Advertisement

Journal of Paleolimnology

, Volume 52, Issue 3, pp 171–184 | Cite as

Sedimentary pigments as indicators of cyanobacterial dynamics in a hypereutrophic lake

  • Bethany N. DeshpandeEmail author
  • Roxane Tremblay
  • Reinhard Pienitz
  • Warwick F. Vincent
Original paper

Abstract

Lac Saint-Augustin is an urban lake located on the outskirts of Quebec City, one of North America’s oldest cities. Anthropogenic inputs from land clearing, agriculture, highway development and urbanization in the surrounding catchment have resulted in strong impacts on the limnology of the lake throughout the past three centuries. In recent years, this lake has experienced severe eutrophication, including persistent cyanobacterial blooms. In winter 2011, a sediment core was extracted from the deepest area of the lake. A detailed paleopigment analysis was used to assess eutrophication processes in the lake and to determine the timing and appearance of cyanobacterial blooms and their subsequent variability. Extracted chlorophyll a, its degradation products and 11 carotenoid pigments were identified and quantified via reverse-phase high performance liquid chromatography to examine relative changes in the phytoplankton. The results revealed large variations in the phytoplankton community structure of Lac Saint-Augustin over the past 356 years. Chlorophyll a concentrations per unit organic matter (OM) increased significantly from the base of the core to present day, rising more than 15-fold from 18.4 µg (g OM)−1 at the base of the core to 287 µg (g OM)−1 in the most recent strata. Biostratigraphical analysis revealed three major periods of enrichment, with episodes of cyanobacterial abundance from the 1890s onwards. The greatest changes occurred in the most recent period (from the 1960s to the present) relative to earlier periods, with pigment increases for all phytoplankton groups. The cyanobacterial pigments canthaxanthin, echinenone and zeaxanthin (also a marker for green algae) showed concentrations in the surface sediments that were significantly above values at the bottom of the core, and these differences were large, even giving consideration to the lesser pigment degradation near the surface. Overall, the results indicate that cyanobacterial blooms are not a recent feature of Lac Saint-Augustin but began to occur soon after catchment modification 150 years ago. The pigment records also imply that cyanobacterial and associated algal populations have risen to unprecedented levels over the last few decades of ongoing development of the Lac Saint-Augustin catchment. This study highlights the utility of multiple pigment analysis of lake sediments for identifying the timing and magnitude of anthropogenic impacts.

Keywords

Pigments Cyanobacteria Eutrophication Phytoplankton Urban lake Human impacts 

Notes

Acknowledgments

This study was funded by NSERC (Ottawa, Canada), the Canada Research Chair program, CIMA+, and FRQNT through the Centre d’études nordiques (CEN). We thank R. Galvez and D. Jobin for their support with sediment sampling, M.-J. Martineau for laboratory assistance in preparing and analysing samples, and D. Antoniades and M. Lionard for advice on protocols.

References

  1. Appleby PG (2001) Chronostratigraphic techniques in recent sediments. In: Last WM, Smol JP (eds) Tracking environmental change using lake sediments. vol 1: basin analysis, coring, and chronological techniques. Kluwer Academic Publishers, Dordrecht, pp 171–203 Google Scholar
  2. Appleby PG, Oldfield F (1978) The calculation of 210-Pb dates assuming a constant rate of supply of unsupported 210-Pb to the sediment. Catena 5:1–8CrossRefGoogle Scholar
  3. Bianchi TS, Canuel EA (2011) Chemical biomarkers in aquatic ecosystems. Princeton University Press, PrincetonGoogle Scholar
  4. Bianchi TS, Engelhaupt E, Westman P, Andren T, Rolff C, Elmgren R (2000) Cyanobacterial blooms in the Baltic Sea: natural or human-induced? Limnol Oceanogr 45:716–726CrossRefGoogle Scholar
  5. Borghini F, Colacevich A, Bargagli R (2010) A study of autotrophic communities in two Victoria Land lakes (Continental Antarctica) using photosynthetic pigments. J Limnol 69:333–340CrossRefGoogle Scholar
  6. Brown MR, Jeffrey SW (1992) Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 1. Amino acids, sugars and pigments. J Exp Mar Biol Ecol 161:91–113CrossRefGoogle Scholar
  7. Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. E & FN Spon, SuffolkCrossRefGoogle Scholar
  8. Dean WE (1974) Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition: comparison with other methods. J Sediment Petrol 44:242–248Google Scholar
  9. Efting A, Snow DD, Fritz SC (2011) Cyanobacteria and microcystin in the Nebraska (USA) Sand Hills Lakes before and after modern agriculture. J Paleolimnol 46:17–27CrossRefGoogle Scholar
  10. Engstrom DR, Schottler SP, Leavitt PR, Havens KE (2006) A reevaluation of the cultural eutrophication of Lake Okeechobee using multiproxy sediment records. Ecol Appl 16:1194–1206CrossRefGoogle Scholar
  11. Fietz S, Nicklisch A, Oberhänsli H (2007) Phytoplankton response to climate changes in Lake Baikal during the Holocene and Kazantsevo interglacials assessed from sedimentary pigments. J Paleolimnol 37:177–203CrossRefGoogle Scholar
  12. Galvez-Cloutier R, Brin M-E, Dominguez G, Leroueil S, Arsenault S (2003) Quality evaluation of eutrophic sediments at Saint-Augustin Lake, Canada. In: Contaminated sediments: characterization, evaluation, mitigation/restoration, and management strategy performance. ASTM STP 1442: 35–52Google Scholar
  13. Grimm EC (1987) CONISS: a FORTRAN 77 program for stratigraphically constrained cluster analysis by the method of incremental sum of squares. Comput Geosci 13:13–35CrossRefGoogle Scholar
  14. Hall RI, Leavitt PR, Smol JP, Zirnhelt N (1997) Comparison of diatoms, fossil pigments and historical records as measures of lake eutrophication. Freshw Biol 38:401–417CrossRefGoogle Scholar
  15. Hart BT, Lake PS, Webb JA, Grace MR (2003) Ecological risks to aquatic systems from salinity increases. Aust J Bot 51:689–702CrossRefGoogle Scholar
  16. Hegewald E, Padisak J, Friedl T (2007) Pseudotetraëdriella kamillae: taxonomy and ecology of a new member of the algal class Eustigmatophyceae (Stramenopiles). Hydrobiologia 586:107–116CrossRefGoogle Scholar
  17. Hodgson DA, Doran PT, Roberts D, McMinn A (2004) Long-term environmental change in Arctic and Antarctic Lakes. In: Pienitz R, Douglas MSV, Smol JP (eds) Developments in paleoenvironmental research, vol 8. Springer, Dordrecht, pp 419–474 Google Scholar
  18. Hu H, Gao K (2006) Response of growth and fatty acid compositions of Nannochloropsis sp. to environmental factors under elevated CO2 concentration. Biotechnol Lett 28:987–992CrossRefGoogle Scholar
  19. Hurley JP, Armstrong DE (1991) Pigment preservation in lake sediments: a comparison of sedimentary environments in Trout Lake, Wisconsin. Can J Fish Aquat Sci 48:472–486CrossRefGoogle Scholar
  20. Leavitt PR (1993) A review of factors that regulate carotenoid and chlorophyll deposition and fossil pigment abundance. J Paleolimnol 9:109–127CrossRefGoogle Scholar
  21. Leavitt PR, Carpenter SR (1990) Aphotic pigment degradation in the hypolimnion: implications for sedimentation studies and paleolimnology. Limnol Oceanogr 35:520–534CrossRefGoogle Scholar
  22. Leavitt PR, Hodgson DA (2001) Sedimentary pigments. In: Smol JP, Birks HB, Last MW (eds) Tracking environmental change using lake sediments. Developments in paleoenvironmental research volume 3: terrestrial, algal, and siliceous indicators. Kluwer Academic, Dordrecht, pp 295–326Google Scholar
  23. Leavitt PR, Schindler DE, Paul AJ, Hardie AK, Schindler DW (1994) Fossil pigment records of phytoplankton in trout-stocked alpine lakes. Can J Fish Aquat Sci 51:2411–2423CrossRefGoogle Scholar
  24. Legendre P, Gallagher E (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280CrossRefGoogle Scholar
  25. McGowan S, Barker P, Haworth EY, Leavitt PR, Maberly SC, Pates J (2012) Humans and climate as drivers of algal community change in Windermere since 1850. Freshw Biol 57:260–277CrossRefGoogle Scholar
  26. Ministère des Richesses Naturelles (1979) Rapport de la diagnose écologique du lac Saint-Augustin. Direction Générale des Eaux, QuébecGoogle Scholar
  27. Nielsen DL, Brock MA, Rees GN, Baldwin DS (2003) Effects of increasing salinity on freshwater ecosystems in Australia. Aust J Bot 51:655–665CrossRefGoogle Scholar
  28. Olaizola M, Roche J, Kolber Z, Falkowski PG (1994) Non-photochemical fluorescence quenching and the diadinoxanthin cycle in a marine diatom. Photosynth Res 41:357–370CrossRefGoogle Scholar
  29. Owens TG, Gallagher JC, Alberte RS (1987) Photosynthetic light-harvesting function of violaxanthin in Nannochloropsis spp. (Eustigmatophyceae). J Phycol 85:79–85Google Scholar
  30. Paerl HW, Valdes LM, Pinckney JL, Piehler MF, Dyble J, Moisander PH (2003) Phytoplankton photopigments as indicators of estuarine and coastal eutrophication. Bioscience 53:953–964CrossRefGoogle Scholar
  31. Patoine A, Leavitt PR (2006) Century-long synchrony of fossil algae in a chain of Canadian prairie lakes. Ecology 87:1710–1721CrossRefGoogle Scholar
  32. Pennington FC, Haxo FT, Borch G, Liaaen-Jensen S (1985) Carotenoids of cryptophyceae. Biochem Syst Ecol 13:215–219CrossRefGoogle Scholar
  33. Pienitz R, Laberge K, Vincent WF (2006) Three hundred years of human-induced change in an urban lake: paleolimnological analysis of Lac Saint-Augustin, Québec City, Canada. Can J Bot 84:303–320CrossRefGoogle Scholar
  34. Reimer PJ, Baillie MGL, Bard E, Bayliss A, Beck JW, Blackwell PG, Ramsey CB, Buck CE, Burr GS, Edwards RL, Friedrich M, Grootes PM, Guilderson TP, Hajdas I, Heaton TJ, Hogg AG, Hughen KA, Kaiser KF, Kromer B, McCormac FG, Manning SW, Reimer RW, Richards DA, Southon JR, Talamo S, Turney CSM, van der Plicht J, Weyhenmeye CE (2009) INTCAL09 and MARINE09 radiocarbon age calibration curves, 0–50,000 years CAL BP. Radiocarbon 51:1111–1150Google Scholar
  35. Reuss N, Leavitt PR, Hall RI, Bigler C, Hammarlund D (2010) Development and application of sedimentary pigments for assessing effects of climatic and environmental changes on subarctic lakes in northern Sweden. J Paleolimnol 43:149–169CrossRefGoogle Scholar
  36. Roberge K, Pienitz R, Arsenault S (2002) Eutrophisation rapide du lac Saint-Augustin, Québec: étude paléolimnologique pour une reconstitution de la qualité de l’eau. Nat Can 126:68–82Google Scholar
  37. Rose NL, Morley D, Appleby PG, Battarbee RW, Alliksaar T, Guilizzoni P, Jeppesen E, Korhola A, Punning JM (2010) Sediment accumulation rates in European lakes since AD 1850: trends, reference conditions and exceedence. J Paleolimnol 45:447–468CrossRefGoogle Scholar
  38. Roy S, Llewellyn CA, Egeland ES, Johnsen G (2011) Phytoplankton pigments: characterization, chemotaxonomy and applications in oceanography. Camb Environ Chem Ser, CambridgeCrossRefGoogle Scholar
  39. Salmaso N, Tolotti M (2009) Other phytoflagellates and groups of lesser importance. In: Likens GE (ed) Encyclopedia of inland waters. Elsevier, Oxford, pp 174–183CrossRefGoogle Scholar
  40. Scheffer M (2004) Ecology of shallow lakes. Kluwer Academic, DordrechtCrossRefGoogle Scholar
  41. Sorgente D, Frignani M, Langone L, Ravaioli M (1999) Chronology of marine sediments. Interpretation of activity-depth profiles of 210-Pb and other radioactive tracers. Part I. Technical Report No. 54. Consiglio Nazionaledelle Ricerche. Institutoperla Geologia MarinaGoogle Scholar
  42. Squier A, Hodgson D, Keely B (2002) Sedimentary pigments as markers for environmental change in an Antarctic lake. Org Geochem 33:1655–1665CrossRefGoogle Scholar
  43. Steenbergen CLM, Korthals HJ, Dobrynin EG (1994) Algal and bacterial pigments in non-laminated lacustrine sediment: studies of their sedimentation, degradation and stratigraphy. FEMS Microbiol Ecol 13:335–352Google Scholar
  44. Stuiver M, Reimer PJ (1993) Extended 14C database and revised CALIB radiocarbon calibration program. Radiocarbon 35:215–230Google Scholar
  45. Tonk L, Bosch K, Visser PM, Huisman J (2007) Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquat Microb Ecol 46:117–123CrossRefGoogle Scholar
  46. Vincent WF (2009) Cyanobacteria. In: Likens GE (ed) Encyclopedia of inland waters, vol 3. Elsevier, Oxford, pp 226–232CrossRefGoogle Scholar
  47. Vinebrooke RD, Hall RI, Leavitt PR, Cumming BF (1998) Fossil pigments as indicators of phototrophic response to salinity and climatic change in lakes of western Canada. Can J Fish Aquat Sci 55:668–681CrossRefGoogle Scholar
  48. Watts CD, Maxwell JR (1977) Carotenoid diagenesis in a marine sediment. Geochim Cosmochim Acta 41:493–497CrossRefGoogle Scholar
  49. Xue B, Yao S, Xia W (2007) Environmental changes in Lake Taihu during the past century as recorded in sediment cores. Hydrobiologia 581:117–123CrossRefGoogle Scholar
  50. Zapata M, Rodriguez F, Garrido JL (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar Ecol Prog Ser 195:29–45CrossRefGoogle Scholar
  51. Züllig H (1981) On the use of carotenoid stratigraphy in lake sediments for detecting past developments of phytoplankton. Limnol Oceanogr 26:970–976CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Bethany N. Deshpande
    • 1
    Email author
  • Roxane Tremblay
    • 2
  • Reinhard Pienitz
    • 2
  • Warwick F. Vincent
    • 1
  1. 1.Département de biologie, Centre d’Études Nordiques (CEN)Université LavalQuebecCanada
  2. 2.Aquatic Paleoecology Laboratory, Département de géographie, Centre d’Études Nordiques (CEN)Université LavalQuebecCanada

Personalised recommendations