Skip to main content Accessibility help

Dynamics of rotifer and cladoceran resting stages during copper pollution and recovery in a subalpine lake

  • Roberta Piscia (a1), Piero Guilizzoni (a1), Diego Fontaneto (a2), Davide A.L. Vignati (a3), Peter G. Appleby (a4) and Marina Manca (a1)...

Despite their ecological importance and ability to react to environmental changes, including pollution, monogonont rotifers have never been used in palaeolimnological studies because they do not leave subfossil remains. In this study, we tested the possibility of using rotifer resting eggs as a proxy for reconstruction of changes in biodiversity during chronic copper pollution and recovery of a deep sudalpine lake (Lake Orta, Italy). The lake was selected owing to a rich history of previous studies that explored species-specific responses to environmental stressors. Rotifer-based results were compared with those on ephippia and on previously investigated Cladocera subfossil remains. Responses of Rotifera resting eggs to environmental changes were clear and consistent with those previously observed on Cladocera. The abundance of resting eggs increased during pollution, and new morphotypes appeared in addition to those already present. However, overall diversity decreased sharply, as a few morphotypes became dominant. Resting eggs of Brachionus calyciflorus as old as ca. 100 years were still fully viable; viability was not affected by toxic conditions of the environment in which the eggs were produced. Over a period of ca. 80 years, all resting eggs of B. calyciflorus belonged to a single clone, the most widely distributed one in North America. Cladocera ephippia started to accumulate later and at a lower level of abundance than rotifer resting eggs. Overall, Cladocera ephippia were, however, less effective than rotifers in tracing lake historical changes. The results point out at the great potential of using rotifer resting eggs in palaeolimnological reconstructions.

Corresponding author
*Corresponding author:
Hide All
[1]Appleby, P.G., 2002. Chronostratigraphic techniques in recent sediments. In: Last, W.M. and Smol, I.P. (eds.), Tracking Environmental Change Using Lake Sediments. Volume 1. Springer Netherlands, 171223.
[2]Appleby, P.G. and Oldfield, F., 1978. The calculation of lead-210 dates assuming a constant rate of supply of unsupported 210Pb to the sediments. Catena, 5, 18.
[3]Appleby, P.G., Nolan, P.J., Gifford, D.W., Godfrey, M.J., Oldfield, F., Anderson, N.J. and Battarbee, R.W., 1986. 210Pb dating by low background gamma counting. Hydrobiologia, 141, 2127.
[4]Appleby, P.G., Richardson, N. and Nolan, P.J., 1992. Self-absorption corrections for well-type germanium detectors. Nucl. Instrum.  Methods B, 71, 228223.
[5]Bachiorri, A., Rossi, V. and Menozzi, P., 1991. Differences in demographic parameters among electrophoretric clones of Daphnia obtusa Kurz (Crustacea, Cladocera). Hydrobiologia, 225, 263268.
[6]Bonacina, C. and Baudo, R. (Guests eds), 2001. Lake Orta: a case study. J. Limnol., 60, 166 p.
[7]Brett, M.T., 1989. Zooplankton communities and acidification processes: a review. Water Air Soil Pollut., 44, 387414.
[8]Cáceres, C.E., 1998. Interspecific variation in the abundance, production, and emergence of Daphnia diapausing eggs. Ecology, 79, 16991710.
[9]Calderoni, A., Mosello, R., Quirci, A. and de Bernardi, R., 1990. Recovery of Lake Orta by liming. Proceedings of theVII International Lime Congress, Rome, September 13–14, 1990, 157171.
[10]Calderoni, A. and Tartari, G.A., 2001. Evolution of the water chemistry of Lake Orta after liming. J. Limnol., 60, 6978.
[11]Cattaneo, A., Asioli, A., Comoli, P. and Manca, M., 1998. Organisms’ response in a chronically polluted lake supports hypothesized link between stress and size. Limnol. Oceanogr., 43, 19381943.
[12]Chick, J.H., Levchuk, A.P., Medley, K.A. and Havel, J.H., 2010. Underestimation of rotifer abundance, a much greater problem than previously appreciated. Limnol. Oceanogr. Methods, 44, 7987.
[13]Dean, W.E. Jr., 1974. Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition: comparison with other methods. J. Sed. Petrol., 44, 242248.
[14]Duggan, I.C., Green, J.D. and Russell, J.S., 2002. Rotifer resting egg densities in lakes of different trophic state, and their assessment using emergence and egg counts. Arch. Hydrobiol., 153, 409420.
[15]Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R., 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Mar. Biotechnol., 3, 294299.
[16]Frey, D.G., 1986. Cladocera analysis. In: Berglund, B.E. (ed.), Handbook of Holocene Paleoecology and Paleohydrobiology, Wiley and Sons, New York, 667692.
[17]Fu, Y., 1991. Studies on genetic variations of the rotifer Brachionus plicatilis O.F. Müller. PhD Thesis, Nagasaki University, 144.
[18]Gama-Flores, J.L. and Castellanos-Paez, M.E., 2007. Effect of pulsed exposure to heavy metals (copper and cadmium) on some population variables of Brachionus calyciflorus Pallas (Rotifera: Brachionide: Monogononta). Hydrobiologia, 593, 201208.
[19]Gilbert, J.J., 1974. Dormancy in rotifers. Trans. Am. Microsc. Soc., 93, 490512.
[20]Gilbert, J.J., 1980. Female polymorphism and sexual reproduction in the rotifer Asplanchna: evolution of their relationship and control by dietary tocopherol. Am. Nat., 116, 409431.
[21]Gilbert, J.J., 1995. Structure, development and induction of a new diapause stage in rotifers. Freshwat. Biol., 34, 263270.
[22]Gilbert, J.J. and Schröder, T., 2004. Rotifers from diapausing, fertilized eggs: unique features and emergence. Limnol. Oceanogr., 49, 13411354.
[23]Gilbert, J.J. and Walsh, E.J., 2005. Brachionus calyciflorus is a species complex: mating behavior and genetic differentiation among four geographically isolated strains. Hydrobiologia, 546, 257265.
[24]Hairston, N.G. Jr., 1996. Zooplankton egg banks as biotic reservoirs in changing environments. Limnol. Oceanogr., 41, 10871092.
[25]Hairston, N.G. Jr., Van Brunt, R.A., Kearns, C.M. and Engstrom, D.R., 1995. Age and survivorship of diapausing eggs in a sediment egg bank. Ecology, 76, 17061711.
[26]Havas, M., Woodfine, D.G., Lutz, P., Young, K., MacIsaac, H.I. and Hutchinson, T.C., 1995. Biological recovery of two previously acidified, metal-contaminated lakes near Sudbury Ontario, Canada. Water Air Soil Pollut., 85, 791796.
[27]Jeppesen, E., Jensen, J.P., Lauridsen, T.L., Amsinck, S.L., Christoffersen, K., Søndergaard, M. and Mitchell, S.F., 2003. Sub-fossils of cladocerans in the surface sediment of 135 lakes as proxies for community structure of zooplankton, fish abundance and lake temperature. Hydrobiologia, 491, 321330.
[28]Kerfoot, W.C., Robbins, J.A. and Weider, L.J., 1999. A new approach to historical reconstruction: combining descriptive and experimental paleolimnology. Limnol. Oceanogr., 44, 12321247.
[29]Kirk, K.L., 1997. Life-history responses to variable environments: starvation and reproduction in planktonic rotifers. Ecology, 78, 434441.
[30]Koste, W., 1978. Rotatoria. Die Rädertiere Mitteleuropas. Ein Bestimmungswerk, begründet von Max Voigt. Überordnung Monogononta 2. Gebrüder Borntraeger, Berlin, Stuttgart, 673.
[31]Li, L., Niu, C. and Ma, R., 2010. Rapid temporal succession identified by COI of the rotifer Brachionus calyciflorus Pallas in Xihai Pond,Beijing, China, in relation to ecological traits. J. Plankton Res., 32, 951959.
[32]Manca, M. and Comoli, P., 1995. Temporal variations of fossils Cladocera in the sediments ofLake Orta (N. Italy) over the last 400 years. J. Paleolimnol., 14, 113122.
[33]Morabito, G., 2001. Six years (1992–1997) evolution of phytoplankton communities inLake Orta (N. Italy) after the recovery by liming. Lakes Reserv. Res. Manage. 6, 305312.
[34]Nevalainen, L., Luoto, T.P., Levine, S. and Manca, M., 2011. Paleolimnological evidence for increased sexual reproduction in chydorids (Chydoridae, Cladocera) under environmental stress. J. Limnol., 70, 255262.
[35]Nipkow, F., 1961. Die Rädertiere im Plankton des Zürichsees und ihre Entwicklungsphasen. Schweiz Z. Hydrol., 23, 398461.
[36]Onbé, T., 1978. Sugar flotation method for sorting the resting eggs of marine Cladocerans and Copepods from sea-bottom sediment. Bull. Jpn. Soc. Fish. Oceanogr., 44, 1411.
[37]Pielou, E.C., 1966. Species-diversity and pattern-diversity in the study of ecological succession. J. Theor. Biol., 10, 370383.
[38]Ponti, B., Piscia, R., Bettinetti, R. and Manca, M., 2010. Long-term adaptation of Daphnia to toxic environment in Lake Orta: the effects of short-term exposure to copper and acidification. J. Limnol., 69, 217224.
[39]Rose, N.L., Morley, D., Appleby, P.G., Battarbee, R.W., Alliksaar, T., Guilizzoni, P., Jeppesen, E., Korhola, A., Punning, J.-M., 2011. Sediment accumulation rates in European lakes since AD 1850: trends, reference conditions and exceedence. J. Paleolimnol., 45, 447468.
[40]Sarmaja-Korjonen, K., 2004. Chydorid ephippia as indicators of past environmental changes – a new method. Hydrobiologia, 526, 129136.
[41]Shannon, C.E. and Wiener, W., 1963. The Mathematical Theory of Communities. University of Illinois Press, Urbana, IL, USA, 117.
[42]Steinberg, A., Ejsmont-Karabin, J., Muirhead, J.R. and MacIsaac, H.J., 2009. Spatial and temporal stability of rotifer communities. Hydrobiologia, 624, 107114.
[43]Sudzuki, M., 1964. New systematical approach to the Japanese planktonic Rotatoria. Hydrobiologia, 23, 1124.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Annales de Limnologie - International Journal of Limnology
  • ISSN: 0003-4088
  • EISSN: 2100-000X
  • URL: /core/journals/annales-de-limnologie-international-journal-of-limnology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Type Description Title
Online Material

OLM - limn110024 - 48(2) 2012 p.151 - Dynamics of rotifer and cladoceran...
Appendix 1

 PDF (174 KB)
174 KB


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed