Abstract
Nutrient supply and herbivores can regulate plant species composition, biodiversity and functioning of terrestrial ecosystems. Nutrient enrichment frequently increases plant productivity and decreases diversity while herbivores tend to maintain plant diversity in productive systems. However, the mechanisms by which nutrient enrichment and herbivores regulate plant diversity remain unclear. Abundance-based mechanisms propose that fertilization leads to the extinction of rare species due to random loss of individuals of all species. In contrast, functional-based mechanisms propose that species exclusion is based on functional traits which are disadvantageous under fertilized conditions. We tested mechanistic links between fertilization and diversity loss in the presence or absence of consumers using data from a 4-year fertilization and fencing experiment in an alpine meadow. We found that both abundance- and functional-based mechanisms simultaneously affected species loss in the absence of herbivores while only abundance-based mechanisms affected species loss in the presence of herbivores. Our results indicate that an abundance-based mechanism may consistently play a role in the loss of plant diversity with fertilization, and that diversity decline is driven primarily by the loss of rare species regardless of a plant’s functional traits and whether or not herbivores are present. Increasing efforts to conserve rare species in the context of ecosystem eutrophication is a central challenge for grazed grassland ecosystems.
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References
Aarssen LW, Schamp BS, Pither J (2006) Why are there so many small plants? Implications for species coexistence. J Ecol 94:569–580
Adler PB, Fajardo A, Kleinhesselink AR, Kraft NJ (2013) Trait-based tests of coexistence mechanisms. Ecol Lett 16:1294–1306
Anderson MJ (2001) A new method for non-parametric multivariate ANOVA. Austral Ecol 26:32–46
Anderson CR, Brzezinski MA, Washburn L, Kudela R (2006) Circulation and environmental conditions during a toxigenic Pseudo-nitzschia australis bloom in the Santa Barbara Channel, California. Mar Ecol Prog Ser 327:119–133
Bakker ES, Olff H (2003) Impact of different-sized herbivores on recruitment opportunities for subordinate herbs in grasslands. J Veg Sci 14:465–474
Bakker ES, Ritchie ME, Olff H, Milchunas DG, Knops JMH (2006) Herbivore impact on grassland plant diversity depends on habitat productivity and herbivore size. Ecol Lett 9:780–789
Borer ET, Seabloom EW, Gruner DS, Harpole WS (2014) Herbivores and nutrients control grassland plant diversity via light limitation. Nature 508:517–520
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48(5):1079–1087
Cohen JS, Rainford ESKD, Blossey EB (2014) Community weighted mean functional effect traits determine larval amphibian responses to litter mixtures. Oecologia 174:1359–1366
Craine J (2009) Resource strategies of wild plants. Princeton University, Princeton
Diaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655
Diaz S, Cabido M, Casanoves F (1998) Plant functional traits and environmental filters at a regional scale. J Veg Sci 9:113–122
Dickson TL, Foster BL (2011) Fertilization decreases plant biodiversity even when light is not limiting. Ecol Lett 14:380–388
Dybzinski R, Tilman D (2007) Resource use patterns predict long-term outcomes of plant competition for nutrients and light. Am Nat 170:305–318
Eskelinen A, Harrison S, Tuomi M (2012) Plant traits mediate consumer and nutrient control on plant community productivity and diversity. Ecology 93:2705–2718
Foster BL, Gross KL (1998) Species richness in a successional grassland: effects of nitrogen enrichment and plant litter. Ecology 79:2593–2602
Galloway JN, Dentener FJ, Capone DG, Boyer EW et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226
Galloway JN, Towsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions and potential solutions. Science 320:889–892
Gao YH, Luo P, Wu N, Chen H, Wang GX (2007) Grazing intensity impacts on carbon sequestration in an alpine meadow on the eastern Tibetan Plateau. Res J Agric Biol Sci 3(6):642–647
Garnier E, Cortez J, Billès G, Navas ML, Roumet C et al (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637
Glenn SM, Collins SL (1992) Effects of spatial scale and disturbance on rates of immigration and extinction of species in prairies. Oikos 63:273–280
Goldberg DE, Miller TE (1990) Effects of different resource additions of species diversity in an annual plant community. Ecology 71:213–225
Grime JP (1973) Competitive exclusion in herbaceous vegetation. Nature 242:344–347
Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194
Harpole WS, Potts DL, Suding KN (2007) Ecosystem responses to water and nitrogen amendment in a California grassland. Glob Change Biol 13:2341–2348
Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–638
Hautier Y, Seabloom EW, Borer ET, Adler PB et al (2014) Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508:521–525
Hillebrand H, Gruner DS, Borer ET et al (2007) Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure. Proc Natl Acad Sci USA 104:10904–10909
Holt RD, Grover J, Tilman D (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am Nat 144:741–771
Hooper DU, Vitousek PM (1997) The effects of plant composition and diversity on ecosystem processes. Science 277:1302–1305
Isbell F, Tilman D, Polasky S et al (2013) Low biodiversity state persists two decades after cessation of nutrient enrichment. Ecol Lett 16:454–460
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Lambers H, Chapin FS, Pons TL (2006) Plant physiological ecology. Springer, New York
Lan Z, Bai Y (2012) Testing mechanisms of N-enrichment induced species loss in a semiarid inner Mongolia grassland: critical thresholds and implications for long-term ecosystem responses. Philos Trans R Soc Lond Ser B-Biol Sci 367:3125–3134
Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24
Loreau M, Naeem S, Inchausti P, Bengtsson J et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294(5543):804–808
Luo Y, Qin G, Du G (2006) Importance of assemblage-level thinning: a field experiment in an alpine meadow on the Tibet Plateau. J Veg Sci 17:417–424
McQuarrie ADR, Tsai CL (1998) Regression and time series model selection. World Scientific, Singapore
Niu K, Luo Y, Choler P, Du G (2008) The role of biomass allocation strategy in diversity loss due to fertilization. Basic Appl Ecol 9:485–493
Oksanen J (1996) Is the humped relationship between species richness and biomass an artefact due to plot size? J Ecol 84:293–295
Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2011) Vegan: community ecology package. R package version 1.17–7
Olff H, Ritchie ME (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265
Pakeman RJ (2004) Consistency of plant species and trait responses to grazing along a productivity gradient: a multi-site analysis. J Ecol 92:893–905
Proulx M, Mazumder A (1998) Reversal of grazing impact on plant species richness in nutrient-poor vs. nutrient-rich ecosystems. Ecology 79:2581–2592
Püttker T, Bueno AA, Prado PI, Pardini R (2014) Ecological filtering or random extinction? Beta-diversity patterns and the importance of niche-based and neutral processes following habitat loss. Oikos 124:206–215
Quétier F, Thébault A, Lavorel S (2007) Plant traits in a state and transition framework as markers of ecosystem response to land-use change. Ecol Monogr 77:33–52
Rajaniemi TK (2002) Why does fertilization reduce plant species diversity? Testing three competition-based hypotheses. J Ecol 90:316–324
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to imagej: 25 years of image analysis. Nat Methods 9:671–675
Shipley B, Vile D, Garnier E (2006) From plant traits to plant communities: a statistical mechanistic approach to biodiversity. Science 314:812–814
Shipley B, Laughlin DC, Sonnier G, Otfinowski R (2011) A strong test of a maximum entropy model of trait-based community assembly. Ecology 92:507–517
Stevens MHH, Carson WP (1999) Plant density determines species richness along an experimental fertility gradient. Ecology 80:455–465
Stevens MHH, Bunker DE, Schnitzer SA, Carson WP (2004) Establishment limitation reduces species recruitment and species richness as soil resources rise. J Ecol 92:339–347
Suding KN, Collins SL, Gough L, Clark C, Cleland EE et al (2005) Functional and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Natl Acad Sci USA 102:4387–4392
Tilman D (1982) Resource competition and community structure. Princeton University, Princeton
Tilman D (1993) Species richness of experimental productivity gradients- how important is colonization limitation. Ecology 74:2179–2191
Tilman D (1999) The ecological consequences of changes in biodiversity: a search for general principles. The Robert H. MacArthur award lecture. Ecology 80:1455–1474
Tilman D, Pacala S (1993) The maintenance of species richness in plant communities. In: Ricklefs RE, Schluter D (eds) Species diversity in ecological communities: historical and geographical perspectives. University of Chicago, Chicago, pp 13–25
Viola DV, Mordecai EA, Jaramillo AG, Sistla SA et al (2010) Competition-defense tradeoffs and the maintenance of plant diversity. Proc Natl Acad Sci USA 107:17217–17222
Vitousek PM, Aber JD, Howarth RW et al (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750
Vitousek PM, Cassman K, Cleveland C et al (2002) Toward an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45
WallisdeVries MF, Bakker JP, van Wieren SE (1998) Grazing and conservation management. Conservation biology series. Kluwer Academic, Dordrecht
Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227
Worm B, Lotze HK, Hillebrand H, Sommer U (2002) Consumer versus resource control of species diversity and ecosystem functioning. Nature 417:848–851
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Yang Z, van Ruijven J, Du GZ (2011) The effects of long-term fertilization on the temporal stability of alpine meadow communities. Plant Soil 345:315–324
Yang ZL, Guo H, Zhang JY, Du GZ (2013) Stochastic and deterministic processes together determine alpine meadow plant community composition on the Tibetan Plateau. Oecologia 171(2):495–504
Young HS, McCauley DJ, Helgen KM, Goheen JR et al (2013) Effects of mammalian herbivore declines on plant communities: observations and experiments in an African savanna. J Ecol 101(4):1030–1041
Acknowledgments
Special thanks to T. K. Rajaniemi for valuable discussion and comments. This project was supported by the Key Program of the National Natural Science Foundation of China (grant no. 41430749), the National Natural Science Foundation of China (grant no. 31300363), and the Postdoctoral Foundation of China (grant nos. 2013M541970, 2014T70675). The experiments comply with the current laws of China, where the experiments were performed.
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Communicated by Bryan Foster.
Z. Yang and Y. Hautier contributed to this paper equally.
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Yang, Z., Hautier, Y., Borer, E.T. et al. Abundance- and functional-based mechanisms of plant diversity loss with fertilization in the presence and absence of herbivores. Oecologia 179, 261–270 (2015). https://doi.org/10.1007/s00442-015-3313-7
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DOI: https://doi.org/10.1007/s00442-015-3313-7