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Advances in the aquatic sciences
RESEARCH ARTICLE

Simulating the potential effects of a carp virus fish kill on water quality and phytoplankton in lentic environments

Joseph B. Pera https://orcid.org/0000-0001-5512-4498 A B C , Alec W. Davie https://orcid.org/0000-0001-6356-8152 A , Ann-Marie Rohlfs A and Simon M. Mitrovic B
+ Author Affiliations
- Author Affiliations

A WaterNSW, Level 14/169 Macquarie Street, Parramatta, NSW 2150, Australia.

B Freshwater and Estuarine Research Group, School of Life Sciences, University of Technology, 15 Broadway, Ultimo, NSW 2007, Australia.

C Corresponding author. Email: joe.pera@waternsw.com.au

Marine and Freshwater Research 73(2) 178-192 https://doi.org/10.1071/MF20368
Submitted: 29 December 2020  Accepted: 21 May 2021   Published: 26 July 2021

Abstract

Decaying fish play an important role in delivering nutrients into rivers and lakes but can create water quality issues. The release of cyprinid herpesvirus-3 (CyHV-3) in Australia with an associated mass common carp mortality may have serious effects on water quality in lakes. To evaluate the effect of a virus-induced fish kill, different biomasses of dead common carp (250–6000 kg ha–1) were placed into 2000-L mesocosms within Prospect Reservoir, Australia, for up to 40 days. Decaying carp created anoxic conditions within all treatments except the 250 kg ha–1 treatment, in which oxygen saturation dropped to 30%. A higher biomass of carp led to longer periods of anoxia. Total nitrogen (TN) increased from a baseline of 0.25 to 1.5–30 mg L–1 in the different treatments, whereas total phosphorus (TP) increased from 0.01 to 0.05–5.0 mg L–1. Chlorophyll-a levels increased from <5 µg L–1 to levels between 100 and 1000 µg L–1 in the different treatments. Mean nutrient levels (TN and TP), chlorophyll-a and phytoplankton biovolume all showed a significant (P < 0.05) linear relationship with carp biomass. This relationship can be used to support the quantification of water quality risk from a known biomass of carp. Our experiment suggests that carp mortality may significantly reduce water quality in shallow lakes where the biomass of dead carp is above moderate levels (250 kg ha–1).


References

Abell, J. M., Özkundakci, D., and Hamilton, D. P. (2010). Nitrogen and phosphorus limitation of phytoplankton growth in New Zealand lakes: implications for eutrophication control. Ecosystems 13, 966–977.
Nitrogen and phosphorus limitation of phytoplankton growth in New Zealand lakes: implications for eutrophication control.Crossref | GoogleScholarGoogle Scholar |

Adámek, Z., and Maršálek, B. (2013). Bioturbation of sediments by benthic macroinvertebrates and fish and its implication for pond ecosystems: a review. Aquaculture International 21, 1–17.
Bioturbation of sediments by benthic macroinvertebrates and fish and its implication for pond ecosystems: a review.Crossref | GoogleScholarGoogle Scholar |

Agency for Toxic Substances and Disease Registry (2018). Toxicological profile for n-Nitrosodimethylamine. CAS#: 62–75–9. (ATSDR.) Available at https://wwwn.cdc.gov/TSP/ToxProfiles/ToxProfiles.aspx?id=884&tid=173 [Verified 24 May 2021].

Ansari, A., and Gill, S. (2014). ‘Eutrophication: Causes, Consequences and Control.’ (Springer: Dordrecht, Netherlands.)

Assemany, P., Calijuri, M., Couto, E., de Souza, M., Silva, N., Santiago, A., and Castro, J. (2015). Algae/bacteria consortium in high rate ponds: Influence of solar radiation on the phytoplankton community. Ecological Engineering 77, 154–162.
Algae/bacteria consortium in high rate ponds: Influence of solar radiation on the phytoplankton community.Crossref | GoogleScholarGoogle Scholar |

Ayers, L. E. (2010). Differential decomposition in terrestrial, freshwater, and saltwater environments: a pilot study. M.Sc. Thesis, Texas State University—San Marcos, San Marcos, TX, USA.

Bajer, P., and Sorensen, P. (2012). Using boat electrofishing to estimate the abundance of invasive common carp in small Midwestern Lakes. North American Journal of Fisheries Management 32, 817–822.
Using boat electrofishing to estimate the abundance of invasive common carp in small Midwestern Lakes.Crossref | GoogleScholarGoogle Scholar |

Bajer, P., and Sorensen, P. (2015). Effects of common carp on phosphorus concentrations, water clarity, and vegetation density: a whole system experiment in a thermally stratified lake. Hydrobiologia 746, 303–311.
Effects of common carp on phosphorus concentrations, water clarity, and vegetation density: a whole system experiment in a thermally stratified lake.Crossref | GoogleScholarGoogle Scholar |

Beamish, F. W. H. (1964). Respiration of fishes with special emphasis on standard oxygen consumption: III. Influence on oxygen. Canadian Journal of Zoology 42, 355–366.
Respiration of fishes with special emphasis on standard oxygen consumption: III. Influence on oxygen.Crossref | GoogleScholarGoogle Scholar |

Beasley, M. (1998). ‘The sweat of their brows. 100 years of the Sydney Water Board.’ (Water Board: Sydney, NSW, Australia.)

Bhateria, R., and Jain, D. (2016). Water quality assessment of lake water: a review. Sustainable Water Resources Management 2, 161–173.
Water quality assessment of lake water: a review.Crossref | GoogleScholarGoogle Scholar |

Bilby, R., Beach, E., Fransen, B., Walter, J., and Bisson, P. (2003). Transfer of nutrients from spawning salmon to riparian vegetation in western Washington. Transactions of the American Fisheries Society 132, 733–745.
Transfer of nutrients from spawning salmon to riparian vegetation in western Washington.Crossref | GoogleScholarGoogle Scholar |

Boros, G., Takács, P., and Vanni, M. (2015). The fate of phosphorus in decomposing fish carcasses: a mesocosm experiment. Freshwater Biology 60, 479–489.
The fate of phosphorus in decomposing fish carcasses: a mesocosm experiment.Crossref | GoogleScholarGoogle Scholar |

Brooker, M., Morris, D., and Hemsworth, R. (1977). Mass mortalities of adult salmon, Salmo salar, in the R. Wye, 1976. Journal of Applied Ecology 14, 409.
Mass mortalities of adult salmon, Salmo salar, in the R. Wye, 1976.Crossref | GoogleScholarGoogle Scholar |

Carney, R. L., Seymour, J. R., Westhorpe, D., and Mitrovic, S. M. (2016). Lotic bacterioplankton and phytoplankton community changes under dissolved organic-carbon amendment: evidence for competition for nutrients. Marine and Freshwater Research 67, 1362–1373.
Lotic bacterioplankton and phytoplankton community changes under dissolved organic-carbon amendment: evidence for competition for nutrients.Crossref | GoogleScholarGoogle Scholar |

Çelik, K., and Ongun, T. (2006). The relationships between certain physical and chemical variables and the seasonal dynamics of phytoplankton assemblages of two inlets of a shallow hypertrophic lake with different nutrient inputs. Environmental Monitoring and Assessment 124, 321–330.
| 16897515PubMed |

Chislock, M. F., Doster, E., Zitomer, R. A., and Wilson, A. E. (2013). Eutrophication: causes, consequences, and controls in aquatic ecosystems. Nature Education Knowledge 4, 10.

Conley, D. J., Carstensen, J., Vaquer-Sunyer, R., and Duarte, C. M. (2009). Ecosystem thresholds with hypoxia. Developments in Hydrobiology 207, 21–29.
Ecosystem thresholds with hypoxia.Crossref | GoogleScholarGoogle Scholar |

Crooks, J. A. (2002). Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97, 153–166.
Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers.Crossref | GoogleScholarGoogle Scholar |

Cuvin-Aralar, M. L., Santiago, A. E., Gonzal, A. C., Santiago, C. B., Romana-Eguia, M. R., Baldia, S. F., and Palisoc, F. Jr (2001). Incidence and causes of mass fish kill in a shallow tropical eutrophic lake (Laguna de Bay, Philippines). In ‘9th International Conference on the Conservation and Management of Lakes. Conference Proceedings’. pp. 233–236. (Shiga Prefectural Government: Shiga, Japan.)

Davis, J. C. (1975). Minimal dissolved oxygen requirements of aquatic life with emphasis on Canadian species: a review. Journal of the Fisheries Research Board of Canada 32, 2295–2332.
Minimal dissolved oxygen requirements of aquatic life with emphasis on Canadian species: a review.Crossref | GoogleScholarGoogle Scholar |

Dean, T., and Richardson, J. (1999). Responses of seven species of native freshwater fish and a shrimp to low levels of dissolved oxygen. New Zealand Journal of Marine and Freshwater Research 33, 99–106.
Responses of seven species of native freshwater fish and a shrimp to low levels of dissolved oxygen.Crossref | GoogleScholarGoogle Scholar |

Dokulil, M., Chen, W., and Cai, Q. (2000). Anthropogenic impacts to large lakes in China: the Tai Hu example. Aquatic Ecosystem Health & Management 3, 81–94.
Anthropogenic impacts to large lakes in China: the Tai Hu example.Crossref | GoogleScholarGoogle Scholar |

Dutton, C., Subalusky, A., Hamilton, S., Rosi, E., and Post, D. (2018). Organic matter loading by hippopotami causes subsidy overload resulting in downstream hypoxia and fish kills. Nature Communications 9, 1951.
Organic matter loading by hippopotami causes subsidy overload resulting in downstream hypoxia and fish kills.Crossref | GoogleScholarGoogle Scholar | 29769538PubMed |

Elser, J., Andersen, T., Baron, J., Bergstrom, A., Jansson, M., Kyle, M., Nydick, K., Steger, L., and Hessen, D. (2009). Shifts in lake N:P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition. Science 326, 835–837.
Shifts in lake N:P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition.Crossref | GoogleScholarGoogle Scholar | 19892979PubMed |

Falconer, I. (1999). An overview of problems caused by toxic blue–green algae (cyanobacteria) in drinking and recreational water. Environmental Toxicology 14, 5–12.
An overview of problems caused by toxic blue–green algae (cyanobacteria) in drinking and recreational water.Crossref | GoogleScholarGoogle Scholar |

Felisberto, S., Leandrini, J., and Rodrigues, L. (2011). Effects of nutrients enrichment on algal communities: an experimental in mesocosms approach. Acta Limnologica Brasiliensia 23, 128–137.
Effects of nutrients enrichment on algal communities: an experimental in mesocosms approach.Crossref | GoogleScholarGoogle Scholar |

Gerardi, M. H. (2003). ‘The Microbiology of Anaerobic Digesters.’ (Wiley.) 10.1002/0471468967

Havens, K. E., James, R. T., East, T. L., and Smith, V. H. (2003). N:P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environmental Pollution 122, 379–390.
N:P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution.Crossref | GoogleScholarGoogle Scholar | 12547527PubMed |

Heisler, J., Glibert, P., Burkholder, J., Anderson, D., Cochlan, W., Dennison, W., Gobler, C., Dortch, Q., Heil, C., Humphries, E., Lewitus, A., Magnien, R., Marshall, H., Sellner, K., Stockwell, D., Stoecker, D., and Suddleson, M. (2008). Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8, 3–13.
Eutrophication and harmful algal blooms: a scientific consensus.Crossref | GoogleScholarGoogle Scholar | 28781587PubMed |

Hickey, C. (2018). Bushells Lagoon drying out is a natural occurrence say locals. In Hawkesbury Gazette. Available at https://www.hawkesburygazette.com.au/story/5227911/bushells-lagoon-drying-out-is-a-natural-occurrence-say-locals/ [Verified 22 October 2018].

Hicks, B. J., Osborne, M. W., and Ling, N. (2006). Quantitative estimates of fish abundance from boat electrofishing. In ‘A Guide to Monitoring Fish Stocks and Aquatic Ecosystems’, 11–15 July 2005, Darwin, NT, Australia. (Eds M. J. Phelan and H. Bajhau.) pp. 104–111. (Northern Territory Department of Primary Industry, Fisheries and Mines: Darwin, NT, Australia.)

Huser, B., Bajer, P., Chizinski, C., and Sorensen, P. (2016). Effects of common carp (Cyprinus carpio) on sediment mixing depth and mobile phosphorus mass in the active sediment layer of a shallow lake. Hydrobiologia 763, 23–33.
Effects of common carp (Cyprinus carpio) on sediment mixing depth and mobile phosphorus mass in the active sediment layer of a shallow lake.Crossref | GoogleScholarGoogle Scholar |

Johnston, N., MacIsaac, E., Tschaplinski, P., and Hall, K. (2004). Effects of the abundance of spawning sockeye salmon (Oncorhynchus nerka) on nutrients and algal biomass in forested streams. Canadian Journal of Fisheries and Aquatic Sciences 61, 384–403.
Effects of the abundance of spawning sockeye salmon (Oncorhynchus nerka) on nutrients and algal biomass in forested streams.Crossref | GoogleScholarGoogle Scholar |

King, A., Robertson, A., and Healey, M. (1997). Experimental manipulations of the biomass of introduced carp (Cyprinus carpio) in billabongs. I. Impacts on water-column properties. Marine and Freshwater Research 48, 435.
Experimental manipulations of the biomass of introduced carp (Cyprinus carpio) in billabongs. I. Impacts on water-column properties.Crossref | GoogleScholarGoogle Scholar |

Koehn, J. D. (2004). Carp (Cyprinus carpio) as a powerful invader in Australian waterways. Freshwater Biology 49, 882–894.
Carp (Cyprinus carpio) as a powerful invader in Australian waterways.Crossref | GoogleScholarGoogle Scholar |

Kolmakov, V., and Gladyshev, M. (2003). Growth and potential photosynthesis of cyanobacteria are stimulated by viable gut passage in crucian carp. Aquatic Ecology 37, 237–242.
Growth and potential photosynthesis of cyanobacteria are stimulated by viable gut passage in crucian carp.Crossref | GoogleScholarGoogle Scholar |

Kolzau, S., Wiedner, C., Rücker, J., Köhler, J., Köhler, A., and Dolman, A. M. (2014). Seasonal patterns of nitrogen and phosphorus limitation in four German lakes and the predictability of limitation status from ambient nutrient concentrations. PLoS One 9, e96065.
Seasonal patterns of nitrogen and phosphorus limitation in four German lakes and the predictability of limitation status from ambient nutrient concentrations.Crossref | GoogleScholarGoogle Scholar | 24755935PubMed |

Kristensen, E., Ahmed, S. I., and Devol, A. H. (1995). Aerobic and anaerobic decomposition of organic matter in marine sediment: which is fastest? Limnology and Oceanography 40, 1430–1437.
Aerobic and anaerobic decomposition of organic matter in marine sediment: which is fastest?Crossref | GoogleScholarGoogle Scholar |

Kushlan, J. (1974). Effects of a natural fish kill on the water quality, plankton, and fish population of a pond in the Big Cypress Swamp, Florida. Transactions of the American Fisheries Society 103, 235–243.
Effects of a natural fish kill on the water quality, plankton, and fish population of a pond in the Big Cypress Swamp, Florida.Crossref | GoogleScholarGoogle Scholar |

Li, R. A., McDonald, J. A., Sathasivan, A., and Khan, S. J. (2019). Disinfectant residual stability leading to disinfectant decay and by-product formation in drinking water distribution systems: a systematic review. Water Research 153, 335–348.
Disinfectant residual stability leading to disinfectant decay and by-product formation in drinking water distribution systems: a systematic review.Crossref | GoogleScholarGoogle Scholar | 30743084PubMed |

Lighten, J., and van Oosterhout, C. (2017). Biocontrol of common carp in Australia poses risks to biosecurity. Nature Ecology & Evolution 1, 0087.
Biocontrol of common carp in Australia poses risks to biosecurity.Crossref | GoogleScholarGoogle Scholar |

Marshall, B. E., and Falconer, A. C. (1973). Eutrophication of a tropical African impoundment (Lake McIlwaine, Rhodesia). Hydrobiologia 43, 109–123.
Eutrophication of a tropical African impoundment (Lake McIlwaine, Rhodesia).Crossref | GoogleScholarGoogle Scholar |

Marshall, J., Davison, A. J., Kopf, R. K., Boutier, M., Stevenson, P., and Vanderplasschen, A. (2018). Biocontrol of invasive carp: risks abound. Science 359, 877.
Biocontrol of invasive carp: risks abound.Crossref | GoogleScholarGoogle Scholar | 29472472PubMed |

Matsui, K., Honjo, M., Kohmatsu, Y., Uchii, K., Yonekura, R., and Kawabata, Z. (2008). Detection and significance of koi herpesvirus (KHV) in freshwater environments. Freshwater Biology 53, 1262–1272.
Detection and significance of koi herpesvirus (KHV) in freshwater environments.Crossref | GoogleScholarGoogle Scholar |

Matsuzaki, S., Usio, N., Takamura, N., and Washitani, I. (2009). Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis. Oecologia 158, 673–686.
Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 18941787PubMed |

McColl, D., Manley, J., Hyles, G., and Winzar, A. (2016). Using herpes virus to eradicate feral fish? Carp diem! In CSIRO blog. Available at https://blog.csiro.au/reclaiming-our-rivers-from-feral-carp [Verified 11 October 2016].

Miller, S. A., and Crowl, T. A. (2006). Effects of common carp (Cyprinus carpio) on macrophytes and invertebrate communities in a shallow lake. Freshwater Biology 51, 85–94.
Effects of common carp (Cyprinus carpio) on macrophytes and invertebrate communities in a shallow lake.Crossref | GoogleScholarGoogle Scholar |

Minamoto, T., Honjo, M., and Kawabata, Z. (2009). Seasonal distribution of cyprinid herpesvirus 3 in Lake Biwa, Japan. Applied and Environmental Microbiology 75, 6900–6904.
Seasonal distribution of cyprinid herpesvirus 3 in Lake Biwa, Japan.Crossref | GoogleScholarGoogle Scholar | 19734343PubMed |

Mitrovic, S., Hardwick, L., and Dorani, F. (2011). Use of flow management to mitigate cyanobacterial blooms in the Lower Darling River, Australia. Journal of Plankton Research 33, 229–241.
Use of flow management to mitigate cyanobacterial blooms in the Lower Darling River, Australia.Crossref | GoogleScholarGoogle Scholar |

Morgan, D. K. J., and Hicks, B. J. (2013). A metabolic theory of ecology applied to temperature and mass-dependence of N and P excretion by common carp. Hydrobiologia 705, 135–145.
A metabolic theory of ecology applied to temperature and mass-dependence of N and P excretion by common carp.Crossref | GoogleScholarGoogle Scholar |

Müller, S., and Mitrovic, S. M. (2015). Phytoplankton co-limitation by nitrogen and phosphorus in a shallow reservoir: progressing from the phosphorus limitation paradigm. Hydrobiologia 744, 255–269.
Phytoplankton co-limitation by nitrogen and phosphorus in a shallow reservoir: progressing from the phosphorus limitation paradigm.Crossref | GoogleScholarGoogle Scholar |

Nagasaka, A., Nagasaka, Y., Ito, K., Mano, T., Yamanaka, M., Katayama, A., Sato, Y., Grankin, A. L., Zdorikov, A. I., and Boronov, G. A. (2006). Contributions of salmon-derived nitrogen to riparian vegetation in the northwest Pacific region. Journal of Forest Research 11, 475–476.
Contributions of salmon-derived nitrogen to riparian vegetation in the northwest Pacific region.Crossref | GoogleScholarGoogle Scholar |

Ning, N. S. P., Petrie, R., Gawne, B., Nielsen, D. L., and Rees, G. N. (2015). Hypoxic blackwater events suppress the emergence of zooplankton from wetland sediments. Aquatic Sciences 77, 221–230.
Hypoxic blackwater events suppress the emergence of zooplankton from wetland sediments.Crossref | GoogleScholarGoogle Scholar |

Nõges, T., Laugaste, R., Noges, P., and Tonno, I. (2008). Critical N:P ratio for cyanobacteria and N2-fixing species in the large shallow temperate lakes Peipsi and Vortsjarv, North-East Europe. Hydrobiologia 599, 77–86.
Critical N:P ratio for cyanobacteria and N2-fixing species in the large shallow temperate lakes Peipsi and Vortsjarv, North-East Europe.Crossref | GoogleScholarGoogle Scholar |

NSW Department of Industry and Investment (2010). NSW control plan for the noxious fish carp (Cyprinus carpio). (NSW DPI.) Available at http://www.dpi.nsw.gov.au/__data/assets/pdf_file/0020/637004/nsw-control-plan-for-carp.pdf

O’Donnell, D. R., Wilburn, P., Silow, E. A., Yampolsky, L. Y., and Litchman, E. (2017). Nitrogen and phosphorus colimitation of phytoplankton in Lake Baikal: Insights from a spatial survey and nutrient enrichment experiments. Limnology and Oceanography 62, 1383–1392.
Nitrogen and phosphorus colimitation of phytoplankton in Lake Baikal: Insights from a spatial survey and nutrient enrichment experiments.Crossref | GoogleScholarGoogle Scholar |

Orihel, D. M., Schindler, D. W., Ballard, N. C., Wilson, L. R., and Vinebrooke, R. D. (2016). Experimental iron amendment suppresses toxic cyanobacteria in a hypereutrophic lake. Ecological Applications 26, 1517–1534.
Experimental iron amendment suppresses toxic cyanobacteria in a hypereutrophic lake.Crossref | GoogleScholarGoogle Scholar | 27755758PubMed |

Parkos, J., Santucci, J., and Wahl, D. (2003). Effects of adult common carp (Cyprinus carpio) on multiple trophic levels in shallow mesocosms. Canadian Journal of Fisheries and Aquatic Sciences 60, 182–192.
Effects of adult common carp (Cyprinus carpio) on multiple trophic levels in shallow mesocosms.Crossref | GoogleScholarGoogle Scholar |

PestSmart Connect (2018). Overview of carp in Australia. (PestSmart, Centre for Invasive Species Solutions.) Available at https://pestsmart.org.au/toolkit-resource/overview-of-carp-in-australia/ [Verified 16 July 2021].

Pick, F. R., and Lean, D. R. S. (1987). The role of macronutrients (C, N, P) in controlling cyanobacterial dominance in temperate lakes. New Zealand Journal of Marine and Freshwater Research 21, 425–434.
The role of macronutrients (C, N, P) in controlling cyanobacterial dominance in temperate lakes.Crossref | GoogleScholarGoogle Scholar |

Proulx, M., Pick, F., Mazumder, A., Hamilton, P., and Lean, D. (1996). Experimental evidence for interactive impacts of human activities on lake algal species richness. Oikos 76, 191.
Experimental evidence for interactive impacts of human activities on lake algal species richness.Crossref | GoogleScholarGoogle Scholar |

Ptacnik, R., Solimini, A., Andersen, T., Tamminen, T., Brettum, P., Lepistö, L., Willén, E., and Rekolainen, S. (2008). Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proceedings of the National Academy of Sciences of the United States of America 105, 5134–5138.
Diversity predicts stability and resource use efficiency in natural phytoplankton communities.Crossref | GoogleScholarGoogle Scholar | 18375765PubMed |

Rakus, K., Ouyang, P., Boutier, M., Ronsmans, M., Reschner, A., Vancsok, C., Jazowiecka-Rakus, J., and Vanderplasschen, A. (2013). Cyprinid herpesvirus 3: an interesting virus for applied and fundamental research. Veterinary Research 44, 85.
Cyprinid herpesvirus 3: an interesting virus for applied and fundamental research.Crossref | GoogleScholarGoogle Scholar | 24073814PubMed |

Randall, D. J., and Tsui, T. K. (2002). Ammonia toxicity in fish. Marine Pollution Bulletin 45, 17–23.
Ammonia toxicity in fish.Crossref | GoogleScholarGoogle Scholar | 12398363PubMed |

Schindler, D. W. (1977). Evolution of phosphorus limitation in lakes. Science 195, 260–262.
Evolution of phosphorus limitation in lakes.Crossref | GoogleScholarGoogle Scholar | 17787798PubMed |

Schindler, D. (1998). Whole-ecosystem experiments: replication versus realism: the need for ecosystem-scale experiments. Ecosystems 1, 323–334.
Whole-ecosystem experiments: replication versus realism: the need for ecosystem-scale experiments.Crossref | GoogleScholarGoogle Scholar |

Schoenebeck, C., Brown, M., Chippss, S., and German, D. (2012). Nutrient and algal responses to winter killed fish-derived nutrient subsidies in eutrophic lakes. Lake and Reservoir Management 28, 189–199.
Nutrient and algal responses to winter killed fish-derived nutrient subsidies in eutrophic lakes.Crossref | GoogleScholarGoogle Scholar |

Sereda, J., Hudson, J., Talyor, W., and Demers, E. (2008). Fish as sources and sinks of nutrients in lakes. Freshwater Biology 2008, 278–289.

Sergeant, C., Bellmore, J., McConnell, C., and Moore, J. (2017). High salmon density and low discharge create periodic hypoxia in coastal rivers. Ecosphere 8, e01846.
High salmon density and low discharge create periodic hypoxia in coastal rivers.Crossref | GoogleScholarGoogle Scholar |

Shearer, K., and Mulley, J. (1978). The Introduction and distribution of the carp, Cyprinus carpio Linnaeus, in Australia. Marine and Freshwater Research 29, 551–563.
The Introduction and distribution of the carp, Cyprinus carpio Linnaeus, in Australia.Crossref | GoogleScholarGoogle Scholar |

Sitta, S., Reed, M., Mortensen, R., Doll, C., Callahan, T., and Greenfield, D. (2018). The influences of nitrogen form and zooplankton grazing on phytoplankton assemblages in two coastal southeastern systems Limnology and Oceanography 63, 2523–2544.
The influences of nitrogen form and zooplankton grazing on phytoplankton assemblages in two coastal southeastern systemsCrossref | GoogleScholarGoogle Scholar |

Smith, V. H. (1983). Low nitrogen to phosphorus ratios favour dominance by blue-green algae in lake phytoplankton. Science 221, 669–671.
Low nitrogen to phosphorus ratios favour dominance by blue-green algae in lake phytoplankton.Crossref | GoogleScholarGoogle Scholar | 17787737PubMed |

Smith, B. B. (2005). The state of the art: a synopsis of information on common carp (Cyprinus carpio) in Australia. Final Technical Report, SARDI Aquatic Sciences Publication Number RDO4/0064-2; SARDI Research Report Series Number 77, South Australian Research and Development Institute (Aquatic Sciences), Adelaide, SA, Australia.

Smith, V., Tilman, G., and Nekola, J. (1999). Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100, 179–196.
Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar | 15093117PubMed |

Staight, K. (2018). Will the carp virus help or hinder Australian water’s native species. In ABC News, 9 September 2018. Available at http://www.abc.net.au/news/2018-05-04/carp-herpes-virus-affects-australian-wildlife-and-envirironment/9726468.

Sterner, R., and George, N. (2000). Carbon, nitrogen, and phosphorus stoichiometry of cyprinid fishes. Ecology 81, 127.
Carbon, nitrogen, and phosphorus stoichiometry of cyprinid fishes.Crossref | GoogleScholarGoogle Scholar |

Strock, J. S. (2008). Ammonification. In ‘Encyclopedia of Ecology’. pp. 162–165. (Elsevier Inc.)10.1016/B978-008045405-4.00256-1

Stuart, I. G., Fanson, B., Lyona, J. P., Stocks, J., Brookes, S., Norris, A., Thwaitese, L., Beitzel, M., Hutchison, M., Yee, Q., Koehna, J. D., and Bennett, A. F. (2021). Continental threat: how many common carp (Cypirinus carpio) are there in Australia? Biological Conservation 254, 108942.
Continental threat: how many common carp (Cypirinus carpio) are there in Australia?Crossref | GoogleScholarGoogle Scholar |

Sunarto, A., Rukyani, A., and Itami, T. (2005). Indonesian experience on the outbreak of koi herpesvirus in koi and carp (Cyprinus carpio). Japan Bulletin of Fisheries Research Agency , 15–21.

Swirepik, J. (1999). Physical disturbance of Potamogeton tricarinatus and sediment by carp (Cyprinus carpio) in experimental ponds. M.Sc. Thesis, University of Canberra, Canberra, ACT, Australia.

Tempero, G. W., Ling, N., Daniel, A. J., and Morgan, D. K. J. (2015). Removal of invasive fish and exclusion of koi carp from Lake Ohinewai. In ‘New Zealand Invasive Fish Management Handbook’. (Eds K. J. Collier and N. P. J. Grainger.) pp. 90–94. (Lake Ecosystem Restoration New Zealand (LERNZ) & Department of Conservation Hamilton, New Zealand.)

Twort, A., Ratnayaka, D., and Brandt, M. (2006). ‘Water Supply’, 5th edn. (Butterworth-Heinemann.)

Uchii, K., and Kawabata, Z. (2009). Biological invasion of a fish pathogen, cyprinid herpesvirus 3, into Japanese freshwater ecosystems. Japanese Journal of Limnology 70, 267–272.
Biological invasion of a fish pathogen, cyprinid herpesvirus 3, into Japanese freshwater ecosystems.Crossref | GoogleScholarGoogle Scholar |

Vertessy, R., Barma, D., Baumgartner, L., Mitrovic, S., Sheldon, F., and Bond, N. (2019). Independent assessment of the 2018-19 fish deaths in the Lower Darling. Final report. Australian Government. Available at https://www.mdba.gov.au/sites/default/files/pubs/Final-Report-Independent-Panel-fish-deaths-lower%20Darling_4.pdf

Vılızzı, L., and Tarkan, A. (2015). Experimental evidence for the effects of common carp (Cyprinus carpio L., 1758) on freshwater ecosystems: a narrative review with management directions for Turkish inland waters. Journal of Limnology and Freshwater Fisheries Research 1, 123–149.
Experimental evidence for the effects of common carp (Cyprinus carpio L., 1758) on freshwater ecosystems: a narrative review with management directions for Turkish inland waters.Crossref | GoogleScholarGoogle Scholar |

Villanueva, C. M., Cordier, S., and Font-Ribera, L. (2015). Overview of disinfection by-products and associated health effects. Current Environmental Health Reports 2, 107–115.
Overview of disinfection by-products and associated health effects.Crossref | GoogleScholarGoogle Scholar | 26231245PubMed |

Wanner, G. A., Nenneman, M. P., Lindvall, M., and Kaemingk, M. A. (2009). Common carp abundance, biomass, and removal from Dewey and Clear lakes on the Valentine National Wildlife Refuge: does trapping and removing carp payoff? (US Fish and Wildlife Service and South Dakota State University.) Available at https://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=1014&context=natlinvasive

Weber, M., and Brown, M. (2011). Relationships among invasive common carp, native fishes and physicochemical characteristics in upper Midwest (USA) lakes. Ecology of Freshwater 20, 270–278.
Relationships among invasive common carp, native fishes and physicochemical characteristics in upper Midwest (USA) lakes.Crossref | GoogleScholarGoogle Scholar |

Weber, M., and Brown, M. (2016). Effects of resource pulses on nutrient availability, ecosystem productivity, and temporal variability following a stochastic disturbance in eutrophic glacial lakes. Hydrobiologia 771, 165–177.
Effects of resource pulses on nutrient availability, ecosystem productivity, and temporal variability following a stochastic disturbance in eutrophic glacial lakes.Crossref | GoogleScholarGoogle Scholar |

Williams, A., Moss, B., and Eaton, J. (2002). Fish induced macrophyte loss in shallow lakes: top–down and bottom–up processes in mesocosm experiments. Freshwater Biology 47, 2216–2232.
Fish induced macrophyte loss in shallow lakes: top–down and bottom–up processes in mesocosm experiments.Crossref | GoogleScholarGoogle Scholar |

Wipfli, M., Hudson, J., and Caouette, J. (1998). Influence of salmon carcasses on stream productivity: response of biofilm and benthic macroinvertebrates in southeastern Alaska, USA. Journal Canadien des Sciences Halieutiques et Aquatiques 55, 1503–1511.
Influence of salmon carcasses on stream productivity: response of biofilm and benthic macroinvertebrates in southeastern Alaska, USA.Crossref | GoogleScholarGoogle Scholar |

Zambrano, L., Scheffer, M., and Martinez-Ramos, M. (2001). Catastrophic response of lakes to benthivorous fish introduction. Oikos 94, 344–350.
Catastrophic response of lakes to benthivorous fish introduction.Crossref | GoogleScholarGoogle Scholar |