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War. Res. Vol. 26. No. 5. pp. 553-568. 1992 0043-1354 92 $5.00 +0.00 Pnnted in Great Bntmn. All rights reserved Copyright ~ 1992 Pergamon Press plc

REVIEW PAPER

EUTROPHICATION AND CORAL REEFS--SOME EXAMPLES IN THE GREAT BARRIER

P. R. F. BELL (~ Department of Chemical Engineering, University of Queensland, St Lucia, Qld 4072, Australia

(First receired March 1991; accepted in ret,ised form October 1991)

Abstract-- or "nuisance" algal growth causes negative impacts on coral reefs via a number of routes and can eventually lead to the replacement of the coral community with various flora and fauna (e.g. attached , and detrital/filter feeders). a appears to be the best water quality indicator of eutrophication and a eutrophication threshold value at or below an annual mean of 0.5 nag m-~ is suggested. The of nutrients N and P associated with the onset eutrophication in communities are less well defined (annual mean DIN ~ I/~ M; P-PO4 ~ 0.1-0.2/A M) but are in accord with eutrophication threshold levels for sensitive freshwater . The proliferation of fixing algae in pristine coral reef regions highlights the importance of and trace components such as Mo and Fe and even soluble organic matter to the overall . The of nutrients and levels of chlorophyll a in some regions of the (GBR) lagoon are comparable to those that would be classed as eutrophic in other coral reef regions of the world. The available evidence points to rivcrine run-offas the cause of elevated P-PO4 levels in the inner lagoon. Historical evidence indicates that the levels of P-PO, and growth, and particularly that of Trichodesmium spp, are relatively high in the river affected areas and that the levels may have significantly increased in the inner lagoon over the past 50-60 years. The nitrogen-fixing ability of Trichodesmium suggests that increased levels of P alone may be driving increased levels of primary in the lagoon, it is hypothesized that the riverine-promoted eutrophication is a significant factor in the demise of fringing reefs in the inner GBR lagoon. The record~ levels of nano growth in some river-affected regions of the GBR lagoon are sullicient to promote the survival of Acanthaster planci (crown of thorns starfish) larvae and as such eutrophication could well be a principal causative factor of the crown of thorns outbreaks. Elevated levels of nutrients and algal growth occur in some outer regions of the GBR but these appear to be due to natural phenomena. The high background concentrations of nutrients and phytoplankton in both the inner and outer GBR, whether they are natural or not, demands that special precautions be exercised in the control of sewage effluents and run-off in the vicinity of coral reefs.

Key words--eutrophication, coral reef, nitrogen fixation, nutrients, Trichodesmium, Acanthaster planci

INTRODUCTION as is discussed below, that the levels of nutrients associated with such "nuisance" algal growth or The term eutrophication has become quite subjective eutrophication in coral reef communities are quite in meaning. As noted by Griffith (in Reynolds, 1978, low, but are in accord with eutrophication threshold p. 226) "no two limnologists agree on what eutrophic levels for sensitive freshwater ecosystems. The limited means". In this paper the term eutrophication refers amount of monitoring that has been completed in the to a situation where an increase in nutrient levels Great Barrier Reef (GBR) lagoon has revealed that has occurred through anthropogenic activities which the background levels for some regions are at or has resulted in "nuisance" algal growth. "Nuisance" above these threshold values. categories defined by Paerl (1988) include: (!) percep- The GBR extends for about 2000km along the tible water quality deterioration, including trophic north east coastline of Australia (see Fig. 1). The changes; (2) chronic or intermittent health , lagoon, due to the harrier effect of the outer reefs and including toxicity; and (3) loss of aesthetic and hence the inherent longshore currents, should be considered recreational values. In their pristine condition coral as a partially enclosed and as such has the reef ecosystems are highly productive but the reef's potential to accumulate nutrients discharged from the waters are usually characterized by low standing ever increasing anthropogenic activities such as agri- crops of phytoplankton. "Nuisance" algal growth cultural, urban and industrial development along the in the water surrounding a coral reef can, through coast of Queensland (Bell, 1991). On the large scale, various routes, lead to the replacement of corals with riverine inputs from agricultural areas would dis- benthic plants and filter/detrital feeders. It appears, charge large amounts of nutrients to the GBR lagoon

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(Cusser, 1987; Walker and O'Donnell, 1981). There islands of Hawaii have suffered considerably due to is some evidence that these riverine inputs are respon- the introduction of European style . The sible for elevated "'background" levels of nutrients in principal impacts noted are those due to increased the inner lagoon (e.g. see Revelante and Gilmartin, sedimentation and freshwater run-off. Duty (cited by 1982). The problem of high background levels is Endean, 1976, p. 232) notes that the nutrients from exacerbated locally in some regions by small-scale sewage discharges may have led to the increased algal run-off from developed areas and point source dis- growth and the demise of the reefs in the vicinity charges (e.g. sewage effluent). The high background of Waikiki beach. Recent observations show that levels pose particular problems for achieving the many of the fringing reefs of the islands of Hawaii are necessary dilution of sewage effluent in coral reef now dominated by algal growth. Particularly heavy regions (Bell and Greenfield, 1987; Bell et al., 1989). growth occurs along the coast of Maul. Much of this There is some evidence that the reefs in the inner algal growth can be attributed to the impacts of to mid GBR lagoon are deteriorating due to anthro- nutrients contained in run-off and groundwaters from pogenic influences including eutrophication (see dis- both agricultural areas and the expanding tourist cussion below). Many of the fringing reefs are now resort regions. dominated by large stands of macro and filamentous No systematic study on the extent of eutrophica- algae which is consistent with the region being eutro- tion in the GBR lagoon has been carried out although phic. Other anthropogenic factors, as are discussed there are some historical data available on nutrient below, such as and increased sedimen- levels and algal growth. This paper summarizes these tation could also encourage such conditions. Many data and compares the levels recorded with those fringing reefs around the world in addition to those found for other coral reef regions. This paper also described in the much cited studies in Kaneohe summarizes the available information which points to Bay (e.g. see Banner, 1974; Smith et al., 1981) and the relatively recent demise of coral reefs in the inner Barbados (Tomascik and Sander, 1985, 1987) appear GBR lagoon. to be facing similar problems, The recent (in the last 20 years) degradation of reefs along the north coast EUTROPHICATION AND CORAL REEFS of Jamaica are attributed to such a combination of anthropogenic influences (Lapointe, 1989). Johannes Coral reef ecosystems appear to be able to out- (1970) notes that many coral reefs fringing the compete other ecosystems when the surrounding Eutrophication in the Great Barrier Reef lagoon 555 water environment is poor in nutrients, having been discharged directly with sewage effluent would have described as oases in the oceanic desert (Salin, 1983; a similar effect. Sorokin, 1973, p. 17; Odum and Odum, 1955). Their Competition for space, sediment traps and disease. ability to do this is not fully understood but it is Increased attached algae will also compete with the known that nitrogen-fixing organisms are often pro- corals for space and will act as traps for sediment lific in coral reef environs and that various symbiotic build-up (Brown and Howard, 1985, p. 19). Kaplan relationships occur within the biological community (1982, p. 116) notes the direct attack on coral polyps structure which result in very efficient recycling of by blue-green Oscillatoria. Also agal infections nutrients. This recycling of nutrients provides longer by blue-green algae (Oscillatoria submembranacea, residence times for the nutrients, or in other words, Phormidium) are believed to cause the black band a storage capacity or capacitance for nutrients. This disease (Brown and Howard, 1985, p. 48; Lapointe, inbuilt capacitance means that the coral reef eco- 1989). Boring-type algae may also be promoted which systems are able to flourish with only periodic inputs could lead to direct destruction of the coral matrix. of nutrients, e.g. from or river run-off. The fact that, given the chance, algae can out- Some coral regions do have what appear to be compete with corals for space is not a new revelation. naturally elevated nutrient levels due to upwellings, Indeed Wood-Jones (1912) notes algal growth as terrestrial run-off and groundwater (Crossland and the cause of the failure of corals to recolonize after Barnes, 1983; Revelante and Gilmartin, 1982). It is some 30 years following a discharge of foul water noted though that high levels of dissolved nitrogen from a supposed volcanic vent in a lagoon of the (N) and/or phosphorus (P) do not always correspond Cocos-Keeling atoll. to high standing crops of algae because other chemi- Reduced coral growth rates and reduced lat'al cal, physical or biological factors may limit the algal settlement/sun'it'al. Evidence is emerging that eutro- population and it is the impact of the elcvated algal phication not only affects coral growth rates but populations on the coral community growth which also affects their recruitment and reestablishment appears to be of importance, not simply the elevated abilities. In studies done in Barbados (Tomascik and Icvcls of the nutrients. It has been demonstrated that Sander, 1985, 1987; Tomascik, 1992) the coral species thc discharge of sewage efflucnt and run-off from Montastrea anmdaris was found to exhibit much dcvcloped areas can cause adverse impacts on coral slower growth rates in the more eutrophic regions. reefs. Near to discharge points toxic effects can be Also benthic algae was more prolific, the diversity of experienced but the impact duc to eutrophication, corals was lower and a significant reduction in the i.e. the increased nutrient Icvels and the associated settlement/survival of coral spats (on artificial sub- incrcase in both phytoplankton and attached algal strates) occurred in the more eutrophic regions. In the populations, can be quite widespread (e.g. see study, Tomascik and Sander (1987) took into account Banner, 1974; Smith et al., 1981; Laws and Redalje, the distributions of herbivorous and conclude for 1979; Tomascik and Sander, 1985). their study area that the high abundance of benthic macrophytes and filamentous algae at the three Impacts of eutrophication on coral reef ecosystems southern more eutrophic reefs is indeed due to the Eutrophication or "nuisance" phytoplankton and increased nutrient levels and not to the exclusion attached algal growth causes negative impacts on of grazers. Also monitoring of permanent sites at coral reef ecosystems via a number of complex and Hayman Island in the GBR lagoon has revealed that sometimes interacting mechanisms. These impacts recruitment of corals is markedly suppressed in the can lead to a reduction in diversity of coral species vicinity of the sewage outlet (van Woesik et al., 1992). and eventually to the replacement of the coral com- The actual mechanism or mechanisms associated munity with various flora and fauna (e.g. attached with the eutrophication which lead to the reduction algae, sea grasses and detrital/filter feeders). The in settlement/survival of spats is not clear. Some principal mechanisms by which eutrophication im- workers have inferred that filamentous algae will pacts on coral reefs will now be briefly discussed. inhibit coral laval settlement but others have noted Reduced light penetration and smothering. Obvious that some biological preconditioning of the substrate negative impacts on corals that result from increased is necessary by some corals (see review by Fadlallah, phytoplankton concentrations are the inhibition of 1983) and that some species exhibit preferential settle- light penetration to the symbiotic zooxanthellae and ment on algal coated substrates (Harriott, 1983). the smothering effects caused by an increased organic However subsequent survival of the settled spats does sediment load. Bass-Becking (as reported by Endean, appear to be inversely related to the density of algal 1976, p. 223) has described coral deaths following cover. Harriott (1983) suggests that once settled, their smothering with the planktonic blue-green spat survival may require slow growth or cropping of alga Trichodesmium. Such an increased organic sedi- the algal layer to prevent competitive dominance ment load could lead to increased production of toxic by algae. Excess cropping may however lead to the hydrogen sulphide and will encourage the growth destruction of the settled spats. of filter and detritai feeders which will compete with Other factors such as ovedishing, sedimentation, the coral for space. Increased organic sediment load freshwater input and physical destruction can act 556 P. R. F. BELL synergistically with eutrophication in leading to the to some extent by the alga Dictyosphaeria cavernosa. demise of coral reefs. On rediversion of the sewage effluent, very good Orerfishing. The effects of increased algal growth coral recovery occurred. However it is noted that due to eutrophication could be magnified in regions there is still today, some fourteen years after the where overfishing occurs. It is noted that overfishing sewage rediversion, a problem with attached algal alone could well cause benthic algal populations growth in some sections of Kaneohe Bay. Also to out-compete with corals, even in pristine waters. some regions of coral, which were destroyed by For the GBR it has been found that algal more recent run-off events, have not reestablished will become more profuse on coral reef sub-strata (personal observations, June, 1990). This lack of if the grazing fish are removed (Wilkinson and reestablishment of the corals could well be due to Sammarco, 1983). This fact complicates the use of eutrophication. The main input of nutrients to the attached algal growth as an indicator of eutrophica- bay now is run-off from the ever increasing coastal tion and it is suggested that phytoplankton levels or development areas. concentration of chlorophyll a in the Importance of hydrodynamic regime would be a better indicator of eutrophication. Sedimentation. Another complicating factor is that The hydrodynamic regime is important in deter- sedimentation can reduce coral laval settlement as mining the magnitude and extent of the impact of well as provide a more suitable substrate for macro eutrophication on coral reef communities. For algae than for coral. Hodgson (1990) found that example, Pastorok and Bilyard (1985) note that large sedimentation, at a level that only partially covers a ouffalls in well flushed open-coastal regions have substrate and that is not directly harmful to adult minimal, at least in the short term, impact on coral colonies, could significantly reduce laval settlement. reefs. However these same discharges could prove Also terrestrial-derived sediments could provide a devastating to near-by or even far-distant bays where significant source of nutrients for benthic plant calmer conditions exist. The longer residence times growth (e.g. sea grasses, micro and macro algae). and the calmer conditions of such bays are conducive For example soluble P tends to sorb to suspended to both the growth of algae and settling of detritus. particulate matter and on settlement could well be- Endean (1976, p. 229) reports that the building of come available to benthic plants. Thus sediment load causeways reduced the renewal of waters around from run-off could not only smother and kill coral Palmyra Atoll in the Line Islands and this resulted communities but also prevent the reestablishment of in the replacement of corals with algal communities corals and greatly enhance the growth of benthic dominated by Lyngbya (Dawson, 1959 cited). It is plants. stressed that even small discharges if not effectively Freshwater inputs, and physical impacts. Of extreme flushed can cause serious problems, e.g. Johannes importance to the ultimate effects of freshwater dis- (1972) has reported that seepage from a single public charges (and associated sediments) and of physical rest room in Honaunau Bay has brought about the impacts on coral reefs is the above finding that degradation of a nearby coral community. Benthic the settlement/survival of spats of some corals is (attached) algae populations were found to be larger significantly reduced in eutrophic regions. This means than normal in this area, with much of the coral dead that the effects of eutrophication on coral reefs may and encrusted. not be obvious until after some other impact on the coral reef. For example the reef may be partially Importance of N-fixation, P and trace components killed by a run-off event or physically Attached or benthic microorganisms which have destroyed by the of a cyclone or crown of the ability to fix large quantities of atmospheric thorns attack or simply damaged by other coral nitrogen have been shown to be prolific in unpolluted predators. If the region is eutrophic, fast growing coral reef regions around the world (e.g. see Johannes algae may be able to take advantage of the situation et al., 1972; Hatcher and Hatcher, 1981; Wilkinson to firmly establish their territory and in doing so, et al., 1984; Wilkinson and Sammarco, 1983). Also prevent the reestablishment of the corals. It is to the planktonic cyanobacterium (or blue-green alga) such a combination of events that the destruction of Trichodesmium spp, which has been found to exhibit many of the reefs in Kaneohe Bay are attributed high nitrogen fixation rates in the tropical Caribbean (Smith et al., 1981). The coral community in the (Carpenter and Price, 1977), often dominates the south east (S.E.) section of Kaneohe Bay, known micro (> 20/~m) phytoplankton in the GBR lagoon originally as the "coral gardens" and purported (Revelante and Gilmartin, 1982). Carpenter and to have been once one of the finest in the world, Price (1977) and Carpenter and McCarthy (1975) was eventually destroyed by a combination of dredg- conclude that nitrogen fixation is the main source of ing activites, run-off and the discharge of sewage N for , the most abundant of effluent (Banner, 1974; Smith et al., 1981). The the three Trichodesmium species identified in their diverse coral community was replaced by algae studies. Thus the usual assumption taken for oceanic and various filter and detrital feeders (e.g. sea cucum- waters that availability of inorganic nitrogen limits bers, , clams). Most of the bay was inundated the rate and yield of primary production is probably Eutrophication in the Great Barrier Reef lagoon 557 not directly applicable to coral reef regions such as The corresponding annual mean nutrient levels the GBR lagoon. were: dissolved (total i.e. NH3-N + NO3-N + NO:-N) Carpenter and Price (1977) found that the high inorganic nitrogen (DIN) concentration of around Trichodesmium levels correlated with elevated P-PO, ! #M and P-PO, levels of 0.06-0.08 /J M. Historical levels and hypothesized that the relatively large popu- data presented by Tomascik and Sander (1985) for lations (in comparison with those in the Sargasso Sea) Barbados indicated that the onset of eutrophication are due to the higher levels of P-PO,. Their data show may be characterized by even lower levels of the that the high cellular nitrogen fixation rates also above water quality parameters. For the Kaneohe correlate with the high P-PO~ region. This finding is Bay studies, chlorophyll a levels were also highly in agreement with the work of Mague et al. (1974) correlated with the degree of eutrophication (Smith which showed that increased levels stimu- et al., 1981; Laws and Redalje, 1979). The results of lated acetylene reduction (a measure of nitrogenase Smith et al. (1981) for the least polluted section of activity and hence nitrogen fixation) in samples Kaneohe Bay before diversion, yet still considered containing Richelia intracellularis / Rhi:osolenia spp. eutrophic by Laws and Redalje, show an annual Stewart and Alexander (1971) found in laboratory mean chlorophyll a level of 0.68 mg/m J and annual studies on freshwater that the acety- mean nutrient levels of 0.23pM P-PO4 and 1.1 #M lene reduction rate is directly proportional to the DIN. Laws and Redalje (1979) report annual mean P-PO4 concentration up to about 0.61tM. As is values for the same region of 0.61 mg/m 3 chlorophyll discussed below, in the river affected regions of the a, 0.20gM P-PO, and 1.97/zM DIN. As noted GBR lagoon, the annual mean (average of results above, after diversion of the sewage considerable collected weekly to bi-weekly throughout year) P-PO4 improvement in the coral community structure levels are around 0.2-0.3 p M and may have more occurred, the annual mean chlorophyll a level in the than doubled over the past 50-60 years (Bell, 1991). least polluted region was now 0.55 mg/m ~ with corre- If the above findings are applicable to the nitrogen sponding levels for P-PO4 of 0. I I # M and for DIN of fixing alga of the GBR then such an increase in P-PO, 0.78/~M (Smith et al., 1981). levels could well have resulted in a significant increase The results from both these sets of studies suggest in the fixation of "new" nitrogen. The nitrogenase that chlorophyll a is a good, if not the best, indicator complex requires some 30 atoms of Fe for every two of eutrophication and that the critical or eutrophica- atoms of Mo and hence Fe could well limit nitrogen tion threshold level in coral reef regions of similar fixation in oceanic waters (Howarth et al., 1988). physical (e.g. , depth, flushing time and High Mo levels have been associated with cyano- turbulence) conditions to those in Kaneohe Bay or blooms and in particular with a Tricho- the fringing reefs of Barbados is around an annual desmium bloom (Howarth et al., 1988). Phosphorus, mean value of 0.4-0.6 mg/m ~. The levels of chloro- Mo and Fe are probably more available to the phyll a corresponding to the onset of eutrophication benthic nitrogen fixing organisms than to the plank- for these two different coral reef communities are tonic organisms in the oxic water column because relatively low yet remarkably similar and suggest a reducing conditions and high dissolved organic car- chlorophyll a threshold value at or below an annual bon (which could act as a chelation agent) are more mean of 0.5 mg/m 3. This chlorophyll a threshold level likely to occur at the bottom (Entch et al., 1983; for eutrophication relates to calmer embayments or Howarth et al., 1988). This could well explain the lagoonal type situations where the phytoplankton proliferation of benthic nitrogen-fixing algae in coral and the resultant detritus is able to settle onto the reef regions, including the Great Barrier Reef. coral reefs. Higher values of suspended particulate organic matter could probably be tolerated in regions with better flushing and higher turbulence, as would TIlRESHOLD LIMITS FOR EUTROPHICATION ON CORAL REEFS be the case, for example, in outer shelf-break regions. The corresponding eutrophication threshold levels Of all the water quality parameters measured in of nutrients are less well defined but the results the Barbados study, the particulate matter concen- for Kaneohe Bay and Barbados suggest levels of trations and chlorophyll a showed the highest nega- 0.1-0.2#M for P-PO4 and around I lzM for DIN tive correlation with coral growth rate (Tomascik and (Connell and Hawker 1987; Bell et al., 1987; Bell, Sander, 1985). The results of Tomascik and Sander 1991). (1985) suggest that mild amounts of eutrophication It is recognized that the N and P threshold levels may have a positive effect on coral growth but quoted here could be only indicators of the degree of beyond the threshold limit adverse impacts occur. A anthropogenic impacts and may for example only comparison of the 1981-1982 results from the least reflect the concentrations of available nutrients in the polluted stations indicates that measurable changes sediments or of other limiting components for algal for decreased coral growth rate occur for annual growth, e.g. other nutrients, such as Mo, Fe, Se, Cu mean suspended particulate matter concentrations and vitamins (Ishimaru et al., 1989), or even dissolved (SPM) greater than 4-5 mg/I with a corresponding organic matter that may be required for chelation of annual mean chlorophyll a level above 0.4 mg/m 3. existing trace metals. Also many tropical marine 558 P.R.F. BELL algae have high phosphatase activity(Lapointe, 1989) mining management policies for the control of such which may allow them to utilize the organically discharges. bound P not recorded by the usual P-PO( analysis. Many studies in the past have recorded levels of STATUS OF EUTROPHICATIONIN THE GBR LAGOON soluble reactive phosphorus (P-PO,) only and hence the true status of the nutrient enrichment levels may It is noted that no systematic study on the extent have been obscured. However the suggested N and of eutrophication in the GBR lagoon has been carried P threshold levels do compare to those found for out although there are some historical data avail- "nuisance" algal growth in other aquatic systems. able on nutrient levels and primary productivity. For example, for DIN, Maclsaac and Dugale (see Revelante and Gilmartin (1982) expressed their Bougis, 1976, p. 39) found a half saturation constant surprise that no seasonal productivity data set had of 0.98 gM for eutrophic waters and Nakamura et al. been collected since the 1928-1929 British Museum (1989) found for antiqua a half saturation expedition. Little has changed since the study of constant for DIN of I gM. Also Revelante and Revelante and Gilmartin (details of data given in Gilmartin (1982) note that NO3 values above I #M Ikeda et al., 1980) as no comprehensive (i.e. weekly are usually considered non-limiting to a pbytoplank- to bi-weekly sampling of nutrients, chlorophyll a and ton crop. The suggested eutrophication threshold phytoplankton enumeration) annual survey has been level for P is also in general agreement with values completed for the inner to mid-lagoon since their found to limit growth of phytoplankton in other work. Walker and O'Donnell (1981) did collect a aquatic systems. Collingwood (1978) notes that fairly comprehensive data set near to Station 1 (see it is generally accepted that mean levels of P-PO4 Fig. l) during the same period as Revelante and in excess of 0.3 #M will cause eutrophication prob- Gilmartin (1982) and Ikeda et al. (1980) but it would lems in static freshwater systems but that differ- appear that they missed some critical data. Some data ent species of algae do require different levels for have been collected for the outer regions of the comparable growth and to reach maximum density. lagoon, but as is discussed below, these data are Brydges (1978) gives data on the effect of fertilization biased towards the summer periods. Other of Middle Ontario. Raising the level from less complete data sets have been published but these 0.08 to 0.27/a M caused a large increase in the phyto- are of little value for establishing the annual or plankton biomass which suggests that a value some- seasonal mean values that are required for com- what less than 0.3/aM is the threshold level for that parison with the suggested eutrophication threshold system. Bougis (1976. Chap. 4) notes for marine algae levels. that the concentration of phosphorus in the environ- As is discussed below the available data show that mcnt below which the growth rate decreases is in on the large scale, the background levels of nutrients the range of 0.22-O.55/aM. Thomas and Dodson and phytoplankton are relatively high, particularly (1968) found that the final cell concentration of in the river impacted regions. Also there is some gracilis, an oceanic isolated from evidence that localized run-off and point source dis- tropical oceanic waters, was directly proportional charges result in localized or small-scale eutrophica- to P-PO, concentration up to 0.89M and that tion. Many of the coral reef communities in these the rate of growth drops off rapidly below about regions are characterized by large stands of macro 0.22/aM. Nakamura et al. (1989) found the half. and filamentous algae. Other reefs, once renowned saturation constant for Chattonella antiqua to be for their prolific coral growth, have either been 0.11/aM P-PO,. destroyed or are now dominated by seagrasses and/or It is recognized that the above analysis for deter- soft corals. These observations although not conclus- mining threshold levels is based on correlations ive proof of eutrophication are consistent with the of the mean values of the temporally variable water region being eutrophic. quality parameters and thus does not prove any direct cause and effect relationship. However the Large-scale impacts and effects fact that both sets of data from two different coral Inner lagoon off Townsville. Information on annual reef environments, one in the Pacific Ocean and mean background levels of chlorophyll a and nutri- one in the Caribbean, give similar values for the ents in the GBR lagoon is quite limited. The most eutrophication threshold levels of chlorophyll a comprehensive study since the Great Barrier Reef and nutrients suggests that similar eutrophication expedition of 1928-1929 is that of Revelante and threshold levels will be applicable for coral reefs Gilmartin (1982) for the region off Townsville (see in the inner GBR lagoon which are near to the Fig. i). Figures 2 and 3 compare the results obtained mainland and or mainland islands. When one con- by Revelante and Gilmartin (1982) for chlorophyll a siders the corresponding nutrient levels in secondary and P-PO( (in surface waters) with the suggested treated sewage and even run-off and groundwater threshold levels. These results indicate that the inner can be orders of magnitude greater than the suggested to mid lagoon off Townsviile could be classed as threshold levels the actual value chosen for the eutrophic (Bell, 1991). If the suggested threshold threshold value is really not so critical when deter- criteria are valid for the GBR lagoon then this means Eutrophication in the Great Barrier Reef lagoon 559

20! - R&G 1.8 i F&M 1.6' ~ 1.4' Andrews 1.2

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Station Number Fig. 2. Cross-shelf variation of chlorophyll a as recorded by Revelante and Gilmartin (1982), Ikeda et al. (1980) (R & G); Furnas and Mitchell (1984) (F & M); and Andrews (1983)---see Fig. 1 for station location.

that coral reefs in this region could now be experienc- the suggested threshold level, that eutrophication ing stress through the effects of eutrophication. The may extend well beyond the immediate vicinity of revelation that the inner region of the GBR lagoon the river discharges (Gabric et aL, 1990; Bell and off Townsville is eutrophic is not new, Revelante and Gabric, 1990). Now it is important to note that, in Gilmartin (1982) came essentially to the same con- the vicinity of reefs fringing the mainland and the clusion using the productivity classification method islands in this region, mean concentrations of nutri- of Koblcntz-Mishke and Vedernikow, however their ents and chlorophyll a would probably be signifi- conclusion has been largely ignored by the scientific cantly higher than the values given in Figs 2 and 3 due community and regulatory bodies. Satellite imagery to the effects of local discharges and hence the need data has shown that the phytoplankton growth for strict control of all discharges into this region is can be quite extensive and indicate that, based on indicated.

0.5- D---- R&G

• F&M 0.4 0 Andrews

.-i 0.3

0.2 ...... : ....

0.1 shelf-break

0.0 I I I l l l I I I I n Ill 1 2 4 5 Station Number Fig. 3. Cross-shelf variation of P-PO4 as recorded by Rcvelante and Gilmartin (1982), Ikeda et al. (1980) (R & G); Furnas and Mitchell (1984) (F & M); and Andrews (1983)--see Fig. I for station location. 560 P.R.F. BELL

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0.4

0.2

0.0 I I l I I I I I I I I I I I I I I I I I D M J S D M J Sampling Date (month) Fig. 4. Comparison of seasonal variation of P-PO4 and mid-lagoon Station II, 1976-1977 (Revelante and Gilmartin. 1982; lkeda et al., 1980) with that recorded 3 miles east of Low Isles, 1928-1929 (Orr, 1933).

Rcvelante and Gilmartin (1982)concluded that results in Fig 4 and 5 do indeed demonstrate a close riverine discharge is the principal source of the elev- correspondence between P-PP,, silicate and lowered ated nutrient levels for the near shore region. The salinity. Walker and O'Donnel's (1981) data also

4O

3O

o~ 20

I0

6 J F M A M J J AS O N D Date (month) Fig. 5. Seasonal variation of NH:N, salinity and silicate at mid-lagoon Station II (see Fig. I) during 1977 (Revelante and Gilmartin, 1982; Ikeda et al., 1980). Eutrophication in the Great Barrier Reef lagoon 561 show a close correspondence between high silicate Isles to confirm whether or not the levels of P-PO, and low salinity but the correspondence between have actually increased in that region. The data P-PO, and salinity is not so clear. However it is noted of Revelante and Gilmanin (1982) also show the that the maximum P-PO, did correspond to the concentration of micro-phytoplankton (i.e. phyto- low salinity period and it would appear that their plankton > 20/~ m, principally Trichodesmium and di- sampling schedule missed the salinity minimum atoms) in the lagoon in the river-impacted regions is and corresponding P-PO, maximum on 21/3/1977 as some 1-2 orders of magnitude greater than that recorded by Ikeda et al. (1980). Neither data set recorded by Marshall (1933) at Low Isles in shows any clear correlation between dissolved inor- 1928-1929 (see Fig. 6). Now the methods used by ganic nitrogen (DIN) and salinity. In fact the data of Revelante and Gilmartin (1982) in enumerating the Ikeda et al. (1980) show that the DIN (see values for phytoplankton differ from those used by Marshall ammonium-N in Fig. 5) actually peaked prior to (1933) and hence an exact comparison of the results the minimum salinity value indicating other factors may not be valid, but the results do indicate that the are involved. Bell and Gabric (1990) note that the levels of micro-phytoplankton are significantly higher observed ammonium-N peak follows a relatively high in the river-affected region off Townsville than was chlorophyll a peak and hence could be produced the case in the lagoon near Low Isles in 1928-1929. by a decaying antecedent algal bloom. Also Ullman From the discussion above on nitrogen fixation, the and Sandstrom (1987) have demonstrated that wind- high level of Trichodesmium growth in the river- driven resuspension is an important factor contribut- affected region offTownsville could well be driven by ing to the DIN flux in the GBR lagoon. the elevated P-PO4 levels of the region. Of course There is some limited evidence (also see Fig. 4) other factors such as increased loads of organics and which suggests that the levels of P-PO, may trace components such as Fe, Mo and vitamins could have more than doubled in the inner lagoon since be as or even more important than the increase in 1928 (Bell, 1991), which is consistent with the P-PO, but there are no data available on these. increased loads of phosphorus suggested by Cosset Outer lagoon off Townsville. Some data for the (1987, 1988). However before any definitive con- outer regions of the GBR lagoon are also available clusion on the increased levels of P-PO4 can be made (see Table I and Figs 2 and 3) but no complete weekly the reliability of analytical techniques used in the or fortnightly annual data set has been collected. 1928-1929 study needs to be assessed and a The results in Table 1 are temporal means of particu- "seasonal" study would have to be repeated at Low lar sampling periods and not annual means and

6e+4

5e+4 ' /T

~ 4e+4t I l II ..~$ 1928-291976.77

3e+4

' ! 2e+4

I e+4

0e+0 ~ ,. D M J S D M J S D Date (month) Fig. 6. Comparison of seasonal variation of Trichodesmium at mid-lagoon Station 11 off Townsville, 1976-1977 (Revelante and Gilmartin, 1982; Ikeda et al., 1980) with that recorded in mid-lagoon 3 miles east of Low Isles, 1928-1929 (Orr, 1933). 562 P. R. F. BELL

Table I. Mean nutrient and chlorophyll a in outer GBR lagoon P-PO, DIN Chl.a Region (/~ M) (p M ) (mg/mJ) Lizard Island t Across reef 0.22 0.99 Offshore 0.26 1.02 Central GB R 2 Lagoon 0.13 (0.07)* 0.39 (0.24) Shelf-break 0.32 (0.22) 0.32 (0.46) Coral sea (surface) 0,13(0.10) 0.13(0.10) Reef zone 0.56 Daries Reef Inside reef~ 0.105 0.39t Outside reef 0.105 0.0St Inside reeP l[ (summer) 0.72 (0.01) I (winter) 0.42 (0.06) Outside reef'* It (summer) 0.36 (0.03) I (winter) 0.27 (0.05) Palm Passage ~ (surface waters) Station I O. 16 (0.05) 0.30 (0.2) 0.42 (0.33) Station 2 0.18 (0.05) 0.22 (0.2) 0.33 (0.20) Station 4 0.20 (0.04) 0.23 (0.2) 0.14 (0.08) Station 5 0.24 (0.10) 0.23 (0.2) 0.10 (0.06) *(SD). f(NO~ + NO:). (I) Crossland and Barnes ([983); (2) Andrews (1983); (3) Entch et aL (1983); (4) Furnas et al. (1990). (5) Furnas and Mitchell (1984a,b). therefore cannot be directly compared with the discharge of run-off and sewage emuent in the outer suggested threshold values. In particular the results regions of the lagoon. of Andrews (1983) and Furnas and Mitchell Low Isles. Since the 1928-1929 British expedition (1984a,b) are probably biased towards the high side to Low Isles, the corals have been subjected to the because these data were mostly collected during the destructive forces of cyclones and to attacks by upwelling periods. However the data do illustrate the crown of thorns starfish. A large portion of the that some regions of the outer lagoon arc charac- reported flourishing hard coral cover in the shallower terized by naturally high levels of nutrients and waters has been replaced by sea grasses, algae and phytoplankton productivity for considerable portions soft corals. These observations, although they are not of the year. The high levels of nutrients are attributed conclusive evidence, are consistent with the region to phenomena such as upwellings (Andrews, 1983; being eutrophic. The principal cause of the eutrophi- Furnas and Mitchell, 1986, 1987) and in addition, in cation is surmised to be due to river discharges the case of DIN, to nitrogen-fixing algae and bacteria transporting nutrients from agricultural areas. The which inhabit the sub-strata of coral reefs (e.g. see fact that the Low Isles region is impacted by river Entch et al., 1983, Hatcher and Hatcher, 1981; run-off has been recognized by various workers. Wilkinson et al., 1984; Wilkinson and Sammarco, Fairbridge and Teichert (1948, as cited by Johannes, 1983). The results show relatively high chlorophyll a 1972) note that many of the corals in the vicinity of levels in the mid-shelf region, and particularly Low Isles had apparently been killed by sedimen- in the of the mid-shelf reefs (see results tation which they attribute to "colossal soil erosion for Davies Reef in Table I). This region is appar- due to unplanned agriculture". Brown and Howard ently characterized by naturally high concentrations (1985) note that Yonge came essentially to the same P-PO4. The results in Fig. 3 show that P-PO~ enrich- conclusion on revisiting Low Isles, 50 years after the ment of the waters occurs towards the outer shelf, 1928 British expedition. The data summarized in which is consistent with the source of P-PO4 being Fig. 7, which were collected over the period 1977- due to upwelling. At these levels of P the growth 1982 (CSIRO, 1989), certainly show significant fresh- of N-fixing algae may only be limited, if at all, by water influence at Low Isles. The correspondence of the availability of micro nutrients such as Fe and low salinities with high silicate levels is an indicator Mo and possibly vitamins (e.g. Bj:). Also the avail- that the freshwater is river derived (Bell and Gabric, ability of such trace components may be only limited 1990) and not simply precipitation. Nitrate levels by the concentration of soluble organic matter. Thus were also recorded (mean 0.33 4-0.52/zM), but not in these naturally enriched outer regions not only P-PO4 as reported incorrectly by Rasmussen and Cuff is the addition of N and P important but most (1990), and these are of similar magnitude to the probably so is the addition of trace components values measured by Revelante and Gilmartin (1982) (e.g. organic matter, Fe, Mo and vitamins). Hence for the river-affected inner lagoon off Townsville. special precautions may be required in controlling the Some more recent results obtained by Rasmussen and Eutrophication in the Great Barrier Reef lagoon 563

~= Salinity(ppt) 50- • Nitrate I,tM

-- Silicate p.M 40 e-e 3o

o o 20

1979 1980 198 i Date (year) Fig. 7. Seasonal variation of nitrate, silicate and salinity off Low Isles (CSIRO. 1989).

show that, following heavy rainfall, the levels of close correspondence between low salinity and high P-PO4 are often relatively high near to Low Isles. silicate, which again indicates that the reduced A more useful assessment of the changed status of salinity is due to the river discharge not simply to eutrophication would be obtained if the Low Isles precipitation (Bell and Gabric, 1990). The fact that study could be repeated. Until this is done definitive this region is probably already enriched by both fiver conclusions on the status of eutrophication in the discharge and upwellings suggests that it may be region are not possible. particularly susceptible to impacts from local run-off, Lizard Island. The results in Table I for Lizard groundwater and sewage discharges. Island, which were collected during September 1977, Importance of Trichodesmium. As noted above indicate relatively high background levels for nutri- the data of Revelante and Gilmartin (1982) show the ents both offshore and across the reefs. The high concentration of Trichodesmium, in a fiver-impacted P-PO4 levels at Lizard Island probably result from region of the GBR lagoon, is some I-2 orders of a combination of terrestrial run-off and upwelling magnitude greater than that recorded by Marshall due to its closeness to both the mainland and the (1933) at Low Isles in 1928-1929 (see Fig 6). If it outer barrier reef. The results in Fig. 8 show a is shown that the levels at Low Isles today are

36 20

"=" 34 10= U

111 33 5

32 i i ) J n 0 F M A M J J Date (month) Fig. 8. Seasonal variation of salinity and silicate at Lizard Island, 1979 (CSIRO, 1989).

WR 26 ~--B 564 P.R.F. BELL much higher than they were in 1928-1929 then this phytoplankton is greater than a critical level. Lucas would be good evidence that eutrophication is indeed notes that this critical level is characterized within the a problem in the GBR lagoon. The importance of ranges 5xl0: to I x l03 cell ml -~, 0.4--Img m -3 Trichodesmium spp lies in its apparent ability to chlorophyll a and 130-300 nl l-E volume of nutri- utilize atmospheric N, as its sole source of nitrogen tious particles. It is considered significant that the under aerobic conditions (e.g. see review by Creagh, suggested chlorophyll a threshold level for eutrophi- 1985) and thus provide "new" nitrogen to the system. cation, 0.5 mg m -3, is in this critical range. Another important point in regard to Trichodesmium Lucas (1982), in reviewing the data set used by is that it should be able to utilize organic forms of Revelante and Gilmartin (1982), notes for the outer phosphorus due to its high alkaline phosphatase regions that during December-February. the breed- activity (Fogg, 1982, p. 505). Hence Trichodesmium ing season for A. planci, the concentrations of phyto- should be able to out-compete with many other algae plankton are low or marginal for the nutritional in waters with low values of combined nitrogen and requirements of A. planci larvae and hence food could even inorganic phosphate, provided of course, that well be a major environmental influence on survival the supply of other essential nutrients is adequate and and development of A. planci in these waters. Further the physical and chemical factors are conducive analysis of the same data set shows the mean annual to nitrogen fixation. It appears that on decay the nano plankton count for the inner, mid and outer Trichodesmium releases "new" nitrogen (and prob- lagoon regions are greater than the critical level ably phosphate) which is then readily available for which suggests that conditions do occur quite fre- other non-nitrogen-fixing algae such as (see quently when there is sufficient food to promote the data of Ikeda et al., 1980; Bell, 1991). Indeed the data growth of the larvae. Hence survival and develop- of Revelante and Gilmartin (1982) show a quick ment of A. planci could well be promoted if the succession of diatoms following the Trichodesmium occurrence of high nano plankton levels coincided bloom of Dec.-Jan. 1976-1977 (see Bell, 1991). with the breeding season. Thus the general hypothesis A more detailed analysis of this succession phenom- that the occurrence of d. planci outbreaks in the enon (see Revclante ctal., 1982) shows that the GBR lagoon have been promoted to some extent bloom also produced a marked rise in the records of by eutrophication appears more than feasible and . Such nutrient enrichment of waters should be followed up by more intensive research. and plankton succession following Trichodesmium It is hypothesized that eutrophication of the inner blooms have been noted previously by Devassy et al. to mid GBR lagoon has provided a link between the (1979) who found a rapid diatom succession after the normal inshore habitat of the ,4. planci and the Trichodesmium followed by cladocerans, then dino- naturally nutrient enriched, highly productive outer and green algae, and finally reef waters. carnivores. Crown of thorns. Endean and co-workers found in Small-scale impacts and effects many cases, particularly in back reef areas, recolo- There is some evidence that small-scale discharges nization was negligible 6-10 years after the corals had of run-off, groundwater and sewage are also con- been destroyed by A. planci. Endean (1976, p. 245) tributing to eutrophication in the GBR lagoon and in notes the extensive cover of alcyonarians (soft corals) doing so are impacting upon coral reef ecosystems. on some reefs, and mats of filamentous and stalked In the GBR region there are some legislative controls algae on others, must hamper recolonization by the on the discharge of sewage but essentially none on the hard corals. These observations are consistent with discharge of run-off. In general the practice in the premise that eutrophication hinders and may even the GBR region is to treat sewage to secondary level prevent the reestablishment and regrowth of corals and to discharge the treated sewage to marine waters. after their destruction by A. planci. Eutrophication Discharges are often located near to fringing reefs and A. planci may be related even more closely than and in several eases near to recreational waters. Over has been suggesed above. Indeed there is some evi- the years there have been exceptions to the general dence that the outbreaks of A. planci could well be rule of secondary treatment. Hamilton Island has due to eutrophication. Birkeland (1982) notes the until recently, discharged primary treated sewage to correspondence between the occurrence of run-off, the marine waters in close proximity to fringing coral phytoplankton blooms and outbreaks of A. planci in reefs. The main discharge from Green Island, while it Guam. He proposes the hypothesis that the coinci- is chlorinated, receives little or no treatment beyond dence of phytoplankton blooms, brought about by primary settling. Septic tanks are used in several areas run-off events, and the spawning of A. planci would and some effluents from plants are increase the survival of the phytoplankton-grazing A. discharged to the groundwater system (e.g. as is done planci larvae. The hypothesis is based to a large extent on the coral cay, Heron Island). The effects of these on the work of Lucas (1974. cited by Birkeland, discharges have not been assessed in detail but some 1982). Lucas (1982) notes that nanoplankton (i.e. pilot programmes have recently been initiated (see phytoplankton < 20 9m) is a suitable food source for van Woesik et al., 1990; Steven et aL, 1990). Evidence the A. planci larvae provided the concentration of the is emerging which is consistent with several of the Eutrophication in the Great Barrier Reef lagoon 565 fringing reefs being adversely affected by this local- city of Townsville flows to Bay. The plant ized or small scale eutrophication. has been undergoing an up-grade for some time now Green Island. The discharge from Green Island, and when completed will discharge around although chlorinated, has at times, a quality worse 35,000 m3/d. Much of the sludge from this sewage than raw sewage in that it is partially fermented in the plant is also discharged to the bay. It is noted that it overloaded septic system prior to discharge. This is normal for such sludge to contain not only high often results in relatively high concentrations of levels of nutrients but also heavy metals and toxic potentially toxic sulphides. Dye tracer studies have organics. Also there is some evidence of seepage of shown that both the north-western and northern sides sewage, from the septic tanks and/or from the irriga- of the cay are impacted by the discharge (Kurchler, tion of treated sewage, into creeks which discharge to 1978; van Woesik, 1989). It is in these very same the coral reef area of Nelly Bay, Magnetic Island. areas that there has been a marked expansion in the Nelly Bay was once renowned for its coral reef extent of beds (Kurchler, 1978) and the platform of Acropora, Turbinaria and Montipora, demise of coral communities. The region nearby much of which emerged at low and was ironically the jetty was known as the "coral gardens" and an also known to many as the "coral gardens" (e.g. see underwater observatory was located to view these Johannes, 1972, p. 366; Collins, 1978; Endean, 1976, corals (Gillett and McNeill, 1959). These corals have p. 227). *'As recently as the latter half of the 1960s the met with a similar fate as their namesake in Kaneohe island still possessed coral gardens that were equal, Bay. The area directly impacted by the sewage is also and in fact often superior, to anything.., on the used for recreational purposes and although the Great Barrier Reef... the diversity and form and effluent is chlorinated, could pose a health delicate colouring of the corals painted an exquisite to bathers. picture of unequaled beauty" (T. Brown as quoted Whitsunday Group--Hamilton and Hayman Islands. by Townsville Daily Bulletin, 8/3/1972). The demise Dye tracer studies carried out on Hamilton Island of the reefs at Nelly Bay and the nearby Geoffrey, in November 1984 by the Water Quality Council Arthur and Florence Bays on Magnetic Island have of Queensland (Water Quality Council, 1985a,b) been attributed to increased sedimentation which showed that effluent of the primary treated sewage results from the dumping of spoil from harbour was transported north of the discharge point on both dredging and also to effects of cyclone "AIthea" ebb and flood . It was postulated that the (Collins, 1978: Endean, 1976, p. 227). However there resultant elevated nutrients had facilitated the pro- is some evidence that eutrophication has played an fuse algal growth to the north of the outfall. Run-off important role in the demise of the reefs. Brown has from the resort area, which is relatively turbid and noted that growth invaded the silt-saturated rich in soluble-P (~6/JM) (Bell et al., 1987), flows environment which effectively eliminated many of the directly into Catseye Bay, the fringing reef of which remaining corals (paraphrased by Townsrille Daily is now overgrown by algae. Bulletin, 8/3/1972). Endean reports (1976, p. 229) Dye tracer studies of the discharge from Hayman that algae invaded many areas after destruction of Island showed that some of the effluent was dis- part of the coral cover and this precipitated further charging through a hole directly onto the reef flat and destruction by trapping sediment. Collins (1978) the rest was discharging through a broken pipe at notes that following the effects of "Althea" and the reef edge. On the flood tide much of the fringing further heavy rainfall between 8 and 12 January 1972 reef was bathed in diluted effluent and much of the majority of Turbinaria and Montipora colonies this was transported towards the main water sports were alive but in contrast very few branches or recreational area (Bell, 1989). Rubble and the few stumps of Acropora could be found and the numerous remaining corals in the vicinity of the discharge dead branches were covered in a film of algae. Less were noted to be covered with filamentous algae. than 5% of the Acropora was alive on the reef to a Monitoring of permanent sites in the region has depth of 2 m by the end of February 1972. Acropora shown that recruitment of corals is markedly sup- was observed to regenerate from fragments in the pressed in the vicinity of the sewage outlet (van deeper waters (> LWD + 2 m) but no recruitment of Woesik et al., 1992). new colonies of Acropora resulting from the settle- Townsville and Magnetic Island. Some of the ment of larvae was observed in the following 15 most diverse fringing coral reefs in the world are months. Collins (1978) notes that both increased struggling for survival in Cleveland Bay along the sedimentation and algal growth make the conditions shoreline of Magnetic Island. The results of Reve- unsuitable for the settlement of larvae on inshore lante and Gilmartin (1982) demonstrate that the reefs and also eludes to the possibility that eutrophi- waters of Cleveland Bay were eutrophic in the late cation may be causing an increase in the algal growth 1970s. In addition to the large scale impact of river on reefs in the Townsville region. These observations discharge on the bay there are a number of local or are consistent with the hypothesis that lack of recov- small scale impacts. The harbour channel is dredged ery of the "coral gardens" of Nelly Bay is not only regularly and the spoil is dumped into Cleveland Bay. due to the impacts of spoil dumping but also due to The discharge of partially treated sewage from the eutrophication. 566 P.R.F. BELL

While there is no quick and easy to increased dominance of macro algae and filamentous controlling the large scale eutrophication of waters algae and expansion of seagrass beds into regions surrounding Magnetic Island, small scale or more which in the past were renowned for their corals, has localized eutrophication due to point source dis- been recorded. Trichodesmium blooms may have been charges such as sewage, can be more easily controlled promoted by the increased nutrient levels, and partic- e.g. by using more appropriate sewage treatment ulary by P-PO, and these blooms could be an import- and disposal technology. The impact of localized ant source of new nitrogen to the system. The run-off from developed areas is also manageable recorded levels of nano plankton growth in some to some extent, particularly if taken into account river-affected regions of the GBR lagoon are suffi- at the design stage. The concept of leaving an un- cient to promote the survival Acanthaster planci developed vegetated buffer zone between the develop- (crown of thorns starfish) larvae and as such eu- ment and the waters edge appears to have worked trophication could well be a principal causative factor on parts of the island of Maui, Hawaii (personal of the crown of thorns outbreaks. Elevated levels of observation, 1990). Another concept gaining accep- nutrients and algal growth occur in some outer tance is to develop with minimal disturbance to regions of the GBR but these appear to be due to the local landscape. For example a resort at Maho natural phenomena. The high background concen- Bay, St John. U.S. Virgin Islands, was built with trations of nutrients and phytoplankton in both the little or no alteration to the natural contours of inner and outer GBR, whether they are natural or the land. All walkways are raised boardwalks and not, demands that special precautions be exercised in accommodation is in separate units, all raised above the control of sewage efltuents and run-off in the the ground so that minimal removal of the natural vicinity of coral reefs. Evidence suggests that waste- vegetation was required, in stark contrast to this water discharges (sewage, run-off, groundwater seep- minimal impact scenario is the maximum impact age) will cause further impact on coral reef systems scenario occurring at Nelly Bay, Magnetic Island. of the GBR unless the appropriate control measures For this development no buffer zone is allowed for. are implemented. The components of most concern In fact the existing buffer zone of parkland, appear to be the nutrients (N, P and trace com- stands and public beach have been taken over by the ponents such as F¢, Mo and organic matter) and, in developer. The development will not only destroy addition with run-off, suspended solids and the fresh- much of the existing buffering capacity of the fore- water carrier itself. Thus tertiary treatment of sewage shores which provides a biological filter for the septic (i.e. the removal of nutrients) is necessary for dis- seepage from the existing local population but will charges in the vicinity of coral reefs if acceptable also increase run-off to the fringing reefs. A most levels (after dilution) of nutrients are to be achieved. beautiful headland dotted with large granite boulders Efforts, preferably at the planning stage, need to be and majestic pines was literally blasted apart and made to ensure that run-off is not discharged in the dumped into Nelly Bay in order to reclaim land and vicinity of fringing reefs. to construct a marina. The entrance to the marina requires the mining of the fringing coral reef. As REFERENCES part of this development it has been proposed to irrigate secondary treated sewage on parts of the Andrews J. C. (1983) Water masses, nutrient levels and seasonal drift on the outer central Queensland shelf remaining public grassed foreshores of Nelly Bay, (Great Barrier Reef). Aust. J. Mar. Freshwat. Res. 34. The impact of wastewater discharges from this devel- 821-834. opment could prove to be disastrous for the remains Banner A. H. (1974) Kaneohe Bay, Hawaii: urban pollution of the "coral gardens" in Nelly Bay and adjacent and a coral reef . Proc. of Second Int. Coral Geoffrey Bay. Reef Syrup. Vol. 2, pp. 685-702. Great Barrier Reef Comm., Brisbane. Bell P. R. F. (1989) Supervision of multi-disciplinary pilot CONCLUSIONS study of Hayman Island. Report to Great Barrier Reef Marine Park Authority, Townsville. Chlorophyll a appears to be the best water Bell P. R. F. (1991) Status of eutrophication in the Great Barrier Reef lagoon. Mar. Pollut. Bull. 23, 89-93. quality indicator of eutrophication in coral reef re- Bell P. R. F. and Gabric A. J. (1990) The use of field survey gions and a eutrophication threshold value (annual and satellite remote sensing in determining the extent and mean) at or below 0.5 mg m -~ is suggested. The causes of eutrophication in the Great Barrier Reef lagoon, concentrations of nutrients N and P associated with Australia. Proceedings of the Fourth Pacific Congress the onset eutrophication in coral reef communities on Marine Science and Technology. PACON 90, Vol. II. pp. 25-32, Tokyo. are less well defined (annual mean DIN,,,, I#M; Bell P. R. and Greenfield P. F. (198"]) Monitoring, treatment P-PO4~ 0.1-0.2~M) but are in accord with eutro- and management of nutrients in wastewater discharges to phication threshold levels for sensitive freshwater the Great Barrier Reef Marine Park. Proc. Workshop on ecosystems. There is evidence that some near-shore Nutrients in the Great Barrier Reef Region, pp. 115-126. GBRMPA, Townsville. regions of the GBR lagoon are already eutrophic Bell P. R. F.. Greenfield P. F., Hawker D. and Connell D. and that this is caused principally by river run-off. (1989) The impact of waste discharges on coral reef Impacts of eutrophication on coral reefs namely, regions. War. Sci. Technol. 21(!), 121-130. Eutrophication in the Great Barrier Reef lagoon 567

Bell P. R. F., Greenfield P. F., Gough G., Hawker D. and nutrient and phytoplankton biomass survey in Palm Connell D. (1987) Guidelines for management of waste Passage (central Great Barrier Reef) during 1983. ALMS- discharges into the Great Barrier Reef Marine Park. OS-84-1, Aust. Inst. Mar. Sci., Cape Ferguson. Final report submitted to Great Barrier Marine Park Furnas M. J. and Mitchell A. W. (1984b) Phytoplankton Authority, Townsville. productivity measurements in Palm Passage (central Birkeland C. (1982) Run-off as a cause of outbreaks of Great Barrier Reef) during 1983. AIMS-OS-84-2. Aust. Acanthaster planci (Echinodermata: Asteriodea). Mar. Inst. Mar. Sei., Cape Ferguson. Biol. 69, 175-185. Furnas M. J. and Mitchell A. W. (1986) Phytoplankton Bougis P. (1976) Marine Plankton Ecology. North-Holland, dynamics in the central Great Barrier Reef--l. Seasonal Oxford. changes in biomass and community structure and their Brown B. E. and Howard L. S. (1985) Assessing the effects relation to intrusive activity. Continent. Shelf Res. 6, of "stress" on reef corals. In Advances in 393-384. (Edited by Baxter J. H. S. and Yonge M.), Vol. 22. Furnas J. M. and Mitchell A. W. (1987) Phytoplankton pp. 1-63. Academic Press. London. dynamics in the central Great Barrier Reef--lI. Primary Brydges T. G. (1978) Phosphorus in the Environment: its production. Continent. Shelf. Res. 7, 1049-1062. Chemistry and Biochemistry (Edited by Porter R. and Furnas M. J., Mitchell A. W., Gilmartin M. and Revelante Fitzsimons D. W.), Discussion. pp. 217-228. Ciba N. (1990) Phytoplankton biomass and primary pro- Foundation Syrup. 57, Elsevier, Amsterdam. duction in semi-enclosed reef lagoons of the central Great Carpenter E. J. and McCarthy J. J. (1975) Nitrogen fixation Barrier Reef, Australia. Coral Reefs 9, 1-10. and uptake of combined nitrogenous by Oscillatoria Gabric A., Hoffenburg P. and Boughton W. 0990) Spacio- (Trichodesmium) thiebautii in the western Sargasso Sea. temporal variability in surface chlorophyll distribution Limnol. Oceanogr. 20(3), 389-401. in the central Great Barrier Reef derived from CZCS Carpenter E. J. and Price C. C. (1977) Nitrogen fixation, imagery. Aust. J. Mar. Freshwat. Res. 41, 313-324. distribution and production of Oscillatoria (Tricho- Gillett K. and McNeill I. (1959) The Great Barrier Reef and desmium) spp. in the western Sargasso and Caribbean Adjacent Isles, pp. 139 and 194. Coral Press. Sydney, . Limnol. Oceanogr. 22,(I) 60-72. Australia. Collingwood R. W. (1978) The dissipation of phosphorus Harriott V. J. (1983) Reproductive seasonality, settlement. in sewage and sewage effluents. In Phosphorus in the and post-settlement mortality of Pocillopora damincornis Em'ironment: its Chemistry and Biochemistry (Edited by (Linnaeus), at Lizard Island, Great Barrier Reef. Coral Porter R. and Fitzsimons D. W.). pp. 229-242. Ciba Reefs 2, 15[-157. Foundation Syrup. 57. Elsevier, Amsterdam. Hatcher A. I. and Hatcher B. G. (1981) Seasonal and spatial Collins J. D. (1978) A study of the interactive biology of variation in dissolved inorganic nitrogen in one tree corals. Ph.D. thesis. James Cook University, Townsville, reef lagoon. Proc. Fourth Int. Coral Reef Syrup., Vo[. I, QId, Australia. pp. 419-424. Manila. Conncll D. W. and liawkcr D. (1987)Tolerance of coral to ttodgson G. (1990) Sediment and the settlement of larvae nutrients and related water quality characteristics. Proc. of the reef coral Pocillopora damicornis. Coral Reefs 9, of Workshop on Nutrients in the Great Barrier Reef 41-43. Region, pp. 97-114. GBRMPA, Townsville. Howarth R. W., Marino R. and Cole J. J. (1988) Nitrogen Cosset P. (1987) Phosphorus loading to the northern Great fixation in freshwater, estuarine and marine ecosystems. Barrier Reef from mainland runoff. Proc. of Workshop on 2. Biogeochemical controls. Limnol. Oceanogr. 33(4 part Nutrients in the Great Barrier Reef Region, pp. 39--43. 2), 688-701. GBRMPA, Townsville. lkeda T., Gilmartin M, Revelante N., Mitchell A. W., Cosser P. (1988) Nutrient loading to the Great Barrier Carleton J. H., Dixon P., Hutchinson S. M., Hing Fay E., Reef region. Presented at 1,4 WPRC Conference on Water Boto G. M. and Iseki K. (1980) Biological. chemical Quality and Management for Recreation and Tourism, and physical observations in inshore waters of the Great Brisbane. Barrier Reef, North Queensland. Aust. Inst. of Mar. Sci. Creagh S. (I 985) Review of literature concerning blue-green Tech. Bull. Series No. 1, AIMS-OS-80-1, algae of the genus Trichodesmium. Dept. of Cons. and Aust. Inst. Mar. Sci., Cape Ferguson. Env., Perth, WA. lshimaru T., Takeuchi T., Fukuyo Y. and Komada M. Crossland C. J. and Barnes D. J. (1983) Dissolved nutrients (1989) The selenium requirement of Gymnodinium naga- and organic in water flowing over coral reefs sakiense. In Red Tides Biology, Environmental Science, at Lizard Island. Aust. J. Mar. Freshwat. Res. 34, and Toxicology (Edited by Okaichi M. et aLL 835-844. pp. 357-366. Elsevier Science, Amsterdam. CSIRO (1989) Hydrological data 1977-1982. Division of Johannes R. E. (1970) How to kill a coral reef--l. Mar. Oceanography, Hobart, Tasmania. Pollut. Bull. 1(12), 186--187. Devassy V. P., Bhattathiri P. M. A. and Qasim S. Z. (1979) Johannes R. E. (1972) Coral reefs and pollution. In Marine Succession of organisms following Trichodesmium Pollution andSea Life (Edited by Ruivo M.), pp. 364-374. phenomenon. Ind. J. Mar. Sci. 8, 89-93. Fishing News (Books), London. Endean R. (1976) Destruction and recovery of coral reef Johannes R. E. and Project Symbios Team (1972) The communities, in Biology and Geology of Coral Reefs of some coral reef communities: a team (Edited by Jones O. A. and Endean R.), Chap. 7, Vol. I11: study of nutrient and energy flux at Eniwetok. Bioscicnce Biology 2. Academic Press, London. 22, 541-543. Entch B., Boto K. G., Sim R. G. and Wellington J. T. Kaplan E. H. (1982) A Field Guide to Coral Reefi of the (1983) Phosphorus and nitrogen in coral reef sediments. Caribbean and Florida. Houghton-Mifflin, Boston, Mass. Limnol. Oceanogr. 28, 465-476. Kurchler D. A. (1978) Coral cay shoreline movements. Fadlallah Y. H. (1983) Sexual reproduction, development Historical and seasonal patterns, Green Island Great and laval biology in scleractinian corals. Coral Reefs 2, Barrier Reef, Austrialia. Honours thesis, James Cook 129-150. University, Townsville, QId, Australia. Fogg G. E. (1982) Marine plankton, in The Biology of Lapointe B. E. 0989) Caribbean coral reefs: are they C)'anobacteria (Edited by Carr N. G. and Whitton B. A.), becoming algal reefs. Sea Frontiers March-April 83-84. Botanical Monographs. Vol. 19. pp. 491-513. Blackwell Laws E. A. and Redalje D. G. (1979) Effect of sewage Scientific. Oxford. enrichment on phytoplankton population of a subtropical Furnas M. J. and Mitchell A. W. (1984a) A hydrographic, . Pac. Sci. 33(2), 129-144. 568 P. R. F. BELL

Lucas J. S. (1982) Quantitative studies of feeding and Steven A., van Woesik R., Brodie J. and Bell P. R. F. (1990) nutrition during laval development of the coral reef A multidiscipliniary water quality monitoring programme asteroid Acanthaster planci(L}. J. exp. Mar. Biol. Ecol. for the Great Barrier Reef: a case study of two resort 65, 173-193. islands, Green Island and Hayman Island. Congress on Mague T. H., Weare N. M. and Holm-Hansem O. (1974) Coastal and Marine Tourism, p. 66. University of Hawaii, Nitrogen fixation in the north Pacific Ocean. Mar. Biol. Honolulu. 24, 109-119. Steven D. M. and Glombitza R. (1972) Oscillatory variation Marshall S. M. (1933) Great Barrier Reef Expedition ofa phytoplankton population in a tropical ocean. 1928-29 Scientific Reports Volll(5), London British 23(May), 105-107. Museum (Nat. History), pp. 111-158. Stewart W. D. P. and Alexander G. A. (1971) Phosphorus Nakamura Y., Takashima J. and Watanabe M. (1989) availability and nitrogenase activity in aquatic blue-green Chemical environments for red tides of Chattonella algae. Freshwat. Biol. 1, 389~4. antiqua. In Red Tides Biology, Enrironmental Science, Thomas W. H. and Dodson A. N. (1968) Effects of phos- and Toxicology (Edited by Okaichi M. et al.), phate concentration on cell division rates and yield of a pp. 249-256. Elsevier Science. Amsterdam. tropical oceanic diatom. Biol. Bull. 34, 199-208. Odum H. A. and Odum E. P. (1955) Trophic structure and Tomascik T. (1992) Settlement patterns of Caribbean juven- productivity of a windward coral reef community on ile scleractinian corals on artificial substrata along a Eniwetok Atoll. Ecol. Monogr. 25, 291-320. eutrophication gradient, Barbados, West Indies. in press. Orr A. P. (1933) Great Barrier Reef Expedition 1928-29 Tomascik T. and Sander F. (1985) Effects of eutrophication Scientific Reports Vol. H(3), London British Museum on reef building corals I. Growth rate of the reef-building (Nat. History), pp, 37-86. coral Montastrea annularis. Mar. Biol. 87, 143-155. Paerl H. W. (1988) Nuisance phytoplankton blooms in Tomascik T. and Sander F. (1987) Effects of eutrophication coastal, estuarine, and inland waters. Limnol. Oceanogr. on reef building corals II. Structure of scleractinian coral 33(4), 823-847. communities on fringing reefs, Barbados, West Indies. Pastorok R. A. and Bilyard G. B. (1985) Effects of sewage Mar. Biol. 94, 53-75. pollution on coral-reef communities. Mar. Ecol. 21, UIIman W. J. and Sandstrom M. W. (1987) Dissolved 175-189. nutrient fluxes from the nearshore sediments of Bowling Rasmussen C. E. and Cuff C. (1990) Enhanced nutrient Green Bay, Central Great Barrier Reef Lagoon levels in the marine environment and their effects on coral (Australia). Estuar. Coast. Shelf Sci. 24, 289-303. reefs. Proceedings of the Fourth Pacific Congress on Walker and O'Donnell (1981) Observations on nitrate, Marine Science and Technoh~g.v, PACON 90, Vol. II, phosphate and silicate in Cleveland B~ty, Northern pp. 13-20, Tokyo. Queensland. Aust. J. Mar. Freshwat. Res. 32, 877-887. Revelante N. and Gilmartin M. (1982) Dynamics of phyto- Water Quality Council (1985a) Section 3 of Water Quality plankton in the Great Barrier Reef lagoon. J. Plankton Council internal investigation report of November 1984. Res. 4, 47-76. ltamilton Island study. Revelante N., Williams W. T. and Bunt J. S. (1982) Tem- Water Quality Council (1985b) Thirteenth annual report-- poral and spatial distribution of diatoms, dinoflagellates The Water Quality Council of Queensland. and Tru'hod,smium in waters of the Great Barrier Reef. Wilkinson C. R. and Sammarco P. W. (1983) Effects of fish J. exp. Mar. Biol. Ecol. 63, 27-45. grazing and damsellish territoriality on coral reef algae. Reynolds C. S. (1978) Phosphorus and the eutrophication of II. Nitrogen fixation. Mar. Ecol. Prog. Ser, 13, 15-19. --a personal view. In Phosphorus in the Em.ironmcnt: Wilkinson C. R., Williams D. McB., Sammarco P. W., its Chemistry and Biochemistry (Edited by Porter R. and Hogg R. W. and Trott L. A. (1984) Rates of nitrogen Fitzsimons D. W.), pp. 201-228. Ciba Foundation Syrup. fixation on coral reefs across the continental shelf of the 57, Elsevier, Amsterdam. central Great Barrier Reef. Mar. Biol. 80, 255-262, Salin R. (1983) Coral reefs of the western Indian Ocean: a van Woesik R. (1989) A preliminary examination of the threatened heritage. Ambio 12, 1149-1160. sedimentology, reef growth and hydrography of Green Smith S. V., Kimmerer W. J., Laws E. A., Brock Island. Draft report to Great Barrier Reef Marine Park R. E. and Walsh T, W. (1981) Kaneohe Bay Authority, Townsville. sewage diversion experiment: perspectives on ecosystem van Woesik R., Bell P. R. F. and Steven (1992) A. responses to nutritional perturbation. Pac. Sci. 35, Discharge from tourist resorts in Queensland, Australia: 279-385. coral community response. Proc. Congress on Coastal and Sorokin Y. I. (1973) Microbiological aspects of the pro- Marine Tourism, East-West Centre, University of ductivity of coral reefs. In Bmlogy and Geology of Coral Honolulu. May 1990. In press. Reefs (Edited by Jones O. A. and Endean R.), Chap. 2, Wood-Jones F. (1912) Coral and Atolls. Lovel, Reeve & Co., Vol I1: Biology I. Academic Press, London. London.