Shifts in Key Leaf Litter Traits Can Predict Effects of Plant Diversity Loss on Decomposition in Streams

Springer Science and Business Media LLC - Tập 24 - Trang 185-196 - 2020
Naiara López-Rojo1, Javier Pérez1, Jesús Pozo1, Ana Basaguren1, Unai Apodaka-Etxebarria1, Francisco Correa-Araneda2, Luz Boyero1,3
1Department of Plant Biology and Ecology, Faculty of Science and Technology, University of the Basque Country (UPV/EHU), Leioa, Spain
2Unidad de Cambio Climático y Medio Ambiente, Instituto de Estudios del Hábitat, Facultad de Arquitectura y Construcción, Universidad Autónoma de Chile, Temuco, Chile
3IKERBASQUE, Basque Foundation for Science, Bilbao, Spain

Tóm tắt

Plant biodiversity loss in riparian forests is known to alter key stream ecosystem processes such as leaf litter decomposition. One potential mechanism mediating this biodiversity–decomposition relationship is the increased variability of plant functional traits at higher levels of biodiversity, providing more varied resources for decomposers and thus improving their function. We explored this in a field experiment exposing litter from different assemblages with low or high trait variability (measured through phylogenetic distance, PD) to microbial decomposers and invertebrate detritivores within litterbags in a low-order stream. Litter assemblages generally lost less mass but more phosphorus (P) than expected from monocultures, and nitrogen (N) tended to increase in the absence of detritivores and decrease in their presence, with little effect of PD. In contrast, there were strong influences of mean values and variability of specific traits (mostly N, P and condensed tannins) on decomposition and on net diversity effects. The negative diversity effect on litter mass loss was mainly driven by negative complementarity (that is, physical or chemical interference among species or traits), although there was positive selection (that is, particular species or traits with large effects on decomposition) in high-PD assemblages with detritivores. High-PD assemblages tended to have more invertebrates and attracted more typical litter-consuming detritivores. Our study suggests that decomposition of litter assemblages is mainly driven by concentration and variability of several key litter traits, rather than overall trait heterogeneity (measured through PD). However, differences in invertebrates colonizing high-PD and low-PD assemblages pointed to potential long-term effects of PD on decomposition.

Tài liệu tham khảo

Ackerly DD, Reich PB. 1999. Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts. Am J Bot 86:1272–81. Allison SD, Martiny JBH. 2008. Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci 102:11512–19. Battin TJ, Luyssaert S, Kaplan LA, Aufdenkampe AK, Richter A, Tranvik LJ. 2009. The boundless carbon cycle. Nat Geosci 2:598–600. Bjelke U, Boberg J, Oliva J, Tattersdill K, McKie BG. 2016. Dieback of riparian alder caused by the Phytophthora alnicomplex: projected consequences for stream ecosystems. Freshw Biol 61:565–79. Boyero L, Graca MAS, Tonin AM, Pérez J, Swafford AJ, Ferreira V, Landeira-Dabarca A, Alexandrou MA, Gessner MO, McKie BG, Albarino RJ, Barmuta LA, Callisto M, Chara J, Chauvet E, Colon-Gaud C, Dudgeon D, Encalada AC, Figueroa R, Flecker AS, Fleituch T, Frainer A, Goncalves JF Jr, Helson JE, Iwata T, Mathooko J, M’Erimba C, Pringle CM, Ramirez A, Swan CM, Yule CM, Pearson RG. 2017. Riparian plant litter quality increases with latitude. Sci Rep 7:10562. Boyero L, Pearson RG, Gessner MO, Barmuta LA, Ferreira V, Graça MAS, Dudgeon D, Boulton AJ, Callisto M, Chauvet E, Helson JE, Bruder A, Albariño RJ, Yule CM, Arunachalam M, Davies JN, Figueroa R, Flecker AS, Ramírez A, Death RG, Iwata T, Mathooko JM, Mathuriau C, Gonçalves JF, Moretti M, Jinggut T, Lamothe S, M’erimba C, Ratnarajah L, Schindler MH, Castela J, Buria LM, Cornejo A, Villanueva VD, West DC. 2011. A global experiment suggests climate warming will not accelerate litter decomposition in streams but may reduce carbon sequestration. Ecol Lett 14:289–94. Boyero L, Pearson RG, Hui C, Gessner MO, Pérez J, Alexandrou MA, Graça MAS, Cardinale BJ, Albariño R, Arunachalam M, Barmuta LA, Boulton AJ, Bruder A, Callisto M, Chauvet E, Death RG, Dudgeon D, Encalada AC, Ferreira V, Figueroa R, Flecker AS, Gonçalves JFJ, Helson JE, Iwata T, Jinggut T, Mathooko J, Mathuriau C, M’Erimba C, Moretti MS, Pringle CM, Ramírez A, Ratnarajah L, Rincón J, Yule CM. 2016. Biotic and abiotic variables influencing plant litter breakdown in streams: a global study. Proc R Soc B Biol Sci 283:20152664. Cadotte MW, Cavender-Bares J, Tilman D, Oakley TH. 2009. Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE 4:e5695. Canty A, Ripley B. 2016. boot: Bootstrap R (S-Plus) Functions. R package version 1.3–18. Vienna: R Foundation for Statistical Computing. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S. 2012. Biodiversity loss and its impact on humanity. Nature 486:59–67. Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O’Connor MI, Gonzalez A. 2011. The functional role of producer diversity in ecosystems. Am J Bot 98:572–92. Casas JJ, Larrañaga A, Menendez M, Pozo J, Basaguren A, Martinez A, Perez J, Gonzalez JM, Molla S, Casado C, Descals E, Roblas N, Lopez-Gonzalez JA, Valenzuela JL. 2013. Leaf litter decomposition of native and introduced tree species of contrasting quality in headwater streams: how does the regional setting matter? Sci Total Environ 458–460:197–208. Cebrian J. 1999. Patterns in the fate of production in plant communities. Am Nat 154:449–68. Chergui H, Haddy L, Markaoui M, Pattee E. 1997. Impact of leaf litter leachates on water oxygen levels and gastropod survival. Acta Oecol 18:531–42. Cornelissen J, Thompson K. 1997. Functional leaf attributes predict litter decomposition rate in herbaceous plants. New Phytol 135:109–14. Cornwell WK, Cornelissen JH, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Diaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M. 2008. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–71. Davison AC, Hinkley DV. 1997. Bootstrap methods and their application. Cambridge: Cambridge University Press. Fernandes I, Pascoal C, Guimarães H, Pinto R, Sousa I, Cássio F. 2012. Higher temperature reduces the effects of litter quality on decomposition by aquatic fungi. Freshw Biol 57:2306–17. Ferreira V, Encalada AC, Graça MAS. 2012. Effects of litter diversity on decomposition and biological colonization of submerged litter in temperate and tropical streams. Freshw Sci 31:945–62. Ferreira V, Raposeiro PM, Pereira A, Cruz AM, Costa AC, Graça MAS, Gonçalves V. 2016. Leaf litter decomposition in remote oceanic island streams is driven by microbes and depends on litter quality and environmental conditions. Freshw Biol 61:783–99. Fugère V, Andino P, Espinosa R, Anthelme F, Jacobsen D, Dangles O. 2012. Testing the stress-gradient hypothesis with aquatic detritivorous invertebrates: insights for biodiversity-ecosystem functioning research. J Anim Ecol 81:1259–67. García-Palacios P, McKie BG, Handa IT, Frainer A, Hättenschwiler S. 2016. The importance of litter traits and decomposers for litter decomposition: A comparison of aquatic and terrestrial ecosystems within and across biomes. Funct Ecol 30:819–29. Gessner MO, Chauvet E, Dobson M. 1999. A perspective on leaf litter breakdown in streams. Oikos 85:377–84. Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S. 2010. Diversity meets decomposition. Trends Ecol Evol 25:372–80. Graça MAS, Bärlocher F. 2005. Radial diffusion assay for tannins. In: Graça MAS, Bärlocher F, Gessner MO, Eds. Methods to study litter decomposition: a practical guide. Dordrecht: Springer. Graça MAS, Cressa C, Gessner MO, Feio MJ, Callies KA, Barrios C. 2001. Food quality, feeding preferences, survival and growth of shredders from temperate and tropical streams. Freshw Biol 46:947–57. Gulis V. 2001. Are there any substrate preferences in aquatic hyphomycetes? Mycol Res 105:1088–93. Handa IT, Aerts R, Berendse F, Berg MP, Bruder A, Butenschoen O, Chauvet E, Gessner MO, Jabiol J, Makkonen M, McKie BG, Malmqvist B, Peeters ET, Scheu S, Schmid B, van Ruijven J, Vos VC, Hattenschwiler S. 2014. Consequences of biodiversity loss for litter decomposition across biomes. Nature 509:218–21. Hillebrand H, Matthiessen B. 2009. Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12:1405–19. Ieno EN, Zuur AF. 2015. A Beginner’s guide to data exploration and visualisation with R: Highland Statistics Limited. Konno K. 2011. Plant latex and other exudates as plant defense systems: roles of various defense chemicals and proteins contained therein. Phytochemistry 72(13):1510–30. Landeira-Dabarca A, Pérez J, Graça MAS, Boyero L. 2019. Joint effects of temperature and litter quality on detritivore-mediated breakdown in streams. Aquat Sci 81:1–10. Lansky EP, Paavilainen HM, Pawlus AD, Newman RA. 2008. Ficus spp.(fig): Ethnobotany and potential as anticancer and anti-inflammatory agents. J Ethnopharmacol 119(2):195–213. Lecerf A, Chauvet E. 2008. Intraspecific variability in leaf traits strongly affects alder leaf decomposition in a stream. Basic Appl Ecol 9:598–605. LeRoy CJ, Hipp AL, Lueders K, Follstad Shah JJ, Kominoski JS, Ardón M, Dodds WK, Gessner MO, Griffiths NA, Lecerf A, Manning DWP, Sinsabaugh RL, Webster JR. 2019. Plant phylogenetic history explains in-stream decomposition at a global scale. J Ecol 108:17–35. LeRoy CJ, Whitham TG, Keim P, Marks JC. 2006. Plant genes link forests and streams. Ecology 87:255–61. Loewenstein NJ, Loewenstein EF. 2005. Non-native plants in the understory of riparian forests across a land use gradient in the Southeast. Urban Ecosyst 8:79–91. López-Rojo N, Martínez A, Pérez J, Basaguren A, Pozo J, Boyero L. 2018. Leaf traits drive plant diversity effects on litter decomposition and FPOM production in streams. PLoS ONE 13:e0198243. López-Rojo N, Pozo J, Pérez J, Basaguren A, Martínez A, Tonin AM, Correa-Araneda F, Boyero L. 2019. Plant diversity loss affects stream ecosystem multifunctionality. Ecology 100(12). Loreau M, Hector A. 2001. Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–6. Makkonen M, Berg MP, Handa IT, Hattenschwiler S, van Ruijven J, van Bodegom PM, Aerts R, Klironomos J. 2012. Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient. Ecol Lett 15:1033–41. Martínez A, Lírio AV, Febra I, Rosa J, Gonçalves AL, Canhoto C. 2020. Functional redundancy in leaf-litter-associated aquatic hyphomycetes: Fine sediment alters community composition but hardly decomposer activity. Int Rev Hydrobiol 105:44–51. McKie BG, Schindler M, Gessner MO, Malmqvist B. 2009. Placing biodiversity and ecosystem functioning in context: environmental perturbations and the effects of species richness in a stream field experiment. Oecologia 160:757–70. Moles AT, Peco B, Wallis IR, Foley WJ, Poore AG, Seabloom EW, Vesk PA, Bisigato AJ, Cella-Pizarro L, Clark CJ, Cohen PS, Cornwell WK, Edwards W, Ejrnaes R, Gonzales-Ojeda T, Graae BJ, Hay G, Lumbwe FC, Magana-Rodriguez B, Moore BD, Peri PL, Poulsen JR, Stegen JC, Veldtman R, von Zeipel H, Andrew NR, Boulter SL, Borer ET, Cornelissen JH, Farji-Brener AG, DeGabriel JL, Jurado E, Kyhn LA, Low B, Mulder CP, Reardon-Smith K, Rodriguez-Velazquez J, De Fortier A, Zheng Z, Blendinger PG, Enquist BJ, Facelli JM, Knight T, Majer JD, Martinez-Ramos M, McQuillan P, Hui FK. 2013. Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat? New Phytol 198:252–63. Naimi B, Hamm N, Groen TA, Skidmore AK, Toxopeus AG. 2014. Where is positional uncertainty a problem for species distribution modelling. Ecography 37:191–203. Nicolai V. 1988. Phenolic and mineral content of leaves influences decomposition in European forest ecosystems. Oecologia 75:575–9. Ostrofsky ML. 1997. Relationship between chemical characteristics of autumn-shed leaves and aquatic processing rates. J N Am Benthol Soc 16:750–9. Pérez J, Galan J, Descals E, Pozo J. 2014. Effects of fungal inocula and habitat conditions on alder and eucalyptus leaf litter decomposition in streams of northern Spain. Microb Ecol 67:245–55. Pérez J, Martínez A, Descals E, Pozo J. 2018. Responses of aquatic hyphomycetes to temperature and nutrient availability: a cross-transplantation experiment. Microb Ecol 76:328–39. Petchey OL, O’Gorman EJ, Flynn DFB. 2009. A functional guide to functional diversity measures. In: Naeem S, Bunker DE, Hector A, Loreau M, Perrings C, Eds. Biodiversity, ecosystem functioning, and human wellbeing. En Ecological and economic perspective. New York: Oxford University Press. p 49–59. Pozo J, Basaguren A, Elósegui A, Molinero J, Fabre E, Chauvet E. 1998. Afforestation with Eucalyptus globulus and leaf litter decomposition in streams of northern Spain. Hydrobiologia 373(374):101–9. R Core Team. 2019. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing v. 3.6.0. Rao CR. 1982. Diversity and dissimilarity coefficients—a unified approach. Theor Popul Biol 21:24–43. Roscher C, Schumacher J, Gubsch M, Lipowsky A, Weigelt A, Buchmann N, Schmid B, Schulze ED. 2012. Using plant functional traits to explain diversity–productivity relationships. PLoS ONE 7:e36760. Sanpera-Calbet I, Lecerf A, Chauvet E. 2009. Leaf diversity influences in-stream litter decomposition through effects on shredders. Freshw Biol 54:1671–82. Schindler MH, Gessner MO. 2009. Functional leaf traits and biodiversity effects on litter decomposition in a stream. Ecology 90:1641–9. Schulze ED, Mooney HA. 1993. Biodiversity and ecosystem function. Berlin: Springer. Srivastava D, Cardinale BJ, Downing AL, Duffy JE, Jouseau C, Sankaran M, Wright JP. 2009. Diversity has stronger top-down than bottom-up effects on decomposition. Ecology 90:1073–83. Swenson NG. 2013. The assembly of tropical tree communities—the advances and shortcomings of phylogenetic and functional trait analyses. Ecography 36:264–76. Tachet H, Bournaud M, Richoux P, Usseglio-Polatera P. 2000. Invertébrés d’eau douce: Systématique, biologie, écologie. Paris: CNRS éditions. Tiegs SD, Peter FD, Robinson CT, Uehlinger U, Gessner MO. 2008. Leaf decomposition and invertebrate colonization responses to manipulated litter quantity in streams. J N Am Benthol Soc 27:321–31. Tonin AM, Boyero L, Monroy S, Basaguren A, Pérez J, Pearson RG, Cardinale BJ, Gonçalves JFJ, Pozo J. 2017. Stream nitrogen concentration, but not plant N-fixing capacity, modulates litter diversity effects on decomposition. Funct Ecol 31:1471–81. Tonin AM, Pozo J, Monroy S, Basaguren A, Pérez J, Goncalves JF Jr, Pearson R, Cardinale BJ, Boyero L. 2018. Interactions between large and small detritivores influence how biodiversity impacts litter decomposition. J Anim Ecol 87:1465–74. Truchy A, Angeler DG, Sponseller RA, Johnson RK, McKie BG. 2015. Linking biodiversity, ecosystem functioning and services, and ecological resilience: towards an integrative framework for improved management. In: Advances in ecological research, vol 53. Academic Press, p 55–96 Valladares F, Gianoli E, Gómez JM. 2007. Ecological limits to plant phenotypic plasticity. New Phytol 176:749–63. Wallace J, Eggert S, Meyer J, Webster J. 1997. Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277:102–4.