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Palaeolimnological records of shallow lake biodiversity change: exploring the merits of single versus multi-proxy approaches

Journal of Paleolimnology volume 49, pages 431–446 (2013)Cite this article

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Abstract

Shallow lakes are among the most threatened ecosystems in the world and many contemporary studies have demonstrated declines in biodiversity due to anthropogenic forcing. Mostly, however, these studies have not covered the full period of human-induced diversity change in lakes which is typically over decades-centuries. Here we provide two examples of palaeoecological studies focussed on reconstructing biodiversity changes in contrasting shallow lake environments that demonstrate the efficacy of the approach—a shallow UK lake and a suite of floodplain lakes (called billabongs) in the Murray-Darling basin, Australia. In the Murray-Darling billabongs, complex sedimentary processes operate, sediment chronologies are less certain and replication of sites is needed to confirm patterns. The combination of sediment records from 10 billabongs showed that diatom diversity changes pre- and post-European (>1850) disturbance were inconsistent; however, reductions in diversity were more common and appear to reflect reductions in macrophyte abundance. At Felbrigg Lake, a multi-proxy study with strong chronological control demonstrated divergent responses of macrophyte, diatom, cladoceran and chironomid richness and diversity to a century of eutrophication. Eutrophication of the site was qualitatively inferred from changes in the macrophyte community in turn reconstructed from plant macrofossils. Benthic cladocerans showed a consistent decline in richness through the record, reflecting the gradual reduction in their macrophyte associated habitat over the past century. Diatom richness and diversity responses were complex, with increases in diversity and richness linked to both increases and decreases in macrophyte species richness and abundance. Chironomid richness and diversity patterns were less consistently linked to eutrophication. The loss of the dominant zooplanktivore (perch) in the 1970s was reflected in the richness and diversity profiles for all groups. Our study reveals clear potential for using sediment cores to infer biodiversity change in shallow lakes and shallow lake regions. However, given the contrasting patterns of diversity change for the different biological groups both in Felbrigg Lake and between Felbrigg and the billabongs, caution is required when interpreting whole-ecosystem biodiversity changes (or the absence of change) based on single as opposed to multi-proxy studies.

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References

  • Ayres K, Sayer CD, Skeate E, Perrow M (2008) Palaeolimnology as a tool to inform shallow lake management: an example from Upton Great Broad, Norfolk, UK. Biodivers Conserv 17:2153–2168

    Article  Google Scholar 

  • Beresford AL, Jones JI (2010) Weedbeds and big bugs: the importance of scale in detecting the influence of nutrients and predation on macroinvertebrates in plant-dominated shallow lakes. Freshw Biol 55:514–530

    Article  Google Scholar 

  • Blanks H (1973) The Story of Yea. The Hawthorn Press, Melbourne, Melbourne

    Google Scholar 

  • Blumenshine SC, Lodge D, Hodgson J (2000) Gradient of fish predation alters body size distributions of lake benthos. Ecology 81:374–386

    Google Scholar 

  • Brodersen K, Odgaard BV, Vestergaard O, Anderson NJ (2001) Chironomid stratigraphy in the shallow and eutrophic lake Sobygaard, Denmark: chironomid-macrophyte co-occurrence. Freshw Biol 46:253–267

    Article  Google Scholar 

  • Brooks J, Dodson S (1965) Predation, body size, and composition of plankton. Science 150:28–35

    Article  Google Scholar 

  • Buxton GL (1974) The middle reaches in the 19th century. In Frith HJ, Sawer G The murray waters. Man, Nature and a River System. Angus and Robertson, Sydney. 109–123

  • Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Fish production and herbivory can regulate lake ecosystems. Bioscience 35:634–639

    Article  Google Scholar 

  • Chilcott S (2011) Effects of anthropogenic stressors across a hydrological connectivity gradient in a dryland river: the recent ecological history of floodplain lakes (billabongs), Macintyre River. BSc (Honours), University of New England, Australia

    Google Scholar 

  • Das B, Nordin R, Mazumder A (2008) Relationship between phytoplankton paleoproduction and diversity in contrasting trophic states. Aquat Ecosys Health Manag 11:78–90

    Article  Google Scholar 

  • Davidson TA, Sayer CD, Perrow MR, Tomlinson ML (2003) Representation of fish communities by scale sub-fossils in shallow lakes: implications for inferring percid-cyprinid shifts. J Paleolimnol 30:441–449

    Article  Google Scholar 

  • Davidson TA, Sayer CD, Bennion H, David C, Rose N, Wade MP (2005) A 250 year comparison of historical, macrofossil and pollen records of aquatic plants in a shallow lake. Freshw Biol 50:1671–1686

    Article  Google Scholar 

  • Davidson TA, Sayer CD, Perrow MR, Bramm M, Jeppesen E (2007) Are the controls of species composition similar for contemporary and sub-fossil cladoceran assemblages? -A study of 39 shallow lakes of contrasting trophic status. J Paleolimnol 38:117–134

    Article  Google Scholar 

  • Davidson TA, Sayer CD, Langdon P, Burgess A, Jackson MJ (2010) Inferring past zooplanktivorous fish and macrophyte density in a shallow lake: application of a new regression tree model. Freshw Biol 55:584–599

    Article  Google Scholar 

  • Davidson TA, Bennion H, Jeppesen E, Clarke GH, Sayer CD, Morley D, Odgaard BV, Rasmussen P, Rawcliffe R, Salgado J, Simpson GL, Amsinck SL (2011) The role of cladocerans in tracking long-term change in shallow lake trophic status. Hydrobiologia 676:299–315

    Article  Google Scholar 

  • Davis J, Sim L, Chambers J (2010) Multiple stressors and regime shifts in shallow aquatic ecosystems in antipodean landscapes. Freshw Biol 55:5–18

    Article  Google Scholar 

  • De’ath G (1999) Principal curves: a new technique for indirect and direct gradient analysis. Ecology 80:2237–2253

    Google Scholar 

  • Declerck SAJ, Vandekerkhove J, Johansson L, Muylaert K, Conde-Porcuna J, Van der Gucht K, Perez-Martinez C, Lauridsen T, Schwenk K, Zwart G, Rommens W, Lopez-Ramos J, Vyverman W, Brendonck L, De Meester L (2005) Multi-group biodiversity in shallow lakes along gradients of phosphorus and water plant cover. Ecology 86:1905–1915

    Article  Google Scholar 

  • Diehl S (1992) Fish predation and benthic community structure: the role of omnivory and habitat complexity. Ecology 73:1646–1661

    Article  Google Scholar 

  • Diehl S, Kornijow R (1998) Influence of submerged macrophytes on trophic interactions among fish and macroinvertebrates. In: Jeppesen E, Søndergaard Ma, Søndergaard Mo, Christoffersen K (eds) The structuring role of submerged macrophytes in lakes. Springer, Berlin, pp 24–46

    Chapter  Google Scholar 

  • Erskine W (1996) Downstream hydrogeomorphic impacts of Eildon Reservoir on the Mid-Goulburn River. Victoria. Proc R Soc Vic 108:1–15

    Google Scholar 

  • Fluin J, Tibby J, Gell P (2010) The palaeolimnological record from Lake Cullulleraine, lower Murray River (south-east Australia): implications for understanding riverine histories. J Paleolimnol 43:309–322

    Article  Google Scholar 

  • Frey DG (1960) The ecological significance of cladoceran remains in lake sediments. Ecology 41:684–699

    Article  Google Scholar 

  • Gell PA, Bulpin S, Wallbrink P, Hancock G, Bickford S (2005) Tareena Billabong-a palaeolimnological history of an ever-changing wetland, Chowilla Floodplain, lower Murray-Darling basin, Australia. Mar Freshw Res 56:441–456

    Article  Google Scholar 

  • Greenwood M, Wood P, Monk W (2006) The use of fossil caddisfly assemblages in the reconstruction of flow environments from floodplain paleochannels of the River Trent, England. J Paleolimnol 35:747–761

    Article  Google Scholar 

  • Gregory-Eaves I, Beisner BE (2011) Palaeolimnological insights for biodiversity science: an emerging field. Freshw Biol 56:2653–2661

    Article  Google Scholar 

  • Hastie T, De’ath G, Walsh C (2011) pcurve: Principal curve analysis. http://CRAN.R-project.org/package=pcurve

  • Howard LC, Wood PJ, Greenwood MT, Rendell HM, Brooks SJ, Armitage PD, Extence CA (2010) Sub-fossil Chironomidae as indicators of palaeoflow regimes: integration into the PalaeoLIFE flow index. J Quat Sci 25:1270–1283

    Article  Google Scholar 

  • Jeppesen E, Jensen JP, Søndergaard M, Lauridsen T, Landkildehus F (2000) Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshw Biol 45:201–218

    Article  Google Scholar 

  • Jeppesen E, Nõges P, Davidson TA, Haberman J, Nõges T, Blank K, Lauridsen TL, Søndergaard M, Sayer CD, Laugaste R, Johansson LS, Bjerring R, Amsinck SL (2011) Zooplankton as indicators in lakes: a scientific-based plea for including zooplankton in the ecological quality assessment of lakes according to the European Water Framework Directive (WFD). Hydrobiologia 676:279–297

    Article  Google Scholar 

  • Jones JI, Sayer CD (2003) Does the fish-invertebrate-periphyton cascade precipitate plant loss in shallow lakes? Ecology 84:2155–2167

    Article  Google Scholar 

  • Jones JI, Moss B, Eaton JW, Johnstone OY (2000) Do submerged aquatic plants influence periphyton community composition for the benefit of invertebrate mutualists? Freshw Biol 43:591–604

    Google Scholar 

  • Kingsford RT (1999) Managing the water of the Border Rivers in Australia: irrigation, government and the wetland environment. Wetl Ecol Manag 7:1–2

    Article  Google Scholar 

  • Kingsford RT (2003) Ecological impacts and institutional and economic drivers for water resource development-a case study of the Murrumbidgee River, Australia. Aqua Ecos Health Manag 6:69–79

    Article  Google Scholar 

  • Lauridsen TL, Lodge DM (1996) Avoidance by Daphnia magna of fish and macrophytes: chemical cues and predator-mediated use of macrophyte habitat. Limnol Oceanogr 41:794–798

    Article  Google Scholar 

  • Lauridsen TL, Jeppesen E, Landkildehus F, Søndergaard M (2001) Horizontal distribution of cladocerans in arctic Greenland lakes—impact of macrophytes and fish. Hydrobiologia 442:107–116

    Article  Google Scholar 

  • Leahy PJ, Tibby JT, Kershaw PA, Heijnis H, Kershaw JS (2005) The impact of European settlement on Bolin billabong a Yarra River floodplain lake, Melbourne, Australia. Riv Res Applics 21:131–149

    Article  Google Scholar 

  • Liboriussen L, Jeppesen E (2003) Temporal dynamics in epipelic, pelagic and epiphytic algal production in a clear and a turbid shallow lake. Freshw Biol 48:418–431

    Article  Google Scholar 

  • Lodge DM (1991) Herbivory on freshwater macrophytes. Aquat Bot 41:195–224

    Article  Google Scholar 

  • Maheshwari BL, Walker KF, Mcmahon TA (1995) Effects of regulation on the flow regime of the River Murray, Australia. Reg Rivers Res Manag 10:15–38

    Article  Google Scholar 

  • McCosker RO (1996) An environmental scan of the border rivers system New South Wales/Queensland. Department of Natural Resources and Department of Land and Water Conservation, Sydney/Brisbane

    Google Scholar 

  • Noble GW (1969) The red gate: a history of Alexandra. Council of the Shire of Alexandra, Alexandra

    Google Scholar 

  • Ogden RW (2000) Modern and historical variation in aquatic macrophyte cover of billabongs associated with catchment development. Reg Rivers Res Manag 16:497–512

    Article  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Stevens MHH, Wagner H (2008) Vegan: Community ecology package. R package version 1.13–2. http://CRAN.R-project.org/package=vegan

  • Pinheiro JC, Bates D, DebRoy S, Sarkar D (2011) nlme: Linear and nonlinear mixed effects models. (R package version 3.1–101)

  • R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rawcliffe R, Sayer CD, Woodward G, Grey J, Davidson TA, Jones JI (2010) Back to the future: using palaeolimnology to infer long-term changes in shallow lake food webs. Freshw Biol 55:600–613

    Article  Google Scholar 

  • Reid MA (2002) A diatom-based palaeoecological study of two billabongs on the Goulburn River floodplain, southeast Australia. Proceedings of the 15th International Diatom Symposium. J. John. Ruggell, Gantner Verlag: 237–253

  • Reid MA (2008) Evidence for catastrophic shifts in the trophic structure of floodplain lakes associated with soil erosion. In: Schmidt J, Cochrane T, Phillips C (eds) Sediment dynamics in changing cnvironments. IAHS Press, Wallingford, pp 584–590

    Google Scholar 

  • Reid MA (2010) Establishing benchmarks and trajectories of change in the Lower Murrumbidgee Floodplain. Sydney, NSW Dept Environment, Climate change and water: 41

  • Reid MA, Ogden RW (2009) Factors affecting diatom distribution in floodplain lakes of the southeast Murray Basin, Australia and implications for palaeolimnological studies. J Paleolimnol 41:453–470

    Article  Google Scholar 

  • Reid MA, Sayer CD, Kershaw AP, Heijnis H (2007) Palaeolimnological evidence for submerged plant loss in a floodplain lake associated with accelerated catchment soil erosion (Murray River, Australia). J Paleolimnol 38:191–208

    Article  Google Scholar 

  • Richard Albert M, Bennett EM, Chen G, Gregory-Eaves I, MacDonald GK, Vermaire JC (2010) Phosphorus and land-use changes are significant drivers of cladoceran community composition and diversity: an analysis over spatial and temporal scales. Can J Fish Aquat Sci 67:1262–1273

    Article  Google Scholar 

  • Rusak JA, Leavitt PR, McGowan S, Chen GM, Olsen O, Wunsam S, Cumming BF (2004) Millennial-scale relationships of diatom species richness and production in two prairie lakes. Limnol Oceanogr 49:1290–1299

    Article  Google Scholar 

  • Salgado J, Sayer CD, Carvalho L, Davidson TA, Gunn I (2010) Assessing aquatic macrophyte community change through the integration of palaeolimnological and historical data at Loch Leven, Scotland. J Paleolimnol 43:191–204

    Article  Google Scholar 

  • Sayer CD, Roberts N, Sadler J, David C, Wade PM (1999) Biodiversity changes in a shallow lake ecosystem: a multi-proxy palaeolimnological analysis. J Biogeogr 26:97–114

    Article  Google Scholar 

  • Sayer CD, Davidson TA, Jones J (2010a) Seasonal dynamics of macrophytes and phytoplankton in shallow lakes: a eutrophication-driven pathway from plants to plankton? Freshw Biol 55:500–513

    Article  Google Scholar 

  • Sayer CD, Davidson TA, Jones IJ, Langdon PG (2010b) Combining contemporary ecology and palaeolimnology to understand shallow lake ecosystem change. Freshw Biol 55:487–499

    Article  Google Scholar 

  • Sayer CD, Burgess A, Kari K, Davidson TA, Peglar S, Yang H, Rose NL (2010c) Long-term dynamics of submerged macrophytes and algae in a small and shallow, eutrophic lake: implications for the stability of macrophyte-dominance. Freshw Biol 55:565–583

    Article  Google Scholar 

  • Scheffer M (1998) Ecology of shallow lakes. Kluwer Academic Publishers, Dordecht 357 pp

    Google Scholar 

  • Smol JP, Wolfe AP, Birks H, Douglas MSV, Jones V, Korhola A, Pienitz R, Rühland K, Sorvari S, Antoniades D, Brooks S, Fallu M-A, Hughes M, Keatley B, Laing T, Michelutti N, Nazarova L, Nyman M, Paterson A, Perren B, Quinlan R, Rautio M, Saulnier-Talbot E, Siitonen S, Solovieva N, Weckström J, Schindler D (2005) Climate-driven regime shifts in the biological communities of arctic lakes. Proc Natl Acad Sci USA 102:4397–4402

    Article  Google Scholar 

  • Sonneman JA, Sincock AJ, Fluin J, Reid MA, Newall P, Tibby JC, Gell PA (2000) An illustrated guide to common stream diatom species from temperate Australia. The Cooperative Research Centre for Freshwater Ecology, Albury

    Google Scholar 

  • Sorvari S, Korhola A, Thompson R (2012) Lake diatom responses to recent Arctic warming in Finnish Lapland. Glob Change Biol 8:171–181

    Article  Google Scholar 

  • Thoms MC, Southwell M, McGinness HM (2005) Floodplain-river ecosystems: fragmentation and water resources development. Geomorphology 71:126–138

    Article  Google Scholar 

  • Tibby J, Reid M, Fluin J, Hart B, Kershaw A (2003) Assessing long-term pH change in an Australian river catchment using monitoring and palaeolimnological data. Environ Sci Technol 37:3250–3255

    Article  Google Scholar 

  • Timms R, Moss B (1984) Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing, in the presence of zooplanktivorous fish, in a shallow wetland ecosystem. Limnol Oceanogr 29:472–486

    Article  Google Scholar 

  • Underwood G, Thomas J (1990) Grazing interactions between pulmonate snails and epiphytic algae and bacteria. Freshw Biol 23:505–522

    Article  Google Scholar 

  • Vadeboncoeur Y, Jeppesen E, Vander Zanden MJ, Schierup H, Christoffersen K, Lodge D (2003) From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnol Oceanogr 48:1408–1418

    Article  Google Scholar 

  • Van Dam H, Mertens A, Sinkeldam J (1994) A coded checklist and ecological indicator values of freshwater diatoms from the Netherlands. Netherlands J Aquat Ecol 28:117–133

    Article  Google Scholar 

  • Velghe K, Vermaire JC, Gregory-Eaves I (2012) Declines in littoral species richness across both spatial and temporal nutrient gradients: a palaeolimnological study of two taxonomic groups. Freshw Biol 57:2378–2389

    Article  Google Scholar 

  • Vestergaard O, Sand-Jensen K (2000) Alkalinity and trophic state regulate aquatic plant distribution in Danish lakes. Aquat Bot 67:85–107

    Article  Google Scholar 

  • Warfe DM, Barmuta LA (2004) Habitat structural complexity mediates the foraging success of multiple predator species. Oecologia 141:171–178

    Article  Google Scholar 

  • Whitehouse NJ, Langdon PG, Bustin R, Galsworthy S (2008) Fossil insects and ecosystem dynamics in wetlands: implications for biodiversity and conservation. Biodivers Conserv 17:2055–2078

    Article  Google Scholar 

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Acknowledgments

We thank the National Trust for supporting our work at Felbrigg Lake, the ARC and University of New England for supporting research at the Australian billabongs and two anonymous reviewers for very useful and supportive comments. We also thank Amy Burgess and Pete Langdon for contributing data. This paper was written with support to CS from the European Union FP7 project ‘BIOFRESH’ (Contract No. 226874). TD’s contribution was supported by the Center for Informatics Research on Complexity in Ecology (CIRCE), funded by the Aarhus University Research Foundation under the AU Ideas program. This is PuBoPeD publication number 46. We would like to take this opportunity to express our gratitude to Rick Battarbee for his inspirational support, encouragement and enthusiasm over the years.

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Authors and Affiliations

  1. Department of Bioscience, Aarhus University, 25 Vejlsøvej, Silkeborg, Denmark

    T. A. Davidson

  2. Department of Bioscience, Ecoinformatics and Biodiversity Group, Aarhus University, Aarhus, Denmark

    T. A. Davidson

  3. Riverine Landscapes Research Laboratory, Geography and Planning, University of New England, Armidale, NSW, Australia

    M. A. Reid & S. Chilcott

  4. Environmental Change Research Centre, Department of Geography, University College London, London, UK

    C. D. Sayer

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  1. T. A. Davidson
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  2. M. A. Reid
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  3. C. D. Sayer
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  4. S. Chilcott
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Correspondence to M. A. Reid.

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A celebration of Prof Rick Battarbee’s contributions to palaeolimnology, edited by Holmes et al.

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Davidson, T.A., Reid, M.A., Sayer, C.D. et al. Palaeolimnological records of shallow lake biodiversity change: exploring the merits of single versus multi-proxy approaches. J Paleolimnol 49, 431–446 (2013). https://doi.org/10.1007/s10933-013-9696-8

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Keywords

  • Shallow Lakes
  • Biodiversity
  • Palaeoecology
  • Diatoms
  • Cladocera
  • Submerged
  • Plants