Oligotrophication; Large rivers; Phosphorus; Corbicula clams; Trend analysis; Loire
Abstract :
[en] Recent studies suggest that climate change, with warmer water temperatures and lower and longer low flows, may enhance harmful planktic cyanobacterial growth in lakes and large rivers. Concomitantly, controlling nutrient loadings has proven effective in reducing phytoplankton biomass especially in North America and Western Europe. In addition, the impact of invasive benthic filter-feeder species such as Corbicula on phytoplankton has largely been overlooked in large rivers, leading to even more uncertainty in predicting future trajectories in river water quality.
To investigate how nutrient control, climate change and invasion of benthic filter-feeders may affect phytoplankton biomass and composition, we assembled a large database on the entire water course of the River Loire (France) over three decades (1991-2019). We focus on cyanobacteria to provide an in-depth analysis of the 30-year trend and insights on future possible trajectories. Since 1991, total phytoplankton and cyanobacteria biomasses have decreased 10-fold despite warmer water temperature (+0.23°C.decade-1) and lower summer flow (-0.25 L.s-1.km-2.decade-1). In the long-term, the contribution of planktic cyanobacteria to total biomass was on average 2.8%. The main factors driving total phytoplankton and cyanobacteria biomasses were total phosphorus (4-fold decrease), the abundance of Corbicula clams (from absence before 1998 to 250-1250 individuals.m-2 after 2010), the duration of summer low flows and the intensity of summer heatwaves. The River Loire constitutes an example in Europe of how nutrient control can be an efficient mitigation strategy, counteracting already visible effects of climate change on the thermal regime and flow pattern of the river. This may hold true under future conditions, but further work is needed to account for the climate trajectory, land and water use scenarios, the risk of enhanced benthic biofilm and macrophyte proliferation, together with the spread of invasive filter-feeding bivalves.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Minaudo, Camille
Abonyi, Andras
Leitao, Maria
Lançon, Anne-Marie
Floury, Mathieu
Descy, Jean-Pierre ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (COU)
Moatar, Florentina
Language :
English
Title :
Long-term impacts of nutrient control, climate change, and invasive clams on phytoplankton and cyanobacteria biomass in a large temperate river
Abbott, B.W., Bishop, K., Zarnetske, J.P., Minaudo, C., Chapin, F.S., Krause, S., Hannah, D.M., Conner, L., Ellison, D., Godsey, S.E., Plont, S., Marçais, J., Kolbe, T., Huebner, A., Frei, R.J., Hampton, T., Gu, S., Buhman, M., Sara Sayedi, S., Ursache, O., Chapin, M., Henderson, K.D., Pinay, G., Human domination of the global water cycle absent from depictions and perceptions. Nat. Geosci. 12 (2019), 533–540, 10.1038/s41561-019-0374-y.
Abonyi, A., Ács, É., Hidas, A., Grigorszky, I., Várbíró, G., Borics, G., Kiss, K.T., Functional diversity of phytoplankton highlights long-term gradual regime shift in the middle section of the Danube River due to global warming, human impacts and oligotrophication. Freshw. Biol. 63 (2018), 456–472, 10.1111/fwb.13084.
Arevalo, E., Lassalle, G., Tétard, S., Maire, A., Sauquet, E., Lambert, P., Paumier, A., Villeneuve, B., Drouineau, H., An innovative bivariate approach to detect joint temporal trends in environmental conditions: application to large French rivers and diadromous fish. Sci. Total Environ., 748, 2020, 141260, 10.1016/j.scitotenv.2020.141260.
Bolam, B.A., Rollwagen-Bollens, G., Bollens, S.M., Feeding rates and prey selection of the invasive Asian clam, Corbicula fluminea, on microplankton in the Columbia River, USA. Hydrobiologia 833 (2019), 107–123, 10.1007/s10750-019-3893-z.
Brancotte, V., Vincent, T., L'invasion du réseau hydrographique français par les mollusques Corbicula Spp. Modalité de colonisation et rôle prépondérant des canaux de navigation. Bull. Fr. Pêche Piscic. 365/366 (2002), 325–337.
Brooks, B.W., Lazorchak, J.M., Howard, M.D.A., Johnson, M.V.V., Morton, S.L., Perkins, D.A.K., Reavie, E.D., Scott, G.I., Smith, S.A., Steevens, J.A., Are harmful algal blooms becoming the greatest inland water quality threat to public health and aquatic ecosystems?. Environ. Toxicol. Chem. 35 (2016), 6–13, 10.1002/etc.3220.
Bustillo, V., Moatar, F., Ducharne, A., Thiéry, D., Poirel, A., A multimodel comparison for assessing water temperatures under changing climate conditions via the equilibrium temperature concept: case study of the middle Loire River, France. Hydrol. Process. 28 (2014), 1507–1524, 10.1002/hyp.9683.
Cleveland, R.B., Cleveland, W.S., McRae, J.E., Terpenning, I., STL: a seasonal-trend decomposition procedure based on loess. J. Off. Stat. 6 (1990), 3–73.
Cohen, R.R.H., Dresler, P.V., Phillips, E.J.P., Cory, R.L., The effect of the Asiatic clam, Corbicula fluminea, on phytoplankton of the Potomac River, Maryland. Limnol. Oceanogr. 29 (1984), 170–180, 10.4319/lo.1984.29.1.0170.
Crouzet, P., L'eutrophisation de la Loire. Water Supply 1 (1983), 131–144.
Descy, J.-P., Leitão, M., Everbecq, E., Smitz, J.S., Deliege, J.-F., Phytoplankton of the river Loire, France: a biodiversity and modelling study. J. Plankton Res. 34 (2011), 120–135, 10.1093/plankt/fbr085.
Dodds, W.K., Smith, V.H., Nitrogen, phosphorus, and eutrophication in streams. Inl. Waters 6 (2016), 155–164, 10.5268/IW-6.2.909.
Floury, M., Delattre, C., Ormerod, S.J., Souchon, Y., Global versus local change effects on a large European river. Sci. Total Environ. 441 (2012), 220–229, 10.1016/j.scitotenv.2012.09.051.
Floury, M., Usseglio-Polatera, P., Ferreol, M., Delattre, C., Souchon, Y., Global climate change in large European rivers: long-term effects on macroinvertebrate communities and potential local confounding factors. Glob. Chang. Biol. 19 (2013), 1085–1099, 10.1111/gcb.12124.
Floury, M., Usseglio-Polatera, P., Delattre, C., Souchon, Y., Assessing long-term effects of multiple, potentially confounded drivers in ecosystems from species traits. Glob. Chang. Biol. 23 (2017), 2297–2307, 10.1111/gcb.13575.
Forastier, M.E., Zalocar, Y., Andrinolo, D., Domitrovic, H.A., Presencia y toxicidad de Microcystis aeruginosa (Cianobacteria) en el río Paraná, aguas abajo de la represa Yacyretá (Argentina). Rev. Biol. Trop., 64, 2016, 203, 10.15517/rbt.v64i1.8993.
Garnier, J., Ramarson, A., Billen, G., Théry, S., Thiéry, D., Thieu, V., Minaudo, C., Moatar, F., Nutrient inputs and hydrology together determine biogeochemical status of the Loire River (France): current situation and possible future scenarios. Sci. Total Environ. 637–638 (2018), 609–624, 10.1016/j.scitotenv.2018.05.045.
Giblin, S.M., Gerrish, G.A., Environmental factors controlling phytoplankton dynamics in a large floodplain river with emphasis on cyanobacteria. River Res. Appl., 2020, 1–14, 10.1002/rra.3658.
Graham, J.L., Dubrovsky, N.M., Foster, G.M., King, L.R., Loftin, K.A., Rosen, B.H., Stelzer, E.A., Cyanotoxin occurrence in large rivers of the United States. Inl. Waters 10 (2020), 109–117, 10.1080/20442041.2019.1700749.
Greulich, S., Guitton, H., Lacroix, P., Habitats et végétation de la plaine inondable. Florentina Moatar, Nadia Dupont, coord. 320 pp La Loire Fluviale et estuarienne: Un milieu en évolution, Collection Synthèses Edition Quae, 2016, 174–185.
Hagmeier, E., Plankton-Äquivalente. Kiel. Meeresforsch. 17 (1961), 32–47.
Hardenbicker, P., Rolinski, S., Weitere, M., Fischer, H., Contrasting long-term trends and shifts in phytoplankton dynamics in two large rivers. Int. Rev. Hydrobiol. 99 (2014), 326–334, 10.1002/iroh.201301680.
Hilt, S., Köhler, J., Kozerski, H.P., van Nes, E.H., Scheffer, M., Abrupt regime shifts in space and time along rivers and connected lake systems. Oikos 120 (2011), 766–775, 10.1111/j.1600-0706.2010.18553.x.
Humbert, J.F., Fastner, J., Ecology of cyanobacteria. Meriluoto, J., Spoof, L., Codd, G., (eds.) Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis, 2017, Wiley, 11–18, 10.4081/aiol.2017.7221.
Ibáñez, C., Prat, N., Duran, C., Pardos, M., Munné, A., Andreu, R., Caiola, N., Cid, N., Hampel, H., Sanchez, R., Trobajo, R., Changes in dissolved nutrients in the lower Ebro river: causes and consequences. Limnetica 27 (2008), 131–142.
Ibelings, B., Admiraal, W., Bijkerk, R., Ietswaart, T., Prins, H., Monitoring of algae in Dutch rivers : does it meet its goals ?. J. Appl. Phycol. 10 (1998), 171–181.
Istvánovics, V., Honti, M., Efficiency of nutrient management in controlling eutrophication of running waters in the middle Danube Basin. Hydrobiologia 686 (2012), 55–71.
Jugnia, L., Debroas, D., Romagoux, J., Dévaux, J., Initial results of remediation activities to restore hypereutrophic Villerest reservoir ( Roanne, France ). Lakes Reserv. Res. Manag. 9 (2004), 109–117.
Kohl, J.-G., Nicklisch, A., Okophysiologie der Algen. Wachstum und Ressourcennutzung Gustav Fisher Verlag, Berlin. 1988 253 p.
Köhler, J., Hoeg, S., Phytoplankton selection in a river—Lake system during two decades of changing nutrient supply. Reynolds, C.S., Dokulil, M., Padisák, J., (eds.) The Trophic Spectrum Revisited. Developments in Hydrobiology, vol 150, 2000, Springer, Dordr.
Kraemer, B.M., Chandra, S., Dell, A.I., Dix, M., Kuusisto, E., Livingstone, D.M., Schladow, S.G., Silow, E., Sitoki, L.M., Tamatamah, R., McIntyre, P.B., Global patterns in lake ecosystem responses to warming based on the temperature dependence of metabolism. Glob. Chang. Biol. 23 (2017), 1881–1890, 10.1111/gcb.13459.
Krogmann, D.W., Butalla, R., Sprinkle, J., Blooms of cyanobacteria on the Potomac River. Plant Physiol. 80 (1986), 667–671, 10.1104/pp.80.3.667.
Larroudé, S., Massei, N., Reyes-Marchant, P., Delattre, C., Humbert, J.F., Dramatic changes in a phytoplankton community in response to local and global pressures: a 24-year survey of the river Loire (France). Glob. Chang. Biol. 19 (2013), 1620–1631, 10.1111/gcb.12139.
Latli, A., Descy, J.-P., Mondy, C.P., Floury, M., Viroux, L., Otjacques, W., Marescaux, J., Depiereux, E., Ovidio, M., Usseglio-Polatera, P., Kestemont, P., Long-term trends in trait structure of riverine communities facing predation risk increase and trophic resource decline. Ecol. Appl. 27 (2017), 2458–2474, 10.1002/eap.1621.
Le Moal, M., Gascuel-Odoux, C., Ménesguen, A., Souchon, Y., Étrillard, C., Levain, A., Moatar, F., Pannard, A., Souchu, P., Lefebvre, A., Pinay, G., Eutrophication: a new wine in an old bottle?. Sci. Total Environ. 651 (2019), 1–11, 10.1016/j.scitotenv.2018.09.139.
Lehman, E.M., Seasonal occurrence and toxicity of Microcystis in impoundments of the Huron River, Michigan, USA. Water Res. 41 (2007), 795–802, 10.1016/j.watres.2006.09.030.
Lim, K.H., Shin, H.C., Yang, J.S., The influence of water temperature and food concentration on the filtration rates of the Asiatic clam, Corbicula fluminea. Kor. J. Malacol. 21 (2005), 19–24.
Lund, J.W.G., Talling, J.F., Botanical limnological methods with special reference to the algae. Bot. Rev. 23 (1957), 489–583, 10.1007/BF02870144.
Lung, W.S., Paerl, H.W., Modeling blue-green algal blooms in the lower neuse river. Water Res. 22 (1988), 895–905, 10.1016/0043-1354(88)90027-9.
Marescaux, J., Falisse, E., Lorquet, J., Van Doninck, K., Beisel, J.-N., Descy, J.-P., Assessing filtration rates of exotic bivalves: dependence on algae concentration and seasonal factors. Hydrobiologia 777 (2016), 67–78, 10.1007/s10750-016-2764-0.
McAllister, T.G., Wood, S.A., Atalah, J., Hawes, I., Spatiotemporal dynamics of Phormidium cover and anatoxin concentrations in eight New Zealand rivers with contrasting nutrient and flow regimes. Sci. Total Environ. 612 (2018), 71–80, 10.1016/j.scitotenv.2017.08.085.
Minaudo, C., Meybeck, M., Moatar, F., Gassama, N., Curie, F., Eutrophication mitigation in rivers: 30 years of trends in spatial and seasonal patterns of biogeochemistry of the Loire River (1980–2012). Biogeosciences 12 (2015), 2549–2563, 10.5194/bg-12-2549-2015.
Minaudo, C., Moatar, F., Coynel, A., Etcheber, H., Gassama, N., Curie, F., Using recent high-frequency surveys to reconstitute 35 years of organic carbon variations in a eutrophic lowland river. Environ. Monit. Assess., 188, 2016, 41, 10.1007/s10661-015-5054-9.
Minaudo, C., Curie, F., Jullian, Y., Gassama, N., Moatar, F., QUAL-NET, a high temporal-resolution eutrophication model for large hydrographic networks. Biogeosciences 15 (2018), 2251–2269, 10.5194/bg-15-2251-2018.
Misson, B., Sabart, M., Amblard, C., Latour, D., Benthic survival of Microcystis: long-term viability and ability to transcribe microcystin genes. Harmful Algae 13 (2012), 20–25, 10.1016/j.hal.2011.09.010.
Moatar, F., Gailhard, J., Water temperature behaviour in the river Loire since 1976 and 1881. Compt. Rendus Geosci. 338 (2006), 319–328, 10.1016/j.crte.2006.02.011.
Moatar, F., Ducharne, A., Thiéry, D., Bustillo, V., Sauquet, E., Vidal, J.-P., La Loire à l’épreuve du changement climatique. Geosciences 12 (2010), 78–87.
Oliver, R.L., Hamilton, D.P., Brookes, J.D., Ganf, G.G., Physiology, blooms and prediction of planktonic cyanobacteria. Whitton, B., (eds.) Ecology of Cyanobacteria II. Their Diversity in Space and Time, 2012, Springer. Springer, Netherlands, Dordrecht, 10.1007/978-94-007-3855-3.
O'Neil, J.M., Davis, T.W., Burford, M.A., Gobler, C.J., The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14 (2012), 313–334, 10.1016/j.hal.2011.10.027.
Oksanen, J., Guillaume Blanchet, F., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Peter Solymos, M., Stevens, H., Szoecs, E., Wagner, H., Vegan: Community Ecology Package. 2019 https://CRAN.R-project.org/package=vegan R package version 2.5-6.
Oudin, L.C., Lair, N., Leitão, M., Reyes-Marchant, P., Mignot, J.-F., Steinbach, P., Vigneron, T., Berton, J.-P., Bacchi, M., Roché, J.E., Descy, J.-P., Tockner, K., Robinson, C.T., (eds.) Rivers of Europe, 2009, British Library, London.
Paerl, H.W., Huisman, J., Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ. Microbiol. Rep. 1 (2009), 27–37, 10.1111/j.1758-2229.2008.00004.x.
Pigneur, L.-M., Falisse, E., Roland, K., Everbecq, E., Deliège, J.-F., Smitz, J.S., Van Doninck, K., Descy, J.-P., Impact of invasive Asian clams, Corbicula spp., on a large river ecosystem. Freshw. Biol. 59 (2014), 573–583, 10.1111/fwb.12286.
Piirsoo, K., Pall, P., Tuvikene, A., Viik, M., Temporal and spatial patterns of phytoplankton in a temperate lowland river (Emajõgi, Estonia). J. Plankton Res. 30 (2008), 1285–1295, 10.1093/plankt/fbn082.
Pohlert, T., Non-Parametric Trend Tests and Change-Point Detection. Trend Non-Parametric Trend Tests Chang. Detect. R Packag. Version 1.1.2. 2020.
Poisvert, C., Curie, F., Moatar, F., Annual agricultural N surplus in France over a 70-year period. Nutr. Cycl. Agroecosyst. 107 (2017), 63–78, 10.1007/s10705-016-9814-x.
R Core Team, R Core Team (2020). R: A Language and Environment for Statistical Computing. 2020, R Foundation for Statistical Computing, Vienna, Austria.
Reinhard, E.G., The plankton ecology of the upper Mississippi, Minneapolis to Winona. Ecol. Monogr. 1 (1931), 395–464, 10.1017/CBO9781107415324.004.
Reynolds, C.S., Hydroecology of river plankton the role of variability in channel flow. Hydrol. Process. 14 (2000), 3119–3132, 10.1002/1099-1085(200011/12)14:16/17<3119::AID-HYP137>3.0.CO;2-6.
Reynolds, C.S., The Ecology of Phytoplankton. 2006, Cambridge University Press, Cambridge.
Reynolds, C.S., Descy, J.-P., The production, biomass and structure of phytoplankton in large rivers. Arch. Hydrobiol. Suppl. 113 (1996), 161–187.
Reynolds, C.S., Descy, J.-P., Padisdak, J., Are phytoplankton dynamics in rivers so different from those in shallow lakes ?. Hydrobiologia 289 (1994), 1–7.
Riegman, R., Mur, L.R., Phosphate uptake by P-limited Oscillatoria agardhii. FEMS Microbiol. Lett. 21 (1984), 335–339, 10.1111/j.1574-6968.1984.tb00332.x.
Robson, B.J., Hamilton, D.P., Three-dimensional modelling of a Microcystis bloom event in the Swan River estuary, Western Australia. Ecol. Model. 174 (2004), 203–222, 10.1016/j.ecolmodel.2004.01.006.
Romero, E., Le Gendre, R., Garnier, J., Billen, G., Fisson, C., Silvestre, M., Riou, P., Long-term water quality in the lower seine: lessons learned over 4 decades of monitoring. Environ. Sci. Pol. 58 (2016), 141–154, 10.1016/j.envsci.2016.01.016.
Rott, E., Some results from phytoplankton counting intercalibrations. Schweizerische Z. Hydrol. 43 (1981), 34–62, 10.1007/BF02502471.
Rücker, J., Wiedner, C., Zippel, P., Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekei in eutrophic shallow lakes. Kufel, L., Prejs, A., Rybak, J.I., (eds.) Shallow Lakes ‘95, 1997, Springer, Netherlands, Dordrecht, 107–115, 10.1007/978-94-011-5648-6_12.
Sabart, M., Pobel, D., Latour, D., Robin, J., Salençon, M.-J., Humbert, J.-F., Spatiotemporal changes in the genetic diversity in French bloom-forming populations of the toxic cyanobacterium, Microcystis aeruginosa. Environ. Microbiol. Rep. 1 (2009), 263–272, 10.1111/j.1758-2229.2009.00042.x.
Scheffer, M., Hosper, S.H., Meijer, M.-L., Moss, B., Jeppesen, E., Alternative equilibria in shallow lakes. Trends Ecol. Evol. 8 (1993), 275–279, 10.1016/0169-5347(93)90254-M.
Smayda, T.J., From phytoplankters to biomass. Sournia, A., (eds.) Phytoplankton manual, 1978, UNESCO, Paris.
Utermöhl, H., Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt. int. Ver. theor. angew. Limnol. 9 (1958), 1–38.
Verbesselt, J., Hyndman, R., Newnham, G., Culvenor, D., Detecting trend and seasonal changes in satellite image time series. Remote Sens. Environ. 114 (2010), 106–115, 10.1016/j.rse.2009.08.014.
Verneaux, J., Faessel, B., Malesieux, G., Note préliminaire à la proposition de nouvelles méthodes de détermination de la qualité des eaux courantes. 1976, Trav. du Lab. d'Hydrobiologie l'Universit é Besançon, Besançon, Fr.
Viergutz, C., Linn, C., Weitere, M., Intra- and interannual variability surpasses direct temperature effects on the clearance rates of the invasive clam Corbicula fluminea. Mar. Biol. 159 (2012), 2379–2387, 10.1007/s00227-012-1902-0.
Vohmann, A., Borcherding, J., Kureck, A., Bij de Vaate, A., Arndt, H., Weitere, M., Strong body mass decrease of the invasive clam Corbicula fluminea during summer. Biol. Invasions 12 (2010), 53–64, 10.1007/s10530-009-9429-0.
Wehr, J.D., Thorp, J.H., Effects of navigation dams, tributaries, and littoral zones on phytoplankton communities in the Ohio River. Can. J. Fish. Aquat. Sci., 1997, 10.1139/f96-283.
Wood, S.A., Kelly, L.T., Bouma-Gregson, K., Humbert, J.F., Laughinghouse, H.D., Lazorchak, J., McAllister, T.G., McQueen, A., Pokrzywinski, K., Puddick, J., Quiblier, C., Reitz, L.A., Ryan, K.G., Vadeboncoeur, Y., Zastepa, A., Davis, T.W., Toxic benthic freshwater cyanobacterial proliferations: challenges and solutions for enhancing knowledge and improving monitoring and mitigation. Freshw. Biol., 1–19, 2020, 10.1111/fwb.13532.
Woolway, R.I., Kraemer, B.M., Lenters, J.D., Merchant, C.J., O'Reilly, C.M., Sharma, S., Global lake responses to climate change. Nat. Rev. Earth Environ., 2020, 10.1038/s43017-020-0067-5 In press.
Wurtsbaugh, W.A., Paerl, H.W., Dodds, W.K., Nutrients, eutrophication and harmful algal blooms along the freshwater to marine continuum. Wiley Interdiscip. Rev. Water 6 (2019), 1–27, 10.1002/wat2.1373.
Xia, R., Zhang, Yuan, Wang, G., Zhang, Yongyong, Dou, M., Hou, X., Qiao, Y., Wang, Q., Yang, Z., Multi-factor identification and modelling analyses for managing large river algal blooms. Environ. Pollut., 254, 2019, 113056, 10.1016/j.envpol.2019.113056.
