Ecosystem recovery after climatic extremes enhanced by genotypic diversity
Open accessAbstract
Contemporary climate change is characterized both by increasing mean temperature and increasing climate variability such as heat waves, storms, and floods. How populations and communities cope with such climatic extremes is a question central to contemporary ecology and biodiversity conservation. Previous work has shown that species diversity can affect ecosystem functioning and resilience. Here, we show that genotypic diversity can replace the role of species diversity in a species-poor coastal ecosystem, and it may buffer against extreme climatic events. In a manipulative field experiment, increasing the genotypic diversity of the cosmopolitan seagrass Zostera marina enhanced biomass production, plant density, and faunal abundance, despite near-lethal water temperatures due to extreme warming across Europe. Net biodiversity effects were explained by genotypic complementarity rather than by selection of particularly robust genotypes. Positive effects on invertebrate fauna suggest that genetic diversity has second-order effects reaching higher trophic levels. Our results highlight the importance of maintaining genetic as well as species diversity to enhance ecosystem resilience in a world of increasing uncertainty.
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Communities with greater diversity are more resilient to environmental change.
“in part because more diverse communities are more resilient to environmental change (Reusch et al. 2005;Hughes et al. 2008;Peterson et al. 1998).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Reusch et al. 2005
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Cites
Biodiversity hotspots for conservation priorities
Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B., & Kent, J. (2000) · Nature · doi:10.1038/35002501 · Cited by 31,710 · see citing works
Extinction risk from climate change
Thomas, C. D., Cameron, A., Green, R. E., Bakkenes, M., Beaumont, L. J., Collingham, Y. C., Erasmus, B. F. N., de Siqueira, M. F., Grainger, A., Hannah, L., et al. (2004) · Nature · doi:10.1038/nature02121 · Cited by 7,722 · see citing works
Biodiversity and ecosystem functioning: Current knowledge and future challenges
Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J. P., Hector, A., Hooper, D. U., Huston, M. A., Raffaelli, D., Schmid, B., et al. (2001) · Science · doi:10.1126/science.1064088 · Cited by 4,649 · see citing works
Partitioning selection and complementarity in biodiversity experiments
Loreau, M., & Hector, A. (2001) · Nature · doi:10.1038/35083573 · Cited by 3,528 · see citing works
The Influence of Functional Diversity and Composition on Ecosystem Processes
Tilman, D. G., Knops, J. M. H., Wedin, D. A., Reich, P. B., Ritchie, M. E., & Siemann, E. (1997) · Science · doi:10.1126/science.277.5330.1300 · Cited by 3,205 · see citing works
The complexity and stability of ecosystems
Pimm, S. L. (1984) · Nature · doi:10.1038/307321a0 · Cited by 3,126 · see citing works
Productivity and sustainability influenced by biodiversity in grassland ecosystems.
Tilman, D., Wedin, D., & Knops, J. (1996) · Nature · doi:10.1038/379718a0 · Cited by 2,803 · see citing works
The role of increasing temperature variability in European summer heatwaves
Schär, C., Vidale, P. L., Lüthi, D., Frei, C., Häberli, C., Liniger, M. A., & Appenzeller, C. (2004) · Nature · doi:10.1038/nature02300 · Cited by 2,787 · see citing works
Biodiversity and Ecosystem Functioning
Tilman, D., Isbell, F., & Cowles, J. M. (2014) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev-ecolsys-120213-091917 · Cited by 2,467 · see citing works
Poleward shifts in geographical ranges of butterfly species associated with regional warming
Parmesan, C., Ryrholm, N., Stefanescu, C., Hill, J. K., Thomas, C. D., Descimon, H., Huntley, B. J., Kaila, L., Kullberg, J., Tammaru, T., et al. (1999) · Nature · doi:10.1038/21181 · Cited by 2,280 · see citing works
THE ECOLOGICAL CONSEQUENCES OF CHANGES IN BIODIVERSITY: A SEARCH FOR GENERAL PRINCIPLES 101
Tilman, D. G. (1999) · Ecology · doi:10.1890/0012-9658(1999)080[1455:tecoci]2.0.co;2 · Cited by 2,156 · see citing works
Plant diversity and productivity experiments in european grasslands
Hector, A., Schmid, B., Beierkuhnlein, C., Caldeira, M. C., Diemer, M., Dimitrakopoulos, P. G., Finn, J. A., Freitas, H., Giller, P. S., Good, J., et al. (1999) · Science · doi:10.1126/science.286.5442.1123 · Cited by 2,125 · see citing works
Biological consequences of global warming: is the signal already apparent?
Hughes, L. (2000) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(99)01764-4 · Cited by 2,107 · see citing works
European Seasonal and Annual Temperature Variability, Trends, and Extremes Since 1500
Luterbacher, J., Dietrich, D., Xoplaki, E., Grosjean, M., & Wanner, H. (2004) · Science · doi:10.1126/science.1093877 · Cited by 1,805 · see citing works
Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity
Huston, M. A. (1997) · Oecologia · doi:10.1007/s004420050180 · Cited by 1,755 · see citing works
Bertness, M. D., Gaines, S. D., & Hay, M. E. (2001) · Cited by 1,507 · see citing works
Communities and Ecosystems: Linking the Aboveground and Belowground Components
Wardle, D. A. (2002) · Project Muse (Johns Hopkins University) · Cited by 1,468 · see citing works
The future of seagrass meadows
Duarte, C. M. (2002) · Environmental Conservation · doi:10.1017/s0376892902000127 · Cited by 1,244 · see citing works
Biodiversity as a barrier to ecological invasion
Kennedy, T. A., Naeem, S., Howe, K. M., Knops, J. M. H., Tilman, D. G., & Reich, P. B. (2002) · Nature · doi:10.1038/nature00776 · Cited by 1,180 · see citing works
Biodiversity and ecosystem functioning : synthesis and perspectives
Loreau, M., Naeem, S., & Inchausti, P. (2002) · Cited by 1,079 · see citing works
Hemminga, M. A., & Duarte, C. M. (2000) · doi:10.1017/cbo9780511525551 · Cited by 1,076 · see citing works
Constraint to Adaptive Evolution in Response to Global Warming
Etterson, J. R., & Shaw, R. G. (2001) · Science · doi:10.1126/science.1063656 · Cited by 934 · see citing works
Species diversity enhances ecosystem functioning through interspecific facilitation
Cardinale, B. J., Palmer, M. A., & Collins, S. L. (2002) · Nature · doi:10.1038/415426a · Cited by 855 · see citing works
Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance
Hughes, A. R., & Stachowicz, J. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402642101 · Cited by 842 · see citing works
Systematics and ecology of the Isefjord marine fauna (Denmark)
Rasmussen, E. (1973) · Ophelia · doi:10.1080/00785326.1973.10430115 · Cited by 692 · see citing works
Expansion of Phragmites australis into tidal wetlands of North America
Chambers, R. M., Meyerson, L. A., & Saltonstall, K. (1999) · Aquatic Botany · doi:10.1016/s0304-3770(99)00055-8 · Cited by 641 · see citing works
Quantifying the risk of extreme seasonal precipitation events in a changing climate
Palmer, T. N., & Räisänen, J. (2002) · Nature · doi:10.1038/415512a · Cited by 620 · see citing works
Biodiversity and Ecosystem Functioning
(2002) · doi:10.1093/oso/9780198515708.001.0001 · Cited by 613 · see citing works
Conservation Genetics: Case Histories from Nature
Toline, C. A., Avise, J. C., & Hamrick, J. L. (1997) · Ecology · doi:10.2307/2265881 · Cited by 549 · see citing works
Climate-Related, Long-Term Faunal Changes in a California Rocky Intertidal Community
Barry, J. P., Baxter, C. H., Sagarin, R. D., & Gilman, S. E. (1995) · Science · doi:10.1126/science.267.5198.672 · Cited by 541 · see citing works
El Niño effects on the dynamics of terrestrial ecosystems
Holmgren, M., Scheffer, M., Ezcurra, E., et al. (2001) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(00)02052-8 · Cited by 510 · see citing works
Effects of macrophyte species richness on wetland ecosystem functioning and services
Engelhardt, K., & Ritchie, M. (2001) · Nature · doi:10.1038/35079573 · Cited by 465 · see citing works
Physical stress and diversity-productivity relationships: The role of positive interactions
Mulder, C. P. H., Uliassi, D. D., & Doak, D. F. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111055298 · Cited by 417 · see citing works
Biodiversity, productivity and stability in real food webs
Worm, B., & Duffy, J. E. (2003) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2003.09.003 · Cited by 404 · see citing works
Self-citationGiller, P. S., Hillebrand, H., Berninger, U., Gessner, M. O., Hawkins, S. J., Inchausti, P., Inglis, C., Leslie, H. M., Malmqvist, B., Monaghan, M. T., et al. (2004) · Oikos · doi:10.1111/j.0030-1299.2004.13253.x · Cited by 398 · see citing works
Grazer diversity effects on ecosystem functioning in seagrass beds
Emmett Duffy, J., Paul Richardson, J., & Canuel, E. A. (2003) · Ecology Letters · doi:10.1046/j.1461-0248.2003.00474.x · Cited by 346 · see citing works
Parks, J. C., & Werth, C. R. (1993) · American Journal of Botany · doi:10.1002/j.1537-2197.1993.tb13837.x · Cited by 337 · see citing works
The biotic crisis and the future of evolution
Myers, N., & Knoll, A. H. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091092498 · Cited by 329 · see citing works
The Largest, Smallest, Highest, Lowest, Longest, and Shortest: Extremes in Ecology
Gaines, S. D., & Denny, M. W. (1993) · Ecology · doi:10.2307/1939926 · Cited by 302 · see citing works
OLSEN, J. L., STAM, W. T., COYER, J. A., REUSCH, T. B. H., BILLINGHAM, M., BOSTRÖM, C., CALVERT, E., CHRISTIE, H., GRANGER, S., LUMIÈRE, R. L., et al. (2004) · Molecular Ecology · doi:10.1111/j.1365-294x.2004.02205.x · Cited by 291 · see citing works
Self-citationWilliams, S. L. (2001) · Ecological Applications · doi:10.1890/1051-0761(2001)011[1472:rgdiet]2.0.co;2 · Cited by 280 · see citing works
Widén, B., Cronberg, N., & Widén, M. (1994) · Folia Geobotanica et Phytotaxonomica · doi:10.1007/bf02803799 · Cited by 277 · see citing works
Neckles, H. A., Wetzel, R. L., & Orth, R. J. (1993) · Oecologia · doi:10.1007/bf00317683 · Cited by 276 · see citing works
Meristematic oxygen variability in eelgrass (Zostera marina)
Greve, T. M., Borum, J., & Pedersen, O. (2003) · Limnology and Oceanography · doi:10.4319/lo.2003.48.1.0210 · Cited by 231 · see citing works
Trophic Control of Production in a Rocky Intertidal Community
Paine, R. T. (2002) · Science · doi:10.1126/science.1069811 · Cited by 227 · see citing works
Vegetative morphology and meristem dependence — The foundation of productivity in seagrasses
TOMLINSON, P. B. (1974) · Aquaculture · doi:10.1016/0044-8486(74)90027-1 · Cited by 221 · see citing works
The design and analysis of biodiversity experiments
Schmid, B., Hector, A., Huston, M. A., lnchausti, P., Nijs, I., Leadley, P., & Tilman, D. G. (2002) · doi:10.1093/oso/9780198515708.003.0006 · Cited by 220 · see citing works
Estuarine Vegetated Habitats as Corridors for Predator Movements
Micheli, F., & Peterson, C. H. (1999) · Conservation Biology · doi:10.1046/j.1523-1739.1999.98233.x · Cited by 202 · see citing works
(1996) · Springer eBooks · doi:10.1007/978-1-4757-2504-9 · Cited by 192 · see citing works
Reusch, T. B. H., Stam, W. T., & Olsen, J. (2000) · Molecular Ecology · doi:10.1046/j.1365-294x.2000.00839.x · Cited by 165 · see citing works
Self-citationReusch, T. B. H., & Williams, S. L. (1998) · Oecologia · doi:10.1007/s004420050395 · Cited by 132 · see citing works
Self-citationReusch, T. B. H. (2002) · Limnology and Oceanography · doi:10.4319/lo.2002.47.1.0078 · Cited by 111 · see citing works
Self-citationInbreeding depression influences genet size distribution in a marine angiosperm
Hämmerli, A., & Reusch, T. B. H. (2003) · Molecular Ecology · doi:10.1046/j.1365-294x.2003.01766.x · Cited by 110 · see citing works
Self-citationD: Fragmented plant populations and their lost interactions
Olesen, J. M., & Jain, S. K. (1994) · Conservation Genetics · doi:10.1007/978-3-0348-8510-2_35 · Cited by 79 · see citing works
Do nutrient availability and plant density limit seagrass colonization in the Baltic Sea?
Worm, B., & Reusch, T. B. H. (2000) · Marine Ecology Progress Series · doi:10.3354/meps200159 · Cited by 66 · see citing works
Self-citationReusch, T. B. H. (2000) · Molecular Ecology · doi:10.1046/j.1365-294x.2000.00874-4.x · Cited by 58 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 4
- [35]Hughes, A. R. & Stachowicz, J. J. (2004) Proc. Natl. Acad. Sci. USA 101, 8998-9002.
- [37]Mulder, C. P. H., Uliassi, D. D. & Doak, D. F. (2001) Proc. Natl. Acad. Sci. USA 98, 6704-6708.
- [53]Olesen, J. M. & Jain, S. K. (1994) in Conservation Genetics , eds. Loeschke, V., Tomiuk, J. & Jain, S. K. (Birkha ¨user, Basel), pp. 417-426.
- [55]Myers, N. & Knoll, A. H. (2001) Proc. Natl. Acad. Sci. USA 98, 53895392.
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- Authors
- Reusch, T. B. H., Ehlers, A., Hämmerli, A., & Worm, B.
- Affiliations
- Dalhousie University (CA)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2005-02-14
- Volume
- 102
- Issue
- 8
- Pages
- 2826-2831
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC549506
- OpenAlex
- W2118337700
- Cited by
- 1,245
- References
- 56
- Citations by year
- 2026: 34 · 2025: 49 · 2024: 43 · 2023: 43 · 2022: 86 · 2021: 65 · 2020: 75 · 2019: 71 · 2018: 67 · 2017: 108 · 2016: 60 · 2015: 66 · 2014: 76 · 2013: 45 · 2012: 74
- FWCI
- 30.71
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Helmholtz Centre for Ocean Research Kiel (GEOMAR) (acceptedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal plant biology
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Ecology and Vegetation Dynamics Studies
- Physical Sciences › Environmental Science › Ecology › Coral and Marine Ecosystems Studies
- Keywords
- genotypic diversity, genetic diversity, species diversity, Zostera marina, seagrass, climate extremes, heat waves, ecosystem resilience, ecosystem recovery, complementarity, biodiversity impacts, coastal ecosystems, invertebrate fauna, trophic levels
- MeSH terms
- Animals, Climate, Genotype, Genetic Variation, Ecosystem, Biodiversity
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