Plant clonality in a soil-impoverished open ecosystem: insights from southwest Australian shrublands

. 2022 Dec 31 ; 130 (7) : 981-990.

Jazyk angličtina Země Velká Británie, Anglie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36282998

BACKGROUND AND AIMS: Clonality is a key life-history strategy promoting on-spot persistence, space occupancy, resprouting after disturbance, and resource storage, sharing and foraging. These functions provided by clonality can be advantageous under different environmental conditions, including resource-paucity and fire-proneness, which define most mediterranean-type open ecosystems, such as southwest Australian shrublands. Studying clonality-environment links in underexplored mediterranean shrublands could therefore deepen our understanding of the role played by this essential strategy in open ecosystems globally. METHODS: We created a new dataset including 463 species, six traits related to clonal growth organs (CGOs; lignotubers, herbaceous and woody rhizomes, stolons, tubers, stem fragments), and edaphic predictors of soil water availability, nitrogen (N) and phosphorus (P) from 138 plots. Within two shrubland communities, we explored multivariate clonal patterns and how the diversity of CGOs, and abundance-weighted and unweighted proportions .of clonality in plots changed along with the edaphic gradients. KEY RESULTS: We found clonality in 65 % of species; the most frequent were those with lignotubers (28 %) and herbaceous rhizomes (26 %). In multivariate space, plots clustered into two groups, one distinguished by sandy plots and plants with CGOs, the other by clayey plots and non-clonal species. CGO diversity did not vary along the edaphic gradients (only marginally with water availability). The abundance-weighted proportion of clonal species increased with N and decreased with P and water availability, yet these results were CGO-specific. We revealed almost no relationships for unweighted clonality. CONCLUSIONS: Clonality is more widespread in shrublands than previously thought, and distinct plant communities are distinguished by specific suites (or lack) of CGOs. We show that weighting belowground traits by aboveground abundance affects the results, with implications for trait-based ecologists using abundance-weighting. We suggest unweighted approaches for belowground organs in open ecosystems until belowground abundance is quantifiable.

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Ackerly  DD, Cornwell WK.  2007. A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecology Letters 10: 135–145. doi:10.1111/j.1461-0248.2006.01006.x. PubMed DOI

Anderson  MJ.  2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46. doi:10.1111/j.1442-9993.2001.01070.pp.x. DOI

Bache  B, Chesworth W, Gessa C, Lewis DT.  2008. Bulk density. In: Chestworth W. ed. Encyclopedia of soil science and earth sciences series. Dordrecht, NL: Springer, 74.

Barton  K.  2020. MuMIn: Multi-Model Inference. https://CRAN.R-project.org/package=MuMIn/index.html (3 March 2022, date last accessed).

Bartušková  A, Filartiga AL, Herben T, Qian J, Klimešová J.  2021. Comparative analysis of root sprouting and its vigour in temperate herbs: anatomical correlates and environmental predictors. Annals of Botany 127: 931–941. doi:10.1093/aob/mcab030. PubMed DOI PMC

Bates  D, Mächler M, Bolker B, Walker S.  2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.

de Bello  F, Botta-Dukát Z, Lepš J, Fibich P.  2021. Towards a more balanced combination of multiple traits when computing functional differences between species. Methods in Ecology and Evolution 12: 443–448.

Bernard-Verdier  M, Navas M-L, Vellend M, Violle C, Fayolle A, Garnier E.  2012. Community assembly along a soil depth gradient: contrasting patterns of plant trait convergence and divergence in a Mediterranean rangeland. Journal of Ecology 100: 1422–1433. doi:10.1111/1365-2745.12003. DOI

Borcard  D, Gillet F, Legendre P.  2018. Numerical ecology with R. Cham: Springer.

Bowen  BJ.  1991. Fire Response Within the Family Proteaceae: A Comparison of Plants Displaying the Seeder and Resprouter Mode of Recovery. PhD dissertation, School of Plant Biology. Perth, AU: The University of Western Australia.

Brooks  ME, Kristensen K, van Benthem KJ, et al. . 2017. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9: 378–400.

Campetella  G, Chelli S, Wellstein C, et al. . 2019. Contrasting patterns in leaf traits of Mediterranean shrub communities along an elevation gradient: measurements matter. Plant Ecology 220: 765–776. doi:10.1007/s11258-019-00951-y. DOI

Chelli  S, Ottaviani G, Tsakalos JL, et al. . 2022. Intra- and inter-specific leaf trait responses of understorey species to changes in forest maturity. Forest Ecology and Management 506: 119977. doi:10.1016/j.foreco.2021.119977. DOI

Cornelissen  JHC, Song Y-B, Yu F-H, Dong M.  2014. Plant traits and ecosystem effects of clonality: a new research agenda. Annals of Botany 114: 369–376. doi:10.1093/aob/mcu113. PubMed DOI PMC

Enright  NJ, Lamont BB.  1992. Survival, growth and water relations of Banksia seedlings on a sand mine rehabilitation site and adjacent scrub-heath sites. Journal of Applied Ecology 29: 663–671. doi:10.2307/2404474. DOI

Falster  D, Gallagher R, Wenk EH, et al. . 2021. AusTraits, a curated plant trait database for the Australian flora. Scientific Data 8: 254. PubMed PMC

Fu  L, Wang S, Liu Z, Nijs I, Ma K, Li Z.  2010. Effects of resource availability on the trade-off between seed and vegetative reproduction. Journal of Plant Ecology 3: 251–258. doi:10.1093/jpe/rtq017. DOI

Gardner  SN, Mangel M.  1999. Modeling investments in seeds, clonal offspring, and translocation in a clonal plant. Ecology 80: 1202–1220. doi:10.1890/0012-9658(1999)080[1202:miisco]2.0.co;2. DOI

Garnier  E, Cortez J, Billès G, et al. . 2004. Plant functional markers capture ecosystem properties during secondary succession. Ecology 85: 2630–2637. doi:10.1890/03-0799. DOI

Grime  JP.  1998. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. Journal of Ecology 86: 902–910. doi:10.1046/j.1365-2745.1998.00306.x. DOI

Groom  PK, Froend RH, Mattiske EM.  2000. Impact of groundwater abstraction on a Banskia woodland, Swan Coastal Plain, Western Australia. Ecological Management and Restoration 1: 117–124.

He  T, Lamont BB, Downes KS.  2011. Banksia born to burn. New Phytologist 191: 184–196. doi:10.1111/j.1469-8137.2011.03663.x. PubMed DOI

Henderson  C, Levett A, Lisle D.  1988. The effects of soil water content and bulk density on the compactibility and soil penetration resistance of some Western Australian sandy soils. Soil Research 26: 391–400. doi:10.1071/sr9880391. DOI

Herath  DN, Lamont BB.  2009. Persistence of resprouting species after fire in natural and post-mine restored shrublands in southwestern Australia. Applied Vegetation Science 12: 451–458. doi:10.1111/j.1654-109x.2009.01040.x. DOI

Herben  T, Klimešová J.  2020. Evolution of clonal growth forms in angiosperms. New Phytologist 225: 999–1010. PubMed

Herben  T, Nováková Z, Klimešová J.  2014. Clonal growth and plant species abundance. Annals of Botany 114: 377–388. doi:10.1093/aob/mct308. PubMed DOI PMC

Herben  T, Vozábová T, Hadincová V, et al. . 2018. Vertical root distribution of individual species in a mountain grassland community: does it respond to neighbours? Journal of Ecology 106: 1083–1095.

Hnatiuk  RJ, Hopkins AJM.  1980. Western Australian species-rich kwongan (sclerophyllous shrubland) affected by drought. Australian Journal of Botany 28: 573–585. doi:10.1071/bt9800573. DOI

Hopper  SD, Gioia P.  2004. The Southwest Australian Floristic Region: evolution and conservation of a global hot spot of biodiversity. Annual Review of Ecology, Evolution, and Systematics 35: 623–650. doi:10.1146/annurev.ecolsys.35.112202.130201. DOI

Jónsdóttir  IS, Watson MA.  1997. Extensive physiological integration: an adaptive trait in resource-poor environments. In: de Kroon H, van Groenendael JM. eds. The ecology and evolution of clonal plants. Leiden: Backhuys Publishers, 109–136.

Kassambara  A.  2020. rstatix: Pipe-friendly framework for basic statistical tests. https://CRAN.R-project.org/package=rstatix/index.html (3 March 2022, date last accessed).

Klimešová  J, Doležal J, Prach K, Košnar J.  2012. Clonal growth forms in Arctic plants and their habitat preferences: a study from Petuniabukta, Spitsbergen. Polish Polar Research 33: 421–442. doi:10.2478/v10183-012-0019-y. DOI

Klimešová  J, Klimeš L.  2007. Bud banks and their role in vegetative regeneration – A literature review and proposal for simple classification and assessment. Perspectives in Plant Ecology, Evolution and Systematics 8: 115–129.

Klimešová  J, Herben T.  2021. The hidden half of the fine root differentiation in herbs: nonacquisitive belowground organs determine fine-root traits. Oikos doi:10.1111/oik.08794. DOI

Klimešová  J, Martínková J.  2022. Clonal growth, resprouting, and vegetative propagation of weeds. In: Upadhyaya MK, Clements DR, Shrestha A, eds. Persistence strategies of weeds. Chichester: John Wiley & Sons, 200–218.

Klimešová  J, Martínková J, Ottaviani G.  2018. Belowground plant functional ecology: Towards an integrated perspective. Functional Ecology 32: 2115–2126. doi:10.1111/1365-2435.13145. DOI

Klimešová  J, Martínková J, Pausas JG, et al. . 2019. Handbook of standardized protocols for collecting plant modularity traits. Perspectives in Plant Ecology, Evolution and Systematics 40: 125485. doi:10.1016/j.ppees.2019.125485. DOI

Klimešová  J, Mudrák O, Martínková J, et al. . 2021b. Are belowground clonal traits good predictors of ecosystem functioning in temperate grasslands? Functional Ecology 35: 787–795. doi:10.1111/1365-2435.13755. DOI

Klimešová  J, Ottaviani G, Charles-Dominique T, et al. . 2021a. Incorporating clonality into the plant ecology research agenda. Trends in Plant Science 26: 1236–1247. doi:10.1016/j.tplants.2021.07.019. PubMed DOI

Laliberté  E, Turner BL, Costes T, et al. . 2012. Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. Journal of Ecology 100: 631–642. doi:10.1111/j.1365-2745.2012.01962.x. DOI

Lambers  H, ed.2014. Plant life on the sandplains in southwest Australia, a global biodiversity hotspot. Crawley: University of Western Australia Publishing.

Lambers  H, Ahmedi I, Berkowitz O, et al. . 2013. Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. Conservation Physiology 1: cot010. PubMed PMC

Lambers  H, de Britto Costa P, Cawthray GR, et al. . 2022. Strategies to acquire and use phosphorus in phosphorus-impoverished and fire-prone environments. Plant and Soil 476: 133–160. doi:10.1007/s11104-022-05464-8. DOI

Lamont  BB, Downes KS.  2011. Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa. Plant Ecology 212: 2111–2125. doi:10.1007/s11258-011-9987-y. DOI

Low  AB, Lamont BB.  1990. Aerial and below-ground phytomass of Banksia scrub-heath at Eneabba, South-western Australia. Australian Journal of Botany 38: 351–359. doi:10.1071/bt9900351. DOI

Millar  MA, Byrne M, Coates DJ.  2010. The maintenance of disparate levels of clonality, genetic diversity and genetic differentiation in disjunct subspecies of the rare Banksia ionthocarpa. Molecular Ecology 19: 4217–4227. doi:10.1111/j.1365-294X.2010.04817.x. PubMed DOI

Mory  A.  1994. Geology of the Arrowsmith – Beagle Islands 1: 100 000 sheet. Perth: Geological Survey of Western Australia, Department of Minerals and Energy.

Mucina  L.  2018. Vegetation of Brazilian campos rupestres on siliceous substrates and their global analogues. Flora 238: 11–23. doi:10.1016/j.flora.2017.06.007. DOI

Mucina  L, Wardell-Johnson GW.  2011. Landscape age and soil fertility, climatic stability, and fire regime predictability: beyond the OCBIL framework. Plant and Soil 341: 1–23. doi:10.1007/s11104-011-0734-x. DOI

Oksanen  J, Blanchet FG, Friendly M, et al. . 2020. vegan: Community Ecology Package. https://CRAN.R-project.org/package=vegan/index.html (3 March 2022, date last accessed).

Ottaviani  G, Lubbe FC, Lepš J, et al. . 2021. Strong impact of management regimes on rhizome biomass across Central European temperate grasslands. Ecological Applications 31: e02317. PubMed

Ottaviani  G, Molina-Venegas R, Charles-Dominique T, et al. . 2020. The neglected belowground dimension of plant dominance. Trends in Ecology and Evolution 35: 763–766. doi:10.1016/j.tree.2020.06.006. PubMed DOI

Pärtel  M, Hiiesalu I, Öpik M, Wilson SD.  2012. Below-ground plant species richness: new insights from DNA-based methods. Functional Ecology 26: 775–782. doi:10.1111/j.1365-2435.2012.02004.x. DOI

Pate  JS, Beard JS, eds.1982. Kwongan. Plant life of the sandplain. Perth: University of Western Australia Press.

Pate  JS, Froend RH, Bowen BJ, Hansen A, Kuo J.  1990. Seedling growth and storage characteristics of seeder and resprouter species of mediterranean-type ecosystems of S.W. Australia. Annals of Botany 65: 585–601. doi:10.1093/oxfordjournals.aob.a087976. DOI

Pausas  JG, Lamont BB, Paula S, Appezzato-da-Glória B, Fidelis A.  2018. Unearthing belowground bud banks in fire-prone ecosystems. New Phytologist 217: 1435–1448. PubMed

Pausas  JG, Verdú M.  2005. Plant persistence traits in fire-prone ecosystems of the Mediterranean basin: a phylogenetic approach. Oikos 109: 196–202. doi:10.1111/j.0030-1299.2005.13596.x. DOI

Peltzer  DA, Wardle DA, Allison VJ, et al. . 2010. Understanding ecosystem retrogression. Ecological Monographs 80: 509–529. doi:10.1890/09-1552.1. DOI

Pennings  SC, Callaway RM.  2000. The advantages of clonal integration under different ecological conditions: a community-wide test. Ecology 81: 709–716. doi:10.1890/0012-9658(2000)081[0709:taociu]2.0.co;2. DOI

Peres-Neto  PR, Dray S, ter Braak CJF.  2017. Linking trait variation to the environment: critical issues with community-weighted mean correlation resolved by the fourth-corner approach. Ecography 40: 806–816. doi:10.1111/ecog.02302. DOI

Playford  P, Cockbain A, Low G.  1976. Geology of the Perth Basin, Western Australia. Perth: Geological Survey of Western Australia, Department of Minerals and Energy.

Pillon  Y, Jaffré T, Birnbaum P, et al. . 2021. Infertile landscapes on an old oceanic island: the biodiversity hotspot of New Caledonia. Biological Journal of the Linnean Society 133: 317–341.

R Core Team.  2021. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.

Rundel  PW, Arroyo MTK, Cowling RM, Keeley JE, Lamont BB, Vargas P.  2016. Mediterranean biomes: Evolution of their vegetation, floras, and climate. Annual Review of Ecology, Evolution, and Systematics 47: 383–407.

Rusch  GM, Wilmann B, Klimešová J, Evju M.  2011. Do clonal and bud bank traits vary in correspondence with soil properties and resource acquisition strategies? Patterns in alpine communities in the Scandian mountains. Folia Geobotanica 46: 237–254.

Shane  MW, McCully ME, Lambers H.  2004. Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). Journal of Experimental Botany 55: 1033–1044. doi:10.1093/jxb/erh111. PubMed DOI

Signorell  A, Aho K, Alfons A, Anderegg N, Aragon T, Arppe A.  2019. DescTools: Tools for descriptive statistics. https://cran.r-project.org/package=DescTools (3 March 2022, date last accessed).

Singh  B, Gilkes RJ.  1991. Phosphorus sorption in relation to soil properties for the major soil types of south-western Australia. Soil Research 29: 603–618. doi:10.1071/sr9910603. DOI

Sosnová  M, van Diggelen R, Klimešová J.  2010. Distribution of clonal growth forms in wetlands. Aquatic Botany 92: 33–39. doi:10.1016/j.aquabot.2009.09.005. DOI

Tavşanoğlu  C, Pausas JG.  2018. A functional trait database for Mediterranean Basin plants. Scientific Data 5: 180135. doi:10.1038/sdata.2018.135. PubMed DOI PMC

Terpstra  TJ.  1952. The asymptotic normality and consistency of Kendall’s test against trend, when ties are present in one ranking. Indagationes Mathematicae 14: 327–333.

Tsakalos  JL, Renton M, Dobrowolski MP, et al. . 2018. Community patterns and environmental drivers in hyper-diverse kwongan scrub vegetation of Western Australia. Applied Vegetation Science 21: 694–722. doi:10.1111/avsc.12399. DOI

Tsakalos  JL, Renton M, Riviera F, Veneklaas EJ, Dobrowolski MP, Mucina L.  2019. Trait-based formal definition of plant functional types and functional communities in the multi-species and multi-traits context. Ecological Complexity 40: 100787. doi:10.1016/j.ecocom.2019.100787. DOI

Tsakalos  JL, Riviera F, Veneklaas EJ, Dobrowolski MP, Mucina L.  2020. Data from: Trait-based formal definition of plant functional types and functional communities in the multi-species and multi-traits context. Dryad. 10.5061/dryad.9kd51c5cb DOI

Veneklaas  EJ.  2022. Phosphorus resorption and tissue longevity of roots and leaves – importance for phosphorus use efficiency and ecosystem phosphorus cycles. Plant and Soil 476: 627–637. doi:10.1007/s11104-022-05522-1. DOI

Verdú  M, Dávila P, García-Fayos P, Flores-Hernández N, Valiente-Banuet A.  2003. ‘Convergent’ traits of Mediterranean woody plants belong to pre-Mediterranean lineages. Biological Journal of the Linnean Society 78: 415–427. doi:10.1046/j.1095-8312.2003.00160.x. DOI

Western Australian Herbarium.  1998. Florabase—the Western Australian Flora. Perth: Department of Biodiversity, Conservation and Attractions.

Yu  FH, Wang N, He WM, Chu Y, Dong M.  2008. Adaptation of rhizome connections in drylands: increasing tolerance of clones to wind erosion. Annals of Botany 102: 571–577. doi:10.1093/aob/mcn119. PubMed DOI PMC

Zelený  D.  2018. Which results of the standard test for community-weighted mean approach are too optimistic? Journal of Vegetation Science 29: 953–966. doi:10.1111/jvs.12688. DOI

Zencich  SJ, Froend RH, Turner JV, Gailitis V.  2002. Influence of groundwater depth on the seasonal sources of water accessed by Banksia tree species on a shallow, sandy coastal aquifer. Oecologia 131: 8–19. doi:10.1007/s00442-001-0855-7. PubMed DOI

Zhang  H, Bonser SP, Chen S-C, Hitchcock T, Moles AT.  2018. Is the proportion of clonal species higher at higher latitudes in Australia? Austral Ecology 43: 69–75.

Zuur  AF, Leno EN, Walker NJ, Saveliev AA, Smith GM.  2009. Mixed effects models and extensions in ecology with R. New York: Springer.

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