Root and shoot competition lead to contrasting competitive outcomes under water stress: A systematic review and meta-analysis
Autoři:
Alicia J. Foxx aff001; Florian Fort aff003
Působiště autorů:
Plant Biology and Conservation; Northwestern University, Evanston, Illinois, United States of America
aff001; Plant Science and Conservation, The Chicago Botanic Garden, Glencoe, Illinois, United States of America
aff002; CEFE, Montpellier SupAgro, Université de Montpellier, CNRS, EPHE, IRD, Université Paul Valéry, Montpellier, France
aff003
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0220674
Souhrn
Background
Competition is a critical process that shapes plant communities and interacts with environmental constraints. There are surprising knowledge gaps related to mechanisms that belie competitive processes, though important to natural communities and agricultural systems: the contribution of different plant parts on competitive outcomes and the effect of environmental constraints on these outcomes.
Objective
Studies that partition competition into root-only and shoot-only interactions assess whether plant parts impose different competitive intensities using physical partitions and serve as an important way to fill knowledge gaps. Given predicted drought escalation due to climate change, we focused a systematic review–including a meta-analysis on the effects of water supply and competitive outcomes.
Methods
We searched ISI Web of Science for peer-reviewed studies and found 2042 results. From which eleven suitable studies, five of which had extractable information of 80 effect sizes on 10 species to test these effects. We used a meta-analysis to compare the log response ratios (lnRR) on biomass for responses to competition between roots, shoots, and full plants at two water levels.
Results
Water availability treatment and competition treatment (root-only, shoot-only, and full plant competition) significantly interacted to affect plant growth responses (p < 0.0001). Root-only and full plant competition are more intense in low water availability (-1.2 and -0.9 mean lnRR, respectively) conditions than shoot-only competition (-0.2 mean lnRR). However, shoot-only competition in high water availability was the most intense (— 0.78 mean lnRR) compared to root-only and full competition (-0.5 and 0.61 mean lnRR, respectively) showing the opposite pattern to low water availability. These results also show that the intensity of full competition is similar to root-only competition and that low water availability intensifies root competition while weakening shoot competition.
Conclusions
The outcome that competition is most intense between roots at low water availability emphasizes the importance of root competition and these patterns of competition may shift in a changing climate, creating further urgency for further studies to fil knowledge gaps addressing issues of drought on plant interactions and communities.
Klíčová slova:
Community structure – Water resources – Biomass – Publication ethics – Plant growth and development – Mechanical stress – Plant communities
Zdroje
1. Godoy O, Kraft N LJ. Phylogenetic relatedness and the determinants of competitive outcomes. Ecol Lett. 2014;17: 836–844. doi: 10.1111/ele.12289 24766326
2. HilleRisLambers J, Adler PB, Harpole WS, Levine JM, Mayfield MM. Rethinking Community Assembly through the Lens of Coexistence Theory. Annu Rev Ecol Evol Syst. 2012;43: 227–248. doi: 10.1146/annurev-ecolsys-110411-160411
3. Kraft NJB, Crutsinger GM, Forrestel EJ, Emery NC. Functional trait differences and the outcome of community assembly: an experimental test with vernal pool annual plants. Oikos. 2014;123: 1391–1399. doi: 10.1111/oik.01311
4. Mayfield MM, Levine JM. Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Lett. 2010;13: 1085–1093. doi: 10.1111/j.1461-0248.2010.01509.x 20576030
5. Chesson P. Quantifying and testing species coexistence mechanisms. Unity in Diversity: Reflections on Ecology after the legacy of Ramon Margalef. 2008. pp. 119–164.
6. Chesson P. Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst. 2000;31: 343–366.
7. Kunstler G, Lavergne S, Courbaud B, Thuiller W, Vieilledent G, Zimmermann NE, et al. Competitive interactions between forest trees are driven by species’ trait hierarchy, not phylogenetic or functional similarity: implications for forest community assembly. Ecol Lett. 2012;15: 831–840. doi: 10.1111/j.1461-0248.2012.01803.x 22625657
8. Schamp BS, Aarssen LW. The assembly of forest communities according to maximum species height along resource and disturbance gradients. Oikos. 2009;118: 564–572. doi: 10.1111/j.1600-0706.2009.16589.x
9. Aerts R. Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot. 1999;50: 29–37. doi: 10.1093/jexbot/50.330.29
10. Acciaresi H, Guiamet J. Below- and above-ground growth and biomass allocation in maize and Sorghum halepense in response to soil water competition. Weed Res. 2010;50: 481–492. doi: 10.1111/j.1365-3180.2010.00794.x
11. Owen SM, Sieg CH, Johnson NC, Gehring CA. Exotic cheatgrass and loss of soil biota decrease the performance of a native grass. Biol Invasions. 2013;15: 2503–2517. doi: 10.1007/s10530-013-0469-0
12. Parkinson H, Zabinski C, Shaw N. Impact of Native Grasses and Cheatgrass (Bromus tectorum) on Great Basin Forb Seedling Growth. Rangel Ecol Manag. 2013;66: 174–180. doi: 10.2111/REM-D-11-00028.1
13. Diaz S., Hodgson J.G.; Thompson K.; Cabido M.; Cornelissen J.H.C.; Jalili A; et al. The plant traits that drive ecosystems: Evidence from three continents. J Veg Sci. 2004;15: 295–304.
14. Bu W, Huang J, Xu H, Zang R, Ding Y, Li Y, et al. Plant Functional Traits Are the Mediators in Regulating Effects of Abiotic Site Conditions on Aboveground Carbon Stock-Evidence From a 30 ha Tropical Forest Plot. Front Plant Sci. 2019;9: 1–10. doi: 10.3389/fpls.2018.01958 30687357
15. Bardgett RD, Mommer L, De Vries FT. Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol. 2014;29: 692–699. doi: 10.1016/j.tree.2014.10.006 25459399
16. Murphy GP, Dudley SA. Above- and below-ground competition cues elicit independent responses. J Ecol. 2007; 261–272. doi: 10.1111/j.1365-2745.2007.01217.x
17. Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, et al. Let the concept of trait be functional! Oikos. 2007;116: 882–892. doi: 10.1111/j.2007.0030–1299.15559.x
18. Funk JL, Cleland EE, Suding KN, Zavaleta ES. Restoration through reassembly: plant traits and invasion resistance. Trends Ecol Evol. 2008;23: 695–703. doi: 10.1016/j.tree.2008.07.013 18951652
19. Kembel SW, Cahill J. Independent Evolution of Leaf and Root Traits within and among Temperate Grassland Plant Communities. PLoS One. 2011;6: 2–10. doi: 10.1371/journal.pone.0019992 21687704
20. Kiaer LP, Weisbach AN, Weiner J. Root and shoot competition: a meta-analysis. Gibson D, editor. J Ecol. 2013;101: 1298–1312. doi: 10.1111/1365-2745.12129
21. Hsiao TC. Plant Responses to Water Stress. Annu Rev Plant Physiol. 1973;24: 519–570. doi: 10.1146/annurev.pp.24.060173.002511
22. Hsiao TC, Xu LK. Sensitivity of with of roots versus leaves to water stress: Biophysical analysis and relation to water. J Exp Bot. 2000;51: 1595–1616. doi: 10.1093/jexbot/51.350.1595 11006310
23. Taiz L, Zeigler E. Plant Physiology (Third Edition). Annals of Botany. 2002. doi: 10.1093/aob/mcg079
24. Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L. Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol. 2012;193: 30–50. doi: 10.1111/j.1469-8137.2011.03952.x 22085245
25. Wang X, Taub DR. Interactive effects of elevated carbon dioxide and environmental stresses on root mass fraction in plants: a meta-analytical synthesis using pairwise techniques. Oecologia. 2010;163: 1–11. doi: 10.1007/s00442-010-1572-x 20155287
26. Jupp A, Newman I. Morphological and anatomical effects of severe drought on the roots of Lolium perenne L. New Phytol. 1987;105: 393–402.
27. Sharp RE, Davies WJ. Solute regulation and growth by roots and shoots of water-stressed maize plants. Planta. 1979;147: 43–49. doi: 10.1007/BF00384589 24310893
28. Berendse F, Móller F. Effects of competition on root-shoot allocation in Plantago lanceolata L.: adaptive plasticity or ontogenetic drift? Plant Ecol. 2009;201: 567–573. doi: 10.1007/sll258-008-9485-z
29. Silva DD, Kane ME, Beeson RC. Changes in root and shoot growth and biomass partition resulting from different irrigation intervals for Ligustrum japonicum Thunb. HortScience. 2012;47: 1634–1640.
30. Sharp R, Davies W. Root growth and water uptake by maize plants in drying soil. J Exp. 1985;36: 1441–1456.
31. Jentsch A, Kreyling J, Elmer M, Gellesch E, Glaser B, Grant K, et al. Climate extremes initiate ecosystem-regulating functions while maintaining productivity. J Ecol. 2011;99: 689–702. doi: 10.1111/j.1365-2745.2011.01817.x
32. Gargallo-Garriga A, Sardans J, Perez-Trujillo M, Rivas-Ubach A, Oravec M, Vecerova K, et al. Opposite metabolic responses of shoots and roots to drought. Sci Repors. 2014;4: 1–7. doi: 10.1038/srep06829 25351427
33. Casper BB, Jackson RB. Plant competition underground. Annu Rev Ecol Syst. 1997;28: 545–570.
34. Lamb EG, Shore BH, Cahill JF. Water and nitrogen addition differentially impact plant competition in a native rough Fescue grassland. Plant Ecol. 2007;192: 21–33. doi: 10.1007/sll258-006-9222-4
35. Dauro D, Mohamed-Saleem M. Shoot and root interactions in intercopped wheat and clover. Trop Agric. 1995;72: 170–172.
36. Weigelt A, Steinlein T, Beyschlag W. Competition among three dune species: the impact of water availability on below- ground processes. Plant Ecol. 2005;176: 57–68.
37. Seager R, Ting M, Held I, Kushnir Y, Lu J, Vecchi G, et al. Model Projections of an Imminent Transition to a More Arid Climate in Southwestern North America. Science (80-). 2007;316: 1181–1185.
38. Rajaniemi TK, Allison VJ, Goldberg DE. Root competition can cause a decline in diversity with increased productivity. J Ecol. 2003;91: 407–416. doi: 10.1046/j.1365-2745.2003.00768.x
39. Liancourt P, Lavorel S. Importance and intensity of competition along a fertility gradient and across species. 2013;17: 455–464.
40. Silvertown J, Araya Y, Gowing D. Hydrological niches in terrestrial plant communities: a review. J Ecol. 2015;103: 93–108. doi: 10.1111/1365-2745.12332
41. Fort F, Cruz P, Jouany C. Hierarchy of root functional trait values and plasticity drive early-stage competition for water and phosphorus among grasses. Funct Ecol. 2014;28: 1030–1040. doi: 10.1111/1365-2435.12217
42. Hanke JM, Ludewig K, Jensen K. Effects of water level and competition on the endangered river corridor plant Cnidium dubium in the context of climate change. Wetl Ecol Manag. 2015;23: 215–226. doi: 10.1007/s11273-014-9371-5
43. Weigelt A, Röttgermann M, Steinlein T. Sandy soils influence of water availability on competitive interactions between plant species. Folia Geobot. 2000;35: 169–178.
44. McCluney KE, Belnap J, Collins SL, González AL, Hagen EM, Nathaniel Holland J, et al. Shifting species interactions in terrestrial dryland ecosystems under altered water availability and climate change. Biol Rev. 2012;87: 563–582. doi: 10.1111/j.1469-185X.2011.00209.x 22098619
45. Prieto I, Padilla FM, Armas C, Pugnaire FI. The role of hydraulic lift on seedling establishment under a nurse plant species in a semi-arid environment. Perspect Plant Ecol Evol Syst. 2011;13: 181–187. doi: 10.1016/j.ppees.2011.05.002
46. Coomes DA, Grubb PJ. Impacts of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecol Monogr. 2000;70: 171–207.
47. Koricheva J, Gurevitch J. Uses and misuses of meta-analysis in plant ecology. J Ecol. 2014;102: 828–844. doi: 10.1111/1365-2745.12224
48. Rohatgi A. WebPlotDigitizer. In: https://automeris.io/WebPlotDigitizer/. 2015 p. Accessed 3-15-19.
49. Salinger S, Bornkamm R. Production of organic matter and interference of two grasses at different levels of water supply. Agro-Ecosystems. 1982;7: 277–292.
50. Bartelheimer M, Gowing D, Silvertown J. Explaining hydrological niches: The decisive role of below-ground competition in two closely related Senecio species. J Ecol. 2010;98: 126–136. doi: 10.1111/j.1365-2745.2009.01598.x
51. Wilkinson S, Gross C. Competition for light, soil moisture and nutrients during Landino clover establishment in Orchardgrass Sod. Agron J. 1964;56: 389–392.
52. Bornkamm R, Salinger S, Strehlow H. Productivity and Chemical Constituents of two Grasses under Pure and Mixed Cultivations. Flor Biodivers. 1975;164: 437–448.
53. R Core Team. R: A language and environment for statistical computing. R Statistical Computing,. Vienna, Austria URL https://wwwR-project.org/. 2019.
54. Viechtbauer W. Conducting Meta-Analyses in R with the metafor package. J Stat Softw. 2010;36.
55. Hedges L V, Gurevitch J, Curtis PS. The Meta-Analysis of Response Ratios in Experimental Ecology. Ecology. 1999;80: 1150–1156.
56. Valentine JC, Pigott TD, Rothstein HR. How Many Studies Do You Need? J Educ Behav Stat. 2010;35: 215–247. doi: 10.3102/1076998609346961
57. Lajeunesse MJ. Recovering Missing or Partial Data from Studies: A Survey of Conversions and Imputations for Meta-analysis. Handbook of Meta-analysis in Ecology and Evolution. 2013. pp. 195–206. doi: 10.1515/9781400846184-015
58. Fox J, Weisberg S. An {R} Companion to Applied Regression. 2019. p. Thousand Oaks, CA. https://socialsciences.mcmaster.
59. Putz F, Canham C. Mechanisms of arrested succession in shrublands: root and shoot competition between shrubs and tree seedlings. For Ecol Manage. 1992;49: 267–275.
60. Cohn LD, Decker BJ. How Meta-Analysis Increases Statistical Power. Psychol Methods. 2003;8: 243–253. doi: 10.1037/1082-989X.8.3.243 14596489
61. Moher D, Liberati A, Tetzlaff J, Altman DG TPG. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med. 2009;6: e1000097. doi: 10.1371/journal.pmed.1000097 19621072
62. Welbank PJ. A Study of the Nitrogen and Water Factors in Competition with Agropyron repens (L.) Beauv. Ann Bot. 1961;25: 116–137. doi: 10.1093/oxfordjournals.aob.a083737
63. Semere T, Froud-Williams RJ. The effect of pea cultivar and water stress on root and shoot competition between vegetative plants of maize and pea. J Appl Ecol. 2001;38: 137–145. doi: 10.1046/j.1365-2664.2001.00570.x
64. Haugland E, Froud-Williams R. Improving grasslands: the influence of soil moisture and nitrogen fertilization on the establishment of seedlings. J Appl Ecol. 1999;36: 263–270. Available: http://scholar.google.com/scholar?hl=en&btnG=Search&q=intitle:Copyright+©2001.+All+Rights+Reserved.#0
65. IPCC. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Intergovernmental Panel on Climage Change In Stocker TF, Qin D, Plattner GK, Tignor MMB, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, eds, Climate Change 2013: The Physical Science Basis Cambridge University Press, New York. 2014. p. 1335.
66. Verwijmeren M, Rietkerk M, Bautista S, Mayor AG, Wassen MJ, Smit C. Drought and grazing combined: Contrasting shifts in plant interactions at species pair and community level. J Arid Environ. 2014;111: 53–60. doi: 10.1016/j.jaridenv.2014.08.001
67. Leguizamón E, Yanniccari M, Guiamet J, Acciaresi H. Growth, gas exchange and competitive ability of Sorghum halepense populations under different soil water availability. Can J Plant Sci. 2011;91: 1011–1025. doi: 10.4141/cjps10202
68. Howard TG, Goldberg DE. Competitive response hierarchies for germination, growth, and survival and their influence on abundance. Ecology. 2001;82: 979–990.
69. Gundel PE, Pierik R, Mommer L, Ballaré CL. Competing neighbors: Light perception and root function. Oecologia. 2014;176: 1–10. doi: 10.1007/s00442-014-2983-x 24894371
70. van Gelderen K, Kang C, Pierik R. Light signaling, root development and plasticity. Plant Physiol. 2017;176: pp.01079.2017. doi: 10.1104/pp.17.01079 28939624
71. Twolan-Strutt L, Keddy P. Above- and Belowground Competition Intensity in Two Contrasting Wetland Plant Communities. Ecology. 1996;77: 259–270.
72. Kraft N, Godoy O, Levine J. Plant functional traits and the multidimensional nature of species coexistence. Proc Natl Acad Sci. 2015;112: 797–802. doi: 10.1073/pnas.1413650112 25561561
73. Bertness MD, Callaway RM. Positive interactions in communities. Trends Ecol Evol. 1994; 191–193. doi: 10.1016/0169-5347(94)90088-4 21236818
74. Fowler N. The Role of Competition in Plant Communities in Arid and Semiarid Regions. Annu Rev Ecol Syst. 1986;17: 89–110. doi: 10.1146/annurev.es.17.110186.000513
75. Sharma RB and Ghidyal B. Soil water-root relations in wheat: water extraction rate of wheat roots that developed under dry and moist conditions. Agron J. 1977;69: 231–233.
76. Gedroc J, McConnaughay D, Coleman J. Plasticity in root/shoot partitioning: optimal, ontogenetic, or both? Funct Ecol. 1996;10: 44–50.
77. Mommer L, van Ruijven J, Jansen C, van de Steeg HM, de Kroon H. Interactive effects of nutrient heterogeneity and competition: implications for root foraging theory? Funct Ecol. 2012;26: 66–73. doi: 10.1111/j.1365-2435.2011.01916.x
78. Treder K, Jastrz M, Kostrzewska MK, Wanic M. Effect of competitive interactions and water stress on morphological characteristics of red clover (Trifolium pratense L.) cultivated with spring barley (Hordeum vulgare L.). Acta Sci Pol Ser Agric. 2016;15: 83–94.
79. Schenk HJ, Jackson RB. Rooting depths, lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems. J Ecol. 2002;90: 480–494. doi: 10.1046/j.1365-2745.2002.00682.x
80. Lamb EG, Kembel SW, Cahill JF. Shoot, but not root, competition reduces community diversity in experimental mesocosms. J Ecol. 2009;97: 155–163. doi: 10.1111/j.1365-2745.2008.01454.x
81. Fortunel C, Valencia R, Wright SJ, Garwood NC, Kraft NJB. Functional trait differences influence neighbourhood interactions in a hyperdiverse Amazonian forest. Ecol Lett. 2016;19: 1062–70. doi: 10.1111/ele.12642 27358248
82. Cahill J. What evidence is necessary in studies which separate root and shoot competition along productivity gradients? J Ecol. 2002;90: 201–205.
83. Adler PB, Smull D, Beard KH, Choi RT, Furniss T, Kulmatiski A, et al. Competition and coexistence in plant communities: intraspecific competition is stronger than interspecific competition. Ecol Lett. 2018;21: 1319–1329. doi: 10.1111/ele.13098 29938882
84. BMJ. What is publication bias in a meta-analysis? 2015;351.
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts