© 1999 Macmillan Magazines Ltd Lake ecosystems Rapid evolution revealed by dormant eggs Natural selection can lead to rapid changes in organisms, which can in turn influence ecosystem processes 1 . A key factor in the functioning of lake ecosystems is the rate at which primary producers are eaten, and major consumers, such as the zooplankton Daphnia 2 , can be subject to strong selection pressures when phytoplankton assemblages change. Lake Constance in central Europe experienced a period of eutrophication (the biological effects of an input of plant nutri- ents) during the 1960s–70s 3 , which caused an increase 4 in the abundance of nutrition- ally poor or even toxic 5 cyanobacteria. By hatching long-dormant eggs 6 of Daphnia galeata found in lake sediments, we show that the mean resistance of Daphnia geno- types to dietary cyanobacteria increased sig- nificantly during this eutrophication. This rapid evolution of resistance has implica- tions for the ways that ecosystems respond to nutrient enrichment through the impact of grazers on primary production. Genetically distinct 3 Daphnia galeata clones were collected as diapausing eggs from sediments of known age 3 obtained from a core taken from Lake Constance in 1997. Parthenogenetic lines were main- tained for each clone for at least 40 genera- tions to minimize maternal effects. We tested 32 clones from three sediment ages for their resistance to dietary cyanobacteria: 12 clones from 1962–64 and 1969–71 (before and just after the appearance of cyanobacteria; Fig. 1), 10 clones from 1978–80 (peak eutrophication), and 10 clones from 1992–94 and 1995–97 (when the period of eutrophication had passed). Resistance to cyanobacteria was mea- sured as the effect of diet on the somatic juvenile growth rate (g j ) of Daphnia 7 : g j ǃ[ln(W m )ǁln(W n )]/t, where W m and W n are the masses of mature and neonate Daph- nia, respectively, and t is the development period. For each clone, g j was measured for animals fed two different diets (supplied at 1 mg carbon per litre): one diet (g j, poor ) con- tained a mixture of a toxic cyanobacterium (Microcystis aeruginosa, 20% by carbon con- tent) and a high-quality algal resource (Scenedesmus obliquus, 80% by carbon con- tent); the other diet (g j, good ) contained only Scenedesmus. Microcystis was originally iso- lated from Lake Constance in 1972, is toxic to Daphnia pulicaria 8 and contains high con- centrations of microcystin-LR hepatotoxin, whereas Scenedesmus promotes growth and reproduction in Daphnia 6 . Microcystis and Scenedesmus were fed to Daphnia as single cells of similar size (4.2 Ȗm). For each clone, g j, good and g j, poor were measured separately by using three replicate flow-through vessels (5–17 individuals each) with food levels in excess of growth- limiting concentrations 9 . Because there was variation among clones in g j, good (likelihood ratio test, ȡ 2 ǃ120.1, d.f.ǃ1, P<<0.0001), resistance to dietary cyanobacteria was standardized as the growth-rate reduction, R, which is the fractional reduction in g j on poor food relative to that on good food: Rǃ(g j, good ǁg j, poor )/g j, good . The Daphnia population evolved an increased ability to cope with a diet con- taining cyanobacteria (Fig. 2). Genotypes from both 1978–80 and the 1990s exhibit lower growth-rate reduction than those from 1962–64 and 1969–71 (ANOVA planned contrasts, Fǃ10.3, d.f.ǃ1, 29, Pǃ0.003, and Fǃ11.9, d.f.ǃ1, 29, Pǃ0.002, respectively). The rapid response observed during 1969–80 is attributable entirely to a reduction in genetic variance (likelihood ratio test, ȡ 2 ǃ8.24, d.f.ǃ1, Pǃ0.002). There was a broad range of Daphnia genotypes of different growth-rate reductions in the lake during 1962–64 and 1969–71, but the genotypes that were most heavily affected by dietary cyanobacteria were virtually eliminated within ten years of continued summertime exposure to cyanobacteria. The mean resistance of Daphnia to cyanobacteria was unchanged between 1978–80 and the 1990s (ANOVA planned contrast, Fǃ0.06, d.f.ǃ1, 29, Pǃ0.82). However, the variance of growth-rate reductions was greater in the 1990s than in 1978–80 (likelihood ratio test, ȡ 2 ǃ4.72, d.f.ǃ1, Pǃ0.015), perhaps as a result of the water column being reinvaded by ani- mals hatching from the dormant egg bank 6 . These short-term evolutionary changes may significantly affect the course of ecosystem change. Greater abundance of cyanobacteria during eutrophication is typ- ically considered to be a response to increased nutrient inputs 10 . However, rapid adaptive evolution in grazing zooplankton populations may be an important feedback mechanism that is critical to understanding the net effect of eutrophication on primary producers in lakes. Nelson G. Hairston Jr*, Winfried Lampert†, Carla E. Cáceres‡, Cami L. Holtmeier*, Lawrence J. Weider†, Ursula Gaedke§, Janet M. Fischer*, Jennifer A. Fox*, David M. Post* *Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853, USA e-mail: ngh1@cornell.edu †Max-Planck-Institut für Limnologie, Postfach 165, 24302 Plön, Germany ‡Center for Aquatic Ecology, Illinois Natural History Survey, Champaign, Illinois 61820, USA §Limnologisches Institut, Universität Konstanz, 78457 Konstanz, Germany 1. Thompson, J. N. Trends Ecol. Evol. 13, 329–332 (1998). 2. Carpenter, S. R. et al. in Comparative Analyses of Ecosystems: Patterns, Mechanisms, and Theories (eds Cole, J., Lovett, G. & Findlay, S.) 67–96 (Springer, New York, 1991). 3. Weider, L. J. et al. Proc. R. Soc. Lond. B 264, 1613–1618 (1997). 4. Kümmerlin, R. Arch. Hydrobiol. Spec. Issue Adv. Limnol. 53, 109–117 (1998). 5. Lampert, W. Mem. Ist. Ital. Idrobiol. 45, 143-192 (1987). 6. Hairston, N. G. Jr Limnol. Oceanogr. 41, 1087–1092 (1996). 7. Lampert, W. Int. Ver. Theor. Angew. Limnol. Verh. 21, 1436–1440 (1981). 8. Lampert, W. & Trubetskova, I. Funct. Ecol. 10, 631–635 (1996). 9. Lampert, W., Schmitt, R. D. & Muck, P. Bull. Mar. Sci. 43, 620–640 (1988). 10.Smith, V. H. in Successes, Limitations, and Frontiers in Ecosystem Science (eds Pace, M. L. & Groffman, P. M.) 7–49 (Springer, New York, 1998). brief communications 446 NATURE | VOL 401 | 30 SEPTEMBER 1999 | www.nature.com 0 1 2 3 4 1960 1970 1980 Year 1990 2000 Cyanobacteria density (cm 3 per m 2 ) Figure 1 The summer density of planktonic cyanobacteria (total cell volume) in Lake Constance 4 . Filled circles, years when cyanobacteria were recorded as extremely rare; thick bars, sedi- ment ages from which dormant Daphnia eggs were studied; the dashed line connects time periods analysed together. Sediment age 0 0.1 0.2 0.3 0.4 0.5 Growth rate reduction 1978-80 1995-97 and 1992-94 high resistance low resistance 1969-71 and 1962-64 Figure 2 Resistance of Daphnia genotypes to dietary cyanobac- teria. Data points represent estimates of growth-rate reduction for individual clones. Correction Food contamination by PCBs and dioxins A. Bernard, C. Hermans, F. Broeckaert, G. De Poorter, A. De Cock, G. Houins Nature 401, 231–232 (1999) The average ratio of polychlorinated biphenyls (PCBs) to polychlorodibenzodi- oxins (PCDDs) or polychlorodibenzofurans (PCDFs) in samples of contaminated feed- stuff, chicken meat and eggs (Fig. 1b) was incorrect as published (see fourth para- graph): the average ratio of PCB:PCDD/F was about 50,000:1 (not 22,000: 1). The conclusions of our report are unchanged.