Effects of varying levels of nutrient inputs to coastal marine systems: a case study of a semi-enclosed bay influenced by a large urban population
Gregory P. Jenkins A * , Kerry P. Black B and Perran L. M. Cook CA
B
C
Abstract
Port Phillip Bay (PPB) is the largest marine bay on the Australian coast and is the site of Australia’s second largest city, Melbourne. A major environmental study in the 1990s recommended a reduction in the nitrogen (N) input to the bay. Subsequently, improvements to sewage treatment efficiency in the 2000s coincided with the longest and most severe drought in recorded history, resulting in N inputs dropping by more than half in the 2000s compared with the 1990s. Here we review studies conducted over the past 30 years to understand the effects of varying nutrient levels on the ecology of PPB. Studies showed that PPB is an N limited system both in time and space. Biological productivity in PPB was markedly affected by reduced N loads during the drought, resulting in declines in seagrass and kelp cover, as well as benthic fish biomass. Overall, research has shown that while setting conservative limits on N input will effectively negate the risk of widespread eutrophication, there will likely be a tradeoff in reduced bay productivity. Managers will need to consider both sides of this equation when managing the load of N entering PPB, and potentially other marine systems around the world.
Keywords: denitrification, drought, ecology, eutrophication, nitrogen, nutrients, Port Phillip Bay, productivity.
References
Australian Bureau of Statistics (2023) Population Projections, Australia. Available at https://www.abs.gov.au/statistics/people/population/population-projections-australia/2022-base-2071
Australian Government (2023) Projections of population changes in our capital cities and rest-of-state areas. Available at https://population.gov.au/data-and-forecasts/dashboards/projections-population-changes-our-capital-cities-and-rest-state
Ayvazian SG, Ray NE, Gerber-Williams A, Grabbert S, Pimenta A, Hancock B, Cobb D, Strobel C, Fulweiler RW (2022) Evaluating connections between nitrogen cycling and the macrofauna in native oyster beds in a New England estuary. Estuaries and Coasts 45(1), 196-212.
| Crossref | Google Scholar | PubMed |
Ball D, Soto-Berelov M, Young P (2014) Historical seagrass mapping in Port Phillip Bay, Australia. Journal of Coastal Conservation 18(3), 257-272.
| Crossref | Google Scholar |
Barbier EB (2017) Marine ecosystem services. Current Biology 27(11), R507-R510.
| Crossref | Google Scholar | PubMed |
Berelson WM, Heggie D, Longmore A, Kilgore T, Nicholson G, Skyring G (1998) Benthic nutrient recycling in Port Phillip Bay, Australia. Estuarine, Coastal and Shelf Science 46, 917-934.
| Crossref | Google Scholar |
Berelson WM, Townsend T, Heggie DT, Ford P, Longmore AR, Skyring GW, Kilgore T, Nicholson GJ (1999) Modelling bio-irrigation rates in the sediments of Port Phillip Bay. Marine and Freshwater Research 50, 573-580.
| Crossref | Google Scholar |
Billen G, Garnier J (2007) River basin nutrient delivery to the coastal sea: Assessing its potential to sustain new production of non-siliceous algae. Marine Chemistry 106(1), 148-160.
| Crossref | Google Scholar |
Black KP, Hatton D, Rosenberg M (1993) Locally and externally-driven dynamics of a large semi-enclosed bay in southern Australia. Journal of Coastal Research 9, 509-538.
| Google Scholar |
Black KP, Longmore AR, Hamer PA, Lee R, Swearer SE, Jenkins GP (2016a) Linking nutrient inputs, phytoplankton composition, zooplankton dynamics and the recruitment of pink snapper, Chrysophrys auratus, in a temperate bay. Estuarine, Coastal and Shelf Science 183, 150-162.
| Crossref | Google Scholar |
Bourke MF, Kessler AJ, Cook PLM (2014) Influence of buried Ulva lactuca on denitrification in permeable sediments. Marine Ecology Progress Series 498, 85-94.
| Crossref | Google Scholar |
Broadley A, Stewart-Koster B, Kenyon RA, Burford MA, Brown CJ (2020) Impact of water development on river flows and the catch of a commercial marine fishery. Ecosphere 11(7), e03194.
| Crossref | Google Scholar |
Bulthuis DA, Axelrad DM, Mickelson MJ (1992) Growth of the seagrass Heterozostera tasmanica limited by nitrogen in Port Phillip Bay, Australia. Marine Ecology Progress Series 89, 269-277.
| Crossref | Google Scholar |
Cai W, Borlace S, Lengaigne M, van Rensch P, Collins M, Vecchi G, Timmermann A, Santoso A, McPhaden M, Wu L, England M, Wang G, Guilyardi E, Jin F-F (2014) Increasing frequency of extreme El Niño events due to greenhouse warming. Nature Climate Change 4(2), 111-116.
| Crossref | Google Scholar |
Cai W, Wang G, Santoso A, McPhaden MJ, Wu L, Jin F-F, Timmermann A, Collins M, Vecchi G, Lengaigne M, England MH, Dommenget D, Takahashi K, Guilyardi E (2015) Increased frequency of extreme La Niña events under greenhouse warming. Nature Climate Change 5(2), 132-137.
| Crossref | Google Scholar |
Carnell PE, Keough MJ (2014) Spatially variable synergistic effects of disturbance and additional nutrients on kelp recruitment and recovery. Oecologia 175(1), 409-416.
| Crossref | Google Scholar | PubMed |
Carnell PE, Keough MJ (2019) Reconstructing historical marine populations reveals major decline of a kelp forest ecosystem in Australia. Estuaries and Coasts 42(3), 765-778.
| Crossref | Google Scholar |
Chen JJ, Erler DV, Wells NS, Huang J, Welsh DT, Eyre BD (2021) Denitrification, anammox, and dissimilatory nitrate reduction to ammonium across a mosaic of estuarine benthic habitats. Limnology and Oceanography 66(4), 1281-1297.
| Crossref | Google Scholar |
Chiew FHS, Zheng H, Potter NJ, Ekstrom M, Grose MR, Kirono DGC, Zhang L, Vaze J (2017) Future runoff projections for Australia and science challenges in producing next generation projections. In ‘Proceedings - 22nd International Congress on Modelling and Simulation’, MODSIM 2017. pp. 1745–1751. (Modelling and Simulation Society of Australia and New Zealand) Available at https://mssanz.org.au/modsim2017/L16/chiew.pdf
Cloern JE, Abreu PC, Carstensen J, Chauvaud L, Elmgren R, Grall J, Greening H, Johansson JOR, Kahru M, Sherwood ET, Xu J, Yin K (2016) Human activities and climate variability drive fast-paced change across the world’s estuarine–coastal ecosystems. Global Change Biology 22(2), 513-529.
| Crossref | Google Scholar | PubMed |
Cook PLM, Evrard V, Woodland RJ (2015) Factors controlling nitrogen fixation in temperate seagrass beds. Marine Ecology Progress Series 525, 41-51.
| Crossref | Google Scholar |
Dalsgaard T (2003) Benthic primary production and nutrient cycling in sediments with benthic microalgae and transient accumulation of macroalgae. Limnology and Oceanography 48(6), 2138-2150.
| Crossref | Google Scholar |
Dayton PJ, Tegner MJ, Edwards PB, Riser KL (1999) Temporal and spatial scales of kelp demography: The role of oceanographic climate. Ecological Monographs 69(2), 219-250.
| Crossref | Google Scholar |
Dey R, Lewis SC, Arblaster JM, Abram NJ (2019) A review of past and projected changes in Australia’s rainfall. WIREs Climate Change 10(3), e577.
| Crossref | Google Scholar |
Drewry JJ, Newham LTH, Greene RSB, Jakeman AJ, Croke BFW (2006) A review of nitrogen and phosphorus export to waterways: context for catchment modelling. Marine and Freshwater Research 57(8), 757-774.
| Crossref | Google Scholar |
Eyre BD, Ferguson AJP (2009) Denitrification efficiency for defining critical loads of carbon in shallow coastal ecosystems. Hydrobiologia 629(1), 137-146.
| Crossref | Google Scholar |
Ford JR, Hamer P (2016) The forgotten shellfish reefs of coastal Victoria: documenting the loss of a marine ecosystem over 200 years since European settlement. Proceedings of the Royal Society of Victoria 128, 87-105.
| Crossref | Google Scholar |
García-Robledo E, Revsbech NP, Risgaard-Petersen N, Corzo A (2013) Changes in N cycling induced by Ulva detritus enrichment of sediments. Aquatic Microbial Ecology 69(2), 113-122.
| Crossref | Google Scholar |
Gaylard S, Waycott M, Lavery P (2020) Review of coast and marine ecosystems in temperate Australia demonstrates a wealth of ecosystem services. Frontiers in Marine Science 7, 453.
| Crossref | Google Scholar |
Glibert PM (2017) Eutrophication, harmful algae and biodiversity — Challenging paradigms in a world of complex nutrient changes. Marine Pollution Bulletin 124(2), 591-606.
| Crossref | Google Scholar | PubMed |
Hirst AJ, Jenkins GP (2017) Experimental test of N-limitation for Zostera nigricaulis seagrass at three sites reliant upon very different sources of N. Journal of Experimental Marine Biology and Ecology 486, 204-213.
| Crossref | Google Scholar |
Hirst AJ, Longmore AR, Ball D, Cook PLM, Jenkins GP (2016) Linking nitrogen sources utilised by seagrass in a temperate marine embayment to patterns of seagrass change during drought. Marine Ecology Progress Series 549, 79-88.
| Crossref | Google Scholar |
Hirst AJ, Giri K, Ball D, Lee RS (2017) Determination of the physical drivers of Zostera seagrass distribution using a spatial autoregressive lag model. Marine and Freshwater Research 68, 1752-1763.
| Crossref | Google Scholar |
Holdgate GR, Geurin B, Wallace MW, Gallagher SJ (2001) Marine geology of Port Phillip, Victoria. Australian Journal of Earth Sciences 48(3), 439-455.
| Crossref | Google Scholar |
Howarth RW (2008) Coastal nitrogen pollution: A review of sources and trends globally and regionally. Harmful Algae 8(1), 14-20.
| Crossref | Google Scholar |
Humborg C, Conley DJ, Rahm L, Wulff F, Adriana C, Ittekkot V (2000) Silicon Retention in River Basins: Far-Reaching Effects on Biogeochemistry and Aquatic Food Webs in Coastal Marine Environments. Ambio 29(1), 45-50.
| Crossref | Google Scholar |
Jenkins GP, Black KP (2019) Contrasting impact of diatoms on dominant calanoid and cyclopoid copepods in a temperate bay. Estuarine, Coastal and Shelf Science 217, 211-217.
| Crossref | Google Scholar |
Jenkins GP, Black KP (2021) Modelling the effects of changing loads of nitrogen discharged from a sewage treatment plant on plankton dynamics in a large, urbanised bay. Regional Studies in Marine Science 45, 101825.
| Crossref | Google Scholar |
Kriegisch N, Reeves S, Johnson CR, Ling SD (2016) Phase-shift dynamics of sea urchin overgrazing on nutrified reefs. PLoS One 11(12), e0168333.
| Crossref | Google Scholar | PubMed |
Kriegisch N, Reeves SE, Johnson CR, Ling SD (2019) Top-down sea urchin overgrazing overwhelms bottom-up stimulation of kelp beds despite sediment enhancement. Journal of Experimental Marine Biology and Ecology 514–515, 48-58.
| Crossref | Google Scholar |
Kriegisch N, Reeves SE, Johnson CR, Ling SD (2020) Sea urchin control of macroalgal communities across a productivity gradient. Journal of Experimental Marine Biology and Ecology 527, 151248.
| Crossref | Google Scholar |
Lee RS, Black KP, Bosserelle C, Greer D (2012) Present and future prolonged drought impacts on a temperate marine embayment. Ocean Dynamics 62, 907-922.
| Crossref | Google Scholar |
Lemley DA, Adams JB, Bornman TG, Campbell EE, Deyzel SHP (2019) Land-derived inorganic nutrient loading to coastal waters and potential implications for nearshore plankton dynamics. Continental Shelf Research 174, 1-11.
| Crossref | Google Scholar |
Maavara T, Akbarzadeh Z, Van Cappellen P (2020a) Global dam-driven changes to riverine N:P:Si ratios delivered to the coastal ocean. Geophysical Research Letters 47(15), e2020GL088288.
| Crossref | Google Scholar |
Maavara T, Chen Q, Van Meter K, Brown LE, Zhang J, Ni J, Zarfl C (2020b) River dam impacts on biogeochemical cycling. Nature Reviews Earth & Environment 1(2), 103-116.
| Crossref | Google Scholar |
Malone TC, Newton A (2020) The globalization of cultural eutrophication in the coastal ocean: causes and consequences. Frontiers in Marine Science 7, 670.
| Crossref | Google Scholar |
Marshall AJ, Longmore A, Phillips L, Tang C, Hayden HL, Heidelberg KB, Mele P (2021) Nitrogen cycling in coastal sediment microbial communities with seasonally variable benthic nutrient fluxes. Aquatic Microbial Ecology 86, 1-19.
| Crossref | Google Scholar |
Marshall AJ, Phillips L, Longmore A, Hayden HL, Heidelberg KB, Tang C, Mele P (2023a) Temporal profiling resolves the drivers of microbial nitrogen cycling variability in coastal sediments. Science of The Total Environment 856, 159057.
| Crossref | Google Scholar |
Marshall AJ, Phillips L, Longmore A, Hayden HL, Tang C, Heidelberg KB, Mele P (2023b) Using metatranscriptomics to better understand the role of microbial nitrogen cycling in coastal sediment benthic flux denitrification efficiency. Environmental Microbiology Reports 15(4), 308-323.
| Crossref | Google Scholar |
Murphy HM, Jenkins GP, Hamer PA, Swearer SE (2012) Interannual variation in larval survival of snapper (Chrysophrys auratus, Sparidae) is linked to diet breadth and prey availability. Canadian Journal of Fisheries and Aquatic Sciences 69, 1340-1351.
| Crossref | Google Scholar |
Murphy HM, Jenkins GP, Hamer PA, Swearer SE (2013) Interannual variation in larval abundance and growth in snapper Chrysophrys auratus (Sparidae) is related to prey availability and temperature. Marine Ecology Progress Series 487, 151-162.
| Crossref | Google Scholar |
Murray AG, Parslow JS (1999) Modelling of nutrient impacts in Port Phillip Bay — a semi-enclosed marine Australian ecosystem. Marine and Freshwater Research 50(6), 597-612.
| Crossref | Google Scholar |
Oczkowski AJ, Nixon SW, Granger SL, El-Sayed A-FM, McKinney RA (2009) Anthropogenic enhancement of Egypt’s Mediterranean fishery. Proceedings of the National Academy of Sciences 106(5), 1364-1367.
| Crossref | Google Scholar | PubMed |
Oviatt C, Smith L, Krumholz J, Coupland C, Stoffel H, Keller A, McManus MC, Reed L (2017) Managed nutrient reduction impacts on nutrient concentrations, water clarity, primary production, and hypoxia in a north temperate estuary. Estuarine, Coastal and Shelf Science 199, 25-34.
| Crossref | Google Scholar |
Parry GD, Black KP (2023) Sewage-derived nitrogen dispersal and N-fixation in Port Phillip Bay in south-eastern Australia. Marine and Freshwater Research 74(16), 1370-1387.
| Crossref | Google Scholar |
Parry GD, Hirst AD (2016) Decadal decline in demersal fish biomass coincident with a prolonged drought and the introduction of an exotic starfish. Marine Ecology Progress Series 544, 37-52.
| Crossref | Google Scholar |
Rauniyar SP, Power SB (2020) The Impact of anthropogenic forcing and natural processes on past, present, and future rainfall over Victoria, Australia. Journal of Climate 33(18), 8087-8106.
| Crossref | Google Scholar |
Rauniyar SP, Power SB (2022) Estimating future rainfall distributions in a changing climate for water resource planning: Victoria, Australia. Climate Dynamics 60, 527-547.
| Crossref | Google Scholar |
Reeves SE, Kriegisch N, Johnson CR, Ling SD (2018) Reduced resistance to sediment-trapping turfs with decline of native kelp and establishment of an exotic kelp. Oecologia 188(4), 1239-1251.
| Crossref | Google Scholar | PubMed |
Reeves SE, Kriegisch N, Johnson CR, Ling SD (2022) Kelp habitat fragmentation reduces resistance to overgrazing, invasion and collapse to turf dominance. Journal of Applied Ecology 59(6), 1619-1631.
| Crossref | Google Scholar |
Risgaard-Petersen N (2003) Coupled nitrification-denitrification in autotrophic and heterotrophic sediments: On the influence of benthic microalgae. Limnology and Oceanography 48, 93-105.
| Crossref | Google Scholar |
Risgaard-Petersen N, Nicolaisen MH, Revsbech NP, Lomstein BA (2004) Competition between ammonia-oxidizing bacteria and benthic microalgae. Applied and Environmental Microbiology 70(9), 5528-5537.
| Crossref | Google Scholar | PubMed |
Rozemeijer J, Noordhuis R, Ouwerkerk K, Dionisio Pires M, Blauw A, Hooijboer A, van Oldenborgh GJ (2021) Climate variability effects on eutrophication of groundwater, lakes, rivers, and coastal waters in the Netherlands. Science of The Total Environment 771, 145366.
| Crossref | Google Scholar | PubMed |
Seitzinger S, Harrison JA, Böhlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Van Drecht G (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecological Applications 16(6), 2064-2090.
| Crossref | Google Scholar | PubMed |
Shim MJ, Yoon YY (2021) Long-term variation of nitrate in the East Sea, Korea. Environmental Monitoring and Assessment 193(11), 720.
| Crossref | Google Scholar | PubMed |
Trimmer M, Nedwell DB, Sivyer DB, Malcolm SJ (2000) Seasonal organic mineralisation and denitrification in intertidal sediments and their relationship to the abundance of Enteromorpha sp. and Ulva sp. Marine Ecology Progress Series 203, 67-80.
| Crossref | Google Scholar |
Ummenhofer CC, England MH, McIntosh PC, Meyers GA, Pook MJ, Risbey JS, Gupta AS, Taschetto AS (2009) What causes southeast Australia’s worst droughts? Geophysical Research Letters 36(4), L04706.
| Crossref | Google Scholar |
Valero-Rodríguez JM, Dempster T, Wong WW, Lewis JA, Cook PLM, Swearer SE (2024) Spatio-temporal patterns in the biomass, species composition and nitrogen content of drift macroalgae in an urbanised coastal embayment. Journal of Applied Phycology 36, 2369-2381.
| Crossref | Google Scholar |
Viaroli P, Bartoli M, Bondavalli C, Christian RR, Giordani G, Naldi M (1996) Macrophyte communities and their impact on benthic fluxes of oxygen, sulphide and nutrients in shallow eutrophic environments. Hydrobiologia 329(1–3), 105-119.
| Crossref | Google Scholar |
Whitall D, Bricker S, Ferreira J, Nobre AM, Simas T, Silva M (2007) Assessment of eutrophication in estuaries: pressure–state–response and nitrogen source apportionment. Environmental Management 40(4), 678-690.
| Crossref | Google Scholar | PubMed |
Wilson RS, Heislers S, Poore GCB (1999) Changes in benthic communities of Port Phillip Bay, Australia, between 1969 and 1995. Marine and Freshwater Research 49(8), 847-861.
| Crossref | Google Scholar |
Wong WW, Greening C, Shelley G, Lappan R, Leung PM, Kessler A, Winfrey B, Poh SC, Cook P (2021) Effects of drift algae accumulation and nitrate loading on nitrogen cycling in a eutrophic coastal sediment. Science of The Total Environment 790, 147749.
| Crossref | Google Scholar | PubMed |
Wong WW, Cartwright I, Poh SC, Cook P (2022) Sources and cycling of nitrogen revealed by stable isotopes in a highly populated large temperate coastal embayment. Science of The Total Environment 806, 150408.
| Crossref | Google Scholar | PubMed |
Zhao H, Yuan M, Strokal M, Wu HC, Liu X, Murk A, Kroeze C, Osinga R (2021) Impacts of nitrogen pollution on corals in the context of global climate change and potential strategies to conserve coral reefs. Science of The Total Environment 774, 145017.
| Crossref | Google Scholar |
Zheng H, Chiew FHS, Potter NJ, Kirono DGC (2019) Projections of water futures for Australia: An update. In ‘23rd International Congress on Modelling and Simulation - Supporting Evidence-Based Decision Making: The Role of Modelling and Simulation’, MODSIM 2019. pp. 1000–1006. (Modelling and Simulation Society of Australia and New Zealand) Available at https://mssanz.org.au/modsim2019/K7/zhengH.pdf