, Volume 796, Issue 1, pp 121–130 | Cite as

Life-history responses to environmental change revealed by resurrected rotifers from a historically polluted lake

  • Naomi L. ZweerusEmail author
  • Stefan Sommer
  • Diego Fontaneto
  • Arpat Ozgul


Life-history adaptations to environmental change can be studied retrospectively in organisms that produce dormant propagules using methods of resurrection ecology. Here, we investigated such responses in a planktonic freshwater rotifer, Brachionus calyciflorus. We resurrected 14 clonal lineages from resting eggs extracted from three distinct sediment layers—representing periods of high, medium and low copper pollution—of a previously contaminated lake (Lake Orta, Italy). We exposed the resurrected clones to four copper concentrations over 14 days and recorded population densities at 48 h intervals. If the original populations in Lake Orta had adapted to the changing pollution levels, we expected to find demographic evidence of this adaptation in the resurrected lineages. However, we found high clonal variation in population-growth dynamics, which was more pronounced within than between pollution periods. Moreover, intrinsic population growth rates (r) increased chronologically. As such, the results did not reveal signs of adaptive evolution. Furthermore, we found that lineages from the period of medium copper pollution invested less into sexual reproduction than lineages from the other periods. By using this bio-demographic perspective, our analysis of resurrected rotifers provides insights into the life-history responses of an aquatic invertebrate in an ever-changing environment.


Brachionus Resurrection ecology Adaptation Population dynamics Copper pollution 



We thank Piero Guilizzoni, Andrea Lami and Stefano Gerli from the Institute of Ecosystem Study (Verbania Pallanza, Italy) for collecting and dating the sediment cores. This research was supported by grants to AO from the European Research Council (#337785) and the Swiss National Science Foundation (#31003A_146445).


  1. Bates, D., M. Maechler, B. Bolker & S. Walker, 2014. lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7.
  2. Baudo, R. & M. Beltrami, 2001. Chemical composition of Lake Orta sediments. Journal of Limnology 60: 213–236.Google Scholar
  3. Birky, C. W., 1967. Studies on the physiology and genetics of the rotifer, Asplanchna. III. Results of outcrossing, selfing, and selection. Journal of Experimental Zoology 164: 105–115.CrossRefPubMedGoogle Scholar
  4. Bonacina, C., 2001a. Lake Orta: the undermining of an ecosystem. Journal of Limnology 60: 53–59.CrossRefGoogle Scholar
  5. Bonacina, C., 2001b. Has Lake Orta completely recovered from its heavy polluted condition? A seventy years long history. Journal of Limnology 60: 285–287.Google Scholar
  6. Bonacina, C., 2001c. Publications on Lake Orta arranged in chronological order. Journal of Limnology 60: 289–300.Google Scholar
  7. Bonacina, C. & A. Pasteris, 2001. Zooplankton of Lake Orta after liming: an eleven years study. Journal of Limnology 60: 101–109.Google Scholar
  8. Bonacina, C. & R. Baudo, 2001. Lake Orta: a case study (part 1). Journal of Limnology 60: 50–52.Google Scholar
  9. Brendonck, L. & L. De Meester, 2003. Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia 491: 65–84.CrossRefGoogle Scholar
  10. Calderoni, A. & G. A. Tatari, 2001. Evolution of water chemistry of Lake Orta after liming. Journal of Limnology 60: 69–78.CrossRefGoogle Scholar
  11. Calderoni, A., R. Mosello & D. Ruggiu, 1992. Sixty years of limnology on Lago d’Orta: a case history of recovery from heavy pollution. Memorie dell’Istituto Italiano di Idrobiologia 50: 201–223.Google Scholar
  12. Carmona, M. J., N. Dimas-Flores, E. M. García-Roger & M. Serra, 2009. Selection of low investment in sex in a cyclically parthenogenetic rotifer. Journal of Evolutionary Biology 22: 1975–1983.CrossRefPubMedGoogle Scholar
  13. De Meester, L., 1993. Inbreeding and outbreeding depression in Daphnia. Oecologia 96: 80–84.CrossRefPubMedGoogle Scholar
  14. De Meester, L., J. Mergeay, H. Michels & E. Decaestecker, 2007. Reconstructing microevolutionary dynamics from layered egg banks. In Alekseev, V. R., B. De Stasio & J. J. Gilbert (eds), Diapause in Aquatic Invertebrates: Theory and Human Use. Springer, Dordrecht: 159–166.CrossRefGoogle Scholar
  15. Decaestecker, E., S. Gaba, J. A. M. Raeymaekers, R. Stoks, L. Van Kerckhoven, D. Ebert & L. De Meester, 2007. Host-parasite ‘Red Queenʼ dynamics archived in pond sediment. Nature 450: 870–873.CrossRefPubMedGoogle Scholar
  16. García-Roger, E. M., M. Serra & M. J. Carmona, 2014. Bet-hedging in diapausing egg hatching of temporary rotifer populations – a review of models and new insights. International Review of Hydrobiology 99: 96–106.CrossRefGoogle Scholar
  17. Geerts, A. N., J. Vanoverbeke, B. Vanschoenwinkel, W. Van Doorslaer, H. Feuchmayr, D. Atkinson, B. Moss, T. A. Davidson, C. D. Sayer & L. De Meester, 2015. Rapid evolution of thermal tolerance in the water flea Daphnia. Nature Climate Change 5: 665–668.CrossRefGoogle Scholar
  18. Gilbert, J. J. & T. Schröder, 2007. Intraclonal variation in propensity for mixis in several rotifers: variation among females and with maternal age. Hydrobiologia 593: 121–128.CrossRefGoogle Scholar
  19. Green, P. & C. J. MacLeod, 2016. SIMR: an R package for power analysis of generalized linear mixed models by simulation. Methods in Ecology and Evolution 7: 493–498.CrossRefGoogle Scholar
  20. Hairston Jr., N. G., 1996. Zooplankton egg banks as biotic reservoirs in changing environments. Limnology and Oceanography 41: 1087–1092.CrossRefGoogle Scholar
  21. Hairston Jr., N. G., W. Lampert, C. E. Cáceres, C. L. Holtmeier, L. J. Weider, U. Gaedke, J. M. Fischer, J. A. Fox & D. M. Post, 1999. Rapid evolution revealed by dormant eggs. Nature 401: 446.CrossRefGoogle Scholar
  22. Halbach, U., 1970. Die Ursachen der Temporalvariation von Brachionus calyciflorus Pallas (Rotatoria). Oecologia 4: 262–318.CrossRefPubMedGoogle Scholar
  23. Havens, K. E., 1994. Structural and functional responses of a freshwater plankton community to acute copper stress. Environmental Pollution 86: 259–266.CrossRefPubMedGoogle Scholar
  24. Hendry, A. P. & M. T. Kinnison, 1999. Perspective: the pace of modern life: measuring rates of contemporary microevolution. Evolution 53: 1637–1653.CrossRefPubMedGoogle Scholar
  25. Hertel, E. W., 1942. Studies on vigor in the rotifer Hydatina senta. Physiological Zoology 15: 304–324.CrossRefGoogle Scholar
  26. Innes, D. J., 1989. Genetics of Daphnia obtusa: genetic load and linkage analysis in a cyclical parthenogen. Journal of Heredity 80: 6–10.CrossRefGoogle Scholar
  27. Janssen, C. R., F. Rodrigo & G. Persoone, 1993. Ecotoxicological studies with the freshwater rotifer Brachionus calyciflorus, I: conceptual framework and applications. Hydrobiologia 255: 21–32.CrossRefGoogle Scholar
  28. Janssen, C. R., G. Persoone & T. W. Snell, 1994. Cyst-based toxicity tests. VIII. Short-chronic toxicity tests with the freshwater rotifer Brachionus calyciflorus. Aquatic Toxicology 28: 243–258.CrossRefGoogle Scholar
  29. Karlen, C., I. O. Wallinder, D. Heijerick & C. Leygraf, 2002. Runoff rates, chemical speciation and bioavailability of copper released from naturally patinated copper. Environmental Pollution 120: 691–700.CrossRefPubMedGoogle Scholar
  30. Kerfoot, W. C., J. A. Robbins & L. J. Weider, 1999. A new approach to historical reconstruction: combining descriptive and experimental paleolimnology. Limnology and Oceanography 44: 1232–1247.CrossRefGoogle Scholar
  31. King, C. E. & M. Serra, 1998. Seasonal variation as a determinant of population structure in rotifers reproducing by cyclical parthenogenesis. Hydrobiologia 387/388: 361–372.CrossRefGoogle Scholar
  32. Lopes, I., D. J. Baird & R. Ribeiro, 2004. Genetic determination of tolerance to lethal and sublethal copper concentrations in field populations of Daphnia longispina. Archives of Environmental Contamination and Toxicology 46: 43–51.CrossRefPubMedGoogle Scholar
  33. Lynch, M. & H.-W. Deng, 1994. Genetic slippage in response to sex. The American Naturalist 144: 242–261.CrossRefGoogle Scholar
  34. Medina, M. H., J. A. Correa & C. Barata, 2007. Micro-evolution due to pollution: possible consequences for ecosystem responses to toxic stress. Chemosphere 67: 2105–2114.CrossRefPubMedGoogle Scholar
  35. Orsini, L., K. Schwenk, L. De Meester, J. K. Colbourne, M. E. Pfrender & L. J. Weider, 2013. The evolutionary time machine: using dormant propagules to forecast how populations can adapt to changing environments. Trends in Ecology & Evolution 28: 274–282.CrossRefGoogle Scholar
  36. Ozgul, A., D. Z. Childs, M. K. Oli, K. B. Armitage, D. T. Blumstein, L. E. Olson, S. Tuljapurkar & T. Coulson, 2010. Coupled dynamics of body mass and population growth in response to environmental change. Nature 466: 482–485.CrossRefPubMedGoogle Scholar
  37. Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar & R Core Team, 2015. nlme: linear and nonlinear mixed effects models. R package version 3.1-120,
  38. Piscia, R., P. Guilizzoni, D. Fontaneto, D. A. L. Vignati, P. G. Appleby & M. Manca, 2012. Dynamics of rotifer and cladoceran resting stages during copper pollution and recovery in a subalpine lake. Annales de Limnologie - International Journal of Limnology 48: 151–160.CrossRefGoogle Scholar
  39. Piscia, R., S. Tabozzi, R. Bettinetti, L. Nevalainen & M. M. Manca, 2016. Unexpected increases in rotifer resting egg abundances during the period of contamination of Lake Orta. Journal of Limnology 75(s2): 76–85.Google Scholar
  40. Pourriot, R. & T. W. Snell, 1983. Resting eggs in rotifers. Hydrobiologia 104: 213–224.CrossRefGoogle Scholar
  41. Pradeep, V., S. W. Van Ginkel, S. Park, T. Igou, C. Yi, H. Fu, R. Johnston, T. Snell & Y. Chen, 2015. Use of copper to selectively inhibit Brachionus calyciflorus (predator) growth in Chlorella kessleri (prey) mass cultures for algae biodiesel production. International Journal of Molecular Sciences 16: 20674–20684.CrossRefPubMedPubMedCentralGoogle Scholar
  42. R Core Team, 2015. R: a language and environment for statistical computing, Vienna. Austria, R Foundation for Statistical Computing.
  43. Reznick, D., 1985. Costs of reproduction: an evaluation of the empirical evidence. Oikos 44: 257–267.CrossRefGoogle Scholar
  44. Reznick, D. N., F. H. Shaw, F. H. Rodd & R. G. Shaw, 1997. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275: 1934–1937.CrossRefPubMedGoogle Scholar
  45. Schoener, T. W., 2011. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331: 426–429.CrossRefPubMedGoogle Scholar
  46. Snell, T. W. & B. L. Garman, 1986. Encounter probabilities between male and female rotifers. Journal of Experimental Marine Biology and Ecology 97: 221–230.CrossRefGoogle Scholar
  47. Snell, T. W. & B. D. Moffat, 1992. A 2-d life cycle test with the rotifer Brachionus calyciflorus. Environmental Toxicology and Chemistry 11: 1249–1257.CrossRefGoogle Scholar
  48. Snell, T. W. & C. R. Janssen, 1995. Rotifers in ecotoxicology: a review. Hydrobiologia 313/314: 231–247.CrossRefGoogle Scholar
  49. Sommer, S., S. Nandini, S. S. S. Sarma, A. Ozgul & D. Fontaneto, 2016. Rotifers in Lake Orta: a potential ecological and evolutionary model system. Journal of Limnology 75(s2): 67–75.Google Scholar
  50. Spaak, P. & B. Keller, 2004. No evidence for adaptive micro-evolution to a decrease in phosphorus-loading of a Daphnia population inhabiting a pre-alpine lake. Hydrobiologia 526: 15–21.CrossRefGoogle Scholar
  51. Stelzer, C. P., 2005. Evolution of rotifer life histories. Hydrobiologia 546: 335–346.CrossRefGoogle Scholar
  52. Tortajada, A. M., M. J. Carmona & M. Serra, 2009. Does haplodiploidy purge inbreeding depression in rotifer populations? PloS ONE 4: e8195.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Wallace, R. L., 2002. Rotifers: exquisite metazoans. Integrative and Comparative Biology 42: 660–667.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Naomi L. Zweerus
    • 1
    Email author
  • Stefan Sommer
    • 1
  • Diego Fontaneto
    • 2
  • Arpat Ozgul
    • 1
  1. 1.Department of Evolutionary Biology and Environmental StudiesUniversity of ZürichZürichSwitzerland
  2. 2.National Research CouncilInstitute of Ecosystem StudyVerbania PallanzaItaly

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