Reproductive Responses to Increased Shoot Density and Global Change Drivers in a Widespread Clonal Wetland Species, Schoenoplectus americanus

Kudoh, Aoi; Megonigal, J. Patrick; Langley, J. Adam; Noyce, Genevieve L.; Sakai, Toshiyuki; Whigham, Dennis F.

doi:10.1007/s12237-023-01249-z

Title: Reproductive Responses to Increased Shoot Density and Global Change Drivers in a Widespread Clonal Wetland Species, Schoenoplectus americanus

Journal Article · 15 September 2023 · Estuaries and Coasts

DOI: https://doi.org/10.1007/s12237-023-01249-z · OSTI ID:2282269

Kudoh, Aoi ^[1]; Megonigal, J. Patrick ^[2]; Langley, J. Adam ^[3]; Noyce, Genevieve L. ^[2]; Sakai, Toshiyuki ^[1];

^[2]

Kyoto University (Japan)
Smithsonian Environmental Research Center, Edgewater, MD (United States)
Villanova University, PA (United States)

The expansion of many wetland species is a function of both clonal propagation and sexual reproduction. The production of ramets through clonal propagation enables plants to move and occupy space near parent ramets, while seeds produced by sexual reproduction enable species to disperse and colonize open or disturbed sites both near and far from parents. The balance between clonal propagation and sexual reproduction is known to vary with plant density but few studies have focused on reproductive allocation with density changes in response to global climate change. Schoenoplectus americanus is a widespread clonal wetland species in North America and a dominant species in Chesapeake Bay brackish tidal wetlands. Long-term experiments on responses of S. americanus to global change provided the opportunity to compare the two modes of propagation under different treatments. Seed production increased with increasing shoot density, supporting the hypothesis that factors causing increased clonal reproduction (e.g., higher shoot density) stimulate sexual reproduction and dispersal of genets. The increase in allocation to sexual reproduction was mainly the result of an increase in the number of ramets that flowered and not an increase in the number of seeds per reproductive shoot, or the ratio between the number of flowers produced per inflorescence and the number of flowers that developed into seeds. Seed production increased in response to increasing temperatures and decreased or did not change in response to increased CO2 or nitrogen. Results from this comparative study demonstrate that plant responses to global change treatments affect resource allocation and can alter the ability of species to produce seeds.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Smithsonian Institute, Washington, DC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth & Environmental Systems Science (EESS)

Grant/Contract Number:: SC0021112; SC0014413; SC0019110

OSTI ID:: 2282269

Journal Information:: Estuaries and Coasts, Vol. 47, Issue 1; ISSN 1559-2723

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (65)

Reproductive Strategies in Dewberries Abrahamson, Warren G. Ecology, Vol. 56, Issue 3 https://doi.org/10.2307/1935508	journal	May 1975
Increased photosynthetic capacity of Scirpus olneyi after 4 years of exposure to elevated CO₂ Arp, W. J.; Drake, B. G. Plant, Cell & Environment, Vol. 14, Issue 9 https://doi.org/10.1111/j.1365-3040.1991.tb00971.x	journal	December 1991
Increasing spring temperatures favor oak seed production in temperate areas Caignard, Thomas; Kremer, Antoine; Firmat, Cyril Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-09172-7	journal	August 2017
Global change accelerates carbon assimilation by a wetland ecosystem engineer Caplan, Joshua S.; Hager, Rachel N.; Megonigal, J. Patrick Environmental Research Letters, Vol. 10, Issue 11 https://doi.org/10.1088/1748-9326/10/11/115006	journal	November 2015
Plant traits and ecosystem effects of clonality: a new research agenda Cornelissen, Johannes H. C.; Song, Yao-Bin; Yu, Fei-Hai Annals of Botany, Vol. 114, Issue 2 https://doi.org/10.1093/aob/mcu113	journal	June 2014
Uptake of organic nitrogen by coastal wetland plants under elevated CO2 Cott, Grace M.; Jansen, Marcel A. K.; Megonigal, J. Patrick Plant and Soil, Vol. 450, Issue 1-2 https://doi.org/10.1007/s11104-020-04504-5	journal	April 2020
Plant density influence on life history traits of a perennial herb in rocky outcrops, southeastern Brazil Demetrio, Guilherme Ramos; Barbosa, Mario Eduardo Avelar; Coelho, Flávia de Freitas Iheringia, Série Botânica, Vol. 75 https://doi.org/10.21826/2446-82312020v75e2020014	journal	July 2020
Clonal integration in homogeneous environments increases performance of Alternanthera philoxeroides Dong, Bi-Cheng; Alpert, Peter; Zhang, Qian Oecologia, Vol. 179, Issue 2 https://doi.org/10.1007/s00442-015-3338-y	journal	May 2015
An Open Top Chamber for Field Studies of Elevated Atmospheric CO 2 Concentration on Saltmarsh Vegetation Drake, B. G.; Leadley, P. W.; Arp, W. J. Functional Ecology, Vol. 3, Issue 3 https://doi.org/10.2307/2389377	journal	January 1989
A Field-Study of the Effects of Elevated CO2 on Ecosystem Processes in a Chesapeake Bay Wetland Drake, Bg Australian Journal of Botany, Vol. 40, Issue 5 https://doi.org/10.1071/BT9920579	journal	January 1992
Rising sea level, temperature, and precipitation impact plant and ecosystem responses to elevated CO ₂ on a Chesapeake Bay wetland: review of a 28-year study Drake, Bert G. Global Change Biology, Vol. 20, Issue 11 https://doi.org/10.1111/gcb.12631	journal	June 2014
Cosmopolitan Species As Models for Ecophysiological Responses to Global Change: The Common Reed Phragmites australis Eller, Franziska; Skálová, Hana; Caplan, Joshua S. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01833	journal	November 2017
Salinity and sea level mediate elevated CO ₂ effects on C ₃ ?C ₄ plant interactions and tissue nitrogen in a Chesapeake Bay tidal wetland Erickson, John E.; Megonigal, J. Patrick; Peresta, Gary Global Change Biology, Vol. 13, Issue 1 https://doi.org/10.1111/j.1365-2486.2006.01285.x	journal	January 2007
Macroclimatic change expected to transform coastal wetland ecosystems this century Gabler, Christopher A.; Osland, Michael J.; Grace, James B. Nature Climate Change, Vol. 7, Issue 2 https://doi.org/10.1038/nclimate3203	journal	January 2017
Interspecific Competition is Prevalent and Stabilizes Plant Production in a Brackish Marsh Facing Sea Level Rise Gabriel, Jared R.; Reid, Jessica; Wang, Le Estuaries and Coasts, Vol. 45, Issue 6 https://doi.org/10.1007/s12237-021-01043-9	journal	January 2022
The growth response of C ₄ plants to rising atmospheric CO ₂ partial pressure: a reassessment Ghannoum, O.; Caemmerer, S. Von; Ziska, L. H. Plant, Cell & Environment, Vol. 23, Issue 9 https://doi.org/10.1046/j.1365-3040.2000.00609.x	journal	September 2000
Seed production, germination rate, and seedling establishment ofScirpus pungens in tidal brackish marshes Giroux, Jean -François; Bédard, Jean Wetlands, Vol. 15, Issue 3 https://doi.org/10.1007/BF03160709	journal	September 1995
CO₂, nitrogen, and diversity differentially affect seed production of prairie plants HilleRisLambers, J.; Harpole, W. S.; Schnitzer, S. Ecology, Vol. 90, Issue 7 https://doi.org/10.1890/07-1351.1	journal	July 2009
Seed and Vegetative Reproduction in Relation to Density in Fragaria Virginiana (Rosaceae) Holler, Linda C.; Abrahamson, Warren G. American Journal of Botany, Vol. 64, Issue 8 https://doi.org/10.1002/j.1537-2197.1977.tb11946.x	journal	September 1977
Scalability and performance tradeoffs in quantifying relationships between elevation and tidal wetland plant communities Holmquist, Jr; Schile-Beers, L.; Buffington, K. Marine Ecology Progress Series, Vol. 666 https://doi.org/10.3354/meps13683	journal	May 2021
Demographic and growth responses of a guerrilla and a phalanx perennial grass in competitive mixtures Humphrey, L. David; Pyke, David A. Journal of Ecology, Vol. 86, Issue 5 https://doi.org/10.1046/j.1365-2745.1998.8650854.x	journal	October 1998
Effects of local density of clonal plants on their sexual and vegetative propagation strategies in a lattice structure model Ikegami, Makihiko; Whigham, Dennis F.; Werger, Marinus J. A. Ecological Modelling, Vol. 234 https://doi.org/10.1016/j.ecolmodel.2012.03.026	journal	June 2012
Biotic resistance, disturbance, and mode of colonization impact the invasion of a widespread, introduced wetland grass Kettenring, Karin M.; Whigham, Dennis F.; Hazelton, Eric L. G. Ecological Applications, Vol. 25, Issue 2 https://doi.org/10.1890/14-0434.1	journal	March 2015
The Role of Propagule Type, Resource Availability, and Seed Source in Phragmites Invasion in Chesapeake Bay Wetlands Kettenring, Karin M.; Whigham, Dennis F. Wetlands, Vol. 38, Issue 6 https://doi.org/10.1007/s13157-018-1034-5	journal	April 2018
Response of Plant Productivity to Experimental Flooding in a Stable and a Submerging Marsh Kirwan, Matthew L.; Guntenspergen, Glenn R. Ecosystems, Vol. 18, Issue 5 https://doi.org/10.1007/s10021-015-9870-0	journal	May 2015
Changes in high arctic tundra plant reproduction in response to long-term experimental warming: WARMING EFFECTS ON TUNDRA PLANT REPRODUCTION Klady, Rebecca A.; Henry, Gregory H. R.; Lemay, Valerie Global Change Biology, Vol. 17, Issue 4 https://doi.org/10.1111/j.1365-2486.2010.02319.x	journal	September 2010
The Genus Scirpus Linn.: Critical Species of the Section Pterolepis Koyama, Tetsuo Canadian Journal of Botany, Vol. 41, Issue 7 https://doi.org/10.1139/b63-091	journal	July 1963
A genetic analysis of hydrologically dispersed seeds of Hibiscus moscheutos (Malvaceae) Kudoh, Hiroshi; Whigham, Dennis F. American Journal of Botany, Vol. 88, Issue 4 https://doi.org/10.2307/2657057	journal	April 2001
Elevated CO2 stimulates marsh elevation gain, counterbalancing sea-level rise Langley, J. A.; McKee, K. L.; Cahoon, D. R. Proceedings of the National Academy of Sciences, Vol. 106, Issue 15 https://doi.org/10.1073/pnas.0807695106	journal	March 2009
Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift Langley, J. Adam; Megonigal, J. Patrick Nature, Vol. 466, Issue 7302 https://doi.org/10.1038/nature09176	journal	July 2010
Global change and marsh elevation dynamics: experimenting where land meets sea and biology meets geology Langley, J. A.; Sigrist, M. V.; Duls, J. Smithsonian Contributions to the Marine Sciences, Vol. 38 https://doi.org/10.5479/si.01960768.38.391	journal	January 2009
Tidal marsh plant responses to elevated CO ₂ , nitrogen fertilization, and sea level rise Adam Langley, J.; Mozdzer, Thomas J.; Shepard, Katherine A. Global Change Biology, Vol. 19, Issue 5 https://doi.org/10.1111/gcb.12147	journal	February 2013
Reply to w. g. Abrahamson Law, Richard; Bradshaw, A. D.; Putwain, P. D. Evolution, Vol. 33, Issue 1Part2 https://doi.org/10.1111/j.1558-5646.1979.tb04706.x	journal	March 1979
Interactive Effect of Elevated Carbon Dioxide and Elevated Temperature on Growth and Yield of Soybean Lenka, Narendra K.; Lenka, Sangeeta; Thakur, J. K. Current Science, Vol. 113, Issue 12 https://doi.org/10.18520/cs/v113/i12/2305-2310	journal	December 2017
Development of Wild and Cultivated Plants under Global Warming Conditions Lippmann, Rebecca; Babben, Steve; Menger, Anja Current Biology, Vol. 29, Issue 24 https://doi.org/10.1016/j.cub.2019.10.016	journal	December 2019
Partitioning of Reproductive Effort in Clonal Plants: A Benefit-Cost Model Loehle, Craig Oikos, Vol. 49, Issue 2 https://doi.org/10.2307/3566027	journal	June 1987
Nitrogen status regulates morphological adaptation of marsh plants to elevated CO2 Lu, Meng; Herbert, Ellen R.; Langley, J. Adam Nature Climate Change, Vol. 9, Issue 10 https://doi.org/10.1038/s41558-019-0582-x	journal	September 2019
Extent and Reproductive Mechanisms of Phragmites australis Spread in Brackish Wetlands in Chesapeake Bay, Maryland (USA) McCormick, Melissa K.; Kettenring, Karin M.; Baron, Heather M. Wetlands, Vol. 30, Issue 1 https://doi.org/10.1007/s13157-009-0007-0	journal	December 2009
Performance of Low‐Cost Open‐Top Chambers to Study Long‐Term Effects of Carbon Dioxide and Climate under Field Conditions Messerli, Jonathan; Bertrand, Annick; Bourassa, Josée Agronomy Journal, Vol. 107, Issue 3 https://doi.org/10.2134/agronj14.0571	journal	May 2015
Elevated CO₂ concentration, nitrogen use, and seed production in annual plants Miyagi, Kay‐May; Kinugasa, Toshihiko; Hikosaka, Kouki Global Change Biology, Vol. 13, Issue 10 https://doi.org/10.1111/j.1365-2486.2007.01429.x	journal	August 2007
Controls on seed production and seed germinability inEriophorum vaginatum Molau, U.; Shaver, G. R. Global Change Biology, Vol. 3, Issue S1 https://doi.org/10.1111/j.1365-2486.1997.gcb130.x	journal	December 1997
Deep rooting and global change facilitate spread of invasive grass Mozdzer, Thomas J.; Langley, J. Adam; Mueller, Peter Biological Invasions, Vol. 18, Issue 9 https://doi.org/10.1007/s10530-016-1156-8	journal	June 2016
Invasive alien plants in marine protected areas: the Spartina anglica affair in the European Wadden Sea Nehring, Stefan; Hesse, Karl-Jürgen Biological Invasions, Vol. 10, Issue 6 https://doi.org/10.1007/s10530-008-9244-z	journal	March 2008
Reproductive Strategies in Herbaceous Plant Communities During Succession Newell, Sandra Jo; Tramer, Elliot J. Ecology, Vol. 59, Issue 2 https://doi.org/10.2307/1936367	journal	March 1978
Asynchronous nitrogen supply and demand produce nonlinear plant allocation responses to warming and elevated CO ₂ Noyce, Genevieve L.; Kirwan, Matthew L.; Rich, Roy L. Proceedings of the National Academy of Sciences, Vol. 116, Issue 43 https://doi.org/10.1073/pnas.1904990116	journal	October 2019
Oxygen priming induced by elevated CO2 reduces carbon accumulation and methane emissions in coastal wetlands Noyce, Genevieve L.; Smith, Alexander J.; Kirwan, Matthew L. Nature Geoscience, Vol. 16, Issue 1 https://doi.org/10.1038/s41561-022-01070-6	journal	January 2023
The Reproductive Strategy of Higher Plants: II. The Reproductive Strategy of Tussilago Farfara L. Ogden, John The Journal of Ecology, Vol. 62, Issue 1 https://doi.org/10.2307/2258894	journal	March 1974
Plant-soil interactions and nutrient availability determine the impact of elevated CO2 and temperature on cotton productivity Osanai, Yui; Tissue, David T.; Bange, Michael P. Plant and Soil, Vol. 410, Issue 1-2 https://doi.org/10.1007/s11104-016-2981-3	journal	July 2016
Inter-annual variation in seed production has increased over time (1900–2014) Pearse, Ian S.; LaMontagne, Jalene M.; Koenig, Walter D. Proceedings of the Royal Society B: Biological Sciences, Vol. 284, Issue 1868 https://doi.org/10.1098/rspb.2017.1666	journal	December 2017
Elevated CO₂ promotes long‐term nitrogen accumulation only in combination with nitrogen addition Pastore, Melissa A.; Megonigal, J. Patrick; Langley, J. Adam Global Change Biology, Vol. 22, Issue 1 https://doi.org/10.1111/gcb.13112	journal	November 2015
Elevated CO2 and nitrogen addition accelerate net carbon gain in a brackish marsh Pastore, Melissa A.; Megonigal, J. Patrick; Langley, J. Adam Biogeochemistry, Vol. 133, Issue 1 https://doi.org/10.1007/s10533-017-0312-2	journal	March 2017
Adaptive plasticity to heterogeneous environments increases capacity for division of labor in the clonal invader Carpobrotus edulis (Aizoaceae) Roiloa, Sergio R.; Rodriguez‐Echeverria, Susana; Lopez‐Otero, Aaron American Journal of Botany, Vol. 101, Issue 8 https://doi.org/10.3732/ajb.1400173	journal	August 2014
Ending Reliance on Statistical Significance Will Improve Environmental Inference and Communication Smith, Eric P. Estuaries and Coasts, Vol. 43, Issue 1 https://doi.org/10.1007/s12237-019-00679-y	journal	December 2019
The Effects of Density on Resource Partitioning in Chamaesyce hirta (Euphorbiaceae) Snell, Terry W.; Burch, Derek G. Ecology, Vol. 56, Issue 3 https://doi.org/10.2307/1935512	journal	May 1975
Impacts of climate change on submerged and emergent wetland plants Short, Frederick T.; Kosten, Sarian; Morgan, Pamela A. Aquatic Botany, Vol. 135 https://doi.org/10.1016/j.aquabot.2016.06.006	journal	November 2016
Seed production and predation in a changing climate: new roles for resource and seed predator feedback? Solbreck, Christer; Knape, Jonas Ecology, Vol. 98, Issue 9 https://doi.org/10.1002/ecy.1941	journal	August 2017
Rapid plant trait evolution can alter coastal wetland resilience to sea level rise Vahsen, M. L.; Blum, M. J.; Megonigal, J. P. Science, Vol. 379, Issue 6630 https://doi.org/10.1126/science.abq0595	journal	January 2023
Grazing response patterns indicate isolation of semi‐natural European grasslands Weiss, Lina; Pfestorf, Hans; May, Felix Oikos, Vol. 123, Issue 5 https://doi.org/10.1111/j.1600-0706.2013.00957.x	journal	February 2014
C3 and C4 Biomass Allocation Responses to Elevated CO2 and Nitrogen: Contrasting Resource Capture Strategies White, K. P.; Langley, J. A.; Cahoon, D. R. Estuaries and Coasts, Vol. 35, Issue 4 https://doi.org/10.1007/s12237-012-9500-4	journal	May 2012
Intraspecific Competition of Purple Nutsedge (Cyperus rotundus) Under Greenhouse Conditions Williams, R. D.; Quimby, P. C.; Frick, K. E. Weed Science, Vol. 25, Issue 6 https://doi.org/10.1017/S0043174500033944	journal	November 1977
Some Effects of Density on the Reproductive Patterns and Patch Dynamics of Aster acuminatus Winn, Alice A.; Pitelka, Louis F. Bulletin of the Torrey Botanical Club, Vol. 108, Issue 4 https://doi.org/10.2307/2484444	journal	October 1981
The response of plants to elevated CO2 Zangerl, A. R.; Bazzaz, F. A. Oecologia, Vol. 62, Issue 3 https://doi.org/10.1007/BF00384276	journal	June 1984
Causes and Consequences of Invasive Plants in Wetlands: Opportunities, Opportunists, and Outcomes Zedler, Joy B.; Kercher, Suzanne Critical Reviews in Plant Sciences, Vol. 23, Issue 5 https://doi.org/10.1080/07352680490514673	journal	September 2004
Accelerated sea-level rise is suppressing CO ₂ stimulation of tidal marsh productivity: A 33-year study Zhu, Chunwu; Langley, J. Adam; Ziska, Lewis H. Science Advances, Vol. 8, Issue 20 https://doi.org/10.1126/sciadv.abn0054	journal	May 2022
Rising Atmospheric Carbon Dioxide and Seed Yield of Soybean Genotypes Ziska, Lewis H.; Bunce, James A.; Caulfield, Frances A. Crop Science, Vol. 41, Issue 2 https://doi.org/10.2135/cropsci2001.412385x	journal	March 2001

Similar Records

Interactive effects of pollination and heavy metals on resource allocation in Potentilla anserina L.

Journal Article · 1998 · Ecology · OSTI ID:638270

Saikkonen, K; Koivunen, S; Vuorisalo, T; +1 more

Assessing root–soil interactions in wetland plants: root exudation and radial oxygen loss

Journal Article · 2024 · Biogeosciences (Online) · OSTI ID:2478313

Haviland, Katherine A.; Noyce, Genevieve L.

Clonality, local population structure, and gametophyte sex ratios in cryptic species of the Sphagnum magellanicum complex

Journal Article · 2023 · Annals of Botany · OSTI ID:1994618

Shaw, A. Jonathan; Duffy, Aaron M.; Nieto-Lugilde, Marta; +10 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
Clonal plants
Wetland
Global warming
Seed production
Sexual reproduction
Schoenoplectus americanus

Title: Reproductive Responses to Increased Shoot Density and Global Change Drivers in a Widespread Clonal Wetland Species, Schoenoplectus americanus

Citation Formats

References (65)

Similar Records

Related Subjects