Skip to main content

Eutrophication erodes inter-basin variation in macrophytes and co-occurring invertebrates in a shallow lake: combining ecology and palaeoecology

Journal of Paleolimnology volume 60, pages 311–328 (2018)Cite this article

Abstract

Aquatic biodiversity is commonly linked with environmental variation in lake networks, but less is known about how local factors may influence within-lake biological heterogeneity. Using a combined ecological and multi-proxy palaeoecological approach we investigated long-term changes in the pathways and processes that underlie eutrophication and water depth effects on lake macrophyte and invertebrate communities across three basins in a shallow lake—Castle Lough, Northern Ireland, UK. Contemporary data allow us to assess how macrophyte assemblages vary in composition and heterogeneity according to basin-specific factors (e.g. variation in water depth), while palaeoecological data (macrophytes and co-occurring invertebrates) enable us to infer basin-specific impacts and susceptibilities to nutrient-enrichment. Results indicate that variability in water depth promotes assemblage variation amongst the lake basins, stimulating within-lake macrophyte assemblage heterogeneity and hence higher lake biodiversity. The palaeo-data indicate that eutrophication has acted as a strong homogenising agent of macrophyte and invertebrate diversities and abundances over time at the whole-lake scale. This novel finding strongly suggests that, as eutrophication advances, the influence of water depth on community heterogeneity is gradually eroded and that ultimately a limited set of eutrophication-tolerant species will become homogeneously distributed across the entire lake.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Aldridge DC, Horne DC (1998) Fossil glocchidia (Bivalvia, Unionidae): identification and value in palaeoenvironmental reconstructions. J Micropalaeontol 17:179–182

    Article  Google Scholar 

  • Allen MR, Vandyke JN, Caceres CE (2011) Metacommunity assembly and sorting in newly formed lake communities. Ecology 92:269–275

    Article  Google Scholar 

  • Anderson M (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson M (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253

    Article  Google Scholar 

  • Anderson M, Ellingsen K, McArdle B (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693

    Article  Google Scholar 

  • Appleby PG, Oldfield F (1978) The calculation of lead-210 dates assuming a constant rate of supply of unsupported 210 Pb to the sediment. Catena 5:1–8

    Article  Google Scholar 

  • Appleby PG, Nolan PJ, Gifford DW, Godfrey MJ, Oldfield F, Anderson NJ, Battarbee RW (1986) 210Pb dating by low background gamma counting. Hydrobiologia 141:21–27

    Article  Google Scholar 

  • Arts GH (2002) Deterioration of Atlantic soft water macrophyte communities by acidification, eutrophication and alkalinisation. Aquat Bot 31:373–393

    Article  Google Scholar 

  • Ayres KR, Sayer CD, Skeate ER, Perrow MR (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 

  • Barko JW, Smart RM (1986) Sediment-related mechanisms of growth limitation in submersed macrophytes. Ecology 67:1328–1340

    Article  Google Scholar 

  • Barrat-Segretain MH (1996) Strategies of reproduction, dispersion, and competition in river plants: a review. Vegetatio 123:13–37

    Article  Google Scholar 

  • Battarbee R (1986) The Eutrophication of Lough Erne inferred from changes in the diatom assemblages of 210Pb- and 37Cs dated sediment cores. Proc R Ir Acad 86B:141–168

    Google Scholar 

  • Birks HH (2001) Plant macrofossils. In: Smol JP, Birks HJB, Lasts WM (eds) Tracking environmental change using lake sediments, Terrestrial, algal and siliceous indicators, vol 3. Kluwer, Dordecht, pp 49–74

    Chapter  Google Scholar 

  • Birks HJ (2014) Challenges in the presentation and analysis of plant-macrofossil stratigraphical data. Veg Hist Archaeobot 23:309–330

    Article  Google Scholar 

  • Brodersen K, Lindegaard C (1999) Classification, assessment and trophic reconstruction of Danish lakes using chironomids. Freshw Biol 42:143–157

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Brooks SJ, Heiri O, Langdon PG (2007) The identification and use of palaearctic chironomidae larvae in palaeoecology. Technical guide No. 10. Quaternary Research Association, London

    Google Scholar 

  • Canfield DE Jr, Shireman J, Colle DE, Haller WT, Watkins CE II, Maceina MJ (1984) Prediction of chlorophyll a concentrations in Florida lakes: importance of aquatic macrophytes. Can J Fish Aquat Sci 41:497–501

    Article  Google Scholar 

  • Carpenter S, Titus JE (1984) Composition and spatial heterogeneity of submersed vegetation in a softwater lake in Wisconsin. Plant Ecol 57:153–165

    Article  Google Scholar 

  • Clarke GH, Sayer CD, Turner S, Salgado J, Meis S, Patmore IR, Zhao Y (2014) Representation of aquatic vegetation change by plant macrofossils in a small and shallow freshwater lake. Veg Hist Archaeobot 23:265–276

    Article  Google Scholar 

  • Cummins RH (1994) Taphonomic processes in modern freshwater molluscan death assemblages: implications for the freshwater fossil record. Palaeogeogr Palaeoclimatol Palaeoecol 108:55–73

    Article  Google Scholar 

  • Davidson TA, Sayer CD, Bennion H, David C, Rose N, Wade M (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, Langdon PG, Burgess A, Jackson M (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 

  • Davis FW (1985) Historical changes in submerged macrophyte communities of upper Chesapeake Bay. Ecology 66:981–993

    Article  Google Scholar 

  • Donohue I, Jackson AL, Pusch MT, Irvine K (2009) Nutrient-enrichment homogenizes lake benthic assemblages at local and regional scales. Ecology 90:3470–3477

    Article  Google Scholar 

  • Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Faith DP, Minchin PR, Belbin L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69:57–68

    Article  Google Scholar 

  • Ford JR, Shima JS, Swearer SE (2016) Interactive effects of shelter and conspecific density shape mortality, growth, and condition in juvenile reef fish. Ecology 97:1373–1380

    Article  Google Scholar 

  • Fukami T, Morin P (2003) Productivity-biodiversity relationships depend on the history of community assembly. Nature 424:423–426

    Article  Google Scholar 

  • Gibson C, Wu Y, Smith S, Wolfe-Murphy S (1995) Synoptic limnology of a diverse geological region: catchment and water chemistry. Hydrobiologia 306:213–227

    Article  Google Scholar 

  • Hartikainen H, Johnes P, Moncrieff C, Okamura B (2009) Bryozoan populations reflect nutrient-enrichment and productivity gradients in rivers. Freshw Biol 54:2320–2334

    Article  Google Scholar 

  • Higgins SN, Vander Zanden MJ (2010) What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecol Monogr 80:179–196

    Article  Google Scholar 

  • Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520

    Article  Google Scholar 

  • Jeppesen E, Sondergaard M, Sondergaard M, Christofferson K (eds) (2012) The structuring role of submerged macrophytes in lakes. Springer Science and Business Media, Dordrecht

    Google Scholar 

  • Keddy PA, Reznicek AA (1986) Great Lakes vegetation dynamics: the role of fluctuating water levels and buried seeds. J Great Lakes Res 12:25–36

    Article  Google Scholar 

  • Korhonen JJ, Soininen J, Hillebrand H (2010) A quantitative analysis of temporal turnover in aquatic species assemblages across ecosystems. Ecology 91:508–517

    Article  Google Scholar 

  • Langdon PG, Ruiz Z, Wynne S, Sayer CD, Davidson TA (2010) Ecological influences on larval chironomid communities in shallow lakes: implications for palaeolimnological interpretations. Freshw Biol 55:531–545

    Article  Google Scholar 

  • Lauridsen T, Lodge D (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 T, Pedersen LJ, Jeppesen E, Sønergaard M (1996) The importance of macrophyte bed size for cladoceran composition and horizontal migration in a shallow lake. J Plankton Res 18:2283–2294

    Article  Google Scholar 

  • Legendre P, Cáceres MD, Borcard D (2010) Community surveys through space and time: testing the space–time interaction in the absence of replication. Ecology 91:262–272

    Article  Google Scholar 

  • Leibold M, Norberg J (2004) Biodiversity in metacommunities: Plankton as complex adaptive systems? Limnol Oceanogr 49:1278–1289

    Article  Google Scholar 

  • Leibold M, Holyoak M, Mouquet N, Amarasekare P, Chase J, Hoopes M, Holt R, Shurin J, Law R, Tilman D (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613

    Article  Google Scholar 

  • Levi EE, Çakıroğlu Aİ, Bucak T, Odgaard B-V, Davidson TA, Jeppesen E, Beklioğlu M (2014) Similarity between contemporary vegetation and plant remains in the sediment surface in Mediterranean lakes. Freshw Biol 59:724–736

    Article  Google Scholar 

  • Madgwick G, Emson D, Sayer CD, Willby N, Rose NL, Jackson MJ, Kelly A (2011) Centennial-scale changes to the aquatic vegetation structure of a shallow eutrophic lake and implications for restoration. Freshw Biol 56:2620–2636

    Article  Google Scholar 

  • Mathers R, De Carlos M, Crowley K, Teangana DÓ (2002) A review of the potential effect of Irish hydroelectric installations on Atlantic salmon (Salmo salar L.) populations, with Particular Reference to the River Erne. Proc R Ir Acad 102B:69–79

    Article  Google Scholar 

  • Moller Pillot HKM (2009) Chironomidae larvae: biology and ecology of the chironomini. KNNV Publishing, Zeist

    Google Scholar 

  • Moller Pillot HKM (2013) Chironomidae larvae: biology and ecology of the aquatic orthocladiinae. KNNV Publishing, Zeist

    Google Scholar 

  • Odgaard B, Rasmussen P (2001) The occurrence of egg-cocoons of the leech Piscicola geometra (L.) in recent sediments and their relationship with the remains of submerged macrophytes. Arch Hydrobiol 52:671–686

    Article  Google Scholar 

  • Økland KA, Økland J (2002) Freshwater bryozoans (Bryozoa) of Norway III: distribution and ecology of Plumatella fruticosa. Hydrobiologia 479:11–22

    Article  Google Scholar 

  • Patmore IR, Sayer CD, Goldsmith B, Davidson TA, Rawcliffe R, Salgado J (2014) Big Ben: a new wide-bore piston corer for multi-proxy palaeolimnology. J Paleolimnol 51:79–86

    Article  Google Scholar 

  • Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625

    Article  Google Scholar 

  • Pinder LCV, Reiss F (1983) The larvae of Chironominae (Diptera: Chironomidae) of the Holartic region. Keys and diagnoses. Entomol Scand Suppl 19:293–435

    Google Scholar 

  • Price J (1890) Lough Erne drainage. P I Civil Eng C1:73–94

    Google Scholar 

  • R Core Development Team (2009) R 2.9.2. R project for statistical computing. Vienna, Austria. www.r-project.com

  • Rasmussen P, Anderson NJ (2005) Natural and anthropogenic forcing of aquatic macrophyte development in a shallow Danish lake during the last 7000 years. J Biogeogr 32:1993–2005

    Article  Google Scholar 

  • Riis T, Sand-Jensen K, Larsen SE (2001) Plant distribution and abundance in relation to physical conditions and location within Danish stream systems. Hydrobiologia 448:217–228

    Article  Google Scholar 

  • Rosell RS, Maguire CM, McCarthy TK (1998) First reported settlement of zebra mussels Dreissena polymorpha in the Erne System, Co. Fermanagh, Northern Ireland. Biol Environ 98:191–193

    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 

  • Sand-Jensen K, Pedersen NL, Thorsgaard I, Moeslund B, Borum J, Brodersen KP (2008) 100 years of vegetation decline and recovery in Lake Fure, Denmark. J Ecol 96:260–271

    Article  Google Scholar 

  • Sayer CD, Davidson TA, Jones JI (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, Burgess AM, Kari K, Davidson TA, Peglar S, Yang H, Rose N (2010b) 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 

  • Sculthorpe CD (1967) The biology of aquatic plants. Edward Arnold Ltd., London

    Google Scholar 

  • Smolders A, Lamers L, Hartog C, Roelofs J (2003) Mechanisms involved in the decline of Stratiotes aloides L. in the Netherlands: sulphate as a key variable. Hydrobiologia 506:603–610

    Article  Google Scholar 

  • Spence D (1967) Factors controlling the distribution of freshwater macrophytes with particular reference to the lochs of Scotland. J Ecol 55:147–170

    Article  Google Scholar 

  • Spence DHN, Chrystal J (1970) Photosynthesis and zonation of freshwater macrophytes. New Phytol 69:217–227

    Article  Google Scholar 

  • Urban MC, De Meester L (2009) Community monopolization: local adaptation enhances priority effects in an evolving metacommunity. Proc R Soc Biol Sci Ser B 276:4129–4138

    Article  Google Scholar 

  • Vallenduuk HJ, Moller Pillot HKM (2007) Chironomidae larvae: general ecology and tanypodinae. KNNV Publishing, Zeist

    Google Scholar 

  • Wood TS, Okamura B (2005) A new key to the freshwater bryozoans of Britain, Ireland and continental Europe, with notes on their ecology. The Freshwater Biological Association, Ambleside

    Google Scholar 

  • Zhao Y, Sayer CD, Birks HH, Hughes M, Peglar S (2006) Spatial representation of aquatic vegetation by macrofossils and pollen in a small and shallow lake. J Paleolimnol 35:335–350

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Department of Zoology of The Natural History Museum, London for funding this work as part of J. Salgado’s Ph.D. A Hugh Cary Gilson Memorial Award from the Freshwater Biological Association provided support for fieldwork. We also thank the Departamento Administrativo de Ciencia, Tecnología e Innovación-COLCINECIAS for supporting J. Salgado under the postdoctoral program “Es tiempo de volver”. T.A. Davidson’s contribution was supported by CIRCE funding under the AU ideas programme. We especially thank the Castle Lough landowners for site access and hospitality, G. Simpson for statistical analysis advice, I. Jones and N. Willby for constructive suggestions and P. Bexell and L. Petetti for fieldwork assistance. We also thank the EU FP7 Project Biofresh (Biodiversity of Freshwater Ecosystems: Status, Trends, Pressures, and Conservation Priorities) Contract No. 226874 for financial support for sediment core dating analysis.

Author information

Author notes

  1. Jorge Salgado

    Present address: Laboratorio de Palinología y Paleoecología Tropical, Departamento de Ciencias Biológicas, Universidad de Los Andes, Carrera Primera # 18A - 12, Bogotá, Colombia

Authors and Affiliations

  1. Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK

    Jorge Salgado, Stephen J. Brooks & Beth Okamura

  2. Environmental Change Research Centre, Department of Geography, University College London, Gower Street, London, WC1E 6BT, UK

    Jorge Salgado & Carl D. Sayer

  3. Lake Group, Department of Bioscience, Aarhus University, Silkeborg, Denmark

    Thomas A. Davidson

  4. Department of Bioscience, Section for Ecoinformatics and Biodiversity, Aarhus, Denmark

    Thomas A. Davidson

Authors
  1. Jorge Salgado
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carl D. Sayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen J. Brooks
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas A. Davidson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Beth Okamura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jorge Salgado.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10933_2017_9950_MOESM1_ESM.eps

Figure ESM1. Radiometric chronologies and sedimentation rates for cores (a) NCAS1; (b) NCAS2; and (c) NCAS3 (EPS 723 kb)

10933_2017_9950_MOESM2_ESM.eps

Figure ESM2. Boxplot of (a) depth variation between basins; (b) Macrophyte average distance to centroid group and perMANOVA (F = 13.414, P = 0.001) and HMD (F = 7.87, P = 0.001) results; (c) Depth distance to centroid group and perMANOVA (F = 137.84, P = 0.001) and HMD (F = 93.155, P < 0.001) results (EPS 329 kb)

10933_2017_9950_MOESM3_ESM.eps

Figure ESM3. Logistic regressions on presence/absence data of macrophyte species sensitive to eutrophication across the observed depth profiles. (a) Chara globularis; (b) Myriophyllum verticillatum; (c) Stratiotes aloides (EPS 1072 kb)

10933_2017_9950_MOESM4_ESM.eps

Figure ESM4. Spatiotemporal maps showing K-means partition of (a) Plant macrofossils, (b) Chironomids; (c) Molluscs; (d) Bryozoans; and (e) Daphnid assemblages in the cores NCAS1, NCAS2 and NCAS3. Simple structure index (ssi) is indicated on the right-hand side of each map. Selected number of groups by ssi is indicated with a bold black circle (EPS 5041 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Salgado, J., Sayer, C.D., Brooks, S.J. et al. Eutrophication erodes inter-basin variation in macrophytes and co-occurring invertebrates in a shallow lake: combining ecology and palaeoecology. J Paleolimnol 60, 311–328 (2018). https://doi.org/10.1007/s10933-017-9950-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10933-017-9950-6

Keywords

  • Anthropogenic impact
  • Community heterogeneity
  • Historical dynamics
  • Light limitation
  • Lough Erne System
  • Multi-proxy study