Plastic responses to hot temperatures homogenize riparian leaf litter, speed decomposition, and reduce detritivores.
climate change
common gardens
decomposition
ecosystem function
foundation species
genotypes
phenotypic plasticity
riparian
stream ecology
subsidy
traits
Journal
Ecology
ISSN: 1939-9170
Titre abrégé: Ecology
Pays: United States
ID NLM: 0043541
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
revised:
12
04
2021
received:
15
12
2020
accepted:
13
05
2021
pubmed:
9
7
2021
medline:
21
10
2021
entrez:
8
7
2021
Statut:
ppublish
Résumé
Efforts to maintain the function of critical ecosystems under climate change often begin with foundation species. In the southwestern United States, cottonwood trees support diverse communities in riparian ecosystems that are threatened by rising temperatures. Genetic variation within cottonwoods shapes communities and ecosystems, but these effects may be modified by phenotypic plasticity, where genotype traits change in response to environmental conditions. Here, we investigated plasticity in Fremont cottonwood (Populus fremontii) leaf litter traits as well as the consequences of plasticity for riparian ecosystems. We used three common gardens each planted with genotypes from six genetically divergent populations spanning a 12°C temperature gradient, and a decomposition experiment in a common stream environment. We found that leaf litter area, specific leaf area, and carbon to nitrogen ratio (C:N) were determined by interactions between genetics and growing environment, as was the subsequent rate of litter decomposition. Most of the genetic variation in leaf litter traits appeared among rather than within source populations with distinct climate histories. Source populations from hotter climates generally produced litter that decomposed more quickly, but plasticity varied the magnitude of this effect. We also found that hotter growing conditions reduced the variation in litter traits produced across genotypes, homogenizing the litter inputs to riparian ecosystems. All genotypes in the hottest garden produced comparatively small leaves that decomposed quickly and supported lower abundances of aquatic invertebrates, whereas the same genotypes in the coldest garden produced litter with distinct morphologies and decomposition rates. Our results suggest that plastic responses to climate stress may constrict the expression of genetic variation in predictable ways that impact communities and ecosystems. Understanding these interactions between genetic and environmental variation is critical to our ability to plan for the role of foundation species when managing and restoring riparian ecosystems in a warming world.
Banques de données
Dryad
['10.5061/dryad.31zcrjdkh']
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
e03461Informations de copyright
© 2021 by the Ecological Society of America.
Références
Akman, M., J. E. Carlson, and A. M. Latimer. 2021. Climate explains population divergence in drought-induced plasticity of functional traits and gene expression in a South African Protea. Molecular Ecology 30:255-273.
Arnold, P. A., L. E. B. Kruuk, and A. B. Nicotra. 2019. How to analyse plant phenotypic plasticity in response to a changing climate. New Phytologist 222:1235-1241.
Barbour, M. A., S. Erlandson, K. Peay, B. Locke, E. S. Jules, and G. M. Crutsinger. 2019. Trait plasticity is more important than genetic variation in determining species richness of associated communities. Journal of Ecology 107:350-360.
Bates, D., M. Mächler, B. M. Bolker, and S. C. Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1-48.
Benfield, E. F., K. M. Fritz, and S. D. Tiegs. 2017. Leaf-litter breakdown. Pages 71-82 in G. A. Lamberti and F. R. Hauer, editors. Methods in stream ecology: Volume 2: Ecosystem function. Third edition. Elsevier, Academic Press, Cambridge, Massachusetts, USA.
Boyero, L., et al. 2011. A global experiment suggests climate warming will not accelerate litter decomposition in streams but might reduce carbon sequestration. Ecology Letters 14:289-294.
Boyero, L., et al. 2017. Riparian plant litter quality increases with latitude. Scientific Reports 7:10562.
Butterfield, B. J., S. M. Copeland, S. M. Munson, C. M. Roybal, and T. E. Wood. 2017. Prestoration: using species in restoration that will persist now and into the future. Restoration Ecology 25:S155-S163.
Chevin, L. M., and A. A. Hoffmann. 2017. Evolution of phenotypic plasticity in extreme environments. Philosophical Transactions of the Royal Society B 372:20160138.
Compson, Z. G., B. A. Hungate, G. W. Koch, S. C. Hart, J. M. Maestas, K. J. Adams, T. G. Whitham, and J. C. Marks. 2015. Closely related tree species differentially influence the transfer of carbon and nitrogen from leaf litter up the aquatic food web. Ecosystems 18:186-201.
Compson, Z. G., et al. 2018. Linking tree genetics and stream consumers: isotopic tracers elucidate controls on carbon and nitrogen assimilation. Ecology 99:1759-1770.
Compson, Z. G., B. A. Hungate, T. G. Whitham, N. Meneses, P. E. Busby, T. Wojtowicz, A. C. Ford, K. J. Adams, and J. C. Marks. 2016. Plant genotype influences aquatic-terrestrial ecosystem linkages through timing and composition of insect emergence. Ecosphere 7:e01331.
Cooper, H. F., K. C. Grady, J. A. Cowan, R. J. Best, G. J. Allan, and T. G. Whitham. 2019. Genotypic variation in phenological plasticity: Reciprocal common gardens reveal adaptive responses to warmer springs but not to fall frost. Global Change Biology 25:187-200.
Cornelissen, J. H. C., N. Pérez-Harguindeguy, S. Díaz, J. P. Grime, B. Marzano, M. Cabido, F. Vendramini, and B. Cerabolini. 1999. Leaf structure and defence control litter decomposition rate across species and life forms in regional floras on two continents. New Phytologist 143:191-200.
Cornwell, W. K., et al. 2008. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology Letters 11:1065-1071.
Covich, A. P., M. A. Palmer, and T. A. Crowl. 1999. The role of benthic invertebrate species in freshwater ecosystems: Zoobenthic species influence energy flows and nutrient cycling. BioScience 49:119-127.
Crutsinger, G. M. 2016. A community genetics perspective: opportunities for the coming decade. New Phytologist 210:65-70.
Davis, M. B., R. G. Shaw, and J. R. Etterson. 2005. Evolutionary responses to changing climate. Ecology 86:1704-1714.
Des Roches, S., D. M. Post, N. E. Turley, J. K. Bailey, A. P. Hendry, M. T. Kinnison, J. A. Schweitzer, and E. P. Palkovacs. 2018. The ecological importance of intraspecific variation. Nature Ecology and Evolution 2:57-64.
Dingemanse, N. J., and N. A. Dochtermann. 2013. Quantifying individual variation in behaviour: Mixed-effect modelling approaches. Journal of Animal Ecology 82:39-54.
Driebe, E. M., and T. G. Whitham. 2000. Cottonwood hybridization affects tannin and nitrogen content of leaf litter and alters decomposition. Oecologia 123:99-107.
Etterson, J. R., and R. G. Shaw. 2001. Constraint to adaptive evolution in response to global warming. Science 294:151-154.
Evans, L. M., S. Kaluthota, D. W. Pearce, G. J. Allan, K. Floate, S. B. Rood, and T. G. Whitham. 2016. Bud phenology and growth are subject to divergent selection across a latitudinal gradient in Populus angustifolia and impact adaptation across the distributional range and associated arthropods. Ecology and Evolution 6:4565-4581.
Fick, S. E., and R. J. Hijmans. 2017. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37:4302-4315.
Fischer, D. G., S. K. Chapman, A. T. Classen, C. A. Gehring, K. C. Grady, J. A. Schweitzer, and T. G. Whitham. 2014. Plant genetic effects on soils under climate change. Plant and Soil 379:1-19.
Fisher, S. G., and G. E. Likens. 1973. Energy flow in Bear Brook, New Hampshire: an integrative approach to stream ecosystem metabolism. Ecological Monographs 43:421-439.
Follstad Shah, J. J., et al. 2017. Global synthesis of the temperature sensitivity of leaf litter breakdown in streams and rivers. Global Change Biology 23:3064-3075.
Fox, J., and S. Weisberg. 2011. An R companion to applied regression. Sage, Thousand Oaks, California, USA.
Franks, S. J., J. J. Weber, and S. N. Aitken. 2014. Evolutionary and plastic responses to climate change in terrestrial plant populations. Evolutionary Applications 7:123-139.
Givnish, T. J. 1987. Comparative studies of leaf form: assessing the relative roles of selective pressures and phylogenetic constraints. New Phytologist 106:131-160.
Grady, K. C., S. M. Ferrier, T. E. Kolb, S. C. Hart, G. J. Allan, and T. G. Whitham. 2011. Genetic variation in productivity of foundation riparian species at the edge of their distribution: Implications for restoration and assisted migration in a warming climate. Global Change Biology 17:3724-3735.
Grady, K. C., T. E. Kolb, D. H. Ikeda, and T. G. Whitham. 2015. A bridge too far: Cold and pathogen constraints to assisted migration of riparian forests. Restoration Ecology 23:811-820.
Grady, K. C., D. C. Laughlin, S. M. Ferrier, T. E. Kolb, S. C. Hart, G. J. Allan, and T. G. Whitham. 2013. Conservative leaf economic traits correlate with fast growth of genotypes of a foundation riparian species near the thermal maximum extent of its geographic range. Functional Ecology 27:428-438.
Hendry, A. P. 2016. Key questions on the role of phenotypic plasticity in eco-evolutionary dynamics. Journal of Heredity 107:25-41.
Hershey, A. E., G. A. Lamberti, D. T. Chaloner, and R. M. Northington. 2010. Aquatic insect ecology, Chapter 17. Pages 659-694 in J. H. Thorp and A. P. Covich, editors. Ecology and classification of North American freshwater invertebrates. Third edition. Academic Press, Cambridge, Massachusetts, USA.
Hoffmann, A. A., and C. M. Sgró. 2011. Climate change and evolutionary adaptation. Nature 470:479-485.
Hultine, K. R., et al. 2020a. Adaptive capacity in the foundation tree species Populus fremontii: implications for resilience to climate change and non-native species invasion in the American Southwest. Conservation Physiology 8:coaa061.
Hultine, K. R., R. Froend, D. Blasini, S. E. Bush, M. Karlinski, and D. F. Koepke. 2020b. Hydraulic traits that buffer deep-rooted plants from changes in hydrology and climate. Hydrological Processes 34:209-222.
Ikeda, D. H., T. L. Max, G. J. Allan, M. K. Lau, S. M. Shuster, and T. G. Whitham. 2017. Genetically informed ecological niche models improve climate change predictions. Global Change Biology 23:164-176.
Jackrel, S. L., and T. C. Morton. 2018. Inducible phenotypic plasticity in plants regulates aquatic ecosystem functioning. Oecologia 186:895-906.
Jackrel, S. L., and J. T. Wootton. 2014. Local adaptation of stream communities to intraspecific variation in a terrestrial ecosystem subsidy. Ecology 95:37-43.
Jeplawy, J., et al. 2021. Plastic responses to hot temperatures homogenize riparian leaf litter, speed decomposition, and reduce detritivores. Dryad, data set. https://doi.org/10.5061/dryad.31zcrjdkh
Johnson, M. T. J., and A. A. Agrawal. 2005. Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology 86:874-885.
Joshi, J., et al. 2001. Local adaptation enhances performance of common plant species. Ecology Letters 4:536-544.
Kelly, M. W., E. Sanford, and R. K. Grosberg. 2012. Limited potential for adaptation to climate change in a broadly distributed marine crustacean. Proceedings of the Royal Society B 279:349-356.
Kuznetsova, A., P. B. Brockhoff, and R. H. B. Christensen. 2017. lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82:1-26.
Lamit, L. J., et al. 2015. Tree genotype mediates covariance among communities from microbes to lichens and arthropods. Journal of Ecology 103:840-850.
Legendre, P., and M. J. Anderson. 1999. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecological Monographs 69:1-24.
LeRoy, C. J., and J. C. Marks. 2006. Litter quality, stream characteristics and litter diversity influence decomposition rates and macroinvertebrates. Freshwater Biology 51:605-617.
LeRoy, C. J., T. G. Whitham, S. C. Wooley, and J. C. Marks. 2007. Within-species variation in foliar chemistry influences leaf-litter decomposition in a Utah river. Journal of the North American Benthological Society 26:426-438.
Lower Colorado River Multi-Species Conservation Program. 2004. Lower Colorado River Multi-Species Conservation Program, Volume II: Habitat conservation plan. Final. Lower Colorado River Multi-Species Conservation Program, Sacramento, California, USA.
Madritch, M., J. R. Donaldson, and R. L. Lindroth. 2006. Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9:528-537.
Marks, J. C. 2019. Revisiting the fates of dead leaves that fall into streams. Annual Review of Ecology, Evolution, and Systematics 50:547-568.
Marks, J. C., G. A. Haden, B. L. Harrop, E. G. Reese, J. L. Keams, M. E. Watwood, and T. G. Whitham. 2009. Genetic and environmental controls of microbial communities on leaf litter in streams. Freshwater Biology 54:2616-2627.
Matesanz, S., E. Gianoli, and F. Valladares. 2010. Global change and the evolution of phenotypic plasticity in plants. Annals of the New York Academy of Sciences 1206:35-55.
Nakagawa, S., and H. Schielzeth. 2013. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution 4:133-142.
Niinemets, Ü., A. Portsmuth, D. Tena, M. Tobias, S. Matesanz, and F. Valladares. 2007. Do we underestimate the importance of leaf size in plant economics? Disproportional scaling of support costs within the spectrum of leaf physiognomy. Annals of Botany 100:283-303.
Noss, R. F., E. T. Laroe, and J. M. Scott. 1995. Endangered ecosystems of the United States: a preliminary assessment of loss and degradation. Biological Report 28. U.S. Department of the Interior, National Biological Service, Washington, D.C., USA.
O’Neill, G. A., A. Hamann, and T. L. Wang. 2008. Accounting for population variation improves estimates of the impact of climate change on species’ growth and distribution. Journal of Applied Ecology 45:1040-1049.
Oksanen, J., R. Kindt, L. Pierre, B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, and H. Wagner. 2016. vegan: Community ecology package, R package version 2.4-0. R package version 2.2-1. https://cran.r-project.org/web/packages/vegan/
Patsiou, T. S., T. A. Shestakova, T. Klein, G. di Matteo, H. Sbay, M. R. Chambel, R. Zas, and J. Voltas. 2020. Intraspecific responses to climate reveal nonintuitive warming impacts on a widespread thermophilic conifer. New Phytologist 228:525-540.
Poff, N. L. R., J. D. Olden, N. K. M. Vieira, D. S. Finn, M. P. Simmons, and B. C. Kondratieff. 2006. Functional trait niches of North American lotic insects: Traits-based ecological applications in light of phylogenetic relationships. Journal of the North American Benthological Society 25:730-755.
Pregitzer, C. C., J. K. Bailey, and J. A. Schweitzer. 2013. Genetic by environment interactions affect plant-soil linkages. Ecology and Evolution 3:2322-2333.
R Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org
Raffard, A., F. Santoul, J. Cucherousset, and S. Blanchet. 2019. The community and ecosystem consequences of intraspecific diversity: a meta-analysis. Biological Reviews 94:648-661.
Reed, T. E., D. E. Schindler, and R. S. Waples. 2011. Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conservation Biology 25:56-63.
Roberts, D. W. 2013. Package labdsv. R package ver. 1.6-1:1-56. https://cran.r-project.org/web/packages/labdsv
Rudman, S. M., M. A. Rodriguez-Cabal, A. Stier, T. Sato, J. Heavyside, R. W. El-Sabaawi, and G. M. Crutsinger. 2015. Adaptive genetic variation mediates bottom-up and top-down control in an aquatic ecosystem. Proceedings of the Royal Society B 282:8-10.
Scheiner, S. M., and C. J. Goodnight. 1984. The comparison of phenotypic plasticity and genetic variation in populations of the grass Danthonia spicata. Evolution 38:845-855.
Schweitzer, J. A., J. K. Bailey, B. J. Rehill, G. D. Martinsen, S. C. Hart, R. L. Lindroth, P. Keim, and T. G. Whitham. 2004. Genetically based trait in a dominant tree affects ecosystem processes. Ecology Letters 7:127-134.
Siders, A. C., Z. G. Compson, B. A. Hungate, P. Dijkstra, G. W. Koch, A. S. Wymore, A. S. Grandy, and J. C. Marks. 2018. Litter identity affects assimilation of carbon and nitrogen by a shredding caddisfly. Ecosphere 9:e02340.
Turcotte, M. M., and J. M. Levine. 2016. Phenotypic plasticity and species coexistence. Trends in Ecology & Evolution 31:803-813.
Walker, T. W. N., W. Weckwerth, L. Bragazza, L. Fragner, B. G. Forde, N. J. Ostle, C. Signarbieux, X. Sun, S. E. Ward, and R. D. Bardgett. 2019. Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes. Ecology Letters 22:159-169.
Wang, T., A. Hamann, D. L. Spittlehouse, and T. Q. Murdock. 2012. ClimateWNA-high-resolution spatial climate data for western North America. Journal of Applied Meteorology and Climatology 51:16-29.
Wang, T., G. A. O’Neill, and S. N. Aitken. 2010. Integrating environmental and genetic effects to predict responses of tree populations to climate. Ecological Applications 20:153-163.
Whitham, T. G., C. A. Gehring, L. J. Lamit, T. Wojtowicz, L. M. Evans, A. R. Keith, and D. S. Smith. 2012. Community specificity: life and afterlife effects of genes. Trends in Plant Science 17:271-281.
Wright, I. J., et al. 2004. The worldwide leaf economics spectrum. Nature 428:821-827.
Wright, I. J., et al. 2017. Global climatic drivers of leaf size. Science 357:917-921.