Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
Shopping Cart: ( empty )
You are here: Home > Journals > MF > MF23137 > Fulltext
RESEARCH ARTICLE
Contents Vol 75(9)

Assessing the aquatic metabolic-balance response to future condition in a Mediterranean site: from an experimental-design perspective

Ismael L. Lozano https://orcid.org/0000-0002-4507-2564 A B *
+ Author Affiliations
- Author Affiliations

A Department of Forest Sciences, University of Helsinki, FI-00014, Helsinki, Finland.

B Institute for Atmospheric and Earth System Research, University of Helsinki, FI-00014, Helsinki, Finland.

* Correspondence to: ismael.lozano@helsinki.fi

Handling Editor: Iwan Jones

Marine and Freshwater Research 75, MF23137 https://doi.org/10.1071/MF23137
Submitted: 21 July 2023  Accepted: 2 May 2024  Published: 31 May 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Metabolic balance determines whether an ecosystem acts as a source or sink of carbon dioxide (CO2) and considering that a substantial portion of inland aquatic ecosystems act as a source of CO2 to the atmosphere, it is important to highlight that there is still no agreement on how global change will affect the ecosystem metabolic-balance response. It then becomes more important to study the interactions between global-change drivers and aquatic metabolism.

Aims

Assess possible shifts in ecosystem metabolic balance owing to global-change factors.

Methods

Collapsed factorial designs and novel experimental units have been used to study responses to future conditions.

Key results

In the study site, bacterial production was not affected by an increased temperature alone; however, increased nutrient availability may unmask UV or CO2 as a source of stress to bacteria. A synergistic effect between temperature and the combined effect of nutrients and CO2 on primary producers was also found.

Conclusions

In future scenarios, some heterotrophic inland water ecosystems may shift from heterotrophic to autotrophic states and therefore act as CO2 sinks.

Implications

This study provides a framework to support a deepening of knowledge on this topic.

Keywords: aquatic ecosystem modelling, bacterial production, climate change, ecosystem respiration, experimental units design, factorial collapsed design, metabolic balance, primary production.

References

Alfonso S, Gesto M, Sadoul B (2021) Temperature increase and its effects on fish stress physiology in the context of global warming. Journal of Fish Biology 98(6), 1496-1508.
| Crossref | Google Scholar | PubMed |

Allen AP, Gillooly JF, Brown JH (2005) Linking the global carbon cycle to individual metabolism. Functional Ecology 19(2), 202-213.
| Crossref | Google Scholar |

Allen R, Hoffmann LJ, Law CS, Summerfield TC (2020) Subtle bacterioplankton community responses to elevated CO2 and warming in the oligotrophic south pacific gyre. Environmental Microbiology Reports 12(4), 377-386.
| Crossref | Google Scholar | PubMed |

Barneche DR, Hulatt CJ, Dossena M, Padfield D, Woodward G, Trimmer M, Yvon-Durocher G (2021) Warming impairs trophic transfer efficiency in a long-term field experiment. Nature 592(7852), 76-79.
| Crossref | Google Scholar | PubMed |

Barnes PW, Williamson CE, Lucas RM, Robinson SA, Madronich S, Paul ND, Bornman JF, Bais AF, Sulzberger B, Wilson SR, Andrady AL, McKenzie RL, Neale PJ, Austin AT, Bernhard GH, Solomon KR, Neale RE, Young PJ, Norval M, Rhodes LE, Hylander S, Rose KC, Longstreth J, Aucamp PJ, Ballaré CL, Cory RM, Flint SD, de Gruijl FR, Häder D-P, Heikkilä AM, Jansen MAK, Pandey KK, Matthew Robson T, Sinclair CA, Wängberg S-Å, Worrest RC, Yazar S, Young AR, Zepp RG (2019) Ozone depletion, ultraviolet radiation, climate change and prospects for a sustainable future. Nature Sustainability 2(7), 569-579.
| Crossref | Google Scholar |

Bell RT (1993) Estimating production of heterotrophic bacterioplankton via incorporation of tritiated thymidine. In ‘Handbook of methods in aquatic microbial ecology’. (Eds PF Kemp, JJ Cole, BF Sherr, EB Sherr) pp. 495–503. (CRC Press)

Blanco Seoane AB, García Abuín A, Gomez Diaz D, Navaza Dafonte JM, Sanjurjo B, Vidal Tato I (2009) Absorción de CO2 en columna de burbujeo por reacción con álcalis. Afinidad: Revista de química teórica y aplicada 66(544), 454-57.
| Google Scholar |

Boscolo-Galazzo F, Crichton KA, Ridgwell A, Mawbey EM, Wade BS, Pearson PN (2021) Temperature controls carbon cycling and biological evolution in the ocean twilight zone. Science 371(6534), 1148-1152.
| Crossref | Google Scholar | PubMed |

Boyd PW, Dillingham PW, McGraw CM, Armstrong EA, Cornwall CE, Feng Y-y, Hurd CL, Gault-Ringold M, Roleda MY, Timmins-Schiffman E, Nunn BL (2016) Physiological responses of a southern ocean diatom to complex future ocean conditions. Nature Climate Change 6(2), 207-213.
| Crossref | Google Scholar |

Bullejos FJ, Carrillo P, Villar-Argaiz M, Medina-Sá Ncheza JM (2010) Roles of phosphorus and ultraviolet radiation in the strength of phytoplankton–zooplankton coupling in a Mediterranean high mountain lake. Limnology and Oceanography 55(6), 2549-2562.
| Crossref | Google Scholar |

Cabrerizo MJ, Medina-Sánchez JM, González-Olalla JM, Sánchez-Gómez D, Carrillo P (2022) Microbial plankton responses to multiple environmental drivers in marine ecosystems with different phosphorus limitation degrees. Science of The Total Environment 816, 151491.
| Crossref | Google Scholar | PubMed |

Carrillo P, Medina-Sánchez JM, Durán C, Herrera G, Villafañe VE, Helbling EW (2015) Synergistic effects of UVR and simulated stratification on commensalistic phytoplankton–bacteria relationship in two optically contrasting oligotrophic mediterranean lakes. Biogeosciences 12(3), 697-712.
| Crossref | Google Scholar |

Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, Striegl RG, Duarte CM, Kortelainen P, Downing JA, Middelburg JJ, Melack J (2007) Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10(1), 172-185.
| Crossref | Google Scholar |

Davidson TA, Audet J, Jeppesen E, Landkildehus F, Lauridsen TL, Søndergaard M, Syväranta J (2018) Synergy between nutrients and warming enhances methane ebullition from experimental lakes. Nature Climate Change 8(2), 156-160.
| Crossref | Google Scholar |

Dorado-García I, Medina-Sánchez JM, Herrera G, Cabrerizo MJ, Presentación C (2014) Quantification of carbon and phosphorus co-limitation in bacterioplankton: new insights on an old topic. PLoS ONE 9(6), e99288.
| Crossref | Google Scholar | PubMed |

Duarte CM, Prairie YT (2005) Prevalence of heterotrophy and atmospheric CO2 emissions from aquatic ecosystems. Ecosystems 8(7), 862-870.
| Crossref | Google Scholar |

Durán C, Medina-Sánchez JM, Herrera G, Carrillo P (2016) Changes in the phytoplankton–bacteria coupling triggered by joint action of UVR, nutrients, and warming in mediterranean high-mountain lakes. Limnology and Oceanography 61(2), 413-429.
| Crossref | Google Scholar |

Feijoó C, Arroita M, Laura Messetta M, Anselmo J, Rigacci L, von Schiller D (2022) Patterns and controls of carbon dioxide concentration and fluxes at the air–water interface in south american lowland streams. Aquatic Sciences 84(2), 23.
| Crossref | Google Scholar |

Feng Y, Roleda MY, Armstrong E, Summerfield TC, Law CS, Hurd CL, Boyd PW (2020) Effects of multiple drivers of ocean global change on the physiology and functional gene expression of the coccolithophore Emiliania huxleyi. Global Change Biology 26(10), 5630-5645.
| Crossref | Google Scholar | PubMed |

Fuhrman JA, Azam F (1982) Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Marine Biology 66(2), 109-120.
| Crossref | Google Scholar |

Gao K, Zhang Y, Häder DP (2018) Individual and interactive effects of ocean acidification, global warming, and UV radiation on phytoplankton. Journal of Applied Phycology 30(2), 743-759.
| Crossref | Google Scholar |

Gao K, Xu J, Gao G, Li Y, Hutchins DA, Huang B, Wang L, Zheng Y, Jin P, Cai X, Häder D-P, Li W, Xu K, Liu N, Riebesell U (2012) Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nature Climate Change 2(7), 519-523.
| Crossref | Google Scholar |

González-Benítez N, García-Corral LS, Morán XAG, Middelburg JJ, Pizay MD, Gattuso J-P (2019) Drivers of microbial carbon fluxes variability in two oligotrophic mediterranean coastal systems. Scientific Reports 9(1), 17669.
| Crossref | Google Scholar | PubMed |

Goudie AS (2018) ‘Human impact on the natural environment.’ (Wiley)

Greenberg AE, Clesceri LS, Eaton AD (Eds) (1992) ‘Standard methods for the examination of water and wastewater.’ (American Public Health Association)

Häder D-P, Gao K (2015) Interactions of anthropogenic stress factors on marine phytoplankton. Frontiers in Environmental Science 3, 14.
| Crossref | Google Scholar |

Hessen DO, Leu E, Færøvig PJ, Petersen SF (2008) Light and spectral properties as determinants of C:N:P-ratios in phytoplankton. Deep-Sea Research – II. Topical Studies in Oceanography 55(20), 2169-2175.
| Crossref | Google Scholar |

Hoellein TJ, Bruesewitz DA, Richardson DC (2013) Revisiting Odum (1956): a synthesis of aquatic ecosystem metabolism. Limnology and Oceanography 58(6), 2089-2100.
| Crossref | Google Scholar |

Hussain I, Rehman A, Işık C (2022) Using an asymmetrical technique to assess the impacts of CO2 emissions on agricultural fruits in Pakistan. Environmental Science and Pollution Research 29(13), 19378-19389.
| Crossref | Google Scholar | PubMed |

Hussner A, Smith R, Mettler-Altmann T, Hill MP, Coetzee J (2019) Simulated global increases in atmospheric CO2 alter the tissue composition, but not the growth of some submerged aquatic plant bicarbonate users growing in DIC rich waters. Aquatic Botany 153, 44-50.
| Crossref | Google Scholar |

Korbee N, Carrillo P, Mata MT, Rosillo S, Medina-Sánchez JM, Figueroa FL (2012) Effects of ultraviolet radiation and nutrients on the structure–function of phytoplankton in a high mountain lake. Photochemical & Photobiological Sciences 11(6), 1087-1098.
| Crossref | Google Scholar | PubMed |

Lee S, Fuhrman JA (1987) Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Applied and Environmental Microbiology 53(6), 1298-1303.
| Crossref | Google Scholar | PubMed |

León-Palmero E, Morales-Baquero R, Reche I (2020) Greenhouse gas fluxes from reservoirs determined by watershed lithology, morphometry, and anthropogenic pressure. Environmental Research Letters 15(4), 044012.
| Crossref | Google Scholar |

Lignell R (1990) Excretion of organic carbon by phytoplankton: its relation to algal biomass, primary productivity and bacterial secondary productivity in the baltic sea. Marine Ecology Progress Series 68(1), 85-99.
| Crossref | Google Scholar |

Lignell R (1992) Problems in filtration fractionation of 14C primary productivity samples. Limnology and Oceanography 37(1), 172-178.
| Crossref | Google Scholar |

Lionello P, Scarascia L (2018) The relation between climate change in the mediterranean region and global warming. Regional Environmental Change 18(5), 1481-1493.
| Crossref | Google Scholar |

Liu S, Kuhn C, Amatulli G, Aho K, Butman DE, Allen GH, Lin P, Pan M, Yamazaki D, Brinkerhoff C, Gleason C, Xia X, Raymond PA (2022) The importance of hydrology in routing terrestrial carbon to the atmosphere via global streams and rivers. Proceedings of the National Academy of Sciences 119(11), e2106322119.
| Crossref | Google Scholar |

López-Urrutia Á, Morán XAG (2007) Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling. Ecology 88(4), 817-822.
| Crossref | Google Scholar | PubMed |

López-Urrutia Á, San Martin E, Harris RP, Irigoien X (2006) Scaling the metabolic balance of the oceans. Proceedings of the National Academy of Sciences 103(23), 8739-8744.
| Crossref | Google Scholar |

Marsay CM, Sanders RJ, Henson SA, Pabortsava K, Achterberg EP, Lampitt RS (2015) Attenuation of sinking particulate organic carbon flux through the mesopelagic ocean. Proceedings of the National Academy of Sciences 112(4), 1089-1094.
| Crossref | Google Scholar |

Medina-Sánchez JM, Carrillo P, Delgado-Molina JA, Bullejos FJ, Villar-Argaiz M (2010) Patterns of resource limitation of bacteria along a trophic gradient in mediterranean inland waters. FEMS Microbiology Ecology 74(3), 554-565.
| Crossref | Google Scholar | PubMed |

Medina-Sánchez JM, Delgado-Molina JA, Bratbak G, Bullejos FJ, Villar-Argaiz M, Carrillo P (2013) Maximum in the middle: nonlinear response of microbial plankton to ultraviolet radiation and phosphorus. PLoS ONE 8(4), e60223.
| Crossref | Google Scholar | PubMed |

Medina-Sánchez JM, Cabrerizo MJ, González-Olalla JM, Villar-Argaiz M, Carrillo P (2022) High mountain lakes as remote sensors of global change. In ‘The landscape of the Sierra Nevada: a unique laboratory of global processes in Spain’. (Eds R Zamora, M Oliva) pp. 261–278. (Springer International Publishing: Cham, Switzerland)

Morales-Baquero R, Pérez-Martínez C (2016) Saharan versus local influence on atmospheric aerosol deposition in the southern iberian peninsula: significance for N and P inputs. Global Biogeochemical Cycles 30(3), 501-513.
| Crossref | Google Scholar |

Morales-Baquero R, Pulido-Villena E, Reche I (2006) Atmospheric inputs of phosphorus and nitrogen to the southwest mediterranean region: biogeochemical responses of high mountain lakes. Limnology and Oceanography 51(2), 830-837.
| Crossref | Google Scholar |

Nielsen ES (1951) Measurement of the production of organic matter in the sea by means of carbon-14. Nature 167(4252), 684-685.
| Crossref | Google Scholar | PubMed |

Pilla RM, Griffiths NA, Gu L, Kao S-C, McManamay R, Ricciuto DM, Shi X (2022) Anthropogenically driven climate and landscape change effects on inland water carbon dynamics: what have we learned and where are we going? Global Change Biology
| Crossref | Google Scholar |

Rodríguez P, Byström P, Geibrink E, Hedström P, Vasconcelos FR, Karlsson J (2016) Do warming and humic river runoff alter the metabolic balance of lake ecosystems? Aquatic Sciences 78(4), 717-725.
| Crossref | Google Scholar |

Saint-Macary AD, Barr N, Armstrong E, Safi K, Marriner A, Gall M, McComb K, Dillingham PW, Law CS (2021) The influence of ocean acidification and warming on DMSP & DMS in New Zealand coastal water. Atmosphere 12(2), 181.
| Crossref | Google Scholar |

Schramski JR, Dell AI, Grady JM, Sibly RM, Brown JH (2015) Metabolic theory predicts whole-ecosystem properties. Proceedings of the National Academy of Sciences 112(8), 2617-2622.
| Crossref | Google Scholar |

Six KD, Kloster S, Ilyina T, Archer SD, Zhang K, Maier-Reimer E (2013) Global warming amplified by reduced sulphur fluxes as a result of ocean acidification. Nature Climate Change 3(11), 975-978.
| Crossref | Google Scholar |

Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar. Microb. Food Webs 6(2), 107-114.
| Google Scholar |

Song C, Dodds WK, Rüegg J, Argerich A, Baker CL, Bowden WB, Douglas MM, Farrell KJ, Flinn MB, Garcia EA, Helton AM, Harms TK, Jia S, Jones JB, Koenig LE, Kominoski JS, McDowell WH, McMaster D, Parker SP, Rosemond AD, Ruffing CM, Sheehan KR, Trentman MT, Whiles MR, Wollheim WM, Ballantyne F, IV (2018) Continental-scale decrease in net primary productivity in streams due to climate warming. Nature Geoscience 11(6), 415-420.
| Crossref | Google Scholar |

Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (2013) ‘Climate change 2013: the physical science basis. Working Group I contribution to the Fifth assessment report of the Intergovernmental Panel on Climate Change.’ (Cambridge University Press).

Sulzberger B, Austin AT, Cory RM, Zepp RG, Paul ND (2019) Solar UV radiation in a changing world: roles of cryosphere–land–water–atmosphere interfaces in global biogeochemical cycles. Photochemical & Photobiological Sciences 18(3), 747-774.
| Crossref | Google Scholar | PubMed |

Tranvik LJ, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, Dillon P, Finlay K, Fortino K, Knoll LB, Kortelainen PL, Kutser T, Larsen S, Laurion I, Leech DM, McCallister SL, McKnight DM, Melack JM, Overholt E, Porter JA, Prairie Y, Renwick WH, Roland F, Sherman BS, Schindler DW, Sobek S, Tremblay A, Vanni MJ, Verschoor AM, von Wachenfeldt E, Weyhenmeyer GA (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnology and Oceanography 54(6-2), 2298-2314.
| Crossref | Google Scholar |

Urabe J, Waki J (2009) Mitigation of adverse effects of rising CO2 on a planktonic herbivore by mixed algal diets. Global Change Biology 15(2), 523-531.
| Crossref | Google Scholar |

van de Waal DB, Verschoor AM, Verspagen JMH, van Donk E, Huisman J (2010) Climate-driven changes in the ecological stoichiometry of aquatic ecosystems. Frontiers in Ecology and the Environment 8(3), 145-152.
| Crossref | Google Scholar |

Villar-Argaiz M, Bullejos FJ, Medina-Sánchez JM, Ramos-Rodríguez E, Delgado-Molina JA, Carrillo P (2012) Disentangling food quantity and quality effects in zooplankton response to P-enrichment and UV radiation. Limnology and Oceanography 57(1), 235-250.
| Crossref | Google Scholar |

Williams PJB, Quay PD, Westberry TK, Behrenfeld MJ (2013) The oligotrophic ocean is autotrophic. Annual Review of Marine Science 5(1), 535-549.
| Crossref | Google Scholar |

Williamson CE, Dodds W, Kratz TK, Palmer MA (2008) Lakes and streams as sentinels of environmental change in terrestrial and atmospheric processes. Frontiers in Ecology and the Environment 6(5), 247-254.
| Crossref | Google Scholar |

Williamson CE, Saros JE, Vincent WF, Smol JP (2009) Lakes and reservoirs as sentinels, integrators, and regulators of climate change. Limnology and Oceanography 54(6-2), 2273-2282.
| Crossref | Google Scholar |

Williamson CE, Zepp RG, Lucas RM, Madronich S, Austin AT, Ballaré CL, Norval M, Sulzberger B, Bais AF, McKenzie RL, Robinson SA, Häder D-P, Paul ND, Bornman JF (2014) Solar ultraviolet radiation in a changing climate. Nature Climate Change 4(6), 434-441.
| Crossref | Google Scholar |

Woodward FI (2007) Global primary production. Current Biology 17(8), R269-R273.
| Crossref | Google Scholar | PubMed |

Wu HY, Zou DH, Gao KS (2008) Impacts of increased atmospheric CO2 concentration on photosynthesis and growth of micro- and macro-algae. Science in China – C. Life Sciences 51(12), 1144-1150.
| Crossref | Google Scholar |

Wu X, Liu H, Ru Z, Tu G, Xing L, Ding Y (2021) Meta-analysis of the response of marine phytoplankton to nutrient addition and seawater warming. Marine Environmental Research 168, 105294.
| Crossref | Google Scholar | PubMed |

Yvon-Durocher G, Jones JI, Trimmer M, Woodward G, Montoya JM (2010) Warming alters the metabolic balance of ecosystems. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 365(1549), 2117-2126.
| Crossref | Google Scholar |

Zhang Y, Li K, Zhou Q, Chen L, Yang X, Zhang H (2021) Phytoplankton responses to solar uvr and its combination with nutrient enrichment in a plateau oligotrophic Lake Fuxian: a mesocosm experiment. Environmental Science and Pollution Research 28(23), 29931-29944.
| Crossref | Google Scholar | PubMed |

Zou F, Li H, Hu Q (2020) Responses of vegetation greening and land surface temperature variations to global warming on the Qinghai–Tibetan Plateau, 2001–2016. Ecological Indicators 119, 106867.
| Crossref | Google Scholar |