Small lakes and ponds occupy an enormous surface area of inland freshwater and represent an important terrestrial-water interface. Disturbances caused by extreme weather events can have substantial effects on these ecosystems. Here, we analysed the dynamics of nutrients and the entire plankton community in two flood events and afterwards, when quasi-stable conditions were established, to investigate the effect of such disturbances on a small forest pond. We show that floodings result in repeated washout of resident organisms and hundredfold increases in nutrient load. Despite this, the microbial community recovers to a predisturbance state within two weeks of flooding through four well-defined succession phases. Reassembly of phytoplankton and especially zooplankton takes up to two times longer and features repetitive and adaptive patterns. Release of dissolved nutrients from the pond is associated with inflow rates and community recovery, and returns to predisturbance levels before microbial compositions recover. Our findings shed light on the mechanisms underlying functional resilience of small waterbodies and are relevant to global change-induced increases in weather extremes.

Berlin Brandenburg Institute of Advanced Biodiversity Research Berlin Germany

Department of Experimental Limnology Leibniz Institute of Freshwater Biology and Inland Fisheries Stechlin Germany

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Institute of Biochemistry and Biology Potsdam University Potsdam Germany

Institute of Hydrobiology Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

See more in PubMed

Battin, T. J. et al. Biophysical controls on organic carbon fluxes in fluvial networks. Nat. Geosci. 1, 95–100 (2008). DOI

Tranvik, L. J. et al. Lakes and reservoirs as regulators of carbon cycling and climate. Limnol. Oceanogr. 54, 2298–2314 (2009). DOI

Raymond, P. A. et al. Global carbon dioxide emissions from inland waters. Nature 503, 355–359 (2013). PubMed DOI

Downing, J. A. Emerging global role of small lakes and ponds: little things mean a lot. Limnetica 29, 9–24 (2010). DOI

Bastviken, D., Tranvik, L. J., Downing, J. A., Crill, P. M. & Enrich-Prast, A. Freshwater methane emissions offset the continental carbon sink. Science 331, 50–50 (2011). PubMed DOI

Fairchild, G. W. & Velinsky, D. J. Effects of small ponds on stream water chemistry. Lake Reserv. Manag. 22, 321–330 (2006). DOI

Yin, C. & Shan, B. Multipond systems: a sustainable way to control diffuse phosphorus pollution. AMBIO 30, 369–375 (2001). PubMed DOI

Stanley, E. H. & Doyle, M. W. A geomorphic perspective on nutrient retention following dam removal: geomorphic models provide a means of predicting ecosystem responses to dam removal. BioScience 52, 693–701 (2002). DOI

Downing, J. A., Cherrier, C. T. & Fulweiler, R. W. Low ratios of silica to dissolved nitrogen supplied to rivers arise from agriculture not reservoirs. Ecol. Lett. 19, 1414–1418 (2016). PubMed DOI

Dickman, M. Some effects of lake renewal on phytoplankton productivity and species composition. Limnol. Oceanogr. 14, 660–666 (1969). DOI

Madsen, H., Lawrence, D., Lang, M., Martinkova, M. & Kjeldsen, T. R. Review of trend analysis and climate change projections of extreme precipitation and floods in Europe. J. Hydrol. 519, 3634–3650 (2014). DOI

Clark, J. M. et al. The importance of the relationship between scale and process in understanding long-term DOC dynamics. Sci. Total Environ. 408, 2768–2775 (2010). PubMed DOI

Vystavna, Y., Hejzlar, J. & Kopáček, J. Long-term trends of phosphorus concentrations in an artificial lake: socio-economic and climate drivers. PLoS ONE 12, e0186917 (2017). PubMed DOI PMC

Reynolds, C. S. Phytoplankton assemblages and their periodicity in stratifying lake systems. Ecography 3, 141–159 (1980). DOI

Sommer, U., Gliwicz, Z. M., Lampert, W. & Duncan, A. The PEG-model of seasonal succession of planktonic events in fresh waters. Arch. Hydrobiol. 106, 433–471 (1986). DOI

Kundzewicz, Z. W. et al. Differences in flood hazard projections in Europe—their causes and consequences for decision making. Hydrol. Sci. J. 62, 1–14 (2017).

Arnell, N. W. & Gosling, S. N. The impacts of climate change on river flood risk at the global scale. Clim. Change 134, 387–401 (2016). DOI

Hirabayashi, Y. et al. Global flood risk under climate change. Nat. Clim. Change 3, 816–821 (2013). DOI

Lynch, L. M. et al. River channel connectivity shifts metabolite composition and dissolved organic matter chemistry. Nat. Commun. 10, 459 (2019). PubMed DOI PMC

Pimm, S. L. The complexity and stability of ecosystems. Nature 307, 321–326 (1984). DOI

Shade, A. et al. Lake microbial communities are resilient after a whole-ecosystem disturbance. ISME J. 6, 2153–2167 (2012). PubMed DOI PMC

Holling, C. S. Resilience and stability of ecological systems. Annu. Rev. Ecol. Evol. Syst. 4, 1–23 (1973). DOI

Holling, C. S. & Gunderson, L. H. in Panarchy Synopsis: Understanding Transformations in Human and Natural Systems (eds Gunderson, L. H. & Holling, C. S.) 25–62 (Island Press, 2002).

Gabaldón, C. et al. Repeated flood disturbance enhances rotifer dominance and diversity in a zooplankton community of a small dammed mountain pond. J. Limnol. 76, 13 (2016).

Porcal, P. & Kopáček, J. Photochemical degradation of dissolved organic matter reduces the availability of phosphorus for aquatic primary producers. Chemosphere 193, 1018–1026 (2018). PubMed DOI

Macarthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377–385 (1967). DOI

Newton, R. J., Kent, A. D., Triplett, E. W. & McMahon, K. D. Microbial community dynamics in a humic lake: differential persistence of common freshwater phylotypes. Environ. Microbiol. 8, 956–970 (2006). PubMed DOI

Neuenschwander, S. M., Ghai, R., Pernthaler, J. & Salcher, M. M. Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria. ISME J. 12, 185–198 (2018). PubMed DOI

Cabello-Yeves, P. J. et al. Reconstruction of diverse verrucomicrobial genomes from metagenome datasets of freshwater reservoirs. Front. Microbiol. 8, 2131 (2017). PubMed DOI PMC

Reznick, D., Bryant, M. J. & Bashey, F. r- and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83, 1509–1520 (2002). DOI

Mac Arthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 1967).

Šimek, K. et al. A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring. Limnol. Oceanogr. 59, 1477–1492 (2014). DOI

Logue, J. B., Mouquet, N., Peter, H. & Hillebrand, H. Empirical approaches to metacommunities: a review and comparison with theory. Trends Ecol. Evol. 26, 482–491 (2011). PubMed DOI

Shabarova, T. et al. Bacterial community structure and dissolved organic matter in repeatedly flooded subsurface karst water pools. FEMS Microbiol. Ecol. 89, 111–126 (2014). PubMed DOI

Shabarova, T., Widmer, F. & Pernthaler, J. Mass effects meet species sorting: transformations of microbial assemblages in epiphreatic subsurface karst water pools. Environ. Microbiol. 15, 2476–2488 (2013). PubMed DOI

Jones, S. E. et al. Typhoons initiate predictable change in aquatic bacterial communities. Limnol. Oceanogr. 53, 1319–1326 (2008). DOI

Shade, A. et al. Fundamentals of microbial community resistance and resilience. Front. Microbiol. 3, 417 (2012). PubMed DOI PMC

Hahn, M. W. Isolation of strains belonging to the cosmopolitan Polynucleobacter necessarius cluster from freshwater habitats located in three climatic zones. Appl. Environ. Microb. 69, 5248–5254 (2003). DOI

Salcher, M. M., Neuenschwander, S. M., Posch, T. & Pernthaler, J. The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign. ISME J. 9, 2442–2453 (2015). PubMed DOI PMC

Vuono, D. C. et al. Disturbance and temporal partitioning of the activated sludge metacommunity. ISME J. 9, 425–435 (2014). PubMed DOI PMC

Shabarova, T. et al. Distribution and ecological preferences of the freshwater lineage LimA (genus Limnohabitans) revealed by a new double hybridization approach. Environ. Microbiol. 19, 1296–1309 (2017). PubMed DOI

Hahn, M. W., Lang, E., Tarao, M. & Brandt, U. Polynucleobacter rarus sp. nov., a free-living planktonic bacterium isolated from an acidic lake. Int. J. Syst. Evol. Microbiol. 61, 781–787 (2011). PubMed DOI

Hahn, M. W. et al. The passive yet successful way of planktonic life: genomic and experimental analysis of the ecology of a free-living Polynucleobacter population. PLoS ONE 7, e32772 (2012). PubMed DOI PMC

Pernthaler, J. Predation on prokaryotes in the water column and its ecological implications. Nat. Rev. Microbiol. 3, 537–546 (2005). PubMed DOI

Sommer, U. et al. Beyond the plankton ecology group (Peg) model: mechanisms driving plankton succession. Annu. Rev. Ecol. Evol. Syst. 43, 429–448 (2012). DOI

Šimek, K. et al. Bacterial prey food characteristics modulate community growth response of freshwater bacterivorous flagellates. Limnol. Oceanogr. 63, 484–502 (2018). DOI

Posch, T. et al. Network of interactions between ciliates and phytoplankton during spring. Front. Microbiol. 6, 1289 (2015). PubMed DOI PMC

Geraldes, A. M. & Boavida, M.-J. Zooplankton assemblages in two reservoirs: one subjected to accentuated water level fluctuations, the other with more stable water levels. Aquat. Ecol. 41, 273–284 (2007). DOI

Nilssen, J. P. & Wærvågen, S. B. Superficial ecosystem similarities vs autecological stripping: the ‘twin species’ Mesocyclops leuckarti (Claus) and Thermocyclops oithonoides (Sars)—seasonal habitat utilisation and life history traits. J. Limnol. 59, 79–102 (2000). DOI

Cole, T. M. & Wells, S. A. CE-QUAL-W2: A Two-Dimensional, Laterally Averaged, Hydrodynamic and Water Quality Model, Version 4.1 (Department of Civil and Environmental Engineering, 2018).

Brussaard, C. P. D. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ. Microb. 70, 1506–1513 (2004). DOI

Porter, K. G. & Feig, Y. S. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25, 943–948 (1980). DOI

Sherr, E. B. & Sherr, B. F. in Handbook of Methods in Aquatic Microbial Ecology (eds Kemp, P. F. et al.) 207–212 (Lewis Publishers, 1993).

Sherr, E. B. & Sherr, B. F. in Handbook of Methods in Aquatic Microbial Ecology (eds Kemp, P. F. et al.) 695–701 (Lewis Publishers, 1993).

Kasalický, V., Jezbera, J., Hahn, M. W. & Šimek, K. The diversity of the Limnohabitans genus, an important group of freshwater bacterioplankton, by characterization of 35 isolated strains. PLoS ONE 8, e58209 (2013). PubMed DOI PMC

Šimek, K. et al. Microbial food webs in hypertrophic fishponds: omnivorous ciliate taxa are major protistan bacterivores. Limnol. Oceanogr. 64, 2295–2309 (2019). DOI

Lund, J. W. G., Kipling, C. & Le Cren, E. D. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11, 143–170 (1958). DOI

Hillebrand, H., Dürselen, C. D., Kirschtel, D., Pollingher, U. & Zohary, T. Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 35, 403–424 (1999). DOI

Straškraba, M. & Hrbáček, J. Net-plankton cycle in slapy reservoir during 1958–1960. Hydrobiol. Stud. 1, 113–153 (1966).

Nercessian, O., Noyes, E., Kalyuzhnaya, M. G., Lidstrom, M. E. & Chistoserdova, L. Bacterial populations active in metabolism of C1 compounds in the sediment of Lake Washington, a freshwater lake. Appl. Environ. Microb. 71, 6885–6899 (2005). DOI

Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016). PubMed DOI PMC

R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

Yilmaz, P. et al. The SILVA and ‘all-species living tree project (LTP)’ taxonomic frameworks. Nucleic Acids Res. 42, D643–D648 (2014). PubMed DOI

Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012). PubMed DOI PMC

Pruesse, E. et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188–7196 (2007). PubMed DOI PMC

Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014). PubMed DOI PMC

Schöfl, G. reutils: talk to the NCBI EUtils. R version 0.2.3 https://CRAN.R-project.org/package=reutils (2016).

Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012). PubMed DOI PMC

Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004). PubMed DOI PMC

Fuchs, B. M., Glöckner, F. O., Wulf, J. & Amann, R. Unlabeled helper oligonucleotides increase the in situ accessibility to 16S rRNA of fluorescently labeled oligonucleotide probes. Appl. Environ. Microb. 66, 3603–3607 (2000). DOI

Buckley, D. H. & Schmidt, T. M. Environmental factors influencing the distribution of rRNA from verrucomicrobia in soil. FEMS Microbiol. Ecol. 35, 105–112 (2001). PubMed DOI

Yilmaz, L. S., Parnerkar, S. & Noguera, D. R. mathFISH, a web tool that uses thermodynamics-based mathematical models for in silico evaluation of oligonucleotide probes for fluorescence in situ hybridization. Appl. Environ. Microb. 77, 1118–1122 (2011). DOI

Sekar, R. et al. An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization. Appl. Environ. Microb. 69, 2928–2935 (2003). DOI

Lorenzen, C. J. Determination of chlorophyll and pheo-pigments: spectrophotometric equations 1. Limnol. Oceanogr. 12, 343–346 (1967). DOI

Golterman, H. L. Methods for Chemical Analysis of Fresh Waters (F. A. Davis Company, 1969).

Murphy, J. & Riley, J. P. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36 (1962). DOI

Kopáček, J. & Hejzlar, J. Semi-micro determination of total phosphorus in fresh waters with perchloric acid digestion. Int. J. Environ. Anal. Chem. 53, 173–183 (1993). DOI

Oksanen, J. et al. vegan: community ecology package. R version 2.5–6 (2019); https://CRAN.R-project.org/package=vegan

Response of aerobic anoxygenic phototrophic bacteria to limitation and availability of organic carbon

Integrating depth-dependent protist dynamics and microbial interactions in spring succession of a freshwater reservoir

Phenology and ecological role of aerobic anoxygenic phototrophs in freshwaters

Global freshwater distribution of Telonemia protists

In the right place, at the right time: the integration of bacteria into the Plankton Ecology Group model

High-resolution metagenomic reconstruction of the freshwater spring bloom