Evolution of competitive ability and the response to nutrient availability: a resurrection study with the calcareous grassland herb, Leontodon hispidus

. 2025 Jan 04 ; 207 (1) : 17. [epub] 20250104

Jazyk angličtina Země Německo Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39754643

Grantová podpora
20020/678 Deutsche Bundesstiftung Umwelt

Odkazy

PubMed 39754643
PubMed Central PMC11700050
DOI 10.1007/s00442-024-05657-1
PII: 10.1007/s00442-024-05657-1
Knihovny.cz E-zdroje

Rapid environmental changes across Europe include warmer and increasingly variable temperatures, changes in soil nutrient availability, and pollinator decline. These abiotic and biotic changes can affect natural plant populations and force them to optimize resource use against competitors. To date, the evolution of competitive ability in the context of changes in nutrient availability remains understudied. In this study, we investigated whether the common calcareous grassland herb Leontodon hispidus recently evolved its competitive ability and response to nutrient availability. We compared ancestors sampled in 1995 and descendants sampled in 2018 and applied a competition treatment in combination with weekly nutrient treatments (no fertilizer, nitrogen, phosphorus, and both). We found evidence for evolution of increased competitive ability, with descendants producing more vegetative biomass than ancestors when grown under competition. Furthermore, supplementing nutrients (especially N) reduced differences in competitive ability between ancestors and descendants, suggesting that nutrients are a limiting factor in interspecific competition, which could be linked to the decreasing nitrogen emissions into the atmosphere since the 1990s. Our study demonstrates rapid contemporary evolution of competitive ability, but also the complexity of the underlying processes of contemporary evolution, and sheds light on the importance of understudied potential selection agents such as nutrient availability.

Zobrazit více v PubMed

Alt F, Oelmann Y, Herold N, Schrumpf M, Wilcke W (2011) Phosphorus partitioning in grassland and forest soils of Germany as related to land-use type, management intensity, and land use-related pH. J Plant Nutr Soil Sci 174:195–209. 10.1002/jpln.201000142

Amtmann A, Blatt MR (2009) Regulation of macronutrient transport. New Phytol 181:35–52. 10.1111/j.1469-8137.2008.02666.x PubMed

Ba̧ba W (2003) Changes in the structure and floristic composition of the limestone grasslands after cutting trees and shrubs and mowing. Acta Soc Bot Pol 72:61–69. 10.5586/asbp.2003.008

Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. 10.18637/jss.v067.i01

BDB (2005) Chemical soil fertility of arable land and grassland in Belgium 2000–2003. Bodemkundige Dienst België, Leuven

Bennett JA, Riibak K, Tamme R, Tamme R, Lewis RJ, Pärtel M (2016) The reciprocal relationship between competition and intraspecific trait variation. J Ecol 104:1410–1420. 10.1111/1365-2745.12614

Bobbink R, Willems JH (1987) Increasing dominance of Brachypodium pinnatum (L.) beauv. in chalk grasslands: a threat to a species-rich ecosystem. Biol Conserv 40:301–314. 10.1016/0006-3207(87)90122-4

Bobbink R, Hornung M, Roelofs JGM (1998) The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. J Ecol 86:717–738. 10.1046/j.1365-2745.1998.8650717.x

Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M et al (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59. 10.1890/08-1140.1 PubMed

Bonser SP, Ladd B (2011) The evolution of competitive strategies in annual plants. Plant Ecol 212:1441–1449. 10.1007/s11258-011-9919-x

Canals RM, Emeterio LS, Durán M, Múgica L (2017) Plant-herbivory feedbacks and selective allocation of a toxic metal are behind the stability of degraded covers dominated by Brachypodium pinnatum in acidic soils. Plant Soil 415:373–386. 10.1007/s11104-016-3153-1

Casal JJ (2012) Shade avoidance, The Arabidopsis Book, 2012(10). 10.1199/tab.0157 PubMed PMC

Ceulemans T, Merckx R, Hens M, Honnay O (2011) A trait-based analysis of the role of phosphorus vs. nitrogen enrichment in plant species loss across North-west European grasslands. J Appl Ecol 48:1155–1163. 10.1111/j.1365-2664.2011.02023.x

Ceulemans T, Merckx R, Hens M, Honnay O (2013) Plant species loss from European semi-natural grasslands following nutrient enrichment—is it nitrogen or is it phosphorus? Glob Ecol Biogeogr 22:73–82. 10.1111/j.1466-8238.2012.00771.x

Ceulemans T, Stevens CJ, Duchateau L, Jacquemyn H, Gowing DJG, Merckx R et al (2014) Soil phosphorus constrains biodiversity across European grasslands. Glob Chang Biol 20:3814–3822. 10.1111/gcb.12650 PubMed

Cheptou PO, Avendaño VLG (2006) Pollination processes and the Allee effect in highly fragmented populations: consequences for the mating system in urban environments. New Phytol 172:774–783. 10.1111/j.1469-8137.2006.01880.x PubMed

Clark CM, Tilman D (2008) Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715. 10.1038/nature06503 PubMed

Cleland EE, Harpole WS (2010) Nitrogen enrichment and plant communities. Ann N Y Acad Sci 1195:46–61. 10.1111/j.1749-6632.2010.05458.x PubMed

Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE et al (2009) Ecology—controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015. 10.1126/science.1167755 PubMed

Craine JM, Dybzinski R (2013) Mechanisms of plant competition for nutrients, water and light. Funct Ecol 27:833–840. 10.1111/1365-2435.12081

Craine JM, Fargione J, Sugita S (2005) Supply pre-emption, not concentration reduction, is the mechanism of competition for nutrients. New Phytol 166:933–940. 10.1111/j.1469-8137.2005.01386.x PubMed

Djodjic F, Börling K, Bergström L (2004) Phosphorus leaching in relation to soil type and soil phosphorus content. J Environ Qual 33:678–684. 10.2134/jeq2004.6780 PubMed

Dore MHI (2005) Climate change and changes in global precipitation patterns: What do we know? Environ Int 31:1167–1181. 10.1016/j.envint.2005.03.004 PubMed

Easlon HM, Bloom AJ (2014) Easy leaf area: automated digital image analysis for rapid and accurate measurement of leaf area. Appl Plant Sci 2:1400033. 10.3732/apps.1400033 PubMed PMC

Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO et al (2010) Plant mating systems in a changing world. Trends Ecol Evol 25:35–43. 10.1016/j.tree.2009.06.013 PubMed

European Environment Agency (2021) EEA emission inventory report

Egan G, McKenzie P, Crawley M, Fornara DA (2019) Effects of grassland management on plant nitrogen use efficiency (NUE): evidence from a long-term experiment. Basic Appl Ecol 41:33–43. 10.1016/j.baae.2019.10.001

Engel EC, Irwin RE (2003) Linking pollinator visitation rate and pollen receipt. Am J Bot 90:1612–1618. 10.3732/ajb.90.11.1612 PubMed

Falster DS, Westoby M (2003) Plant height and evolutionary games. Trends Ecol Evol 18:337–343. 10.1016/S0169-5347(03)00061-2

Frachon L, Libourel C, Villoutreix R, Carrère S, Glorieux C, Huard-Chauveau C et al (2017) Intermediate degrees of synergistic pleiotropy drive adaptive evolution in ecological time. Nat Ecol Evol 1:1551–1561. 10.1038/s41559-017-0297-1 PubMed

Franks SJ, Sim S, Weis AE (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc Natl Acad Sci U S A 104:1278–1282. 10.1073/pnas.0608379104 PubMed PMC

Franks SJ, Hamann E, Weis AE (2018) Using the resurrection approach to understand contemporary evolution in changing environments. Evol Appl 11:17–28. 10.1111/eva.12528 PubMed PMC

Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892. 10.1126/science.1136674 PubMed

Gao Y, Liang Y, Fu Y, Si Z, Hamani AKM (2022) Interactive effects of intraspecific competition and drought on stomatal conductance and hormone concentrations in different tomato genotypes. Horticulturae. 10.3390/horticulturae8010045

Grime JP (1973) Competitive exclusion in herbaceous vegetation. Nature 242:344–347. 10.5860/choice.45-3516

Habel JC, Dengler J, Janišová M, Török P, Wellstein C, Wiezik M (2013) European grassland ecosystems: threatened hotspots of biodiversity. Biodivers Conserv 22:2131–2138. 10.1007/s10531-013-0537-x

Hamann E, Weis AE, Franks SJ (2018) Two decades of evolutionary changes in Brassica rapa in response to fluctuations in precipitation and severe drought. Evolution 8:2682–2696. 10.1111/evo.13631 PubMed

Hamann E, Pauli CS, Joly-Lopez Z, Groen SC, Rest JS, Kane NC et al (2021) Rapid evolutionary changes in gene expression in response to climate fluctuations. Mol Ecol 30:193–206. 10.1111/mec.15583 PubMed PMC

Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–638. 10.1126/science.1169640 PubMed

Hoste I, Van Landuyt W, Verloove F (2006) Atlas van de flora van Vlaanderen en het Brussels Gewest. Hoofdstuk 4. Landschap en flora in beweging, 19de en 20ste eeuw. pp 44–67

IPCC (2018) Summary for Policymakers. In: Global warming of 1.5 °C. An IPCC Special Report on the impacts of global warming of 1.5 °C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global

Janssens F, Peeters A, Tallowin JRB, Bakker JP, Bekker RM, Fillat F et al (1998) Relationship between soil chemical factors and grassland diversity. Plant Soil 202:69–78. 10.1023/A:1004389614865

Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? 3:749–757. 10.2307/1942106 PubMed

Karitter P, March-Salas M, Ensslin A, Rauschkolb R, Godefroid S, Scheepens JF (2024) Combining the resurrection approach with transplant experiments to investigate adaptation of plant populations to environmental change. Perspect Plant Ecol Evol Syst. 10.1016/j.ppees.2023.125773

Ketterings QM, Kahabka JE, Reid WS (2005) Trends in phosphorus fertility of New York agricultural land. J Soil Water Conserv 60:10–20

Klein H, Gauss M, Nyíri Á, Tsyro S (2019) Transboundary air pollution by main pollutants (S, N, O3) and PM in 2017. EMEP Status Report Norwegian Meteorological Institute

Kühn I, Klotz S (2002) BIOLFLOR - a database on biological and ecological traits of vascular plants in Germany. In: Verhandlungen der Gesellschaft für Ökologie. p 42

Lafuma L, Maurice S (2007) Increase in mate availability without loss of self-incompatibility in the invasive species Senecio inaequidens (Asteraceae). Oikos 116:201–208. 10.1111/j.0030-1299.2007.15220.x

Lenth R V. (2021) emmeans: Estimated marginal means, aka least-squares means. https://cran.r-project.org/package=emmeans

Li Y, Wang C, Tang H (2006) Research advances in nutrient runoff on sloping land in watersheds. Aquat Ecosyst Heal Manag 9:27–32. 10.1080/14634980600559379

Liao J, Li Z, Wang J, Tian D, Di T, Niu S (2021) Nitrogen use efficiency of terrestrial plants in China: geographic patterns, evolution, and determinants. Ecol Process 10, 69. 10.1186/s13717-021-00338-w

Lüdecke D, Ben-Shachar M, Patil I, Waggoner P, Makowski D (2021) Performance: an R package for assessment, comparison and testing of statistical models. J Open Source Softw 6:3139. 10.21105/joss.03139

Marschner H (1995) Mineral nutrition in higher plants. Academic Press, London

McGoey BV, Stinchcombe JR (2009) Interspecific competition alters natural selection on shade avoidance phenotypes in Impatiens capensis. New Phytol 183:880–891. 10.1111/j.1469-8137.2009.02934.x PubMed

Mosquin T (1971) Competition for pollinators as a stimulus for the evolution of flowering time. Oikos 22:398–402. 10.2307/3543864

Nevo E, Fu YB, Pavlicek T, Khalifa S, Tavasi M, Beiles A (2012) Evolution of wild cereals during 28 years of global warming in Israel. Proc Natl Acad Sci U S A 109:3412–3415. 10.1073/pnas.1121411109 PubMed PMC

Newman EI (1973) Competition and diversity in herbaceous vegetation. Nature 244:310–311. 10.1038/244310a0

Newman EI (1995) Phosphorus inputs to terrestrial ecosystems. Br Ecol Soc 83:713–726. 10.2307/2261638

Occhipinti A (2013) Plant coevolution: evidences and new challenges. J Plant Interact 8:188–196. 10.1080/17429145.2013.816881

Olsson PA, Tyler G (2004) Occurrence of non-mycorrhizal plant species in south Swedish rocky habitats is related to exchangeable soil phosphate. J Ecol 92:808–815. 10.1111/j.0022-0477.2004.00912.x

Parkhurst T, Standish RJ, Prober SM (2022) P is for persistence: soil phosphorus remains elevated for more than a decade after old field restoration. Ecol Appl 32:1–13. 10.1002/eap.2547 PubMed

Peñuelas J, Sardans J, Rivas-ubach A, Janssens IA (2012) The human-induced imbalance between C, N and P in Earth’s life system. Glob Chang Biol 18:3–6. 10.1111/j.1365-2486.2011.02568.x

Phoenix GK, Hicks WK, Cinderby S, Kuylenstierna JCI, Stock WD, Dentener FJ et al (2006) Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Glob Chang Biol 12:470–476. 10.1111/j.1365-2486.2006.01104.x

Piqueray J, Bottin G, Delescaille L-M, Bisteau E, Colinet G, Mahy G (2011) Rapid restoration of a species-rich ecosystem assessed from soil and vegetation indicators: the case of calcareous grasslands restored from forest stands. Ecol Indic 11:724–733. 10.1016/j.ecolind.2010.06.007

Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. 10.1016/j.tree.2010.01.007 PubMed

R Core Team (2020) R: a language and environment for statistical computing

Rauschkolb R, Li Z, Godefroid S, Dixon L, Durka W, Májeková M et al (2022) Evolution of plant drought strategies and herbivore tolerance after two decades of climate change. New Phytol 235:773–785. 10.1111/nph.18125 PubMed

Rauschkolb R, Durka W, Godefroid S, Dixon L, Bossdorf O, Ensslin A et al (2023) Recent evolution of flowering time across multiple European plant species correlates with changes in aridity. Oecologia. 10.1007/s00442-023-05414-w PubMed PMC

Reijneveld JA, Ehlert PAI, Termorshuizen AJ, Oenema O (2010) Changes in the soil phosphorus status of agricultural land in the Netherlands during the 20th century. Soil Use Manag 26:399–411. 10.1111/j.1475-2743.2010.00290.x

Ruosteenoja K, Markkanen T, Venäläinen A, Räisänen P, Peltola H (2018) Seasonal soil moisture and drought occurrence in Europe in CMIP5 projections for the 21st century. Clim Dyn 50:1177–1192. 10.1007/s00382-017-3671-4

Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. 10.1126/science.287.5459.1770 PubMed

Samaniego L, Thober S, Kumar R, Wanders N, Rakovec O, Pan M et al (2018) Anthropogenic warming exacerbates European soil moisture droughts. Nat Clim Chang 8:421–426. 10.1038/s41558-018-0138-5

Sekor MR, Franks SJ (2018) An experimentally introduced population of Brassica rapa (Brassicaceae). 2. rapid evolution of phenotypic traits. Plant Ecol Evol 151:293–302. 10.5091/plecevo.2018.1401

Silva EC, Jurema R, Custódio M (2010) Drought stress and plant nutrition. Plant Stress 5:32–41

Simon J, Schmidt S (2017) Editorial: Plant competition in a changing world. Front Plant Sci 8:8–10. 10.3389/fpls.2017.00651 PubMed PMC

Smith VH, Tilman GD, Nekola JC (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 8:179–196. 10.1016/S0269-7491(99)00091-3 PubMed

Stevens CJ, Dise NB, Mountford JO, Gowing DJG (2004) Impact of nitrogen deposition grasslands. Science 303:1876–1879. 10.1126/science.1094678 PubMed

Stevens CJ, Dupr C, Dorland E, Gaudnik C, Gowing DJG, Bleeker A et al (2010a) Nitrogen deposition threatens species richness of grasslands across Europe. Environ Pollut 158:2940–2945. 10.1016/j.envpol.2010.06.006 PubMed

Stevens CJ, Thompson K, Grime JP, Long CJ, Gowing DJG (2010b) Contribution of acidification and eutrophication in species richness of calcifuge grasslands along a gradient of atmospheric nitrogen deposition. Funct Ecol 8:478–484. 10.1111/j.1365-2435.2009.01663.x

Sultan SE, Horgan-Kobelski T, Nichols LM, Riggs E, Waples RK (2013) A resurrection study reveals rapid adaptive evolution within populations of an invasive plant. Evol Appl 6:266–278. 10.1111/j.1752-4571.2012.00287.x PubMed PMC

Taiz L, Zeiger E (2006) Plant Physiology, 4th edn. Sinauer Associates, Massachusetts

Thomann M, Imbert E, Devaux C, Cheptou PO (2013) Flowering plants under global pollinator decline. Trends Plant Sci 18:353–359. 10.1016/j.tplants.2013.04.002 PubMed

Thomann M, Imbert E, Cheptou PO (2015a) Is rapid evolution of reproductive traits in Adonis annua consistent with pollinator decline? Acta Oecologica 69:161–166. 10.1016/j.actao.2015.10.007

Thomann M, Imbert E, Engstrand RC, Cheptou PO (2015b) Contemporary evolution of plant reproductive strategies under global change is revealed by stored seeds. J Evol Biol 28:766–778. 10.1111/jeb.12603 PubMed

Thompson J, Charpentier A, Bouguet G, Charmasson F, Roset S, Buatois B et al (2013) Evolution of a genetic polymorphism with climate change in a Mediterranean landscape. Proc Natl Acad Sci U S A 110:2893–2897. 10.1073/pnas.1215833110 PubMed PMC

Tilman D, Fargione J, Wolff B et al (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284. 10.1126/science.1057544 PubMed

van Dobben HF, Wamelink GWW, Slim PA, Kamiński J, Piórkowski H (2017) Species-rich grassland can persist under nitrogen-rich but phosphorus-limited conditions. Plant Soil 411:451–466. 10.1007/s11104-016-3021-z

Walsh B, Lynch M (2018) The nonadaptive forces of evolution. Evol Sel Quant Trait

Weinig C (2000) Differing selection in alternative competitive environments: shade-avoidance responses and germination timing. Evolution 54:124–136. 10.1111/j.0014-3820.2000.tb00013.x PubMed

Weis AE (2018) Detecting the “invisible fraction” bias in resurrection experiments. Evol Appl 11:88–95. 10.1111/eva.12533 PubMed PMC

Wilson PJ, Wheeler BR (2016) A survey and assessment of soil pH and nutrient status on sites of high botanical value 2014

Wilson SD, Tilman D (1993) Plant competition and resource availability in response to disturbance and fertilization. Ecology 74:599–611. 10.2307/1939319

Wooliver R, Tittes SB, Sheth SN (2020) A resurrection study reveals limited evolution of thermal performance in response to recent climate change across the geographic range of the scarlet monkeyflower. Evolution 74:1699–1710. 10.1111/evo.14041 PubMed

Ziska LH (2017) Could recent increases in atmospheric CO2 have acted as a selection factor in Avena fatua populations? A case study of cultivated and wild oat competition. Weed Res 57:399–405. 10.1111/wre.12271

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...