Responses of Seagrass to Nutrients in the Great Barrier Reef, Australia
MARINE ECOLOGY PROGRESS SERIES Published August 20 Mar Ecol Prog Ser I
Responses of seagrass to nutrients in the Great Barrier Reef, Australia
James W. ~dyl~~.*,William C. Dennisonl, Warren J. Lee Long3,Len J. ~c~enzie~
'~epartmentof Botany, University of Queensland, Brisbane, 4072 Queensland, Australia 2Centre for Catchment and In Strearn Research, Griffith University, Nathan, 411 1 Queensland, Australia 'Queensland Department of Primary Industries, Northern Fisheries Centre, Cairns, 4870, Queensland, Australia
ABSTRACT- Declines in seagrass biomass and growth have been widely reported in response to anthropogenic irnpacts. In contrast, the distnbution and biornass of seagrass in the carbonate sedirnent around Green Island reef, part of Australia's Great Barrier Reef (GBR), has measurably increased dur- ing the past 50 yr, possibly due to increases in the availability of nutrients from local and regional anthropogenic sources Using historical aerial photography, increases in seagrass distribution at Green lsland have been mapped. The growth, morphological and physiological responses of 2 seagrass spe- cies (Halodule uninervis and Synngodium isoetifolium) to elevated sedirnent nitrogen (N; lOOx control) and/or phosphorus (P; 1Ox control) were measured to investigate whether increased nutrients could account for the observed increase in distribution. Increases in the growth rate, amino acid composition and tissue nutrient content of both species occurred in response to elevated sediment N, but not P. Con- centrations of the N-rich amino acids asparagine and glutainine ~ncreased3- to 100-fold in seagrass leaves from N treatments. The 6"~values of leaves decreased in response to additions of nitrogen, probably due to increased discrimination against the I5N isotope. because N availability was surplus to demand. The low 6"~value of seagrasses in the Green Island back reef suggests that their prirnary source of N is either from N2 fixation or fertilisers and that the N from sewage is not a large component of their N budget. This study is the first to dernonstrate N, rather than P, as the primary limiting nutri- ent for growth of seagrass in carbonate sedirnents and Supports the hypothesis that the increase in the seagrass distnbution and biomass at Green Island was caused by an increase in nutnent availability. We also hypothesise that seagrass distribution and biomass in many regions of the GBR may be limited by nutnents and that the lack of substantial seagrass meadows in the southern GBR could be due to these reefs receiving less nutrients from the mainland.
KEY WORDS: Seagrass - Great Barrier Reef . Nutnents
INTRODUCTION seagrass in carbonate sediments could also be limited by the availability of micronutrients such as iron, which Phosphorus is the most likely nutrient to limit the are derived from terrigenous soil (Duarte et al. 1995). growth of seagrass in carbonate substrata due to strong Anthropogenic nutrient inputs to reef ecosystems binding of ~0~~-by carbonate ions (Lide 1994) and fast have caused a detrimental effect On, or loss of, the rates of N, fixation by microorganisms in tropical sedi- existing coral communities in many parts of the world. ments (Smith & Hayasaka 1982, Capone et al. 1992, The discharge of sewage into Kaneohe Bay, Hawaii, Welsh et al. 1996). Experimental fertilisation of sea- resulted in the ecosystem becoming dominated by grasses growing in carbonate sediment in the Bahamas plankton, benthic filter feeders and algae with sections and Flonda Bay, USA, have reported limitation of sea- of the bay losing 99.9% of their corals (Maragos et al. grass growth by P availability (Short et al. 1985, 1990, 1985). Loss of corals and the proliferation of macroal- Fourqurean et al. 1992a, b). Carbonate sediment usu- gae have also been associated with the discharge of ally dominates in regions that receive little or no river- sewage and anthropogenic nutnent sources in the Red ine inputs of sediment or nutnents. Thus, the growth of Sea (Walker & Ormond 1982), Japan (Kuhlman 1988), Bermuda (Bach & Josselyn 1978) and Florida, USA (Lapointe 1989).
O Inter-Research 1999 Resale of full article not permitted 258 Mar Ecol Prog Cer 185. 257-271, 1999
At Green Island, a tropical coral cay on the Great Barrier Reef (GBR), 27 km northeast of the Australian mainland, sea- grasses grow in predominantly carbonate sands (>90% CaC03; Allan & Johns 1989). The distribution of seagrass has in- itralia L creased substantially over the last 50 yr (Kuchler 1978, Baxter 1990) and now extends from the intertidal reef flat to a 1 depth of at least 15 m on the back-reef ,W 0 I -m.TrnWn
Cymodocea rotundata, C. serrulata, Halophila ovalis). The fertilisation study was situated in the subtidal (-2 m deep at mean low water) 400 m northwest of Green Island (Fig. 2). A 7 ha National Park is located at the eastern end of Green Island with a tourist resort located on the west- ern end. The first lease for resort development on Green Island was granted in 1938. Since then tourism has increased and Green Island is currently the most highly visited location on the GBR receiving -300 000 tounsts yr-' (Great Adven- tures pers. coinm.). Green Island changed from septic to sewage treat- ment in 1972 with effluent discharge occurnng on the southwest reef edge until December 1992, when tertiary treatment was installed. Tertiary treated water is currently reused on the island or discharged into the main channel and the sludge is removed by barge for disposal on the mainland. Mapping methods. Digitally scanned and rectified vertical aerial photography (1:12000 and 1:6000) was used to map the present (1994) Fig. 2. Seagrass distnbution and abundance at Green Island in 1994. 1972, 1959 and past (1936, 1959 and 1972) sea- and 1936. The fertilisation of the seagrass meadow dominated by Halodule uni- grass distribution to the northwest of nervis (1) and the mixed meadow of H. uninervis and Syringodiumisoetifoljum (2) were located off the NW side of GreenIsland Green Island cay. Seagrass rneadows in 1994 were ground-truthed be- tween 17 August 1994 and 2 September 1994. Esti- tified to Australian Map Grid (AMG) Zone 55 co-ordi- mates of aboveground seagrass biomass (3 replicates nates, as the base map. of a 0.25 m' quadrat) and the relative proportion of Boundanes of the seagrass meadow were deter- each seagrass species were recorded at 95 sites in the mined based on the theodolite fix at each site and aer- seagrass meadow. The sites were located, at least ial photograph interpretation. Errors, which should be every 20 m, along north-south transects, which were considered when interpreting GIS maps, include those between 100 and 500 m apart. associated with digitising and rectifying aenal pho- Aboveground biomass was determined by a 'visual tographs onto base maps and theodolite fixes for sites. estimates of biomass' technique described by Mellors The error in determining the seagrass distnbution in (1991). At each site, divers recorded an estimated rank this study was Set at +5 m either side of the meadow of seagrass biomass. To estirnate the relative above- edge. Other errors associated with mapping, such as ground biomass for each ranking, samples were col- GPS and the position of a diver under the vessel, were lected and dned for each diver's rankings. Seagrass embedded within this range. species were identified according to Kuo & McComb Past seagrass distribution was determined by scan- (1989). ning a vertical aerial photo from 1972 and visually A theodolite was used to accurately determine geo- interpreting and rectifying oblique aerial photos from graphic location of survey sites (11.5 m). All data was 1936 and 1959 onto a GIS. entered onto a geographic information System (GIS) Fertilisation experiment. Fertilisation: Seagrasses using aerial photographic images (Queensland Beach were fertilised in situ at 2 sites: (1) an area dominated Protection Authority, 28 June 1994, altitude 914 rn) rec- by Halodule uninervis with small amounts of Cymodo- 260 Mar Ecol ProgSer 185: 257-271, 1999
cea rotundata, C. serrulata and Halophila ovalis; (2) a into a homogeneous slurry and subsampled for adsorbed mixed bed of Syringodium isoetifolium and H. uni- NH4+(KCl extraction), adsorbed (Fe strip method) nervis. Slow release fertiliser was applied in Apnl and and porosity (see Udy & Dennison 1996, 1997a). September 1994 (5 to 6 mo release Osmocote with Biomass. morphology and shoot density. A core of phosphorus as 18% POd3-and nitrogen as 11.5 % NH,' seagrass (15 cm diameter) was collected from each and 11.5% NO3-, Scotts Australia). Three replicates of replicate plot prior to rhizome tagging (Aug) and at the 4 treatments were used at each site; Control (C: sedi- conclusion of the experiment (Nov) for measurement of ment disturbed but no fertiliser added), phosphorus seagrass biomass, morphology and shoot density. Sea- (+P; 23 g P m-2), nitrogen (+N;88 g N m-2) and nitrogen grass tissue was separated into new leaves (the plus phosphorus (N+P; 23 g P m-2, 88 g N m-'1. These youngest leaf, plus the bottom section of the second treatments were randomly assigned to twelve 1 m youngest leaf required to make up the equivalent of 1 diameter circular plots located along 2 parallel lines in full size leaf), old leaves (all other leaf tissue), rhizomes a homogeneous seagrass meadow of equal water and roots, dried (60°C for 3 d) and weighed. The depth. In April 1994, sites were marked and fertiliser longest 5 leaves and roots in every core were mea- was applied by spreading it evenly over the plot and sured to estimate the seagrass canopy height and max- mixing it with the surface sediment until only a few imal root length. The number of shoots in every core pellets were visible. In September 1994, each plot had were counted to obtain a measure of shoot density. the surface sediment removed by gently creating a Growth rates. Ten Halodule uninervis shoots in each water current by hand motion over the sediment until plot were rhizome tagged (Dennison 1990a) in August the rhizomes were visible. Terminal shoots were and most were recovered in November. Leaf growth tagged and the relevant fertiliser pellets were added. per shoot was calculated by multiplying the number of Five to 10 mm of sediment was then added to recover leaf scars produced since the rhizome was tagged the rhizomes and fertiliser. The seagrass was collected (80 d) by the average leaf weight of each treatment after 80 d of growth in November 1994. This method of (November biornass). The rhizome and root growth fertilising was used as it increases the nutnent avail- was counted as all biomass between the growing tip ability in the sediments and water column adjacent to and the rhizome tag. These growth rates were con- the seagrass (Udy & Dennison 1997a, Jones 1999). It verted to areal growth (g m-2 d-') using the average also simulates the effect of chronic adsorbed nutnent number of shoots m-2 in the August and November supply to seagrass meadows, the most likely source of biomass samples. Control and +P shoot densities were nutnents to effect the mid to outer GBR (Furnas et al. not significantly different (p > 0.05) so values from both 1988, Mitchell et al. 1996, Steven et al. 1996). treatments were pooled. However, the shoot density in Sediment nutrients: Nutnent pools for both the pore- the +N and N+P treatments were significantly (p < water and adsorbed sediment nutnents were deter- 0.05) higher than the other treatments, so the shoot mined at the end of the expenment (Nov 1994). A sip- densities of these treatments were used separately to Per, constructed of an external PVC pipe and an inner convert g shoot-' d-' to g m-2 d-'. 10 pm screen (Udy & Dennison 1996), was inserted into Due to high sedimentation rates at the mixed Syring- the sediment to a depth of 10 cm to collect in situ pore- odium isoetifolium and Halodule uninervis bed be- water samples. Porewater samples were collected in tween August and November, the rhizome tags were acid washed, N2 purged, evacuated serum bottles, lost and S. isoetifolium growth was estimated in immediately placed on ice and frozen within 4 h of November by a modification of the leaf hole punching sampling. Samples were later analysed colonmetn- technique (Dennison 1990b). Twenty leaves in each cally for [NH,'] and dissolved reactive [POA3-](Parsons replicate were cut 1 to 2 cm above where the newest et al. 1989). leaf emerged from the leaf sheath. These leaves were Sulfide concentrations in the porewater were also then allowed to grow for 8 d prior to collection. New sampled using the sipper, by collecting 6 ml of pore- growth was measured as all leaf material above the cut water in acid washed, N2 purged, evacuated serum on the oldest non-growing leaf. Leaf growth as mg bottles containing 3 ml of 9 O/ozinc acetate, which pre- shoot-' d-' was converted to g m-2 d-' using the shoot vents sulfide from being oxidised. The samples were density in the November biomass. stored at -4°C prior to determining the sulfide concen- Tissue nutrient content and isotopic analysis. Bio- tration colorimetrically (Hines et al. 1989). mass samples were ground to a fine powder in a vibra- One sediment core from each replicate was obtained tory ball mill (Retsch MM-2, Haan, Germany). Sub- from the top 10 cm using syringes (50 ml) with ends re- samples were then used for determination of tissue moved. Cores were placed 011 ice and returned to the nutrient content and 6I5N. The percent nitrogen (N) laboratory within 2 h for extraction of the adsorbed nu- and phosphorus (P) in the tissue parts were deter- trient fraction. The sediment from each core was mixed mined for new leaves, rhizomes and roots by digesting
Udy et al.: Responses of seagrass to nutrients 263
creased 10- to 100-fold; PO,^-]increased 2- to 10-fold). Hoioduie uninenlis The sulfide concentration in the interstitial water was highly variable and did not show a significant effect due to the nutrient treatments, with values ranging froin 0.1 to 129 PM. Dissolved NH,', POd3-,and adsorbed POd3- concen- trations were not significantly affected by the site, Syringodium isoetifoiium however, the dissolved sulfide was significantly lower and adsorbed NH,' was significantly higher in the Syringodium isoetifolium l Halodule uninervis mixed - bed coinpared to the site where H. uninervis was the dominant species. The differente between sites could be due to differences in the Sedimentation rate and dis- N+P turbance due to boat traffic affecting the hydrology of Control +P +N the porewater or differences in the microbial popula- tions of the Sediment due to the different species pre- Fig. 4. Growth of Halodule uninervis and Syringodium isoeti- folium in the control, phosphorus (+P), nitrogen (+N) and sent. nitrogen plus phosphorus (N+P) treatments: H. uninervis, length of leaves and roots represents the average leaf canopy height and root length, number of shoots represents the mean Biomass, shoot density, canopy height and growth number of new shoots formed since the rhizomes were tagged (80 d) and the rhizome leaf scars are equal to the mean num- ber of leaves produced. S. isoetifolium, length of leaves is Halodule unlnervis equal to leaf growth after cutting (8 d), dotted line represents the location where leaves were cut Halodule uninervis leaf biomass, canopy height, shoot density and growth all significantly (p < 0.01) in- creased in the treatments with added nitrogen (+N and the growth response, the rhizome and root biomass N+P) (Tables 2 & 3, Figs. 4 & 5). Leaf growth in the was not significantly different (p > 0.05) between treat- nitrogen treatments (+N and N+P) was 4 times greater ments. This suggests that the microbial decay of roots than in the control, while the rhizome and root growth and rhizomes may be more rapid in the N treatments. increased by 3- and 2-fold, respectively. In contrast to The lack of a significant (p > 0.05) effect of P for any
Table 2. Halodule uninervis and Syringodium isoetifolium. Biomass, growth, tissue nutrient content and 615N ratios in 2 seagrass species exposed to 4 nutrient treatments. control (C),phosphorus added (+P),nitrogen added (+N)and nitrogen plus phosphorus added (N+P) Values in brackets are standard errors; nd = no data
Halodule uninervi Synngodium isoetifolium C +P +N Ll+P C +P +N N+P
Density (shoots m-') 4450 (330) 4810 (400) 6680 (110) 8000 (470) 2905 (190) 1434 (n=l) 1019 (90) 1302 (60) Biomass (g m-') Leaves 35 (4) 37 (3) 99 (1) 129 (7) 34 (6) 17 (n=l) 12 (2) 24 (7) Rhizomes 149 (21) 162 (11) 185 (26) 161 (20) 41 (11) 23 (n=l) 43 (15) 13 (10) Roots 28 (5) 33 (1) 30 (11) 22 (3) 13 (4) 14 (n=l) 3 (0 3) 5 (2) Growth rate (g m-2 d-') Leaves 2 0 (0.3) 1.7 (0.2) 7.5 (1.4) 8.1 (1.1) 0.3 (0.0) 0.3 (n=l) 0.4 (0 1) 0.5 (0 0) Rhizomes ll(0.3) l.O(O.2) 3.1(0.7) 3.6(0.6) nd nd nd nd Roots 0.19 (0.0) 0.19 (0.0) 0.34 (0.1) 0.40 (0.1) nd nd nd nd Tissue nutnents N (%) Leaves 2.4 (0.1) 2.5 (0.1) 3.0 (0.1) 3.0 (0.1) 1.6(0.0) 1.6(n=l) 210.1) 2.1(0.0) Rhizomes 0.5 (0.0) 0.5 (0.0) 1.0 (0 2) 1.0 (0.1) 0.9 (0.1) 0.6 (n=l) 1.4 (0.1 16 (0.1) Roots 1.310.2) l.l(O.1) 1.2(0.0) 1.2(0.1) nd nd nd nd P (%) Leaves 0.26 (0 00) 0.29 (0.01) 0.30 (0.00) 0.30 (0.01) 0.21 (0.01) 0.28 (n=l) 0.11 (0.03) 0.17 (0 02) Rhizomes 0.11 (0.00) 0.16 (0.01) 0.09 (0.03) 0.13 (0.01) 0.23 0.25 0.14 (0.06) 0.31 Roots 0.14 (n=1) 0.12 (n=l) 0.07 (n=l) 0.10 (n=1) nd nd nd nd
6I5N 1%)Leaves 1.7 (0.0) 1.3 (0.1) -2.0 (0.2) -4.1 (1.6) 1.3 (0.0) 1.3 (n=l) -3.6 (2.0) -1.6 (1.1) 264 Mar Ecol Prog Ser 185: 257-271, 1999
Table 3. Fvalues from 2-way analyses of vanance performed on data using presence and absence of N and P as the main effects. The interaction term represents the interaction between N and P. 'Significant difference at p < 0.05, "significant difference at p C 0.01, "'significant difference at p < 0.001; nd = no data
Halodule uninervis Syringodium isoetifolium Main effects Interaction Main effects Interaction P N P N
I Density (shoots m-2) Biomass (gm-') Leaves Rhizomes Roots Growth rate (gm-' d-') Leaves Rhizomes Roots Tissue nutnents N (%) Leaves Rhizomes P (%) Leaves Rhizomes IS1'N (%) Leaves nd 9.0"'
I 'X' statistic from Kruskal-Wallis Lest. due to non-parametnc data
growth Parameter indicates that H. unlnervis was not limited by P availability. However, there was a significant main effect of P on leaf biomass and significant interactions between P and N for leaf biomass and the growth rate of leaves, rhi- zomes and roots (Table 3).
Syringodium isoetifolium
The biomass and growth rate of Syringo- dium isoetifolium expressed in g m-2 was not significantly (p > 0.05) increased by either the N or P treatments (Tables 2 & 3). However, the growth per shoot was significantly higher in the N treatments (Fig. 4). In contrast, the shoot density of S. isoetifolium decreased, relative to Fig. 5 The response of the control, in all the fertilisation treatments nutnent concentrations in the seagrass leaves to (Table 2), with the main effect of N and the fertilisation with phos- interaction being significant (p < 0.05). Shoot phorus (+P), nitrogen lengths for S. isoetifolium were highly variable (+N) and nitrogen plus between replicates and were not significantly phosphorus (N+P). Zero (0) represents the con- different (p > 0.05) between treatments. During trol concentration for ni- the study period this site increased its sediment trogen (%N) and phos- depth by 30 to 40 cm, probably due to the ero- phorus [%P). Increases, sion of the NW Corner of Green Island (Fig. 3). N+p relative to the control, This rapid sedimentation resulted in some of are positive and de- Fertilisation Treatment creases are neoative, the replicate sites not being relocated and may < H. wiinervk .S.ü.oetifolium Bars represent SE have contnbuted to the high variability be- Udy et al. Responses of seagrass to nutrients 265
tween plots and the lack of significant differences Halodule uninervis between the nutrient treatments.
Tissue nutrient content
Halodule uninervis
The %N present in Halodule uninervis leaves and rhizomes was significantly (p i 0.01) increased by N Pro additions (+N and N+P) and there was no significant Syrirzgodiurn isoetifolium main effect or interaction with P (Fig. 5, Tables 2 & 3). 4 r WI Asn Although the N content of roots had the opposite trend, no replication was possible due to the small quantity of biomass requiring replicates to be pooled. Tissue phosphorus content of Halodule uninervis leaves was not significantly (p > 0.05) different between any of the treatments (Tables 2 & 31, while the %P in the rhizomes was significantly (p i 0.01) increased by the addition of P and there was a trend (p < 0.06) for N to re- duce the %P in the rhizomes (Tables 2 & 3). Fertilisation Treatment Fig 6. Amino acid concentrations in the seagrass leaves Synngodium isoetifolium exposed to different fertilisation treatments; control (C),phos- phorus (+P),nitrogen (+N),nitrogen plus phosphorus (N+P). Changes in the tissue nitrogen content due to ele- Proline (Pro) has 1 amine group (IN) while both glutamine vated Sediment nutrients were similar for Halo- (Gln) and asparagine (Asn) have 2 (2N). Other amino acids (aa) make up less than 50% of the total amino acid pool in dule uninervis and Syrinyodium isoetifolium (Fig. 5), both species with the leaves and rhizomes of S. isoetifolium having significantly (p < 0.01) higher %N in the N treatments and no significant main effect or interaction with P (p > concentration of asparagine and glutamine being 1.8 0.05) (Tables 2 & 3). The %P, however, had a signifi- I 0.4 pmol g in H. uninervis and <0.1 pmol cant main effect from both N and P additions, with +P g-llresh ,, in S. isoetifolium. When N was added (+N increasing the %P and +N decreasing the %P. This and N+P), an increase in glutamine and asparagine resulted in the %P of leaves from the N+P treatment concentrations of 3-fold occurred in H. uninervis not being significantly different (p > 0.05) from the leaves (2.9 2 1.1 pmol g-Ifmsh ,,) and an increase of control due to the combination of both main effects 100-fold occurred in the S. isoetifolium leaves (2.7 I (Fig. 5). The %P content of the rhizomes did not show 1.2). There was no significant (p > 0.05) increase in a significant effect of any treatment, possibly due to the concentration of other amino acids in H. uninervis the low replication (Tables 2 & 3). The tissue nutrient (all treatments 1.6 ? 0.3 pn~olg-'l„,h ,,I; however, content of S. isoetifolium, in all the treatments, was S. isoetLfolium demonstrated a 2-fold increase in the lower in leaves and higher in rhizomes than the equiv- concentration of 'other amino acids' with the addition alent plant portion of H. uninervis. of N (control and +P 0.5 I 0.1 pmol g-'fre,h,,; +N and N+P 1.1 +. 0.3 pinol g-lfresh
Amino acids
Halodule uninervis had 3 times the total amino acid content of Synngodium isoetifolium, which was due Seagrass leaf material from the control and +P treat- primarily to a large proline content in H. uninervis (69 ment had 615N values between 1.1 and 1.7 %o. The 615N to 81%; Fig. 6). With the exception of proline, the values of the seagrass in the +N and N+P treatments amino acid content in the leaves of the 2 species were more negative than the 6"~of the fertiliser (O%o) responded in a similar manner to the fertilisation in most samples and had higher variation between treatments. The control and +P treatment were not replicates than the control or +P plants, with values significantly different (p > 0.05) with the coinbined bet~veen0.2 and -7.3%0 (Table 2). 266 Mar Ecol Prog Cer
DISCUSSION raw sewage discharge in 1992. However, due to inter- nal recycling of N in the seagrass, Ft5N values tend to Expansion of seagrass meadow be highly conservative (Gnce et al. 1996), suggesting that the contnbution of sewage N to the Green Island Observations of changes in seagrass abundance at seagrass has been minimal. Green Island reef allows inferences on historical The pattern of gradual increase in seagrass distribu- events, which may have influenced seagrass growth, tion obsewed at Green Island since the 1950s suggests to be made. Oblique photographs from 1936 and 1946 that the most likely causal factor has been an increase show very little evidence of dense seagrass habitat to in nutnent availability due to anthropogenic activity in the northwest of Green Island, but photographs from this region of the GBR. However, it is also important to the late 1950s (Kuchler 1982) clearly show the first consider other possible causes, such as disturbance by dense seagrass habitat in this area. By 1972, a dense cyclones, changes in the grazing pressure and other seagrass meadow of 6.5 k 3..3 ha, consisting predomi- environmental changes. Firstly, the last major cyclone nantly of Halodule uninervis, Cymodocea serrulata to affect this section of coast occurred in 1927 (Bureau and Halophila ovalis, was well established in this area of Meteorology, Brisbane), pnor to the first aenal pho- (Kuchler 1978, current study). The expansion of sea- tograph. If the observed seagrass expansion was due to grass habitat before the sewage pipe was installed recovery from the 1927 cyclone, this suggests that indicates that increased nutnent availability associated there was approximately 20 yr with no recovery, fol- with the reef crest sewage outfall in 1972 was not a pn- lowed by 20 yr of gradual recovery and a further 20 yr mary cause for this expansion in sea.grass distnbution of rapid recovery. However, this is not consistent with at Green Island. This suggests that other factors in- observations from the Gulf of Carpentaria, Australia, cluding water seepage and nutnent translocation from where Halodule uninervis recovered within 5 yr of a the cay as well as regional changes in nutnent avail- major cyclone (Poiner et al. 1993). A second possibility ability in GBR waters may have caused the observed is that a reduction in grazing pressure may have expansion pnor to 1972. The continued expansion of allowed the expansion of seagrass at Green Island. The the seagrass meadow after 1972 may have been influ- authors consider this is unlikely as there is no evidence enced by the sewage discharge in addition to regional that extensive grazing of seagrass is occurnng as changes in nutrient availability. observed by McGlathery (1995), in Bermuda, and most Between 1952 and 1.974 the area of sugarcane in the herbivorous fish feed on turf algae or the epiphytic Cairns region increased from 53403 to 91 040 ha (Aus- algae on the seagrass leaves rather than the seagrass tralian Bureau of Statistics, cited in Hopley 1988). This itself (Hixon 1997, McClanahan 1997). Green Island 70% increase in sugarcane and its accompanying in- has also been identified as having a more diverse fish creases in fertiliser application would have increased population than neighbouring coral atolls (Baxter N input by nvers to the GBR 'lagoon'. Increased rates 1990), suggesting that there has not been a large of erosion associated with land cleanng practices decline in herbivorous fish species, which would be would have also increased the nutrient load delivered necessary to explain the large expansion in the distnb- to the GBR adsorbed to sediment particles by approxi- ution of seagrass. A third possibility, suggested by mately 400% (Moss et al. 1996). Prior to 1972, an Kuchler (1978), is that a reduction in the sediment underground septic System and the daily disposal of grain size due to a beach replenishment program in food waste into Green Island waters could have con- the 1970s may have contnbuted to the increase in sea- tnbuted to nutrient enrichment and the initial grass distribution. Although it is possible that finer sed- increases in seagrass distribution. Since 1972, large iment m.ay have facilitated seagrass growth in the increases in visitation rates and the use of a sewage 1970s this 1s clearly not the primary cause for thc sca- outfall may have enhanced nutnent availability near grass expansion as the aenal photographs clearly show Green Island and could have changed the pnmary lim- that the expansion began prior to the 1970s. iting nutnent from P to N. However, at the time of sam- pling, it is unlikely that sewage provided the major N source for seagrasses on the Green Island reef. Leaf tis- Sediment nutrients sue SI5N values ranged from 1.3 to 1.7%0,suggesting that their pnmary N source Comes from either fertilis- Ambien.t porewater POA3-concentrations in carbon- ers or NI fixation (Udy & Dennison 1997a). If their pri- ate sediments of Green Island (0.9 to 1.3 PM) were sim- mary N source was from sewage, the seagrass would ilar to values reported from seagrass beds in the be expected to have leaf tissue F15N values closer to 10 Bahamas (1.5 PM; Short et al. 1985) and Flonda Bay, (Gnce et al. 1996, Udy & Dennison 199713). It is possible USA (0.5 to 3 PM; Fourqurean et al. 1992b). Stimula- that 615N values were higher prior to the cessation of tion of seagrass growth by P ad.dition and changes in Udy et al.: Responses of seagrass to nutnents 267
the C:N:P ratio of seagrass leaves indicated that P was with siliceous sediment (Bulthius et al. 1992, Kenwor- the primary limiting nutrient for seagrass growth at the thy & Fonseca 1992, Short et al. 1993).However, N lim- Bahamas and Florida Bay study sites, which had N:P itation of seagrass growth in carbonate sediment has ratios in their porewater of 67:l and 93-232:1, respec- not been experimentally demonstrated previously. tively (Short et al. 1990, Fourqurean et al. 1992a). The However, Agawin et al. (1996) suggest, based on tissue low porewater POq3-concentration in the ciirrent study nutrient content, that N is the pnmary limiting nutrient would suggest that P could also limit seagrass growth for Enhalus acoroides growth in carbonate Sediments at Green Island. However, the low NH,' concentra- of the NW Philippines. The N content in new H. uni- tions and a N:P ratio of 6:l in the porewater, well below nervis leaves from the control and +P treatment the N:P ratio required for seagrass growth of 19:1 (this (2.4 %N) were higher than the 1.8 %N suggested by study), suggests that seagrass growth is limited by the Duarte (1990) to represent N limitation, yet the Same as availability of N rather than P (Table 4). found in new H. uninervis leaves from Moreton Bay Ambient concentrations of adsorbed NH4+ (74 to (2.4 %N) which were N limited (Udy & Dennison 114 pmol were higher at Green Island than in the 1997a). While, the N content of new S. isoetifoliurn siliceous sediinent of Moreton Bay, Southeast Queens- leaves was below the 1.8 %N critical level (Duarte land (48 pmol 1-'„,), where N has been demonstrated 1990) and 0.8 % lower than H. uninervis, yet both spe- to limit seagrass growth (Udy & Dennison 1997a). cies demonstrated similar increases in N content when Bioavailable P, measured using the Fe strip method, fertilised with N (0.5 to 0.6%N). This contrast in the N was less at Green Island (311 to 415 pmol 1-I„,) com- content of H. uninervis and S. jsoetifolium leaves, yet pared with Moreton Bay (492 pmol 1-ISed;Udy & Denni- similar fertilisation response is probably due to spe- son 1996, 1997a). However, the N:P ratio for adsorbed cies-specific variation in the cntical levels of N which nutnents at Green Island of 1:4 still suggests that the represent nutrient limitation, as previously observed availability of N is more likely to limit seagrass growth (Udy & Dennison 1997a). It is also important to note than the availability of P. that the ioN in new leaves (used in the current study) would be expected to be higher than the %N of the total leaves used in the Duarte (1990) study (Penderson Seagrass response to elevated sediment nutrients & Borum 1992, Penderson et al. 1997, Udy unpubl. data for Zostera capncorni]. The responses of Halodule uninervis and Syringo- Duarte (1990) also found that a P content of leaves dium isoetifolium to fertilisation indicate N is the pri- less than 0.2 %P corresponded to P limitation of sea- mary limiting nutrient for seagrass growth at Green grass growth. In the current study the P content of new Island, with H. uninervis demonstrating 'exclusive N leaves from Halodule uninervis and Syringodium iso- limitation' and S. isoetifolium 'pnmary N limitation' etifolium was above 0.2 %P in all samples, except with secondary P limitation (defined in Fisher & Butt S. isoetifolium +N and N+P treatments. In conjunction 1994, Udy & Dennison 1997a). Nitrogen limitation of with the seagrass growth responses this suggests P H. uninervis (Udy & Dennison 1997a) and other sea- secondarily limits S. isoetifolium growth, but not grass species have been reported previously from sites H. uninervis growth. The only characteristic of H. uni-
Table 4. Comparison of porewater nutrient concentrations from various locations worldwide. N = N lirnitation of seayrass growth; P = P lirnitation of seagrass growth, 110 limit = no limitation of seagrass growth
Location Sediment Porewater nutrients N:P Pnmary Source type INH4'J [PO,"] ratio nutnent (PM) (PM) limitation
Green Island, Qld, Aust. Carbonate 5.6 1.3 4.3 N This study San Salvador ls., Bahamas Carbonate 100 1.5 67 P Short et al. (1985. 1990) Flonda, USA Carbonate 98 0.5-3 93-232 P Fourqurean et al. (1992b) Rottnest Island, WA, Aust. Carbonate 9.2 2.0 4.6 No Limit Udy & Dennison (1999) S. Sulawesi, lndonesia Carbonate 107 6 18 No lirnit Eiftemeijer et al. (1994) Moreton Bay, Qld, Aust. Siliceous 7.1 4.7 1.5 N Udy & Dennison (1997a) Victona, Aust. Siliceous 11-19 6-8 2 N Bulthius et al. (1992) Netherlands Siliceous 20-50 - - N van Lent et al. (1995) Alaska, USA Siliceous 30-130 6-25 5 N Short (1983) C. Sulawesi, Indonesia Siliceous 60 10 6 No limit Eiftemeijer et al. (1994) Victoria, Aust. Siliceous 200-1700 3-60 67 No limit Bulthius & Woelkerling (1981) 268 Mar Ecol Prog Ser 1
nervis which was significantiy higher in the N+P treat- yr-' being contnbuted by rivenne input. This would ment relative to the +N treatment was leaf canopy supply -1.5 % of the nutnents turned over each year in height and biomass, suggesting that P availability rnay the seagrass bed NW of Green Island. As the seagrass secondarily lirnit some charactenstics of H. uninervis. nutrient requirements can be met by nutrient recy- As seagrasses at Green Island demonstrated pnmar- cling, N2 fixation and external supply, it is possible that ily N-lirnited growth responses, we can assume their the continuous and increasing addition of nutrients by demand for P and micronutnents, such as iron, is satu- nvers to the Cairns region of the GBR 'lagoon' over the rated under ambient nutrient conditions. This contrasts past 50 yr could have provided sufficient nutrients to with previous studies which suggest that the availabil- sustain the gradual increase in seagrass distnbution ity of P or iron is most likely to limit seagrass growth in which has been observed. If nutrients denved from carbonate environments (Entsch et al. 1983, Short et al. mainland catchments are influencing Green Island it is 1990, Fourqurean et al. 1992a, Duarte et al. 1995). It is likely that the N:P ratio of nutnents reaching the island possible that anthropogenic factors and/or characteris- will be lower than that of the riverine discharge and tics of Australian soils influence the relative irnpor- hence favour N limitation of the seagrass at Green tance of different nutrients to seagrasses and result in Island. Since NO3- and NH,' are more soluble than N limitation rather than P or Fe lirnitation. the N fraction would dissolve in the water col- The availability of P relative to N in Green Island urnn and most likely be assimilated by phytoplankton sediments rnay have increased dunng the last 50 yr and algae before reaching Green Island. However, the due to tounst activities on the island and changes in PO4" fraction is more likely to remain adsorbed to the mainland land use practices. Van Woesik (1990) sediment particles and be transported dunng major demonstrated that water circulation patterns around storm events to Green Island. Green Island caused water and suspended particles Micronutnent bioavailability in Green Island sedi- from the sewage outfall to accumulate in the NW ment rnay have also been elevated by local and/or region, where the major seagrass accumulation has regional sources. The iron present in water and sedi- occurred. Sewage loads rnay also have altered the lim- ment would chelate with the increased organics from iting nutnent for seagrass growth at Green Island from resort waste (sewage and food scraps),hence, increas- P to N limitation as sewage often has a low N:P ratio ing their bioavailability (Howarth & Marino 1988). (Howarth 1988). Changes in land use on the mainland Regionally, it is likely that changes in land use on the have also increased the nutnents supplied by nvers to mainland have resulted in increased erosion and the GBR lagoon and rnay be resulting in wide spread hence higher supply rates of iron-nch sediment to the eutrophication of the inner reefs (Kinsey 1991, Beil GBR lagoon. 1992). Furnas et al. (1995) estimated that 1947 t N yr-' Alternatively, the observed N limitation of sea- and 193 t P yr-' are delivered by nvers (Daintree and grasses at Green Island rnay not be due to anthro- Barron) to the Cairns region (Cape Tribulation to Cape pogenic impacts and rnay represent a typical Aus- Grafton) of the GBR 'lagoon' as dissolved and adsorbed tralian phenomenon. This is supported by P043- nutnents, a 100 to 500% increase on nutnents deliv- concentrations in the GBR 'lagoon' (0.16 to 0.21 pM) ered to this region by nvers pnor to agncultural and being much higher than in other reefal environments, urban development. Most of the adsorbed nutnents such as the Canbbean (0.03 PM) (Baldwin 1992, Fur- settle within 10 km of the coast (Larcombe & Woolfe nas et al. 1988), where P limitation of seagrass growth 1995); however, storms and cyclones resuspend de- has been demonstrated (Short et al. 1990). Nitrogen posited sediment and can produce sediment plumes Limitation has also been demonstrated, using fertilisa- extending more than 30 km from the coast (Gagan et tion experirnents, in the manne carbonate environ- al. 1990). Recent nver plumes generated by cyclones ment of Rottnest Island, Western Australia (Udy & Den- 'Sadie' (1994) and 'Violet' (1995) have reached beyond nison 1999) and is suggested to dominate Australian Green Island (Steven et al. 1996), demonstrating that freshwater ecosystems (Harns 1996).However, marine terngenous sediment and nutnents have the potential carbonate environments and freshwater environments to reach Green Island. elsewhere in the world are usually P limited (Smith The current study has estimated that 280 kg N ha-' 1984, Short et al. 1990, Fourqurean et al. 1992a). Nitro- yr-l and 24 kg P ha-I yr-' are required to Support the gen fixation requires large inputs of fixed carbon for measured rates of growth and tissue nutrient content energy and is inhibited by the presence of available N in the dense seagrass bed on the NW side of Green in the environment. Hence, high N2 fixation rates sug- Island. If we assume the nutnents deiivered by nvers gest high N demand in a low-N environment (Capone (estimated by Furnas et al. 1995) are evenly distnbuted 1983). Vegetated manne sediments in Australia have across the 'Cairns Box' (descnbed by Fumas et al. N2 fixation rates 10 to 100 times higher than in sirnilar 1995) this results in 3.3 kg N ha-' yr-' and 0.3 kg P ha-' environments worldwide (Alongi et al. 1992, Perry & Udy et al.: Responses of seagrass to nutrients 269
Dennison unpubl.), suggesting that N availability is and reefs are more distant from the mainland. These very low in Australian mangrove and seagrass envi- factors reduce the rate of nutrient supply, which in turn, ronments. lirnits the nutrient availability to seagrass on the south- Increased nutrient supplies to the coastal Zone has ern cays and restncts the seagrass distribution to a few often led indirectly to seagrass decline through sparse patches at the base of the reef slope (pers. obs.). reduced light availability due to increased epiphyte, In conclusion, the evidence from histoncal aenal phytoplankton and macroalgal growth (Orth & Moore photos confirms a rapid and many-fold increase in 1983, Cambridge & McComb 1984, Silberstein et al. abundance and distnbution of seagrasses at Green 1986, Abal & Dennison 1996). However, at Green Island since the expansion of human influences. The Island, increases in local and/or regional nutnent increases of dense seagrass habitat at Green Island availability have led to increases in seagrass biomass have occurred over a penod of rapid increases in and distribution. Seagrass declines have histoncally anthropogenic nutrient impacts both locally and occurred in regions where large seagrass communities regionally. We have established that the growth of occurred prior to anthropogenic elevation of nutrients seagrass at Green Island is primanly Lirnited by the and therefore where the 'pre-anthropogenic impact' availability of N. The availability of P is secondanly nutrient availability was likely to already be relatively important to Syringodium isoetifolium and possibly high. Hence, increases in nutnent availability due to Halodule uninervis. Results of nutnent ennchment anthropogenic inputs were sufficient to change the expenments support the hypothesis that the dramatic ecosystem to a phytoplankton/algal dominated System increase in seagrass distribution and biomass at Green (Duarte 1995).resulting in seagrass decline due to light Island over the past 50 yr has been caused by increases limitation (Tomasko & Lapointe 1991, Short et al. 1995, in nutrient availability. We suggest that nutnent limita- Taylor et al. 1995). In contrast, we hypothesise that tion of seagrass growth is probably widespread on the Green Island had insufficient nutnents to support an GBR and may explain the absence of seagrass mead- extensive seagrass meadow pnor to anthropogenic ows froin the cays of the southern GBR. increases in nutrient availability. Hence, the addition of nutrients from sewage, organic waste and/or Acknowledgements. We would iike to thank the many volun- regional sources has resulted in sufficient nutrients to teers and staff who helped with this project; Nicola Udy, establish and sustain an extensive seagrass meadow. Tracey O'Conneii, Christine Perry, Michael Rasheed, Frank Increases in seagrass biomass and distribution due to Nissen and Karen Vidler for assistance with fieldwork, Louise Johns for laboratory assistance and Sharlene Blakeney for her anthropogenic nutnent inputs have also been sug- assistance with the production of the GIS base map. The gested at other locations in the GBR. Klumpp et al. research was supported through postgraduate funding from (1997) have suggested that the dense seagrass beds the Botany Department, University of Queensland. a grant to surrounding the sewage pipe at Great Palm Island are W.C.D. from the ARC. The CRC for the Ecological Sustainable Development of the GBR through the Queensland Depart- a result of increased local nutnent availability. While ment of Primary Industry (QDPI) provided field support and increases in seagrass at Low Isles, which has no signif- mapping. Scotts Australia kindly provided the Osmocoate for icant nutrient point source, could result from increases this research. Aenal photographs were reproduced with per- in regional nutrient availability. The combination of mission of the Department of Natural Resources. Queensland. these studies and observations suggest that increases in nutrient availability can have both a negative and LITERATURE CITED positive effect on seagrass biomass and growth. In tur- Abal E, Dennison WC (1996) Seagrass depth range and water bid estuarine water, where light availability generally quality in southern Moreton Bay, Queensland, Australia. limits seagrass growth, increases in nutrient availabil- Mar Freshw Res 47(6):763-771 ity are expected to result in a decline in seagrass Agawin NSR, Duarte CM, Fortes MD (1996) Nutnent lumta- tion of Philippine seagrasses (Cape Bolina, NW Philip- growth and/or biomass. While in clear oligotrophic pines): in situ experimental evidence. Mar Ecol Prog Ser water where light is not limiting seagrass growth it is 138:233-243 possible that an increase in nutnent availability could Allan R. Johns RB (1989) Anthropogenic inputs into Green cause an increase in seagrass growth and biomass. Island sediments. Unpublished report to GBRMPA (Great Seagrasses are an important ecosystem in Australia's Barner Reef Marine Park Authonty), Townsville Alongi DM, Boto KG, Robertson AI (1992) Nitrogen and phos- GBR region, covenng well over 4000 km2 of coastal, phorous cycles. In: Robertson AI. Alongi DM (eds) Tropi- reef and inter-reef habitat (Lee Long et al. 1993, 1997). cal mangrove ecosystems, Coastal and estuanne studies Seagrass is more common in the northern GBR than in edn, Vol 41. American Geophysical Union, Washington, the southern GBR, which Supports little or no seagrass DC Australian Littoral Society (1990) Great Barner Reef resource on its coral reefs (pers. obs.). The reefs of the southern inventory. Cairns section reefs and islands. (Accessed GBR receive less fluvial nutrients than the northern through GBRMPA; Great Barner Reef Marine Park GBR, as rainfall and erosion rates are less (Rose 1993) Authonty) 270 Mar Ecol Prog Se
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Editorial responsibility: Otto Kinne (Editor), Submitted: January 12, 1998; Accepted: March 2, 1999 Oldendorf/Luhe, Germany Proofs received from author[s): August 9, 1999