Abstract
Studies on small, shallow lakes are few and have traditionally focused on humic lakes, whereas transparent, oligotrophic lakes dominated by submerged macrophytes have been overlooked. This may have given rise to a skewed perception of shallow lakes as being well mixed, turbid and dominated by ecosystem respiration relative to primary production. Mixing patterns and ecosystem metabolism in five oligotrophic shallow lakes dominated by charophytes were investigated in order to determine gross primary production, ecosystem respiration, their regulation and mutual coupling in this very common lake type. Although lakes were very shallow (<0.5 m), high charophyte biomass caused strong daytime stratification followed by nocturnal mixing. Despite the nutrient-poor water, volumetric rates of production and respiration during spring–summer were high compared to most medium to large lakes. This intensive metabolism is likely a result of the high charophyte biomass and the shallow mixed surface layer. Areal rates of production and respiration were also high compared to values from other aquatic systems. Strong coupling between daily rates of production and respiration suggested that the majority of organic substrates for ecosystem respiration were produced within the lakes. Net ecosystem production was slightly positive during the growth season. This study highlights the role of submerged macrophytes as primary drivers of temperature dynamics, stratification-mixing as well as high metabolism in small, shallow lakes with dense vegetation.
Similar content being viewed by others
References
Alnoee AB, Riis T, Andersen MR, Baattrup-Pedersen A, Sand-Jensen K (2015) Whole-stream metabolism in nutrient-poor calcareous streams on Öland, Sweden. Aquat Sci 77:207–219. doi:10.1007/s00027-014-0380-5
Andersen MR (2015) Ecology in small aquatic ecosystems. Ph.D. thesis, University of Copenhagen
Andersen MR, Sand-Jensen K, Iestyn Woolway R, Jones ID (2016) Profound daily vertical stratification and mixing in a small, shallow, wind-exposed lake with submerged macrophytes Aquat Sci. doi:10.1007/s00027-016-0505-0
Binzer T, Sand-Jensen K, Middelboe A-L (2006) Community photosynthesis of aquatic macrophytes. Limnol Oceanogr 51:2722–2733. doi:10.4319/lo.2006.51.6.2722
Brighenti LS et al (2015) Seasonal changes in metabolic rates of two tropical lakes in the Atlantic forest of Brazil. Ecosystems 18:589–604. doi:10.1007/s10021-015-9851-3
Christensen J, Sand-Jensen K, Staehr PA (2013) Fluctuating water levels control water chemistry and metabolism of a charophyte-dominated pond. Freshw Biol 58:1353–1365. doi:10.1111/fwb.12132
Dale HM, Gillespie TJ (1977) Influence of submersed aquatic plants on temperature-gradients in shallow-water bodies. Can J Bot 55:2216–2225. doi:10.1139/b77-251
Del Giorgio PA, Cole JJ, Caraco NF, Peters RH (1999) Linking planktonic biomass and metabolism to net gas fluxes in northern temperate lakes. Ecology 80:1422–1431. doi:10.2307/177085
Downing JA (2010) Emerging global role of small lakes and ponds: little things mean a lot. Limnetica 29:9–24
Downing J et al (2006) The global abundance and size distribution of lakes, ponds, and impoundments. Limnol Oceanogr 51:2388–2397. doi:10.4319/lo.2006.51.5.2388
Duarte CM, Agustí S (1998) The CO2 balance of unproductive aquatic ecosystems. Science 281:234–236. doi:10.1126/science.281.5374.234
Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Monographs on statistics and applied probability, vol 57. Chapman & Hall, New York
Geertz-Hansen O, Montes C, Duarte CM, Sand-Jensen K, Marbà N, Grillas P (2011) Ecosystem metabolism in a temporary Mediterranean marsh (Doñana National Park, SW Spain). Biogeosciences 7:6495–6521. doi:10.5194/bgd-7-6495-2010
Gran G (1952) Determination of the equivalence point in potentiometric titrations. Part II. Analyst 77:661–671. doi:10.1039/an9527700661
Hanson PC, Bade DL, Carpenter SR, Kratz TK (2003) Lake metabolism: relationships with dissolved organic carbon and phosphorus. Limnol Oceanogr 48:1112–1119. doi:10.4319/lo.2003.48.3.1112
Hanson PC, Carpenter SR, Kimura N, Wu C, Cornelius SP, Kratz TK (2008) Evaluation of metabolism models for free-water dissolved oxygen methods in lakes. Limnol Oceanogr Methods 6:454–465. doi:10.4319/lom.2008.6.454
Hilborn R, Mangel M (1997) The ecological detective: confronting models with data. Monographs in population biology, vol 28. Princeton University Press, New Jersey
Hoellein TJ, Bruesewitz DA, Richardson DC (2013) Revisiting Odum (1956): a synthesis of aquatic ecosystem metabolism. Limnol Oceanogr 58:2089–2100. doi:10.4319/lo.2013.58.6.2089
Holgerson MA, Raymond PA (2016) Large contribution to inland water CO2 and CH4 emissions from very small ponds. Nature Geosci 9:222–226. doi:10.1038/ngeo2654
Holgerson MA, Zappa CJ, Raymond PA (2016) Substantial overnight reaeration by convective cooling discovered in pond ecosystems. Geophys Res Lett 43:8044–8051. doi:10.1002/2016gl070206
Jähne B, Heinz G, Dietrich W (1987) Measurement of the diffusion coefficients of sparingly soluble gases in water. J Geophys Res 92:10767–10776. doi:10.1029/jc092ic10p10767
Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547. doi:10.4319/lo.1976.21.4.0540
Jørgensen SE, Bendoricchio G (2001) Fundamentals of ecological modelling vol 21. Developments in environmental modelling. Elsevier, Amsterdam
Kalff J (2002) Limnology: inland water ecosystems. Prentice Hall, New Jersey
Kragh T, Andersen MR, Sand-Jensen K (2017) Profound afternoon depression of ecosystem production and nighttime decline of respiration in a macrophyte-rich shallow lake. Oecologia (in press)
Krause-Jensen D, Sand-Jensen K (1998) Light attenuation and photosynthesis of aquatic plant communities. Limnol Oceanogr 43:396–407. doi:10.4319/lo.1998.43.3.0396
Lauster GH, Hanson PC, Kratz TK (2006) Gross primary production and respiration differences among littoral and pelagic habitats in northern Wisconsin lakes. Can J Fish Aquat Sci 63:1130–1141. doi:10.1139/f06-018
Lewis E, Wallace D (1998) Program Developed for CO2 System Calculations (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, TN) ORNL/CDIAC-105
Lucas WJ, Berry JA (1985) Inorganic carbon transport in aquatic photosynthetic organisms. Physiol Plant 65:539–543. doi:10.1111/j.1399-3054.1985.tb08687.x
MacIntyre S, Jonsson A, Jansson M, Aberg J, Turney DE, Miller SD (2010) Buoyancy flux, turbulence, and the gas transfer coefficient in a stratified lake Geophys Res Lett. doi:10.1029/2010gl044164
Madsen TV, Sand-Jensen K (1991) Photosynthetic carbon assimilation in aquatic macrophytes. Aquat Bot 41:5–40. doi:10.1016/0304-3770(91)90037-6
McNair JN, Gereaux LC, Weinke AD, Sesselmann MR, Kendall ST, Biddanda BA (2013) New methods for estimating components of lake metabolism based on free-water dissolved-oxygen dynamics. Ecol Model 263:251–263. doi:10.1016/j.ecolmodel.2013.05.010
Odum HT (1956) Primary production in flowing waters. Limnol Oceanogr 1:102–117. doi:10.4319/lo.1956.1.2.0102
Politis DN (2003) The impact of bootstrap methods on time series analysis. Stat Sci 18:219–230. doi:10.1214/ss/1063994977
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Read JS et al (2011) Derivation of lake mixing and stratification indices from high-resolution lake buoy data. Environ Model Softw 26:1325–1336 doi:10.1016/j.envsoft.2011.05.006
Read JS et al (2012) Lake-size dependency of wind shear and convection as controls on gas exchange Geophys Res Lett. doi:10.1029/2012gl051886
Richardson DC, Carey CC, Bruesewitz DA, Weathers KC (2016) Intra-and inter-annual variability in metabolism in an oligotrophic lake Aquat Sci. doi:10.1007/s00027-016-0499-7
Sadro S, Melack JM, Maclntyre S (2011) Spatial and temporal variability in the ecosystem metabolism of a high-elevation lake: integrating benthic and pelagic habitats. Ecosystems 14:1123–1140. doi:10.1007/s10021-011-9471-5
Sand-Jensen K, Staehr PA (2007) Scaling of pelagic metabolism to size, trophy and forest cover in small Danish lakes. Ecosystems 10:128–142. doi:10.1007/s10021-006-9001-z
Sand-Jensen K, Båstrup-Spohr L, Andersen MR, Christensen JPA, Alnoee AB, Jespersen TS (2015) Mellan torka och översvämning på Öland Sven Bot Tidskr 109:28–35
SMHI Swedish Meteorological and Hydrological Institute. http://www.smhi.se/klimatdata. Accessed June 2016
Solomon CT et al (2013) Ecosystem respiration: drivers of daily variability and background respiration in lakes around the globe. Limnol Oceanogr 58:849–866. doi:10.4319/lo.2013.58.3.0849
Staehr PA, Sand-Jensen K (2007) Temporal dynamics and regulation of lake metabolism. Limnol Oceanogr 52:108–120. doi:10.4319/lo.2007.52.1.0108
Staehr PA, Testa JM, Kemp WM, Cole JJ, Sand-Jensen K, Smith SV (2012) The metabolism of aquatic ecosystems: history, applications, and future challenges. Aquat Sci 74:15–29. doi:10.1007/s00027-011-0199-2
Van de Bogert MC, Carpenter SR, Cole JJ, Pace ML (2007) Assessing pelagic and benthic metabolism using free water measurements. Limnol Oceanogr Methods 5:145–155. doi:10.4319/lom.2007.5.145
Van de Bogert MC, Bade DL, Carpenter SR, Cole JJ, Pace ML, Hanson PC, Langman OC (2012) Spatial heterogeneity strongly affects estimates of ecosystem metabolism in two north temperate lakes. Limnol Oceanogr 57:1689–1700. doi:10.4319/lo.2012.57.6.1689
Van den Berg MS, Coops H, Simons J, Pilon J (2002) A comparative study of the use of inorganic carbon resources by Chara aspera and Potamogeton pectinatus. Aquat Bot 72:219–233. doi:10.1016/s0304-3770(01)00202-9
Vermeer CP, Escher M, Portielje R, de Klein JJM (2003) Nitrogen uptake and translocation by Chara. Aquat Bot 76:245–258. doi:10.1016/s0304-3770(03)00056-1
Verpoorter C, Kutser T, Seekell DA, Tranvik LJ (2014) A global inventory of lakes based on high-resolution satellite imagery. Geophys Res Lett 41:6396–6402. doi:10.1002/2014gl060641
Wanninkhof R (1992) Relationship between wind speed and gas exchange over the ocean. J Geophys Res Oceans 97:7373–7382. doi:10.1029/92jc00188
Weiss RF (1970) The solubility of nitrogen, oxygen and argon in water and seawater. Deep Sea Res Oceanogr Abstr 17:721–735. doi:10.1016/0011-7471(70)90037-9
Woolway RI et al (2016) Diel surface temperature range scales with lake size. PLoS One 11:e0152466. doi:10.1111/j.1365-2656.2010.01731.x
Acknowledgements
This work was supported by grants to KSJ from the Carlsberg Foundation to the study of small lakes and Center of Excellence to Lake Restoration from the Villum Kann Rasmussen Foundation. We thank Sara Schousboe for linguistic corrections.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
27_2017_550_MOESM1_ESM.eps
Fig. S1 Examples from analysis of one lake day in Lake 1, summer 2016. Upper panel shows oxygen concentration (g m-3) at saturation (DOsat), observed concentration (DOobs) and modeled concentration (DOmod) from sunrise to sunrise. The lower panel shows an example from the accompanying bootstrap analysis of the free parameters Pmax, Rmax and α with histograms including nominal fit (solid line) and 95% CI limits (dotted lines) (EPS 147 KB)
27_2017_550_MOESM2_ESM.eps
Fig. S2 Linear relationship of daily rates of R (g O2 m-3 day-1) versus GPP (g O2 m-3 day-1) in Lake 4 loc B and C (2015). Shown are 95% CI (grey area), the 1:1 linear relationship (dotted line) and standard major axis regression (solid line). Rates are per unit volume and normalized to 20 °C. Regression parameter estimates of intercept (Rbase) and slope (β) with 95% CI in parenthesis are: Lake 4 loc B: Rbase= -0.55 (-1.9-0.7) and β = 0.93 (0.87-1.0), Lake 4 loc C: Rbase= -0.19 (-3.6-2.6) and β = 0.62 (0.51-0.76) (EPS 117 KB)
27_2017_550_MOESM3_ESM.eps
Fig. S3 Surface water dissolved oxygen concentrations (solid line, g m-3) and water temperature (dotted line, °C) in Lake 4 loc A and Lake 5 loc A during spring 2015. Raw values measured every 10 minutes are plotted (EPS 768 KB)
Rights and permissions
About this article
Cite this article
Martinsen, K.T., Andersen, M.R., Kragh, T. et al. High rates and close diel coupling of primary production and ecosystem respiration in small, oligotrophic lakes. Aquat Sci 79, 995–1007 (2017). https://doi.org/10.1007/s00027-017-0550-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00027-017-0550-3