Skip to main content

Advertisement

Log in

Shallow lake sediments provide evidence for metapopulation dynamics: a pilot study

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

The aim of this pilot study is to test the hypotheses that sediment cores can provide evidence for metapopulation dynamics and that these can be linked with site characteristics. We focus on temporal patterns of incidence and abundance of overwintering stages (statoblasts) produced by the freshwater bryozoan Cristatella mucedo, an organism characterised by a metapopulation ecology, in sediment cores retrieved from 18 UK lakes. Runs and goodness-of-fit tests provided evidence for population instability, periods of low abundance and absence, and of asynchrony—all signatures of metapopulation dynamics. Further hypothesis testing indicated that extinction risk is greater in more isolated sites and in sites of smaller size. Absence of statoblasts from the top sections of spatially separated, replicate cores provided independent evidence for extinction in one site. Our study demonstrates how the abundances of sedimentary-bound propagules may be analysed initially for metapopulation dynamics and subsequently how this may lead to working hypotheses regarding the drivers of such dynamics. The sediment archive represents a unique historical record whose potential for characterising metapopulation dynamics has previously been untapped but is broadly relevant for understanding the population biology of freshwater organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

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

    Article  Google Scholar 

  • Bilton D, Freeland JR, Okamura B (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Syst 32:159–181

    Article  Google Scholar 

  • Birks HH (2001) Plant macrofossils. In: Smol JP, Birks HJB, Last B (eds) Tracking environmental change using lake sediments. Volume 3: terrestrial, algal, and siliceous indicators. Kluwer Academic Publishers, Dordrecht, pp 49–74

    Google Scholar 

  • Böcher J (1995) Palaeoentomology of the Kap Kobenhavn Formation, a Plio-Pleistocene sequence in Peary Land, North Greenland. Meddelelser om Grønland, Geoscience 33, pp 82

  • Bushnell JH, Rao KS (1979) Freshwater Bryozoa: micro-architecture of statoblasts and some Aufwuchs animal associations. In: Larwood GP, Abbott MB (eds) Advances in bryozoology. Academic Press, London, pp 75–91

    Google Scholar 

  • Canning EU, Okamura B, Curry A (1997) A new microsporidium, Nosema cristatellae n. sp. in the bryozoan Cristatella mucedo (Bryozoa, Phylactolaemata). J Invert Pathol 70:177–183

    Article  Google Scholar 

  • Cousyn C, De Meester L, Colbourne JK, Bendonck L, Verschuren D, Volckaert F (2001) Rapid local adaptation of zooplankton behavior to changes in predation pressure in absence of neutral genetic changes. Proc Natl Acad Sci USA 98:6256–6266

    Article  PubMed  CAS  Google Scholar 

  • Crisman TL, Crisman UAM, Binford MW (1986) Interpretation of bryozoan microfossils in lacustrine sediment cores. Hydrobiology 143:113–118

    Article  CAS  Google Scholar 

  • Davidson TA, Appleby PG (2003) The environmental history of Kenfig Pool cSAC. Countryside Council for Wales, Contract Science Report No. 561. ECRC Research Report 89

  • Davidson TA, Sayer CD, 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, Hoare D, Morley D, Sayer CD (2006) Reconstructing the macrophyte flora of three Norfolk Broads: a palaeolimnological analysis. Report to the Broads Authority. ECRC Research Report 106

  • 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 

  • De Meester L, Gómez A, Okamura B, Schwenk K (2002) The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecolog 23:121–135

    Article  Google Scholar 

  • De Stasio BT Jr (1990) The role of dormancy and emergence patterns in the dynamics of a freshwater zooplankton community. Limnol Oceanogr 35:10170–11090

    Article  Google Scholar 

  • Decaestecker E, Gaba S, Raeymaekers JAM, Stoks R, Van Kerckhoven L, Ebert D, De Meester L (2007) Host-parasite ‘Red Queen’ dynamics archived in pond sediments. Nature 450:870–874

    Article  PubMed  CAS  Google Scholar 

  • Duffy MA, Perry LJ, Kearns CM, Weider LJ, Hairston NG Jr (2000) Paleogenetic evidence for a past invasion of Onondaga Lake, New York, by exotic Daphnia curvirostris using mtDNA from dormant eggs. Limnol Oceanogr 45:1409–1414

    Article  Google Scholar 

  • Ebert D, Payne RJH, Weisser WW (1997) The epidemiology of parasitic diseases in Daphnia. In: Dettner K, Bauer G, Völkl W (eds) Vertical food web interactions: evolutionary patterns and driving forces. Springer, Heidelberg, pp 91–111

    Chapter  Google Scholar 

  • Ehrlich PR, Hanski I (2004) On the wings of checkerspots: a model system for population biology. Oxford University Press, Oxford

    Google Scholar 

  • Figuerola J, Green AJ, Michot T (2005) Invertebrate eggs can fly: evidence of waterfowl-mediated gene flow in aquatic invertebrates. Am Nat 165:274–280

    Article  PubMed  Google Scholar 

  • Francis DR (1997) Bryozoan statoblasts in the recent sediments of Douglas Lake, Michigan. J. Paleolimnol 17:255–261

    Article  Google Scholar 

  • Freeland JR, Noble LR, Okamura B (2000) Genetic consequences of the metapopulation biology of a facultatively sexual freshwater invertebrate. J Evol Biol 13:383–395

    Article  Google Scholar 

  • Giles BE, Goudet J (1997) Genetic Differentiation in Silene dioica metapopulations: estimation of spatiotemporal effects in a successional plant species. Am Nat 149:507–526

    Article  Google Scholar 

  • Gosling LM, Baker SJ (1980) Acidity fluctuations at a Broadland site in Norfolk. J Appl Ecol 17:479–490

    Article  Google Scholar 

  • Hairston NG Jr, Kearns CM (2002) Temporal dispersal: ecological and evolutionary aspects of zooplankton egg banks and the role of sediment mixing. Int Comp Biol 42:481–491

    Article  Google Scholar 

  • Hairston NG Jr, Ellner S, Kearns CM (1996) Overlapping generations: the storage effect and the maintenance of biotic diversity. In: Rhodes OE, Chesser RK, Smith MH (eds) Population dynamics in space and time. Chicago University Press, Chicago, pp 109–145

    Google Scholar 

  • Hairston NG Jr, Lampert W, Càceres CE, Holtmeier CL, Weider LJ, Gaedke U, Fischer JM, Fox JA, Post DM (1999) Rapid evolution revealed by dormant eggs. Nature 401:446

    Article  Google Scholar 

  • Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford

    Google Scholar 

  • Harrison S, Taylor AD (1997) Empirical evidence for metapopulation dynamics. In: Hanski I, Gilpin ME (eds) Metapopulation biology. Ecology, genetics, and evolution. Academic Press, San Diego, pp 27–42

    Chapter  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  CAS  Google Scholar 

  • Hengherr S, Schill RO (2011) Dormant stages in freshwater bryozoans—an adaptation to transcend environmental constraints. J Insect Physiol 57:595–601

    Article  PubMed  CAS  Google Scholar 

  • Hill SLL, Sayer CD, Hammond PM, Rimmer V, Davidson TA, Hoare DJ, Burgess A, Okamura B (2007) Are rare species rare or just overlooked? Assessing the distribution of the freshwater bryozoan, Lophopus crystallinus. Biol Cons 135:223–234

    Article  Google Scholar 

  • Hoare DJ (2006) Ecological change in shallow lakes through antifoul biocide contamination. Dissertation, University College London

  • Holmes J, Sayer CD, Liptrott E, Hoare DJ (2010) Complex controls on ostracod faunal palaeoecology in a shallow, coastal brackish-water lake: implications for palaeosalinity reconstruction. Freshw Biol 55:2484–2498

    Article  Google Scholar 

  • Jeppesen E, Leavitt P, De Meester L, Jensen JP (2001) Functional ecology and palaeolimnology: using cladocern remains to reconstruct anthropogenic impact. Trends Ecol Evol 16:191–198

    Article  PubMed  Google Scholar 

  • Kerfoot WC, Weider LJ (2004) Experimental paleoecology (resurrection ecology): chasing Van Valen’s Red Queen hypothesis. Limnol Oceanogr 49:1300–1316

    Article  Google Scholar 

  • Kindvall O (1996) Habitat heterogeneity and survival in a bush cricket metapopulation. Ecology 77:207–214

    Article  Google Scholar 

  • Kuc M (1973) Fossil statoblasts of Cristatella mucedo Cuvier in the Beaufort Formation and in interglacial and postglacial deposits of the Canadian Arctic. Department of Energy, Mines and Resources, Ottawa

    Google Scholar 

  • Madgwick G, Emson D, Sayer CD, Willby NJ, Rose N, 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 

  • Marcus E (1934) Uber Lophophus crystallinus (Pall.). Zool Jahr 58:34–40

    Google Scholar 

  • Mergeay J, Vanoverbeke J, Verschuren D, De Meester L (2007) Extinction, recolonization, and through time in a planktonic crustacean. Ecology 88:3032–3043

    Article  PubMed  Google Scholar 

  • Miner BE, De Meester L, Pfrender ME, Lampert W, Hairston NG Jr (2012) Linking genes to communities and ecosystems: Daphnia as an ecogenomic model. Proc R Soc B 279:1873–1882

    Article  PubMed  Google Scholar 

  • Moilanen A, Hanski I (1998) Metapopulation dynamics: effects of habitat quality and landscape structure. Ecology 79:2503–2515

    Article  Google Scholar 

  • Moilanen A, Smith AT, Hanski I (1998) Long-term dynamics in a metapopulation of the American Pika. Am Nat 152:530–542

    Article  PubMed  CAS  Google Scholar 

  • Moss B (2001) The broads. Harper Collins Publishers, London

    Google Scholar 

  • Mouquet N, Loreau M (2003) Community patterns in source-sink metacommunities. Am Nat 162:544–557

    Article  PubMed  Google Scholar 

  • Okamura B (1994) Variation in local populations of the freshwater bryozoan Cristatella mucedo. In: Hayward PJ, Ryland RS, Taylor PD (eds) Biology and palaeobiology of bryozoans. Olsen & Olsen, Fredensborg, pp 145–149

    Google Scholar 

  • Okamura B (1996) Occurrence, prevalence, and effects of the myxozoan Tetracapsula bryozoides Canning, Okamura and Curry, 1996, parasitic in the freshwater bryozoan Cristatella mucedo Cuvier (Bryozoa, Phylactolaemata). Fol Parasitol 43:262–266

    Google Scholar 

  • Okamura B (1997) The ecology of subdivided populations of a clonal freshwater bryozoan in southern England. Arch Hydrobiol 141:13–34

    Google Scholar 

  • Okamura B (2000) Metapopulation biology of freshwater bryozoans. In: Cubilla AH, Jackson JBC (eds) Proceedings of the 11th international bryozoology association conference. Smithsonian Tropical Research Institute, Balboa, Republic of Panama, pp 316–332

  • 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 

  • Rose NL, Appleby PG (2005) Regional applications of lake sediment dating by spheroidal carbonaceous particle analysis I: United Kingdom. J Paleolimnol 34:349–361

    Article  Google Scholar 

  • Sayer CD (2001) Problems with the application of diatom-total phosphorus transfer functions: examples from a shallow English Lake. Freshw Biol 46:743–757

    Article  CAS  Google Scholar 

  • Sayer CD, Jackson MJ, Hoare D, Simpson GL, Henderson ACG, Liptrot ER, Appleby PG, Boyle JF, Jones IJ, Waldock MJ (2006) TBT causes regime shift in shallow lakes. Environ Sci Technol 40:5269–5275

    Article  PubMed  CAS  Google Scholar 

  • Sayer CD, Davidson TA, Kelly A (2008) Ornamental lakes—an overlooked conservation resource? Aquat Conserv Mar Freshw Ecosyst 18:1046–1051

    Article  Google Scholar 

  • Sayer CD, Burgess A, Kari K, Peglar S, Davidson TA, Yang H, Rose N (2010a) 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  CAS  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, Bennion H, Davidson TA, Burgess A, Clarke G, Hoare D, Frings P, Hatton-Ellis T (2012) The application of palaeolimnology to evidence-led lake management and conservation: examples from UK lakes. Aquat Conserv Mar Freshw Ecosyst 22:165–180

    Article  Google Scholar 

  • Sjögren P (1991) Extinction and isolation gradients in metapopulations: the case of the pool frog (Rana lessonae). Biol J Linn Soc 42:135–147

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research, 3rd edn. W.H. Freeman and Company, New York

    Google Scholar 

  • SPSS for Windows, Rel. 16.0.1. (2007). Chicago: SPSS Inc.

  • Thomas CD, Wilson RJ, Lewis OT (2002) Short-term studies underestimate 30-generation changes in a butterfly metapopulation. Proc R Soc Ser B 269:563–569

    Article  Google Scholar 

  • Vernon JG, Okamura B, Jones CS, Noble LR (1996) Temporal patterns of clonality and parasitism in a population of freshwater bryozoans. Proc R Soc Ser B 263:1313–1318

    Article  CAS  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. Freshwater Biological Association Scientific Publication No. 63. Freshwater Biological Association, Ambleside, UK

  • Wood TS, Anurakpongsatorn P, Chaichana R, Mahujchariyawong J, Satapanajaru T (2005) Predation on freshwater bryozoans by the apple snail, Pomacea canaliculata, Ampulariidae, an invasive species in Southeast Asia: a summary report. Denisia 16:283–286

    Google Scholar 

Download references

Acknowledgments

We thank K. Benyon, K. Evans, K. Kari, V. Rimmer, C. Shutts and Y. Zhao for data collection and J. Freeland, P. Spaak and anonymous reviewers for comments on the manuscript. This work was partly funded by a Natural Environment Research Council Fellowship (GT5/98/22/CB) awarded to C. Sayer, by consultancy projects undertaken for the Broads Authority and the Countryside Council for Wales as administered by ENSIS Ltd. and by undergraduate project research funds provided by the University of Reading to B. Okamura.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Beth Okamura.

Additional information

Handling Editor: Piet Spaak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Okamura, B., Ayres, K., Salgado, J. et al. Shallow lake sediments provide evidence for metapopulation dynamics: a pilot study. Aquat Ecol 47, 163–176 (2013). https://doi.org/10.1007/s10452-013-9432-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-013-9432-5

Keywords

Navigation