear equation (Fig. 18). Temperatures of less than 15°C severely limited productivity, and at 10°C no growth occurred at all, although the plants did not die. There was a seven-fold increase in productivity from 15 to 20°C, and a further 30% increase from 20 to 25°C. A maximum growth rate of approximately 2.1 mg DW per apex d a y - t was reached at 25°C. With the exception of leaf width, which did not vary significantly, all morphological parameters measured increased in size with increasing temperature (Figs. 13b and 16b). Over the temperature range 15-25°C, rhizome internode length increased by 40%, root

27

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

1D

j/

2.0

7 O. ca

1.5

"0

1.0 >~ >

.5

"0 0 Q.

0

f

10

15

20

Temperature

y= -87.5+

25

( o C )

7.5x

Fig. 18. The effect of temperatureon productivityof Halophilaovalis in culture.Productivitywas calculatedas the averageincreasein dry weight per day for the durationof the experiment. length by 75%, leaf length by 30% and petiole length by 100%. Root and rhizome morphology was most affected over the range 20-25°C, and leaf morphology over the range 15-20°C. 3. Z3. Light

Halophila exhibited classic photosynthesis versus irradiance (P-I) behaviour (Fig. 19), with light saturation at approximately 200/zE m -2 s-~ (Ik according to Tailing, 1957), and compensation point at approximately 40/zE m - 2 s - ~ (2% of full sunlight). Saturation and compensation PAR levels were calculated by linear regression analysis of growth rates at lower PAR levels according to the method of Drew (1979). A maximum productivity of 2.8 mg DW per apex day- ~ was obtained at saturating light intensifies, and an r2 value (goodness of fit) of 0.95 indicated productivity rates were proportional to PAR levels over the range 0 - 2 0 0 / x E m - 2 s-~ according to the equation y = 0 . 0 1 5 x - 0 . 6 7 where y is the productivity (in mg DW per apex day -1) and x is the PAR level (in ~E m -2 s--l). The data were also extrapolated to estimate respiratory loss in the dark; the value obtained of 0.67 mg DW per apex day- 1, when referred to the weight of the shoots at the beginning of the experiment, represented a loss of 1.5% of original biomass per day for the duration of the experiment had the plants been kept entirely in the dark. PAR over 7 0 / z E m - 2 s - ~ had little effect on root morphology, but rhizome internodes at saturating light intensifies were 50% longer than those at lower light levels (Fig. 17c). There was little effect of light on leaf width, but PAR between 70 and 150/zE m -2 s-1, leaf lengths and petiole lengths were 20% and 50% greater respectively than those at saturating light intensifies (Fig. 14c). In view of the small variation in apportioning of biomass under non-stressed conditions, it is of particular note that in the light experiment, leaves produced under saturating light were smaller and heavier than under non-saturating light. Thus leaves produced at saturating

28

K. Hillman et al./ Aquatic Botany 51 (1995) 1-54

3. "o

T x

2" ai

"o

E >,

1"

>

a.

0 ////

lOO

2o0 PAR

3()0

46o

(~Ein. m-2 . s-1)

y= -24.8"1".576x

Fig. 19. The effect of light on productivity of Halophila ova~is in culture. Productivity was calculated as the average increase in dry weight per day for the duration of the experiment. l i g h t c o n d i t i o n s w e r e o f s l i g h t l y thicker, d e n s e r tissues. C o n v e r s e l y , a l t h o u g h r h i z o m e i n t e r n o d e s a n d r o o t s w e r e l o n g e r u n d e r s a t u r a t i n g light, they w e r e o f slightly less d e n s e tissues ( T a b l e 7 ) .

3.7.4. General

For those conditions of salinity, temperature and PAR levels that overlapped between the three experiments (i.e. 25°C, 35%o and 120/zE m -2 s - l ) , there was good agreement in leaf sizes and rhizome internode length. Root biomass, however, was the same in all the experiments, but roots were longer in the salinity experiment than under identical conditions in t h e t e m p e r a t u r e a n d l i g h t e x p e r i m e n t s . I n t h e last t w o e x p e r i m e n t s , roots w e r e r e l a t i v e l y Table 7 Weights of different tissues of H. ovalis grown in laboratory experiments Experimental variable Roots Rhizomes Leaves (mg DW mm- ~mature root) (mg DW mm- ~mature rhiz.) (mg DW mm- ~mature leaf) Salinity (%o) < 15 15-35 45 Temperature (°C)

Light (/zE) < 220 > 200

0.114 4-0.0010 0.0834-0.008 0.179 4- 0.015

0.218 4-0.019 0.2184-0.012 0.230 4- 0.011

5.9 4- 0.2 6.34-0.5 4.8 + 0.1

15

0.168 4- 0.011

20-25

0.155 4- 0.006

0.219 4- 0.017 0.225 4- 0.014

6.0 4- 0.4 6.7 4- 0.6

0.160 4- 0.013 0.145 + 0.013

0.232 4- 0.011 0.210 4- 0.010

6.8 4- 0.5 7.9 + 0.3

K. Hillmanet al. /Aquatic Botany51 (1995) 1-54

29

shorter and thicker, and also had many fine root hairs which the roots of the salinity experiment lacked. This may have resulted from differences in aeration of the culture vessel which was more vigorous in the salinity experiment allowing aeration of the sediments and deeper root penetration. In overview, of particular note were the opposite effects of increased light and increased temperature on leaf and petiole lengths. Maximum leaf and petiole lengths were recorded at 25°C under non-saturating light conditions, but at 25°C and saturating light conditions, leaf and petiole lengths decreased considerably. Of the remaining morphological parameters, all reached maximum size under optimum conditions for growth. These morphological changes were not associated with differences in the apportioning of biomass into above- and below-ground tissues, except when the plants were severely stressed. Generally, above-ground biomass constituted around 45-55% of total biomass under "non-stressed" conditions, but below 15°C, or below 15%o, above 40%o, or below 70/zE m-2 s - l, relatively more new growth (up to 68% of total biomass) was channelled into the leaves. Of the below-ground biomass, under non-stressed conditions roots and rhizomes comprised about half each, but again this altered under stress to 70-75 % of belowground biomass in the rhizomes, and 20-25% in the roots. Root lengths were relatively more affected by stressed conditions than rhizome internode lengths (Fig. 17). 3.8. Computer simulation of growth

Growth rates measured in the field are compared with those produced by model simulation in Fig. 20. Environmental data used in the simulation were the monthly data collected for each site. Both real and simulated data followed identical seasonal trends; growth rates increased during spring to reach a summer maximum, then declined during autumn. Although productivity was not measured in the field during winter, simulated data suggested productivity reached a seasonal minimum during July, and a negative productivity at the deepest site (site 5A) suggesting respiratory losses during winter. Agreement between absolute rates was generally good except during the spring months, when simulated rates were consistently higher than field rates. It was also noticeable that at site 6, observed growth rates in summer were higher than the model predicted. Model predictions of the factor(s) that limited growth are listed for each month of the year in Table 8. Two sets of figures are presented; one in which the model was run with observed attenuation coefficients (sampling was more frequently conducted on days with clear, calm conditions), and the other with attenuation coefficients such as typically caused by wind-stirring or phytoplankton blooms. The data indicate clearly the importance of light penetration to the growth of Halophila ovalis. Under clear, calm conditions, the data in Table 8 indicate that temperature limited growth for most of the year, although light was the major limiting factor during winter. However, under conditions of wind-stirring or a phytoplankton bloom, light became the major limiting factor for most days throughout the year, particularly from April to September. Presumably this effect would be less pronounced for shallower sites, but at deeper sites light would be limiting all year. Interestingly, even when higher attenuation coefficients were used (see Fig. 20), the model predicted much higher growth rates than were observed in the field during those months (October, November', December) when light was (theoretically) less likely to be limiting than temperature.

30

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

/e

simulated

*---.

32-

,

/

\,,

s,te2

.

16 "lk

/~

,~.... {.. ~ .,~"

',~,

site

5

,.

///

"13 o

o.

"o t

48

.>

32.

0

32 • _ _ g"

OIN~D

"~,

J I F'

MI

site 8

Arid

1981 Fig. 20. Growth rates of

' J

w

d

r

A

J

S

i

O

i

1982

Halophila ovalis measured at four sites in the Swan/Canning Estuary compared with

those produced by computer

model simulation.

Either light is not sufficiently well-described in the model or some other factor was limiting growth in the field. 3.9. Nutrients in biomass 3.9.1. Seasonal changes in nutrient concentration

There was little seasonal variation in AFDW and carbon concentration of the roots, rhizomes and leaves of Halophila ovaIis (Table 9), and little difference between the six sites analysed. There were small seasonal changes in nitrogen and phosphorus concentra-

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

31

Table 8 Computermodelpredictionsof the majorfactor( s) limitingthe growthof H. ovalis in the Swan/ CanningEstuary. The model was run with both measured and adjusted (+0.2) attenuationcoefficient;the latter allowed for the effects of wind stirringand/or phytoplanktonblooms Month

Major limitingfactor(s) a

January February March April May June July August September October November December

Undermeasured field conditions

With increased b light attenuation

Temperature Temperature Light/temperature Light Light/temperature Light/temperature Light Light/temperature Light/temperature Temperature Temperature Temperature

Light Light Light Light Light Light Light Light Light Light/ temperature Temperature Light/ temperature

Two factors are listed if the computermodel indicatedthey both limitedgrowth to the same degree. Owing to wind stirringand/or phytoplanktonblooms. tions in the rhizomes and leaves o f H a l o p h i l a ovalis (Fig. 21 ), but little change in the roots. As with carbon content, there was little difference between sites in nutrient concentrations, and data are presented as the statistical means of the six sites analysed. In contrast, there were marked differences in the nitrogen and phosphorus concentrations of the different organs (Fig. 21), although differences in phosphorus concentration were less pronounced than for nitrogen. From early summer to mid-winter leaf and rhizome nitrogen concentrations remained relatively constant at 17 mg and 8 mg N g - ~ DW respectively, but by late winter concentrations had almost doubled. Maximum nitrogen content was reached by early spring in both 1981 and 1982, but fell rapidly to " s u m m e r " levels by late spring. Seasonal changes in phosphorus concentration underwent the same seasonal trends as nitrogen concentrations, but were less pronounced. From early summer to midwinter leaf and rhizome concentrations averaged 2.3 mg and 1.8 mg P g - l DW respectively. Table 9 Ash-free dry weight (AFDW), ash content and carbon content of various tissues of Halophila in the Swan/ CanningEstuary (mean 5: SE) Tissue type

Leaves Rhizomes Roots

Summer phase (Sept.-May)

Winterphase (June-Aug.)

AFDW (%)

Ash (%)

Carbon (%)

AFDW (%)

Ash (%)

Carbon (%)

61.7+0.3 63.25:0.3 38.15:0.8

38.3+0.3 36.85:0.3 61.95:0.4

30.2+0.2 31.05:0.2 18.75:0.4

70.4+0.3 69.55:0.4 39.75:1.1

29.65:0.3 30.55:0.4 60.3+1.1

34.5+0.2 34.05:0.2 19.55:4

32

K.

H i l l m a n et al. / A q u a t i c B o t a n y

51

(1995)

1-54

_ _

a)

leaves

....

--

d~.~es roots

30"

25" A j 20"5

~ 15. i/

~ z

10-

I

I" - P - - - i - - - "~" . . . .

{

I" !

I

.!

:'M'

A'M'

I

t

I" "'I.

f I z

]

J ' J 'A'S'O'N'O'

J 'F

1961

i. • .}

..........

'M'A'M'

J'

l

S'O'

1982

IMvee

m

b)

J'A'

•I

.....

5-

g

,~"J ~ m ,, 6

.

roots

"'r

o.

z ...... ~

F'M'A'Mr

t. . . . . . t....... t....}....~

d ' J'A' 1981

t

S'O'N'

1....I. t °

D'

J' J

.....' 1 . . . t

F'M'

1

I

A' M' J

t

~

~

1

J'A'fl'O'

1982

Change in the roots, rhizomes and leaves of H a l o p h i l a ova~is in the S w a n / C a n n i n g Estuary, February to October 1 9 8 2 : ( a ) total nitrogen concentration; (b) total phosphorus concentration. Data are shown as the mean for six sites, with standard error bars included. Fig.

21.

1981

Rhizomes had proportionally far more phosphorus relative to nitrogen.Nitrogen concentrations in rhizomes were about half those in leaves for most of the year (excluding spring), whilst phosphorus concentrations were almost 80% of leaf concentrations for the same period (Table 10). Rhizome N:P ratios were approximately half those of leaves for most of the year. The N:P ratios of roots and leaves showed little seasonal variation, and roots contained slightly more phosphorus relative to nitrogen than leaves. Fig. 22 shows the amounts of nitrogen and phosphorus bound up in the various organs on a unit area basis. In

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

33

Table 10 N : P ratios by atom of various tissues of Halophila in th Swan/Canning Estuary, 1981-1982. Values are shown for the seasonal extremes of nutrient content, August representing the seasonal maximum and April the seasonal minimum (mean + SE) Date

Tissue N: P ratio

April 1981 August 1981 April 1982 August 1982

Leaves

Rhizomes

Roots

6.87 ± 0.25 7.13 + 0.28 7.19 + 0.58 7.40 ± 0.30

3.77 5:0.09 7.18 + 0.44 4.28 + 0.27 6.72 ± 0.31

5.80 5:0.22 6.94 + 0.67 5.78 ± 0.51 5.64 ± 0.26

a) 2700.2400" 2100. 180~ 1500-

E z1200-

900-

I~lve6

600-

300,i

1.

b)

-

"

o

-

-

F'M'A'M'J'J'A'S'O'N'D'J'F'I~'A'M'J'~'A'S'~'

S'O'N'D'J

i

,.,1

I

1.2

400-

300-

,°'E O. 2 0 0 -

F 100-

S

0

N

1980

D

J l

FVM

AIM

J

J

1961

A

S

0

N

0

J l

F

M

A

M

J

J

A

S

0

1962

Fig. 22. Changes in the amount of nutrients bound in a uniform stand of Halophila ot,alis in the Swan/Canning Estuary, September 1980 to October 1982: (a) total nitrogen; (b) total phosphorus. Data are presented as cumulative plots of the contributions of roots, rhizomes and leaves.

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

34

Table 11 Total biomass (t DW) of Halophila in the Swan/Canning Estuary during maximumseasonal biomass, with correspondingamountsof nitrogenand phosphorus bound in the tissues Depth ainterval (m) 1976 0-1

1-2

Seagrass cover(%)

Area occupied ( × 106m2)

Biomassb (t DW)

Nitrogenc (kg)

Phosphorusc (kg)

85-100 45-80 5-40 85-100 45-80 5-40

1.43 1.59 1.28 0.47 0.28 0.58

146 109 32 35 14 10

1716 1281 376 411 t64 118

263 196 58 63 25 18

5.63

346

4066

623

1.38 1.55 1.57 0.48 0.38 0.57

140 107 39 36 19 10

1645 1257 458 423 223 118

252 193 70 65 34 18

5.93

351

4214

632

Total 1982 0-1

1-2

Total

85-100 45-80 5-40 85-100 45-80 5-40

a Depth relativeto datum. Biomass was calculatedfor 1976 using maximumseasonal biomass (g DW m-2) values obtainedfor 19801982. Biomasswas calculatedfor 1982 using a maximumseasonalbiomassof 100 g DW m-2. c Nutrientvalues were calculated using N and P contentsobtainedduring thisstudy ( 17 mg, 8 mg and 5 mg N g- 1DW and 2.3 mg, 1.3 mg and 0.8 mg P g- 1DW for leaves, rhizomes and roots, respectively),and assuming a 2: 1: 1 proportioningof total biomassinto leaves, rhizomesand roots. a typical meadow, leaves contained approximately 70-80% of the total nitrogen of the plant material and 60% of the phosphorus, rhizomes contained 15-20% of the nitrogen and 30% of the phosphorus, and roots contained 5 - 1 0 % of the nitrogen and 10% of the phosphorus. Seasonal changes in the total amount of nitrogen and phosphorus per unit area largely followed seasonal trends in biomass, with the exception of the unusually high levels in August 1982, which were due to a combination of high biomass and high nutrient concentrations in leaves and rhizomes.

3.9.2. Total biomass and nutrients bound in Halophila ovalis The total biomass of Halophila ovalis in the estuary during periods of maximum seasonal biomass in 1976 and 1982 is shown in Table 11, along with the total amounts of nitrogen and phosphorus in plant tissue. These were calculated using typical tissue concentrations of nitrogen and phosphorus (leaves, 18 nag N g-~ D W and 2.3 mg P g-~ DW; rhizomes, 8 mg N g - 1 D W and 1.8 mg P g - 1 DW; roots, 5 mg N g - ~ D W and 0.8 mg P g - ~ D W ) , and biomass weight proportions of 50% leaves, 25% rhizomes and 25% roots. Despite changes in distribution patterns, the total biomass in the estuary differed very little between 1976 and 1982. Although errors associated with such calculations are large, values of approximately 350 t of dry weight of biomass, 4100 kg nitrogen and 630 kg of

K. Hillmanet al. /Aquatic Botany 51 (1995) 1-54

35

Table 12 Approximation of biomass and nutrients bound in Halophila in the Swan/Canning Estuary during seasonal minimum biomass, 1981 Depth" interval (m)

Seagrasscover (%)

Area occupied ( N 106 m2)

Biomassb (t DW)

0-1

85-100 45-80 5-40 85-100 45-80 5-40

1.38 1.55 1.57 0.48 0.38 0.57

25 19 7 14 7 4

433 329 121 243 121 69

57 43 16 31 16 9

5.93

76

1316

172

1-2

Total

Nitrogenc (kg)

Phosphorusc (kg)

a Depth relative to datum. b A maximum seasonal biomass of 20 g DW m- 2 was used. Nitrogencontents of 24 mg, 18 mg and 5 mg N g- ~DW of leaves, rhizomesand roots respectively,corresponding phosphorus content values of 3.5 mg, 2.5 mg and 0.8 mg P g - 1DW, and assuming a 1: 1 : 1 proportioningof total biomass into leaves, rhizomes and roots. phosphorus can be assumed as reasonably representative of the nutrients locked in Halophila ovalis during periods of m a x i m u m biomass. The greater importance of the shallower waters was also apparent, with over 80% of the total biomass, nitrogen and phosphorus in Halophila ovalis found in waters less than 1 m deep (relative to datum). Similar estimates of the total biomass in the estuary during periods of minimum seasonal biomass could not be made since water turbidity during the winter phase made aerial photography impossible, and the distribution maps could not be drawn. However, approximations were made (Table 12) using biomass data and nutrient concentrations for early spring 1981, and the distribution areas in Table 11. Thus from April 1981 to September 1981, Halophila ovalis beds in the estuary lost at least 280 t of biomass, 2800 kg of nitrogen and 460 kg of phosphorus.

4. Discussion 4.1. General distribution In Australian estuarine waters, Halophila ovalis has been recorded from brackish coastal lagoons in New South Wales (King, 1986), the estuaries of Sydney Basin, New South Wales (Larkum, 1976), the P e e l / H a r v e y estuarine system (Carstairs, 1978), and Leschenault Inlet, Western Australia (Hodgkin, 1978), but only in the Swan/Canning Estuary and Leschenault Inlet is it the dominant species. Cambridge (1980) notes that although it is common in Australian coastal waters, it usually occurs as a minor species at the edges of communities of larger species of seagrass, notably the genera Posidonia and Amphibolis. Halophila ovalis is a small, fragile plant that is easily detached by wave action, but it also roots easily from fragments, and is often the first seagrass to settle on newly available substrata (Den Hartog, 1970; Kirkman, 1985). Den Hartog (1970) further notes that in

36

K. Hillmanet al. /Aquatic Botany51 (1995)1-54

very sheltered places it is capable of forming dense stands, but it rarely does so, because where Halodule uninervis or Halodule pinifolia are present, they will dominate the community. In the estuaries of southwestern Australia this competition does not arise; Halodule uninervis only extends as far south as Dongara (29°S) and the characteristic extremes of the local estuarine hydrology exclude the larger, more stenohaline species (Cambridge, 1980). Halophila ovalis is capable of surviving in very turbid and/or polluted waters, and is also markedly eurybiontic (Den Hartog, 1970). In different parts of the world it occurs over a wide range of salinities, temperatures and light levels, and is found on substrata from soft mud to coarse coral rubble. This ecological tolerance may explain its dominance in the Swan/Canning Estuary, which has diverse sediments, and mesotrophic waters which undergo extremes in salinity, temperature and turbidity (Hillman, 1985). The relatively sheltered conditions in the estuary have also enabled it to form unusually dense stands. The distribution of Halophila ovalis in the main estuarine basin has changed little since 1976, and resembles that described by Allender (1970). Halophila ovalis has re-established in the Canning since this study ended, and so although its distribution in the main estuarine basin appears relatively stable, it is more ephemeral in the Canning. The distribution ofHalophila ovalis appeared to be affected by salinity, light, and duration of emersion. In both this study and that of Allender (1970), Halophila ovalis was not found above the summer extreme low water mark, illustrating the importance of emersion. Similar observations have been made in local coastal waters (Cambridge, 1980). Halophila ovalis was not found in the upper estuary; this exclusion could have been due to either the salinity regime or the turbidity of the waters. Salinity levels in the upper estuary were less than 10%o for most of the year, and the photic zone was too narrow to allow the establishment of benthic plants (Hillman, 1985). However, it was not clear if light or salinity was the more important factor in determining the limit of Halophila ovalis distribution upstream. Conditions of low light and low salinity were probably also responsible for the dieback observed in the Canning. The physiography of the Canning, its relative isolation from tidal influence, and the high volumes of winter runoff in 1981, combined to produce essentially freshwater conditions for almost 4 months, and during this period less than 1% of incident light reached the bottom when depths were greater than 1 m. In the estuarine basin similar conditions only prevailed for approximately 2 months. The vertical distribution of Halophila ovalis in the estuary was apparently determined by light (Spence, 1976). Howard-Williams and Liptrot (1980) and Bulthuis (1983), using both experimental work and literature surveys, indicate that benthic angiosperms are excluded at depths where light intensities are less than 5-15% of surface levels. In the estuarine basin of the Swan/Canning Estuary, Halophila ovalis was not found where light levels during the summer period were less than 2-5% of incident light, although conditions of lower light (0-1.1% of incident light) were tolerated during the winter phase. Halophila ovalis was found at depths of up to 4.5 m in the clearer waters of the inlet channel, but again the vertical depth limit corresponded to 2-5% of incident light. 4.2. Biomass Lipkin (1979) reported a standing crop of 16-20 g DW m - 2 for Halophila ovalis in the coastal waters of Israel, Ogden and Ogden (1982) found a standing crop of 2 g DW m -2,

K. Hillman et al. /Aquatic Botany 51 (1995) 1-54

37

and Nair et al. (1983b) reported a maximum seasonal standing crop of 48 g DW m -2. Values reported for Halophila ovalis in this study are therefore amongst the highest known for the species. The unimodal seasonal variation of biomass reported here for Halophila ovalis, with peak biomass in late summer/early autumn, followed by a decline in winter, is reported for many temperate seagrass beds (e.g. Jacobs, 1979; West and Larkum, 1979; Pinnerup, 1980; Harrison, 1982; Bulthuis and Woelkerling, 1983; Sand-Jensen and Borum, 1983; Wetzel and Penhale, 1983; Wium-Anderson and Borum, 1984). In the above studies, conditions of light, temperature and (for estuaries) salinity were most favourable for seagrass growth during summer, by the end of which peak biomass was achieved. Exceptions to this trend can occur; for example Aioi (1980) reported a maximum seasonal biomass in spring for Zostera marina L. growing in Odawa Bay, Japan, where the rainy season (and therefore decreased insolation) occurs in June. Light appeared to be an important factor determining seasonal trends in the biomass of Halophila ovalis in the Swan/Canning Estuary during the study period as was found by Nair et al. (1983a,b) for the growth of tropical Halophila ovalis beds--whilst salinity was implicated as an important factor in causing biomass declines during winter months. During the winter phase of 1981, when seagrass beds experienced almost freshwater conditions, biomass declines were more severe in the shallower sites, where lower salinities prevailed for longer periods. During the winter of 1982, salinity rarely fell below 20%0, and since temperatures were similar to 1981, and light levels were also low during this period, it is suggested that biomass decline was slight because salinity remained relatively high. Differences in the winter decline in biomass between the 2 years were also responsible for the different trends in attaining maximum biomass (Fig. 6), since the seagrass meadows took longer to recover from the reduction during the more severe 1981 winter. Unfortunately, as pointed out by Hillman et al. (1989), there are few complete measurements of all the components of seagrass biomass, largely because of the problems in collecting root material. Sand-Jensen (1975) found a seasonal variation in the ratio of above-groundtobelow-groundbiomassofZosteramarinaofl:2 (winter) to 1:1 (summer), and Jacobs (1979) and Aioi (1980) reported similar results for the same species. In this study, the ratio of above-ground to below-ground biomass of Halophila ovalis also varied from 1:1 (summer) to 1:2 (winter) during 1981, but remained relatively constant at 1:1 during 1982 owing to the less severe dieback of above-ground parts in winter. No change was found in the apportioning of total biomass between various plant parts of Halophila ovalis with increasing depth as was also found by Lipkin (1979) for Halodule uninervis over a narrow depth range similar to that occupied by Halophila ovalis in this study. There was, however, a pronounced change in the biomass of Halophila ovalis with depth. Maximum biomass appeared to increase with depth up to 0.8 m (relative to datum), and thereafter declined. The effect of depth on biomass attained by seagrass has been noted by a number of other workers. For example, Jacobs (1979) reported an increase in the standing crop of Z. marina down to 0.5 m, followed by a decline with increased depth, and Lipkin (1979) reported an increase in the biomass of Halophila stipulacea (Forssk.) Aschers. down to a depth of 10 m, then a decrease with increasing depth, with a similar trend within a much narrower depth range for Halodule uninervis. Hulings (1979) also reported a decrease in standing crop of Halophila stipulacea from 1 to 45 m. Although other

38

K. Hillman et al./Aquatic Botany 51 (1995) 1-54

factors may alter with depth (e.g. pressure, sediment type, water motion), light has been implicated as the cause of these changes. Certainly the work of Backman and Barilotti (1976), Congdon and McComb (1979) and Bulthuis (1983), in which manipulation of light regimes by shade screens affected the density of Z. marina, Ruppia maritima L. and Heterozostera tasmanica (Martens ex Aschers.) den Hartog respectively, suggests that light is the critical factor. It can be concluded that 0.8 m was the depth at which maximum biomass was achieved because the light regime was optimum for the seagrass at this depth, with higher light levels during summer causing photoinhibition, as has been demonstrated for Halophila stipulacea by Drew (1979), and/or depths less than 0.8 m were insufficient to protect the seagrass from some other environmental factor(s), such as salinity or temperature extremes, or excessive sediment movement due to wave action caused by wind stirring in the shallows. At depths greater than 0.8 m, light levels were presumably insufficient to maintain maximum possible biomass. The density of growing shoots (apices) was, predictably, dependent on rhizome biomass, and therefore seasonal trends in shoot density closely followed seasonal trends in rhizome biomass. Although no values are reported in the literature for shoot density of Halophila ovalis, the maximum values reported in this study are comparable to the highest values reported for temperate seagrass meadows of Z. marina (e.g. Jacobs, 1979; Aioi, 1980; Harrison, 1982) and Heterozostera tasmanica (Bulthuis and Woelkerling, 1983). However, the maximum shoot density of 2500 m - 2 recorded here for Halophila ovalis is much lower than the high values reported by McMahan (cited by McRoy and McMillan, 1977) for a tropical meadow of Halodule beaudettei (den Hartog) den Hartog (in excess of 15 000 shoots m - 2). Shoot density of Halophila ovalis was related to rhizome biomass, but the marked difference in this relationship between the shallowest and deeper sites was somewhat unexpected. This could not be attributed to differences in rhizome weight per unit length since this differed little between sites. The higher shoot densities at the two shallowest sites were probably due to exposure to greater environmental extremes than those experienced in deeper waters, which caused activation of lateral meristems due to removal of or damage to the apical meristem: wave action in the shallower sites commonly resulted in breakage of the brittle rhizomes.

4.3. Primary production Although Halophila ovalis is one of the smallest seagrasses, in terms of primary production it compares well with much larger species (Table 13). The high primary production and low biomass of Halophila ovalis result in a high specific growth rate (4-9% day-1, or a crop replacement time of 11-24 days), that is matched by other small species of seagrass such as Halophila decipiens Ostenfeld, Halophila hawaiiana Doty et Stone and Syringodium filiforme Ktitz. (see Table 13). As pointed out previously (Hillman et al., 1989), two categories of seagrass can be recognised on the basis of annual production, specific growth rates and turnover times. Small colonising genera such as Halodule, Halophila and Syringodium often have specific growth rates greater than 4% day- ~and may produce more than five crops per year, whilst the larger "climax" species usually have specific growth rates

K. HiUman et al. /Aquatic Botany 51 (1995) 1-54

39

Table 13 The productivity of Halophila ovalis in the Swan/Canning Estuary compared with other measurements of seagrass productivity from the literature in which tagging methods were used Species

Plant part

Halophila ovalis

Leaves 0.8-2.0 Whole plant 1.6-3.3 Leaves 0.8

Swan/Channing Estuary

This study

Florida, USA

Leaves Leaves Leaves Leaves Leaves Leaves Leaves Leaves Whole plant Leaves Whole plant Temperate Tropical

Victoria, Australia New South Wales, Australia Westem, Australia New South Wales, Australia Westem Australia Western Australia Westem Australia Florida USA Denmark France

Zieman, cited in Zieman and Wetzel, 1980 Kirkman and Reid, 1979 Kirkman and Reid, 1979 Cambridge, 1980 West and Larkum, 1979 Walker and McComb, 1988 Cambridge, 1980 Walker and McComb, 1990 Zieman, 1975 Sand-Jensen and Borum, 1983 Jacobs, 1979

Syringodiumfiliforrne Heterozostera tasmanica Posidonia australis Posidonia australis Posidonia australis Posidonia australis Posidonia sinuosa Amphibolis antarctica Thalassia testudinum Zostera marina Zostera marina Annual agricultural plants

Productivity a Locality (g C m -2 year - ~)

0.43-0.63 2.4 1.9 0.5-1.2 0.8 1.4 1.3 0.8-1.8 1.1-2.2 1.1 1.6 1.8-2.5 2.4-3.6

Reference

Westlake, 1963

Productivity values were calculated as g carbon m -2 day- 1 averaged over 1 year. In most cases published figures were for grams dry weight, but have been multiplied by the fraction 0.37 to convert to carbon, based on determinations for Swan River material, and if necessary converted to a daily rate.

less than 4% day- 1 and produce two to five crops per year. Certainly the ability to establish and grow quickly is a useful attribute for a coloniser species, which in general, and certainly for Halophila ovalis, is said to be the role played by the smaller species (Den Hartog, 1977). In view of the measurements obtained in this and other studies (Herbert, 1986; Josselyn et al., 1986; Kenworthy et al., 1989), it seems fair to conclude that if appreciable amounts of smaller species of seagrass are present in a mixed community, measurements of their primary production are justified, since their contribution to overall community productivity may be significant. The high productivity of Halophila ovalis may also explain its low epiphyte load. The small size and fragile tissues of this species make it mechanically incapable of supporting heavy epiphytic loads, but in addition, as discussed by Sand-Jensen (1975) and Johnstone (1979), a high leaf turnover rate ensures that epiphytic loads are kept low. Epiphytes have a better chance of establishing on leaves with a longer life span, if other conditions are equal. Den Hartog (1977) has noted in a qualitative sense that rapidly establishing colonies of the smaller seagrasses carry few epiphytes, and Jacobs and Noten (1980) have reported that seasonal changes in the life span of Z. marina leaves influenced epiphyton community structure. However, as has been pointed out by Penhale (1977) and Harlin (1980), the turnover of epiphytic algae is often greater than that of the host plant, and it is easy to underestimate their importance. Ogden (1980) and Orth and van Montfrans (1984) also emphasise that the contribution of epiphytes to the total productivity of a seagrass meadow may be considerable, but this may not be apparent if grazing keeps epiphytic biomass low. These points may well apply to beds ofHalophila ovalis in the Swan/Canning Estuary.

40

K. Hillmanet al. /AquaticBotany51 (1995) 1-54

4.3.1. Below-ground production There are few data on the below-ground primary production of seagrasses. The belowground productivity of Halophila ovalis constituted 40--60% of total productivity at all sites. These data contrast strongly with those for large-leaved species, which usually have a below-ground production of 10-30% of the total production (Hillman et al., 1989). Since the below-ground and above-ground biomass ofHalophila ovalis also each constituted 50% of total biomass at these sites, the turnover rates of above-ground and below-ground tissues were approximately the same. An apparent anomaly at site 2 (where above-ground productivity comprised 40% of the total, implying that the turnover rate of below-ground parts was higher than above-ground parts) could be attributed to difficulties in fully recovering root material from the coarse, shelly sediments at this site. 4.4. Seasonal changes in productivity 4.4.1. Light The unimodal seasonal pattern of productivity observed for Halophila ovalis during this study, with its summer maximum and winter minimum, is typical of most sub-tidal seagrasses growing in temperate waters (e.g. Sand-Jensen, 1975; Jacobs, 1979; West and Larkum, 1979; Clough and Attiwill, 1980; Sand-Jensen and Borum, 1983). Most studies attribute this pattern to seasonal changes in insolation, although Bulthuis and Woelkerling (1983) concluded that some other factor(s) appeared to be important since they measured declines in the productivity of Heterozostera tasmanica that were proportionally much greater than the reduction in insolation. However, in this study and most of the above studies, of the environmental factors investigated, seasonal changes in primary production most closely resembled the curve for seasonal changes in insolation. The pronounced effect of depth on annual productivity in this study (Table 5) also demonstrated clearly the importance of light. The most likely cause of the difference between maximum productivity reached in 1981 and 1982 (Fig. 9) was short-term changes in light reaching the seagrass beds, since salinity and temperature conditions during the summer months in both years were essentially the same. It should be emphasized that since environmental parameters were measured at monthly intervals, it was not possible to detect short-term changes. Given the climate and hydrology of the Perth region, it is unlikely that significant short-term changes in salinity and temperature would have affected the seagrass, but as so effectively shown by Wetzel and Penhale (1983), both incoming insolation and attenuation of PAR by estuarine waters can change rapidly within days. In the Swan/Canning Estuary ephemeral phytoplankton blooms and/or wind-stirring can cause marked increases in the attenuation of light by the water column, and since the estuarine waters are relatively turbid, tidal fluctuations may also have a significant effect. In addition, under certain wind conditions during the study, free floating algae were observed to accumulate over some of the seagrass beds, effectively blocking out the light supply, sometimes for up to 3 days. 4.4.2. Temperature In addition to the obvious importance of light, temperature was indicated as an important factor affecting growth, which was expected for an essentially tropical species growing in temperate waters. Statistical analyses suggested that temperature was the most important

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41

factor, but it was difficult to decide if this was a correct interpretation because there was a strong correlation between temperature and insolation. Certainly conditions would be more favourable for this species during the warm summer months, but since temperature varied little in the summer and large fluctuations in productivity still occurred, it was probably not the major limiting factor. However, it is possible that temperature was a major limiting factor in early spring and late autumn, when apparent light levels should have supported a higher productivity than was measured, although it was not possible to certify this on field data alone. It is also possible that Halophila ovalis never experienced optimum temperatures for growth during this study.

4.4.3. Salinity The effect of salinity on the growth of Halophila oval& was even less clear, since periods of low salinity coincided with conditions of low light and low temperature. Although it is a euryhaline species, it seems unlikely that Halophila ovalis would tolerate prolonged conditions of freshwater. Prolonged periods of low salinity during years of heavy winter runoff would probably severely affect its growth, but the maintenance of healthy stands of seagrass during the winter of 1982 indicated that salinities as low as 15-20%o were tolerated. Broad salinity tolerances have been demonstrated for a variety of seagrass species both in the field (Zieman, 1975; Pinnerup, 1980; Walker, 1985) and the laboratory (McMillan and Moseley, 1967; McMahan, 1968; Biebl and McRoy, 1971; McMillan, 1974; Drysdale and Barbour, 1975; Walker and McComb, 1990) although most species appear to tolerate hypersaline conditions better than hyposaline. From these studies it may be postulated that spring salinities could have suppressed the growth of Halophila ovalis during the study period. Laboratory studies would be needed to confirm this.

4.5. Morphological changes As yet few workers have examined seasonal changes in the biometry of seagrasses in temperate waters. Bulthuis and Woelkerling (1983) found no seasonal variation in leaf lengths or widths in Heterozostera tasmanica, although differences in leaf sizes between sites were noted with the largest, widest leaves were at sites receiving lowest irradiance. In contrast, Cambridge (1980) reported a summer maximum for leaf length in Posidonia sinuosa Cambridge & Kuo and Sand-Jensen and Borum (1983) reported summer maxima for leaf and rhizome internode lengths of Z. mar/na. In the last two studies, light was implicated as the environmental factor responsible, maximum light coinciding with maximum leaf and rhizome internode size. In contrast with seasonal changes, studies of between-site differences indicate that decreasing light corresponds to increased leaf size, as noted by Bulthuis and Woelkerling (1983). Bulthuis (1983) also found that leaf lengths of Heterozostera tasmanica increased when light supply was reduced in situ using shade cloth. In sub-tropical waters, Hulings (1979) and Lipkin (1979) reported an increase in the length of Halophila stipulacea leaves with increasing depth, and attribute this trend to decreasing irradiance. Both workers also noted that whilst the trend was consistent at all sites measured, there were significant differences in leaf sizes between sites which appeared to be genetically determined.

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K. Hillmanet al. /Aquatic Botany51 (1995)1-54

Much work has been carried out on morphological variation in seagrasses using laboratory cultures and field transplants (e.g. McMillan, 1978, 1983; McMillan and Phillips, 1979; Phillips and Lewis, 1983). These show that whilst environmental factors influence leaf size and/or shape in situ, there are definite genotypic differences between different populations of any one species. Thus whilst the width and/or length of a seagrass leaf depends on its immediate environment, its size, and the limits of its ecoplasticity are determined by genotype. In the Swan/Canning Estuary, maximum root and rhizome internode lengths, and minimum petiole lengths, were clearly correlated with conditions of high irradiance, temperature and salinity, but on the basis of field results alone it was not possible to discern which factor was most important. The above-mentioned studies of Hulings (1979), Lipkin (1979), Bulthuis (1983) and Bulthuis and Woelkerling (1983) suggest that the occurrence of maximum petiole lengths in Halophila ovalis during spring and autumn may well be a response to lower light levels than in Summer. The occurrence of maximum leaf blade lengths during summer at the two deeper sites (5A and 5B) may also have been a response to higher light levels. At the shallower sites, the short, broader leaves that were produced during summer could conceivably indicate a saturating light supply (for a large part of the day), whilst at the deeper sites, where light was usually limiting (according to field data), larger leaf blades may have been produced when conditions for growth were most favourable. This could not be confirmed on the basis of field data alone. Although seasonal trends in morphology were consistent between sites of similar depth, the considerable variation in leaf size between sites showed that several distinct populations were present, either genotypic or related to habitat. The results of McMillan (1983) on Halophila ovalis from sub-tropical waters suggest that the significantly larger leaves at site 6 compared with site 2 were probably a result of the environmental stress of constant wave action and sediment movement rather than genotypic differences, but further work incorporating laboratory cultures and transplants would be necessary to confirm this. 4.6. Growth in the laboratory The biometry of Halophila ovalis grown in the laboratory was well within the range recorded for plants in the field. Laboratory production rates did not usually reach field rates, but this was probably a consequence of comparing excised segments of plants several internodes long with intact plants. For this reason, laboratory responses were expressed as percent of maximum growth attained in the field rather than absolute growth rates for the purpose of computer simulation. However, the fact that even the severed segments of Halophila ovalis achieved growth rates in excess of 3 mg DW per apex day-1 further emphasised the ability of this species to attain high levels of productivity. 4. 7. The effect of light The saturating irradiance of approximately 200/zE m-2 s-1 (10% of surface PAR) measured for Halophila ovalis in the laboratory was lower than the 350/zE m -2 s - l predicted from field data (Hillman, 1985). Buesa (1975) also reports that Thalassia testudinum Banks ex K6nig and Syringodium filiforme saturated at lower light levels under

K. Hillmanet al./ AquaticBotany51 (1995)1-54

43

laboratory conditions than in the field. Buesa (1975) offers no explanation for this, but it seems probable that it is caused by the difference between the uniform light conditions produced by an artificial light source, and the constantly changing light climate experienced by plants in the field. The light response of Halophila ovalis recorded here is very similar to responses reported for other seagrasses cultured under artificial light (Buesa, 1975; Drew, 1979; Beer and Waisel, 1982). The ten species of seagrass examined in the above studies (including the present one) all saturated at irradiances corresponding to 10-15% of full sunlight PAR (temperate and subtropical latitudes), and reached compensation points at 1-2% of full sunlight PAR.

4.8. Ecology ofHalophila ovalis in the Swan~Canning Estuary The low saturation and compensation irradiances obtained for Halophila oval& indicate that it is well adapted for survival in turbid estuarine waters. The compensation irradiance obtained closely approximates light levels at the depth limit of Halophila ovalis in Swan/ Canning Estuary, and it is clear that light levels alone would exclude this species from the upper estuary. The ability of Halophila ovalis to maintain high growth rates at low light levels conforms to the behaviour of the "coloniser species" discussed by Williams and McRoy (1982). This ability enables Halophila ovalis to maintain maximum growth rates more often in the widely fluctuating light environment of the turbid waters of the Swan/Canning Estuary, although shallow water populations may occasionally be photoinhibited in summer. Results also suggest it is capable of enduring very low light levels for at least a month, which would enable it to maintain populations during winters of average runoff. However, the extended period of low light that plants would have experienced in the Canning Estuary during the 1981 winter would certainly have been sufficient to cause the dieback observed, and the less severe light conditions experienced in the estuarine basin during the same period were sufficient to have caused the observed biomass decline.

4.9. The effect of temperature The linear response of Halophila ovalis to temperature recorded in this study is very similar to temperature responses obtained by Biebl and McRoy ( 1971 ) for Z. marina, by Drew (1979) for four species of seagrass, and by Barko et al. (1982) for three species of submerged freshwater angiosperms. However, it should be pointed out that only the last two studies measured responses under saturating light conditions. The temperature response of Halophila ovalis in this study was studied at just under saturating light levels, so that results may not depict full sensitivity to temperature, although general trends should be colxect. The results indicate clearly that growth of Halophila ovalis is severely restricted below 15°C. The absence of growth at 10°C is also consistent with the observation by Den Hartog (1970) that this species is not found in waters experiencing temperatures below 10°C. However, it is equally clear that temperatures experienced during winter in the Swan/ Canning Estuary would alone not be sufficient to have caused the 1981 biomass decline, nor is the temperature regime of the upper estuary sufficiently extreme to exclude Halophila ovalis.

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The temperature optimum of Halophila ovalis remains to be determined, since this study only looked at the range experienced in the field. It is unlikely that 25°C is the optimum, since all other seagrasses examined have had optima in excess of 28°C, regardless of whether they are tropical, subtropical or temperate species. However, these studies were largely based on either survival or short term photosynthetic rates, not on growth responses. Walker and Cambridge (1995) found that maximum survival rates were at 15°C for Amphibolis species, although maximum growth rates were at 25°C. The data presented here suggest that over the range of temperatures experienced in the Swan/Canning Estuary Halophila oualis is capable of active growth. They also indicate that this species is much more sensitive to temperature changes over the range 15-20°C than 20-25°C, and that temperatures in the estuary during the early spring and late autumn of the study may have been sufficiently low to explain the low growth rates measured. However, the suggestion by Bittaker and Iverson (1976), Drew (1979) and Wetzel and Penhale (1983) that seagrasses may undergo seasonal adaptation to environmental conditions should not be discounted. Such effects are certainly well documented for algae (e.g. Aruga, 1965; Steemann Nielsen and Jrrgensen, 1968; Gordon et al., 1980). The plants used in this study were harvested during mid-autumn, and it would be interesting to see if temperature responses differ for plants harvested in summer or winter. The importance of light-temperature interactions, as discussed above, also deserves further investigation. Ideally, a series of curves depicting the light responses of Halophila ovalis at different temperatures should be generated.

4.10. The effect of salinity The demonstrated ability of Halophila oualis to grow actively at salinities at 10--40%o clearly establishes it as a euryhaline species, although it is equally certainly an obligate halophyte. The results suggest that it is capable of withstanding both hypersaline conditions and very low salinities for periods of up to 1 month. The effect of salinity on net growth of Halophila oualis is similar to the response of net photosynthesis to salinity reported for Zosterajaponica Aschers. & Graebn. (as Zostera nana Roth) (Ogata and Matsui, 1965) and Z. marina (Biebl and McRoy, 1971), two other euryhaline seagrasses. Few other direct comparisons can be made since most other laboratory studies on seagrasses only report survival rather than growth rates at different salinities (e.g. McMillan and Moseley, 1967; McMahan, 1968; McMillan, 1974). Nor have any laboratory studies examined the effect of salinity-temperature interactions on seagrasses. The work of Zieman (1975) certainly suggests this may be important, since in situ extremes of temperature appeared to increase the sensitivity of Thalassia testudinum to low salinities. As with light-temperature interactions, ideal data should consist of a series of curves depicting salinity responses at different temperatures. These results suggest that the conditions of low salinity (less than 119%o) which prevail for months in the upper estuary (Hillman, 1985) would alone be sufficient to exclude Halophila ovalis from that region, even if light conditions were favourable. Salinity levels during the winter/spring of 1981 were also certainly low enough to have caused the disappearance of Halophila ovalis from the Canning Estuary, and the biomass decline in the estuarine basin. However, although the data suggest that Halophila ovalis prefers oceanic

K. Hilhnan et aL /Aquatic Botany 51 (1995) 1-54

45

salinities, it appears it would be little stressed by salinities prevailing during winters of low to average runoff (around 2(F/oo). 4.11. Morphological responses

On the basis of laboratory results, the morphology of Halophila ovalis in the field would be little affected by salinities between 15 and 35%0, but outside this range plant size would be severely reduced, particularly under hypersaline conditions. New growth produced by laboratory plants at 45%0 appeared extremely stressed; plant parts were half normal size, leaf margins were noticeably wrinkled, and leaves were extremely brittle. Plants of this appearance were not seen in the Swan/Canning Estuary (which did not become hypersaline during the study period), but have been noticed under hypersaline conditions in the Peel/ Harvey estuarine system by S. Carstairs (personal communication, 1983). The morphological effect of low salinities was also not seen in the Swan/Canning Estuary during the study, since concurrent conditions of low light and low temperature prevented the production of new tissues. The literature offers few data as yet on the effects of salinity extremes on seagrass morphology. Presumably this is because most seagrass studies have involved coastal areas rather than estuaries, and light and temperature have been more important. Zieman (1975) reported that low salinities caused shorter leaves of T. testudinum to be produced in Biscayne Bay, Florida, and Walker (1985) reported significantly narrower leaves of Amphibolis antarctica growing in hypersaline areas of Shark Bay, compared with plants growing in nearby areas under marine salinities. Concerning light and temperature, the results suggested that these factors were equally important in affecting the morphology of Halophila ovalis in the field. The data demonstrated the importance of light-temperature interactions, but effects on root and rhizome morphology were quite different to that on leaves. Under non-saturating light conditions, rhizome internode and root length increased as temperatures increased from 15 to 25°C, but maximum sizes were only realised at 25°C under saturating irradiances. In contrast, increasing light and increasing temperature caused opposing responses in petiole length (and to a much lesser extent leaf blade length). Under non-saturating light levels, petiole lengths increased as temperatures rose from 15 to 25°C, but at 25°C saturating light levels overrode the temperature response, and petiole lengths decreased significantly. The opposing effects of light and temperature on seagrass leaf morphology can also be discerned from the literature. Increasing leaf size with decreasing light has been reported for Halophila stipulacea (Hulings, 1979; Lipkin, 1979) and Heterozostera tasmanica (Bulthuis, 1983). Increasing leaf size with increasing temperature has been reported for T. testudinurn (Zieman, 1975) and Halophila ovalis (McMillan, 1983). Of course results for a few species are not necessarily universally applicable, and laboratory studies on the effect of light-temperature interactions on seagrass morphology are yet to be carried out. Such studies have been carried out on the morphology of submerged freshwater angiosperms (e.g. Spence, 1976; Barko et al., 1982), and also demonstrate the opposing effects of light and temperature, notably on shoot length. In the Swan/Canning Estuary, it seems certain that the shorter petiole lengths produced in summer (compared with spring and autumn) were due to higher light levels. This may

46

K. Hillmanet al. /Aquatic Botany51 (1995)1-54

have been the beginning of a photoinhibition response, and is worth investigating since although production rates were not depressed at higher light levels in the laboratory (greater than 200/zE m - 2 s - ~), leaves were almost colourless, in the same manner as shallow water populations in the field during summer (Hillman, 1985). However, petiole shortening in summer was still recorded at the deepest field site (which apparently never received photoinhibitory light levels), though the effect was less dramatic than at the shallower sites (Hillman, 1985). 4.12. Computer simulation of growth Despite the relative simplicity of the computer model, and the limited set of data on which it was based, agreement between simulated and real growth rates is remarkably good, particularly in regard to seasonal patterns. The failure of the model to predict spring growth rates accurately can be attributed to two factors; in the Perth region tidal amplitude is particularly variable during spring, and this is also the season for phytoplankton blooms. Since the model only used average daily tidal depth and attenuation coefficients based on monthly measurements, the unpredictable light climate in spring was not fully simulated. The inability of the model to account for daily variations in water depth due to tidal fluctuations can be considered its main fault in view of the turbidity of the waters of the estuary. Mathematical modelling of the complex tidal patterns in southwestern Australian waters was, however, beyond the scope of this study. Additional improvements to the model would involve expressions allowing for interactions between light, salinity and temperature, and diurnal temperature variations. The latter refinement could have significant effects on spring and autumn results. As has been previously mentioned, sampling logistics were such that sites in the estuarine basin were sampled in the morning, and diurnal studies have indicated afternoon temperatures 2-3°C warmer. Of course, this would result in the model predicting even higher growth rates in spring (and autumn), which further emphasises the importance of light for plants in the field. The model reinforces the seasonal pattern of Halophila ovalis productivity measured in situ, and adds support to the proposal that light and temperature are important factors in controlling the growth of this species in the estuary. The extreme sensitivity of the model to changes in attenuation coefficient and water depth suggested that light was the most important factor during the study period, except perhaps during calm, cloud-free days. Although the model did not always accurately predict field growth rates, agreement is good enough to suggest that simple modelling based on a relatively limited data set could be an important tool in environmental management, particularly when little time is available to carry out an extensive research programme. The nitrogen and phosphorus concentrations obtained for the various organs of Halophila ovalis in this study are compared with data for other seagrasses from the literature in Table 14. Peak concentrations of nitrogen reported for Halophila ovalis in this study are amongst the highest reported, and the phosphorus concentrations are higher than any other value listed. The only values reported for Halophila ovalis in the literature are those of Birch (1975), who quotes nitrogen and phosphorus contents for whole plants of 5.9 mg and 1.5 mg g - ~DW respectively. Corresponding values for this study would be 12 mg N g - ~ DW and 1.6 mg P g - 1 DW, excluding the extremely high winter and spring values. Since the

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47

13.25 Table 14 Concentrations of nitrogen and phosphorus reported for various species of seagrass in the literature Species

Tissue

N ( m g g -~)

P ( m g g -~)

Syringodium isoetiJblium

Leaves Rhizomes Leaves Rhizomes Leaves Rhizomes Leaves Rhizomes

16.0 4.0 15.8 5.3 15.7 3.7 14.8 4.6

2.1 0.9 2.0 1.5 2.2 1.7 1.7 0,8

7.7 4.4 7.9 3.5 7.1 2.2 8.7 5.7

Leaves Rhizomes Whole plant

9.2 11.4 2.8

1.5 1,8 0,7

5.9 6.3 4.0

Birch, 1975

Whole plant

4.7

1,0

4.7

Birch, 1975

Whole plant

5.9

1,5

3.9

Birch, 1975

Whole plant

12.9

2.6

5.0

Birch, 1975

Leaves Rhiz./roots Leaves

13-14 6-10 13.25

-

-

Harlin and Thorne-Miller, 1981 Thayer et al., 1977

Leaves Rhizomes Roots Leaves

12-13.8 2.6-5.3 5.8 27.5

1.0-1.2 0.5-1.6 0.4 -

Leaves

13-37.6

-

-

Pir6, 1985

Leaves Rhizomes

14-19.5 7.5-11.0

2.0-2.4 1.2-2.1

7.5 5.8

Bulthuis and Woelkerling, 1981

Leaves

13.8-17.6

-

-

Augier et al., 1982

Leaves Rhizomes

16.9-30.5 6.4-20.4

0.93-2.29 0.50-2.28

(Aschers.) Dandy

Zostera capricorni Aschers.

Enhalus acaroides (L.f.) Royle

Cymodocea serrulata ( R.Br. ) Aschers. et Magnus

Halodule uninervis (Forssk.) Aschers.

Halophila ovata

N :P

Reference

Birch, 1975 Birch, 1975 Birch, 1975 Birch, 1975

Birch, 1975

Gaud.

Halophila spinulosa (RBr.) Aschers.

Halophila ovalis (RBr.) Hook. f.

Halophila decipiens Ostenfeld

Zostera marina L. Zostera marina L. Posidonia australis Hook. f.

Posidonia australis

l 1.3 4.3 14.5 -

Hocking et al., 1981 Augier et al., 1982

Hook. f.

Posidonia oceanica (L.) Del.

Heterozostera tasmanica (Martens ex Aschers. ) den Hartog

Cymodocea nodosa (Ucria) Aschers.

Thalassia testudinum Banks ex K6nig

14.6 9.1

Patriquin, 1972

nutrient concentrations during summer and autumn were in themselves high compared with literature values, it is suggested that the exceptionally high winter and spring values represent "luxury consumption" of nutrients beyond immediate needs for growth. The overall high nutrient concentrations can be attributed to the nutrient-rich sediments of the Swan/Canning Estuary, given the ability of benthic angiosperms to absorb nutrients through their roots (e.g. Zieman and Wetzel, 1980; Carignan, 1982). However, the unusually high winter and spring nutrient concentrations may have been caused by leaf uptake from the nutrient rich water associated with winter runoff, since seasonal increases in nutrient

48

K. Hillmanet al. /Aquatic Botany51 (1995)1-54

concentrations were marked in leaf and rhizome material, while roots remained relatively unchanged. Carignan and Kalff (1980) and Carignan (1982) attribute differences in relative contributions of roots and shoots to phosphorus uptake by aquatic macrophytes in response to differences in the availability of phosphorus from sediments and water column. On the basis of their (Carignan and Kalff) results, it seems logical to conclude that uptake of nutrients from the water column was important for Halophila ovalis during winter and early spring. The ability of seagrasses to accumulate nutrients from the water column whilst not growing actively has also been demonstrated by Harlin and Thorne-Miller ( 1981) in work involving nutrient enrichment of the water column over beds of Z. marina. The high nutrient concentrations in Halophila ovalis indicated that its growth was unlikely to be limited by nitrogen or phosphorus. In work on several submerged freshwater angiosperms, Gerloff and Krombholz (1966) have suggested that leaf concentrations below 14 mg N g - 1 DW and 1.3 mg P g - 1 DW may indicate growth limitations by these nutrients. At no stage in this study did leaf nutrient concentrations drop below 15 mg N g- ~DW and 1.8 mg P g-1 DW, and in fact average nutrient concentrations in Halophila ovalis were comparable to those obtained in seagrasses subjected to nutrient enrichment studies (Bulthuis and Woelkerling, 1981; Harlin and Thorne-Miller, 1981). The rich sediment nutrient pool, and the relatively small biomass of Halophila ovalis (compared with other seagrasses) presumably ensured that nutrient demand did not exceed supply, unlike the findings of Bulthuis and Woelkerling (1981), who suggested that the growth of a larger seagrass, Heterozostera tasmanica, was limited by nitrogen during the active growth phase in spring and early summer owing to microgradients of nutrient depletion in the sediments surrounding the roots. The fact that nitrogen and phosphorus concentrations in Halophila ovalis remained relatively constant during periods of increasing biomass further indicated that growth was unlikely to be limited by nutrient supply. The apportioning of nutrients amongst the leaves, rhizomes and roots ofHalophila ovalis is similar to those reported for Posidonia australis Hook f. (Hocking et al., 1981) and for a number of freshwater macrophytes (Congdon and McComb, 1980). The accumulation by leaves of the major proportion of the plant's nitrogen and phosphorus, and the importance of rhizomes for storage of phosphorus are points emphasised in all these studies. The rhizomes of Halophila ovalis also accumulate soluble sugars during autumn; nutrient reserves in the rhizome may be important in helping the plant to re-establish after the typically unfavourable winter conditions of the estuary (Masini, 1982). The importance of Halophila ovalis as a nutrient pool in the Swan/Canning Estuary compared with phytoplankton can be estimated by assigning appropriate nutrient concentrations for phytoplankton from the literature. Redfield et al. (1963), and the more recent work of Rhoads et al. (1975) and Fisher et al. (1982) on estuarine phytoplankton, indicate that a C:N ratio of 6:1 would be appropriate for phytoplankton in the Swan/Canning Estuary. The work of Ryther and Dunstan (1971) indicates that N:P ratios of between 5:1 and 15:1 are most common for phytoplankton, with assimilation of nutrients proportional to the concentration of the nutrient in the water up to a maximum nutrient concentration (beyond which "luxury consumption" may occur). The N:P ratio of inorganic nitrogen and phosphorus in the Swan/Canning Estuary (Hillman, 1985) suggested an N:P ratio of 5:1 was appropriate for phytoplankton communities.

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49

When applied to estimates of phytoplankton biomass in the estuary, these nutrient concentrations yield annual average amounts of nutrients bound in the phytoplankton of the estuarine basin of 11 250 kg C, 1875 kg N and 375 kg P. Thus at maximum seasonal biomass, beds of Halophila ovalis in the Swan/Canning Estuary contained approximately ten times more carbon, and twice as much nitrogen and phosphorus as phytoplankton (see Table 11 ). Obviously these figures do not take into account phytoplankton below the photic zone, or seagrass detritus in the sediments or washed on the shores, but they do indicate that Halophila ovalis was the major plant nutrient pool during the study period. What these figures fail to indicate is the importance of Halophila ovalis in concentrating nutrients in the shallow waters of the estuary. For instance, during summer a dense seagrass bed overlain by 2 m of water would contain approximately 33 g C m -2, 1,500 mg N m -2 and 200 mg P m - 2. Since typical phytoplankton levels in the estuarine basin during summer are of the order 2 - 6 / z g 1-~ chlorophyll-a, the phytoplankton community over such a seagrass bed would contain approximately 0.22 g C m -2, 39 mg N m-2 and 8 mg P m -2. That is, in the shallow waters of the estuarine basin, seagrass beds may contain up to 150 times more carbon, 40 times more nitrogen and 25 times more phosphorus than overlying phytoplankton on a per unit area basis. Thus it can be seen that shallow waters of the estuarine basin carrying seagrass beds represent a considerably greater concentration of plant-available nutrients than the deeper waters which contain only phytoplankton. The main plant nutrient pool in estuaries is usually the fringing marshes, followed by the benthic plant community, and lastly, phytoplankton (Woodwell et al., 1973; Pomeroy et al., 1981; Wiegert et al., 1981; McComb, 1984). However, in southwestern Australia, McComb (1984) notes that fringing marshes are not as well developed as those of Europe and North America because of the small tidal amplitude, and studies on local estuaries (Congdon and McComb, 1980) have indicated that the size, structure and infrequent inundation of the fringing vegetation results in little detritus (and therefore nutrients) being contributed to the open water. In the Swan/Canning Estuary, the importance of fringing vegetation is even less, since once-extensive tracts of fringing vegetation have been all but removed during urban development. For this reason, seagrass beds in the estuary presumably play a relatively more important role as a nutrient pool than in other estuarine ecosystems, both local and overseas. In addition, given that the major nutrient pool in estuaries is the sediments (Webb, 1981 ), that seagrasses are known to transfer sediment nutrients to their epiphytes and the water column (Harlin, 1973, 1975; McRoy and Goering, 1974; Wetzel and Penhale, 1979), and that bacterial communities in the rhizosphere and phyllosphere of seagrass beds can actively fix nitrogen and mobilise nutrients in the sediments (Klug, 1980; Capone, 1983 and references cited therein), it is clear that Halophila ovalis must play a major role in nutrient cycling in the estuarine basin of the Swan/Canning Estuary. The annual production of seagrass meadows (above- and below-ground material) in the Swan/Canning Estuary of 1500 g DW m - 2 (approximately 500 g C m - 2 year- 1 ) becomes approximately 100 g C m -2 year-~ when expressed on the basis of the entire area of the estuarine basin. Thus if phytoplankton productivity in the estuary is taken as 300-500 g C m - 2 year- l, seagrass primary production represents 15-25 % of the combined production of the two. However, these figures fail to convey the importance of the seagrass in the shallow waters. For example, if a dense stand of Halophila ovalis is considered, the combined productivity of seagrass and phytoplankton may reach 1700 g C m -2 year-t, of

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which up to 80% is contributed by seagrass. Thus areas in the estuary carrying seagrass may be up to five times more productive than deeper waters carrying only phytoplankton. This situation has been found in other estuarine studies. In Great South Bay, New York, Lively et al. (1983) calculated that phytoplankton and seagrass meadows (including epiphytes) respectively contributed 85% and 15% of total estuarine productivity, but that areas carrying uniform stands of Z. marina were twice as productive per unit area than unvegetated areas. In Sydfynske Ohav, Denmark, Sand-Jensen and Borum (1983) calculated that Z. marina contributed 56% of total estuarine productivity, but that areas carrying dense stands of seagrass were up to six times more productive than deeper, unvegetated areas. In both the present study and the above two, the importance of shallow areas carrying seagrass meadows to estuarine productivity and ecology is clearly demonstrated. At least half the productivity of Halophila ovalis is probably made available to food chains in the estuary as dissolved organic matter, and the remainder in particulate form (Hillman, 1985). Both forms of organic matter would be rapidly utilised by benthic microorganisms and the epiphytic "felt" that develops on decomposing seagrass (Fenchel, 1977; Klug, 1980). The rich supply of detritus in the shallows compared with deeper waters is reflected in an abundance of benthic invertebrates in the shallows (Wallace, 1977), which in turn makes the shallows a favoured feeding site for fish (Lenanton, 1978). Since meadows of Halophila ovalis clearly supply the major proportion of detritus in the shallows, it seems reasonable to conclude that they are largely responsible for the high secondary productivity of the estuary.

Acknowledgements The Waterways Commission of Western Australia provided logistic support for field trips, and we thank W. Hosja and C. Scrimshaw for their assistance. G. Bastyan, F. Salleo and G. Kendrick also assisted with fieldwork. Matt Jury carried out revisions to figures and tables for the final manuscript.

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