, Volume 22, Issue 6, pp 1406–1423 | Cite as

Reduced Rainfall Increases Metabolic Rates in Upper Mixed Layers of Tropical Lakes

  • Laura Martins Gagliardi
  • Ludmila Silva BrighentiEmail author
  • Peter Anton Staehr
  • Francisco Antônio Rodrigues Barbosa
  • José Fernandes Bezerra-Neto


Ecosystem-level metabolism is a good sentinel for human and natural disturbances in freshwater systems, responding from local changes (for example, land use) to regional and global changes (for example, climate). Despite the increasing understanding of metabolic processes in tropical lakes, our knowledge on how morphometric and catchment characteristics affect metabolic responses to those changes in tropical lakes is still very scarce. We investigated how metabolic rates in the upper mixed layer of twelve Brazilian tropical lakes responded to reduced rainfall, considering their lake area and drainage area ratio and the percentage of native forest cover in their drainage area. An 80% reduction in the 2013 rainy season rainfall, compared with 2012, resulted in a reduction of approximated 1 m in the water column depth, a 1–2 m deepening of the upper mixed layer, a 50% reduction in mean light availability, and a doubling in total phosphorus concentrations. These changes were associated with 38% increases in gross primary production (GPP), stimulated by higher nutrient concentrations and reduced photoinhibition. These effects of reduced rainfall were strongest in lakes with a small volume in relation to their catchment areas. Our results show that climatic-related reductions in precipitation in this tropical region will reduce lake volumes, affect temperature, water mixing, and nutrient supply with pronounced effects on lake metabolic processes and carbon cycling in this region.


primary production respiration drought climate change lake size southeastern Brazil 



We appreciate the logistical support of the post-graduation program (ECMVS, UFMG), laboratory colleagues (LIMNEA), and the team of Rio Doce State Park (IEF) and neighboring communities. We thank the National Space Research Institute for providing the meteorological data. We thank Master Ciro Lófti Vaz for morphometric analyses in ArcGIS and Dr. Robert M. Hughes and Dr. Ronaldo Reis for the paper review. We also thank all fieldwork collaborators and Marcelo Costa and Patricia Ferreira for laboratory analyses. This work was supported by Foundation Research Support of Minas Gerais—FAPEMIG (APQ-02623-10), Long-Term Ecological Research/National Research Council—CNPq (No. 403698/2012-0), and Higher Education Personnel Improvement Coordination—CAPES (No. 88881.030499/2013-01; COCLAKE project).

Supplementary material

10021_2019_346_MOESM1_ESM.pdf (531 kb)
Supplementary material 1 (PDF 530 kb).


  1. Adrian R, Reilly CMO, Zagarese H, Baines SB, Hessen DO, Keller W, Livingstone DM, Sommaruga R, Straile D, Van Donk E. 2009. Lakes as sentinels of climate change. Limnol Oceanogr 54:2283–97.CrossRefGoogle Scholar
  2. APHA. 2005. Standard methods for the examination of water and wastewater. 21st edn. Washington: American Public Health Association.Google Scholar
  3. Barbosa FAR, Tundisi JG. 1980. Primary production of phytoplankton and environmental characteristics of a shallow quaternary lake at Eastern Brazil. Archiv für Hydrobiol 90:139–61.Google Scholar
  4. Barbosa FAR, Tundisi JG. 1989. Diel variations in a shallow tropical Brazil lake. The influence of temperature variation on the distribution of dissolved oxygen and nutrients. Arch für Hydrobiologie 116:333–49.Google Scholar
  5. Barbosa FAR, Padisák J. 2002. The forgotten lake stratification pattern: atelomixis, and its ecological importance. Verhn des Int Ver Limnol 28:1385–95.Google Scholar
  6. Bezerra-Neto JF, Briguenti LS, Pinto-Coelho RM. 2010. A new morphometric study of Carioca Lake, Parque Estadual do Rio Doce (PERD), Minas Gerais State, Brazil. Acta Sci Biol Sci 32:49–54.CrossRefGoogle Scholar
  7. Bezerra-Neto JF, Gagliardi LM, Brandao LPM, Brighenti LS, Barbosa FAR. 2019. Effects of precipitation on summer epilimnion thickness in tropical lakes. Limnologica 74:42–50.CrossRefGoogle Scholar
  8. Bezerra-Neto JF, Pinto-Coelho RM. 2008. Morphometric study of Lake Dom Helvécio, Parque Estadual do Rio Doce (PERD), Minas Gerais, Brazil: a re-evaluation. Acta Limnologica Brasiliensia 20:161–7.Google Scholar
  9. Biddanda BA, Cotner JB. 2002. Love handles in aquatic ecosystems: the role of dissolved organic carbon drawdown, resuspended sediments, and terrigenous inputs in the carbon balance of Lake Michigan. Ecosystems 5:431–45.CrossRefGoogle Scholar
  10. Bouchard JN, Longhi ML, Roy S, Campbell DA, Ferreyra G. 2008. Interaction of nitrogen status and UVB sensitivity in a temperate phytoplankton assemblage. J Exp Mar Biol Ecol 359:67–76.CrossRefGoogle Scholar
  11. Bracchini L, Cózar A, Dattilo AM, Falcucci M, Gonzales R, Loiselle S, Hull V. 2004. Analysis of extinction in ultraviolet and visible spectra of water bodies of the Paraguay and Brazil wetlands. Chemosphere 57:1245–55.CrossRefGoogle Scholar
  12. Brandão LPM, Brighenti LS, Staehr PA, Asmala E, Massicotte P, Tonetta D, Pujoni DFG, Barbosa FAR, Bezerra-Neto JF. 2018. Distinctive effects of allochthonous and autochthonous organic matter on CDOM spectra in a tropical lake. Biogeosciences 15:1–13.CrossRefGoogle Scholar
  13. Brasil J, Attayde JL, Vasconcelos FR, Dantas DDF, Huszar VLM. 2016. Drought-induced water-level reduction favors cyanobacteria blooms in tropical shallow lakes. Hydrobiologia 770:145–64.CrossRefGoogle Scholar
  14. Brighenti LS, Staehr PA, Gagliardi LM, Brandão LPM, Elias EC, de Mello NAST, Barbosa FAR, Bezerra-Neto JF. 2015. Seasonal changes in metabolic rates of two tropical lakes in the Atlantic forest of Brazil. Ecosystems 18:589–604.CrossRefGoogle Scholar
  15. Brighenti LS, Staehr PA, Brandão LPM, Barbosa FAR, Bezerra-Neto JF. 2018. Importance of nutrients, organic matter and light availability on epilimnetic metabolic rates in a mesotrophic tropical lake. Freshw Biol 63:1143–60.CrossRefGoogle Scholar
  16. Brown JF, Allen AP, Savage VM, West GB. 2004. Toward a metabolic theory of ecology. Ecology 85:1771–89.CrossRefGoogle Scholar
  17. Carpenter SR, Cole JJ, Hodgson JR, Kitchell JE, Pace ML, Bade D, Cottinngham KL, Essington TE, Houser JN, Schindler DE. 2001. Trophic cascades, nutrients, and lake productivity: whole-lake experiments. Ecol Monogr 71:163–86.CrossRefGoogle Scholar
  18. Charlton MN, Lean DRS. 1987. Sedimentation, resuspension, and oxygen depletion in Lake Erie (1979). J Great Lakes Res 13:709–23.CrossRefGoogle Scholar
  19. Cole JJ, Caraco NF. 1998. Atmospheric exchange of carbon dioxide in a low-wind oligotrophic the addition of SF, lake measured by. Limnol Oceanogr 43:647–56.CrossRefGoogle Scholar
  20. Cole JJ, Pace ML, Carpenter SR, Kitchell JF. 2000. Persistence of net heterotrophy in lakes during nutrient addition and food web manipulations. Limnol Oceanogr 45:1718–30.CrossRefGoogle Scholar
  21. 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 10:172–85.CrossRefGoogle Scholar
  22. Coloso JJ, Cole JJ, Pace ML. 2011. Short-term variation in thermal stratification complicates estimation of lake metabolism. Aquatic Sci 73:305–15.CrossRefGoogle Scholar
  23. Diehl S, Berger S, Ptacnik R, Wild A. 2002. Phytoplankton, light, and nutrients in a gradient of mixing depths: field experiments. Ecology 83:399–411.CrossRefGoogle Scholar
  24. Downing J. 2010. Emerging global role of small lakes and ponds: little things mean a lot. Limnetica 29:9–24.Google Scholar
  25. Fee EJ, Hecky RE, Kasian SEM, Cruikshank DR. 1996. Effects of lake size, water clarity, and climatic variability on mixing depths in Canadian Shield lakes. Limnol Oceanogr 41:912–20.CrossRefGoogle Scholar
  26. Ganf GG, Horne AJ. 1975. Diurnal stratification, photosynthesis and nitrogen fixation in a shallow, equatorial lake (Lake George, Uganda). Freshw Biol 5:13–39.CrossRefGoogle Scholar
  27. Gergel SE, Turner MG, Kratz TK. 1999. Dissolved organic carbon as an indicator of the scale of watershed influence on lakes and rivers. Ecol Appl 9:1377–90.CrossRefGoogle Scholar
  28. Giling DP, Staehr PA, Grossart HP, Andersen MR, Boehrer B, Escot C, Evrendilek F, Gómez-Gener L, Honti M, Jones ID, Karakaya N, Laas A, Moreno-Ostos E, Rinke K, Scharfenberger U, Schmidt SR, Weber M, Woolway RI, Zwart JA, Obrador B. 2017. Delving deeper: metabolic processes in the metalimnion of stratified lakes. Limnol Oceanogr 62:1288–306.CrossRefGoogle Scholar
  29. Häder D-P, Williamson CE, Wängberg S-Å, Rautio M, Rose KC, Gao K, Helbling EW, Sinha RP, Worrest R. 2015. Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochem Photobio Sci 14:108–26.CrossRefGoogle Scholar
  30. Håkanson L. 2005. The importance of lake morphometry and catchment characteristics in limnology—ranking based on statistical analyses. Hydrobiologia 541:117–37.CrossRefGoogle Scholar
  31. Hanson PC, Bade DL, Carpenter SR, Kratz TK. 2003. Lake metabolism: relationships with dissolved organic carbon and phosphorus. Limnol Oceanogr 48:1112–19.CrossRefGoogle Scholar
  32. IPCC. 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, R.K. Pachauri and L.A. Meyer (eds.)]. Geneva, Switzerland.Google Scholar
  33. Jeppesen E, Meerhoff M, Davidson TA, Trolle D, Søndergaard M, Lauridsen TL, Beklioglu M, Brucet S, Volta P, González-Bergonzoni I, Nielsen A. 2014. Climate change impacts on lakes: an integrated ecological perspective based on a multi-faceted approach, with special focus on shallow lakes. J Limnol 73:88–111.CrossRefGoogle Scholar
  34. Landkildehus F, Søndergaard M, Beklioglu M, Adrian R, Angeler DG, Hejzlar J, Papastergiadou E, Zingel P, Çakiroğlu AI, Scharfenberger U, Drakare S, Nõges T, Šorf M, Stefanidis K, Tavşanoğlu N, Trigal C, Mahdy A, Papadaki C, Tuvikene L, Larsen SE, Kernan M, Jeppesen E. 2014. Climate change effects on shallow lakes: design and preliminary results of a cross-European climate gradient mesocosm experiment. Est J Ecol 63:71–89.CrossRefGoogle Scholar
  35. Lewis WJ. 1996. Tropical lakes: how latitude makes a difference. In: Schiemer F, Boland KT, Eds. Perspectives in tropical limnology. Amsterdam: SPB Academic Publishing.Google Scholar
  36. Lewis WJ. 2010. Biogeochemistry of tropical lakes. Verhn des Int Ver Limnol 30:1595–603.Google Scholar
  37. Mackereth FJH, Heron J, Talling JF. 1978. Water analysis and some revised methods for limnologists. Freshwater Biological Association.Google Scholar
  38. Maia-Barbosa P, Barbosa L, Brito S, Garcia F, Barros C, Souza M, Mello N, Guimarães A, Barbosa F. 2010. Limnological changes in Dom Helvécio Lake (South-East Brazil): natural and anthropogenic causes. Braz J Biol 70:795–802.CrossRefGoogle Scholar
  39. Marengo J, Ambrizzi T, da Rocha RP, Alves LM, Cuadra SV, Valverde MC, Torres RR, Santos DC, Ferraz SET. 2009. Future change of climate in South America in the late twenty-first century: intercomparison of scenarios from three regional climate models. Climate Dyn 35:1073–97.CrossRefGoogle Scholar
  40. Marotta H, Duarte CM, Sobek S, Enrich-Prast A. 2009. Large CO2 disequilibria in tropical lakes. Global Biogeochemical Cycles 23:GB4022.Google Scholar
  41. Marotta H, Duarte CM, Pinho L, Enrich-Prast A. 2010. Rainfall leads to increased pCO2 in Brazilian coastal lakes. Biogeosciences 7:1607–14.CrossRefGoogle Scholar
  42. Maynard JJ, Dahlgren RA, O’Geen AT. 2012. Quantifying spatial variability and biogeochemical controls of ecosystem metabolism in a eutrophic flow-through wetland. Ecol Eng 47:221–36.CrossRefGoogle Scholar
  43. Nõges T. 2009. Relationships between morphometry, geographic location and water quality parameters of European lakes. Hydrobiologia 633:33–43.CrossRefGoogle Scholar
  44. Obrador B, Staehr PA, Christensen JPC. 2014. Vertical patterns of metabolism in three contrasting stratified lakes. Limnol Oceanogr 59:1228–40.CrossRefGoogle Scholar
  45. O’Reilly CM, Alin SR, Plisnier P-D, Cohen AS, McKee BA. 2003. Climate change decreases aquatic ecosystem productivity of Lake Tanganyika, Africa. Nature 424:766–8.CrossRefGoogle Scholar
  46. Orihel DM, Schindler DW, Ballard NC, Graham MD, O’Connell DW, Wilson LR, Vinebrooke RD. 2015. The ‘nutrient pump:’ Iron-poor sediments fuel low nitrogen-to-phosphorus ratios and cyanobacterial blooms in polymictic lakes. Limnol Oceanogr 60:856–71.CrossRefGoogle Scholar
  47. Odum HT. 1956. Primary Production in Flowing Waters. Limnology and Oceanography:103–17.Google Scholar
  48. Petrucio MM, Barbosa FAR. 2004. Diel variations of phytoplankton and bacterioplankton production rates in four tropical lakes in the middle Rio Doce basin (southeastern Brazil). Hydrobiologia 513:71–6.CrossRefGoogle Scholar
  49. Petrucio MM, Barbosa FAR, Furtado ALS. 2006. Bacterioplankton and phytoplankton production in seven lakes in the Middle Rio Doce basin, south-east Brazil. Limnologica 36:192–203.CrossRefGoogle Scholar
  50. Pinheiro J, Bates D. 2006. Mixed-effects models in S and S-PLUS. New York: Springer.Google Scholar
  51. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. 2014. nlme: Linear and nonlinear mixed effects models.Google Scholar
  52. Pinheiro MHO, Carvalho LN, Arruda R, Guilherme FAG. 2015. Consequences of suppressing natural vegetation in drainage areas for freshwater ecosystem conservation: considerations on the new “Brazilian forest code”. Acta Bot Bras 29:262–9.CrossRefGoogle Scholar
  53. Pinho L, Duarte CM, Marotta H, Enrich-Prast A. 2015. Temperature-dependence of the relationship between pCO2 and dissolved organic carbon in lakes. Biogeosciences 12:2787–808.CrossRefGoogle Scholar
  54. Read JS, Hamilton DP, Jones ID, Muraoka K, Winslow LA, Kroiss R, Wu CH, Gaiser E. 2011. Derivation of lake mixing and stratification indices from high-resolution lake buoy data. Environ Model Softw 26:1325–36.CrossRefGoogle Scholar
  55. Read JS, Rose KC. 2013. Physical responses of small temperate lakes to variation in dissolved organic carbon concentrations. Limnol Oceanogr 58:921–31.CrossRefGoogle Scholar
  56. Rivera VF, Diehl S, Rodríguez P, Karlsson J, Byström P. 2018. Effects of terrestrial organic matter on aquatic primary production as mediated by pelagic–benthic resource fluxes. Ecosystems 21:1255–68.CrossRefGoogle Scholar
  57. Sadro S, Melack JM. 2012. The effect of an extreme rain event on the biogeochemistry and ecosystem metabolism of an oligotrophic high-elevation lake. Arctic Antarctic Alpine Res 44:222–31.CrossRefGoogle Scholar
  58. Sadro S, Melack JM, MacIntyre S. 2011. Spatial and temporal variability in the ecosystem metabolism of a high-elevation lake: integrating benthic and pelagic habitats. Ecosystems 14:1123–40.CrossRefGoogle Scholar
  59. Sand-Jensen K, Staehr PA. 2007. Scaling of pelagic metabolism to size, trophy and forest cover in small Danish Lakes. Ecosystems 10:128–42.CrossRefGoogle Scholar
  60. Smith SV. 1985. Physical, chemical and biological characteristics of CO2 gas flux across the air-water interface. Plant Cell Environ 8:387–98.CrossRefGoogle Scholar
  61. Solomon CT, Jones SE, Weidel BC, Buffam I, Fork ML, Karlsson J, Larsen S, Lennon JT, Read JS, Sadro S, Saros JE. 2015. Ecosystem Consequences of Changing Inputs of Terrestrial Dissolved Organic Matter to Lakes: current Knowledge and Future Challenges. Ecosystems 18:376–89.CrossRefGoogle Scholar
  62. Staehr PA, Baastrup-Spohr L, Sand-Jensen K, Stedmon C. 2012a. Lake metabolism scales with lake morphometry and catchment conditions. Aquatic Sci 74:155–69.CrossRefGoogle Scholar
  63. Staehr PA, Bade D, Van de Bogert MC, Koch GR, Williamson C, Hanson P, Cole JJ, Kratz T. 2010a. Lake metabolism and the diel oxygen technique: state of the science. Limnol Oceanogr Methods 8:628–44.CrossRefGoogle Scholar
  64. Staehr PA, Brighenti LS, Honti M, Christensen J, Rose KC. 2016. Global patterns of light saturation and photoinhibition of lake primary production. Inland Waters 6:593–607.CrossRefGoogle Scholar
  65. Staehr PA, Christensen JPA, Batt R, Read J. 2012b. Ecosystem metabolism in a stratified lake. Limnol Oceanogr 57:1317–30.CrossRefGoogle Scholar
  66. Staehr PA, Sand-Jensen K. 2007. Temporal dynamics and regulation of lake metabolism. Limnol Oceanogr 52:108–20.CrossRefGoogle Scholar
  67. Staehr PA, Sand-Jensen K, Raun AL, Nilsson B, Kidmose J. 2010b. Drivers of metabolism and net heterotrophy in contrasting lakes. Limnol Oceanogr 55:817–30.CrossRefGoogle Scholar
  68. Talling JF. 1957. Diurnal changes of stratification and photosynthesis in some Tropical African waters. Proc R Soc B Biol Sci 147:57–83.CrossRefGoogle Scholar
  69. Tonetta D, Staehr PA, Schmitt R, Petrucio MM. 2016. Physical conditions driving the spatial and temporal variability in aquatic metabolism of a subtropical coastal lake. Limnologica 58:30–40.CrossRefGoogle Scholar
  70. Tonetta D, Staehr PA, Obrador B, Brandão LPM, Brighenti LS, Petrucio MM, Barbosa FAR, Bezerra-Neto JF. 2018. Effects of nutrients and organic matter inputs in the gases CO2 and O2: a mesocosm study in a tropical lake. Limnologica 69:1–9.CrossRefGoogle Scholar
  71. 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. Limnol Oceanogr 54:2298–314.CrossRefGoogle Scholar
  72. Vincent WF. 2009. Effects of climate change on lakes. In: Likens GE, Ed. Encyclopedia of inland waters. Amsterdam: Elsevier. p 55–60.CrossRefGoogle Scholar
  73. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM. 1997. Human domination of earth’s ecosystems. Science 277:494–9.CrossRefGoogle Scholar
  74. Wanninkhof R. 1992. Relationship between wind speed and gas exchange over the ocean. J Geophys Res 97:7373–82.CrossRefGoogle Scholar
  75. Webster KE, Soranno PA, Baines SB, Kratz TK, Bowser CJ, Dillon PJ, Campbell P, Fee EJ, Hecky RE. 2000. Structuring features of lake districts: landscape controls on lake chemical responses to drought. Freshw Biol 43:499–515.CrossRefGoogle Scholar
  76. Williamson CE, Brentrup JA, Zhang J, Renwick WH, Hargreaves BR, Knoll LB, Overholt EP, Rose KC. 2014. Lakes as sensors in the landscape: optical metrics as scalable sentinel responses to climate change. Limnol Oceanogr 59:840–50.CrossRefGoogle Scholar
  77. Williamson CE, Saros JE, Vincent WF, Smol JP. 2009. Lakes and reservoirs as sentinels, integrators, and regulators of climate change. Limnol Oceanogr 54:2273–82.CrossRefGoogle Scholar
  78. Yvon-Durocher G, Cescatti A, del Giorgio P, Gasol JM, Montoya JM, Pumpanen J, Staehr PA, Trimmer M, Woodward G, Allen AP. 2012. Reconciling differences in the temperature-dependence of ecosystem respiration across time scales and ecosystem types. Nature 487:472–6.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Laura Martins Gagliardi
    • 1
  • Ludmila Silva Brighenti
    • 1
    Email author
  • Peter Anton Staehr
    • 2
  • Francisco Antônio Rodrigues Barbosa
    • 1
  • José Fernandes Bezerra-Neto
    • 1
  1. 1.Laboratório de Limnologia, Ecotoxicologia e Ecologia Aquática - Limnea, ICBUniversidade Federal de Minas GeraisPampulha, Belo HorizonteBrazil
  2. 2.Department of BioscienceAarhus UniversityRoskildeDenmark

Personalised recommendations