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Plant-herbivory feedbacks and selective allocation of a toxic metal are behind the stability of degraded covers dominated by Brachypodium pinnatum in acidic soils

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Abstract

Background and aims

Perennial tall-grasses have experienced a successful expansion in the last decades leading in some cases to extremely degraded communities, which remain in an alternate stable state. This research focuses on the mechanisms of persistence of the spreading native Brachypodium pinnatum in acidic soils. We hypothesize that plant-herbivory feedbacks and an adapted response to soil constraints, promote species cover stability.

Methods

Eight on-site populations of the species growing in two contrasted situations (high-diversity grazed and low-diversity ungrazed communities) were sampled during a growing season and analysed for nutrient (N, P and K), metal (Al) and C allocation, biomass production and tissue quality.

Results

The species showed a high capacity for belowground accumulation of Al and an efficient reallocation and resorption of nutrients, which may explain its success in acidic, poor soils. The lack of attractiveness to herbivores of the species-poor stands prevented biomass removal, which strengthened some effects and enhanced the build-up of a thick layer of recalcitrant tissues, an effective barrier (aboveground and belowground) for the establishment of sympatric species.

Conclusions

Density-dependent feedback mechanisms (herbivory attractiveness), and the particular attributes of B. pinnatum (i.e. powerful rhizomes with a selective performance for nutrients and aluminium) may lead to critical processes of community domination and degradation.

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References

  • Baba 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

    Article  Google Scholar 

  • Babai D, Molnar Z (2014) Small-scale traditional management of highly species-rich grasslands in the Carpathians. Agric Ecosyst Environ 182:123–130. doi:10.1016/j.agee.2013.08.018

    Article  Google Scholar 

  • Baker A (1981) Accumulations and excluders. Strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654. doi:10.1080/01904168109362867

    Article  CAS  Google Scholar 

  • Bergvall UA, Rautio P, Kesti K, Tuomi J, Leimar O (2006) Associational effects of plant defences in relation to within- and between-patch food choice by a mammalian herbivore: neighbour contrast susceptibility and defence. Oecologia 147:253–260. doi:10.1007/s00442-005-0260-8

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bobbink R, Willems JH (1991) Impact of different cutting regimes on the performance of Brachypodium pinnatum in dutch chalk grassland. Biol Conserv 56:1–21

    Article  Google Scholar 

  • Bobbink R, Bik L, Willems JH (1988) Effects of nitrogen-fertilization on vegetation structure and dominance of Brachypodium pinnatum (L) Beauv in chalk grassland. Acta Botanica Neerlandica 37:231–242

    Article  Google Scholar 

  • Bobbink R, Dendubbelden K, Willems J (1989) Seasonal dynamics of phytomass and nutrients in chalk grassland. Oikos 55:216–224. doi:10.2307/3565425

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bonanomi G, Allegrezza M (2004) Effetti della colonizzazione di Brachypodium rupestre (Host) Roemer et. Schultes sulla diversità di alcune fitocenosi erbacee dell’Appennino centrale. Fitosociologia 41:51–69

    Google Scholar 

  • Buckland SM, Thompson K, Hodgson JG, Grime JP (2001) Grassland invasions: effects of manipulations of climate and management. J Appl Ecol 38:301–309

    Article  Google Scholar 

  • Callaway R, Kikodze D, Chiboshvili M, Khetsuriani L (2005) Unpalatable plants protect neighbors from grazing and increase plant community diversity. Ecology 86:1856–1862. doi:10.1890/04-0784

    Article  Google Scholar 

  • Canals RM, Pedro J, Ruperez E, San-Emeterio L (2014) Nutrient pulses after prescribed winter fires and preferential patterns of N uptake may contribute to the expansion of Brachypodium pinnatum (L.) P. Beauv. In highland grasslands. Appl Veg Sci 17:419–428. doi:10.1111/avsc.12088

    Article  Google Scholar 

  • Dawson W, Fischer M, van Kleunen M (2011) The maximum relative growth rate of common UK plant species is positively associated with their global invasiveness. Glob Ecol Biogeogr 20:299–306

    Article  Google Scholar 

  • de Kroon H, Bobbink R (1997) Clonal plant dominance under elevated nitrogen deposition with special reference to Brachypodium pinnatum chalk grassland. In: de Kroon H, van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys Publ, Leiden

    Google Scholar 

  • de Silva J, Tuwei G, Zhao FJ (2016) Environmental factors influencing aluminium accumulation in tea (Camellia sinensis L.). Plant Soil 400:223–230. doi:10.1007/s11104-015-2729-5

    Article  Google Scholar 

  • Delhaize E, Ryan P (1995) Aluminium toxicity and tolerance in plants. Plant Physiol 107:315–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Díaz S, Lavorel S, McIntyre S, Falczuk V, Casanoves F, Milchunas D, Skarpe C, Rusch G, Sternberg M, Noy-Meir I, Landsberg J, Zhang W, Clark H, Campbell B (2007) Plant trait responses to grazing - a global synthesis. Glob Chang Biol 13:313–341. doi:10.1111/j.1365-2486.2006.01288.x

    Article  Google Scholar 

  • Díaz C, Lemaitre T, Christ A, Azzopardi M, Kato Y, Sato F, Morot-Gaudry JF, Le Dily F, Masclaux-Daubresse C (2008) Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol 147:1437–1449. doi:10.1104/pp.108.119040

    Article  PubMed  PubMed Central  Google Scholar 

  • Eschtruth AK, Battles JJ (2009) Assessing the relative importance of disturbance, herbivory, diversity, and propagule pressure in exotic plant invasion. Ecol Monogr 79:265–280. doi:10.1890/08-0221.1

    Article  Google Scholar 

  • Falkengren-Grerup U (1998) The effects of winter exposure to acid soil conditions on the subsequent survival and growth of herbaceous, forest perennials: a preliminary investigation. Ann Bot 82:893–897. doi:10.1006/anbo.1998.0761

    Article  Google Scholar 

  • Ferraro D, Oesterheld M (2002) Effect of defoliation on grass growth. A quantitative review. Oikos 98:125–133. doi:10.1034/j.1600-0706.2002.980113.x

    Article  Google Scholar 

  • Ferrer V, Canals RM (2008) Proyecto de ordenación de los recursos pascícolas forestales del Monte Aezkoa n° 1 del CUP. Consultoría Belardi & Universidad Pública de Navarra, Pamplona-España

    Google Scholar 

  • Fuhlendorf S, Engle D, Kerby J, Hamilton R (2009) Pyric herbivory: rewilding landscapes through the recoupling of fire and grazing. Conserv Biol 23:588–598. doi:10.1111/j.1523-1739.2008.01139.x

    Article  PubMed  Google Scholar 

  • Garcia-Pausas J, Casals P, Romanya J, Vallecillo S, Sebastià M (2011) Seasonal patterns of belowground biomass and productivity in mountain grasslands in the Pyrenees. Plant Soil 340:315–326. doi:10.1007/s11104-010-0601-1

    Article  CAS  Google Scholar 

  • Gloser V (2005) The consequences of lower nitrogen availability in autumn for internal nitrogen reserves and spring growth of Calamagrostis epigejos. Plant Ecol 179:119–126. doi:10.1007/s11258-004-6736-5

    Article  Google Scholar 

  • Grime JP, Cornelissen JHC, Thompson K, Hodgson JG (1996) Evidence of a causal connection between anti-herbivore defence and the decomposition rate of leaves. Oikos 77:489–494. doi:10.2307/3545938

    Article  Google Scholar 

  • Hanstein S, Mattsson M, Jaeger H, Schjoerring J (1999) Uptake and utilization of atmospheric ammonia in three native Poaceae species: leaf conductances, composition of apoplastic solution and interactions with root nitrogen supply. New Phytol 141:71–83. doi:10.1046/j.1469-8137.1999.00330.x

    Article  Google Scholar 

  • Hartnett D (1989) Density and growth stage-dependent responses to defoliation in two rhizomatous grasses. Oecologia 80:414–420. doi:10.1007/BF00379045

    Article  CAS  PubMed  Google Scholar 

  • Hurst A, John E (1999) The biotic and abiotic changes associated with Brachypodium pinnatum dominance in chalk grassland in south-East England. Biol Conserv 88:75–84

    Article  Google Scholar 

  • Illius A, Gordon I (1993) Diet selection on mammalian herbivores: constraints and tactics. In: Hughes R (ed) Diet selection: an interdisciplinary approach to foraging behaviour. Blackwell, London

    Google Scholar 

  • Kahlert B, Ryser P, Edwards P (2005) Leaf phenology of three dominant limestone grassland plants matching the disturbance regime. J Veg Sci 16:433–442. doi:10.1111/j.1654-1103.2005.tb02383.x

    Article  Google Scholar 

  • Kellogg CH, Bridgham SD (2004) Disturbance, herbivory, and propagule dispersal control dominance of an invasive grass. Biol Invasions 6:319–329. doi:10.1023/B:BINV.0000034606.84830.d5

    Article  Google Scholar 

  • Keser L, Dawson W, Song Y, Yu F, Fischer M, Dong M, van Kleunen M (2014) Invasive clonal plant species have a greater root-foraging plasticity than non-invasive ones. Oecologia 174:1055–1064. doi:10.1007/s00442-013-2829-y

    Article  PubMed  Google Scholar 

  • Kindt R, Coe R (2005) Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi

    Google Scholar 

  • Köhler B, Gigon A, Edwards PJ, Krusi B, Langenauer R, Lüscher A, Ryser P (2005) Changes in species composition and conservation value of limestone grasslands in northern Switzerland after 22 years of contrasting managements. Perspect Plant Ecol, Evol Syst 7:51–67

    Article  Google Scholar 

  • Kormann U, Rösch V, Batáry P, Tscharntke T, Orci KM, Samu F, Scherber C (2015) Local and landscape management drive trait-mediated biodiversity of nine taxa on small grassland fragments. Divers Distrib 21:1204–1217. doi:10.1111/ddi.12324

    Article  Google Scholar 

  • Kuebbing S, Rodriguez-Cabal MA, Fowler D, Breza L, Schweitzer JA, Bailey JK (2013) Resource availability and plant diversity explain patterns of invasion of an exotic grass. J Plant Ecol 6:141–149. doi:10.1093/jpe/rts018

    Article  Google Scholar 

  • Lehsten V, Sykes M, Scott A, Tzanopoulos J, Kallimanis A, Mazaris A, Verburg P, Schulp C, Potts S, Vogiatzakis I (2015) Disentangling the effects of land-use change, climate and CO2 on projected future European habitat types. Glob Ecol Biogeogr 24:653–663. doi:10.1111/geb.12291

    Article  Google Scholar 

  • Lenth R (2013) lsmeans: Least-squares means. R package version 1.06–06 edn

  • López-Marsico L, Altesor A, Oyarzabal M, Baldassini P, Paruelo J (2015) Grazing increases below-ground biomass and net primary production in a temperate grassland. Plant Soil 392:155–162. doi:10.1007/s11104-015-2452-2

    Article  Google Scholar 

  • Massey F, Hartley S (2006) Experimental demonstration of the antiherbivore effects of silica in grasses: impacts on foliage digestibility and vole growth rates. Proc R Soc B Biol Sci 273:2299–2304. doi:10.1098/rspb.2006.3586

    Article  CAS  Google Scholar 

  • Milchunas D, Lauenroth W (1993) Quantitative effects of grazing on vegetation and soils over a global range of environments. Ecol Monogr 63:327–366. doi:10.2307/2937150

    Article  Google Scholar 

  • Milchunas D, Noy-Meir I (2002) Grazing refuges, external avoidance of herbivory and plant diversity. Oikos 99:113–130. doi:10.1034/j.1600-0706.2002.990112.x

    Article  Google Scholar 

  • Navarro L, Proença V, Kaplan J, Pereira H (2015) Maintaining disturbance-dependent habitats. Rewilding European Landscapes. Springer International Publishing

  • Parachnowitsch AL, Cook-Patton SC, McArt SH (2014) Neighbours matter: natural selection on plant size depends on the identity and diversity of the surrounding community. Evol Ecol 28:1139–1153. doi:10.1007/s10682-014-9727-6

    Article  Google Scholar 

  • Pauchard A, Kueffer C, Dietz H, Daehler C, Alexander J, Edwards P, Arevalo J, Cavieres L, Guisan A, Haider S, Jakobs G, McDougall K, Millar C, Naylor B, Parks C, Rew L, Seipel T (2009) Ain’t no mountain high enough: plant invasions reaching new elevations. Front Ecol Environ 7:479–486. doi:10.1890/080072

    Article  Google Scholar 

  • Pinheiro J, Bates D (2000) Mixed-effects models in S and S-PLUS. Springer-Verlag, New York

    Book  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RDC (2009) Nlme: linear and nonlinear mixed effects models. R package. Version 3.1–96. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • R Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rengel Z, Reid R (1997) Uptake of Al across the plasma membrane of plant cells. Plant Soil 192:31–35. doi:10.1023/A:1004265913770

    Article  CAS  Google Scholar 

  • Ryser P, Lambers H (1995) Root and leaf attributes accounting for performance of fast-growing and slow-growing grasses at different nutrient supply. Plant Soil 170:251–265

    Article  CAS  Google Scholar 

  • Ryser P, Verduyn B, Lambers H (1997) Phosphorus allocation and utilization in three grass species with contrasting response to N and P supply. New Phytol 137:293–302. doi:10.1046/j.1469-8137.1997.00807.x

    Article  Google Scholar 

  • San Emeterio L, Múgica L, Ugarte M, Goicoa T, Canals R (2016) Sustainability of traditional pastoral fires in highlands under global change: effects on soil function and nutrient cycling. Agric Ecosyst Environ 235:155–163. doi:10.1016/j.agee.2016.10.009

    Article  Google Scholar 

  • Seabloom EW, Borer ET, Buckley Y, Cleland EE, Davies K, Firn J, Harpole WS, Hautier Y, Lind E, Macdougall A, Orrock JL, Prober SM, Adler P, Alberti J, Anderson TM, Bakker JD, Biederman LA, Blumenthal D, Brown CS, Brudvig LA, Caldeira M, Chu CJ, Crawley MJ, Daleo P, Damschen EI, D’Antonio CM, Decrappeo NM, Dickman CR, GZ D, Fay PA, Frater P, Gruner DS, Hagenah N, Hector A, Helm A, Hillebrand H, Hofmockel KS, Humphries HC, Iribarne O, Jin VL, Kay A, Kirkman KP, Klein JA, Knops JMH, La Pierre KJ, Ladwig LM, Lambrinos JG, Leakey ADB, Li Q, Li W, McCulley R, Melbourne B, Mitchell CE, Moore JL, Morgan J, Mortensen B, O’Halloran LR, Partel M, Pascual J, Pyke DA, Risch AC, Salguero-Gomez R, Sankaran M, Schuetz M, Simonsen A, Smith M, Stevens C, Sullivan L, Wardle GM, Wolkovich EM, Wragg PD, Wright J, Yang L (2013) Predicting invasion in grassland ecosystems: is exotic dominance the real embarrassment of richness? Glob Chang Biol 19:3677–3687. doi:10.1111/gcb.12370

    Article  PubMed  Google Scholar 

  • Silva S (2012) Aluminium toxicity in target plants. J Bot ID 219462:8. doi:10.1155/2012/219462

  • Soda S, Hamada T, Yamaoka Y, Ike M, Nakazato H, Saeki Y, Kasamatsu T, Sakurai Y (2012) Constructed wetlands for advanced treatment of wastewater with a complex matrix from a metal-processing plant: Bioconcentration and translocation factors of various metals in Acorus gramineus and Cyperus alternifolius. Ecol Eng 39:63–70. doi:10.1016/j.ecoleng.2011.11.014

    Article  Google Scholar 

  • Suding KN, Hobbs RJ (2009) Threshold models in restoration and conservation: a developing framework. Trends Ecol Evol 24:271–279. doi:10.1016/j.tree.2008.11.012

    Article  PubMed  Google Scholar 

  • Suding K, Gross K, Houseman G (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53. doi:10.1016/j.tree.2003.10.005

    Article  PubMed  Google Scholar 

  • Tomlinson KW, O’Connor TG (2004) Control of tiller recruitment in bunchgrasses: uniting physiology and ecology. Funct Ecol 18:489–496. doi:10.1111/j.0269-8463.2004.00873.x

    Article  Google Scholar 

  • Tsegai AT, Wang L, Wang DL, Huang Y, Lin HJ, Li J, Liu C (2013) Effects of spatial distribution on plant associational defense against herbivory. Basic Appl Ecol 14:680–686. doi:10.1016/j.baae.2013.09.007

    Article  Google Scholar 

  • Underwood N, Inouye BD, Hamback PA (2014) A conceptual framework for associational effects: when do neighbors matter and how would we know? Q Rev Biol 89:1–19. doi:10.1086/674991

    Article  PubMed  Google Scholar 

  • van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. doi:10.1111/1365-2745.12054

    Article  Google Scholar 

  • van der Putten WH, Bradford MA, Brinkman EP, van de Voorde TFJ, Veen GF (2016) Where, when and how plant-soil feedback matters in a changing world. Funct Ecol 30:1109–1121. doi:10.1111/1365-2435.12657

    Article  Google Scholar 

  • van Heerwaarden L, Toet S, van Logtestijn R, Aerts R (2005) Internal nitrogen dynamics in the graminoid Molinia caerulea under higher N supply and elevated CO2 concentrations. Plant Soil 277:255–264. doi:10.1007/s11104-005-7140-1

    Article  CAS  Google Scholar 

  • Van Soest P, Robertson J, Lewis B (1991) Methods for dietary fiber, neutral detergent fiber and non-starch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597

    Article  CAS  PubMed  Google Scholar 

  • Vaness B, Wilson S, MacDougall A (2014) Decreased root heterogeneity and increased root length following grassland invasion. Funct Ecol 28:1266–1273. doi:10.1111/1365-2435.12277

    Article  Google Scholar 

  • Willems JH (2001) Problems, approaches and results in restoration of Dutch calcareous grassland during the last 30 years. Restor Ecol 9:147–154. doi:10.1046/j.1526-100x.2001.009002147.x

    Article  Google Scholar 

  • Zedler J (2009) Feedbacks that might sustain natural, invaded and restored states in herbaceous wetlands. In: Hobbs R, Suding K (eds) New models for ecosystem dynamics and restauration. Island Press, Washington

    Google Scholar 

  • Zuur A, Ieno E, Walker N, Saveliev A, Smith G (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

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Acknowledgements

The research was financially supported by Spanish Ministry of Science and Innovation (CGL2011-29746). The authors are grateful to J. Blanco, V. Ferrer and J. Pedro for assistance in different stages of manuscript preparation, and to Aezkoa Valley Committee for its interest and willingness in the research. We are indebted to the reviewers and the editor, whose remarks and suggestions helped to improve earlier versions of the manuscript.

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Correspondence to Rosa M. Canals.

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Canals, R.M., Emeterio, L.S., Durán, M. et al. 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 (2017). https://doi.org/10.1007/s11104-016-3153-1

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