Abstract
Biodiversity and ecosystem functioning (BEF) research advocates that biodiversity loss has a drastic alteration on ecosystem functioning. However, studies have barely investigated how the evolutionary dependence of species traits affects EF. Here, we developed an integrated approach combining functional (FD) and phylogenetic diversity (PD) into a single space to disentangle the effects of diversity on leaf decomposition. We conducted an experiment manipulating plant leaves into litterbags containing four species (from a pool of 27) combined in four different treatments represented by low or high FD and PD; these treatments present different scenarios of trait evolution and, therefore, a treatment with high FD and low PD, for instance, mimics a community assembled by divergent trait evolution of close relatives. We found that leaf decomposition was 30% slower in pools with high FD and PD. We show species pool with higher FD and PD have non-additive effects on decomposition, which means there is a negative effect of mixtures combining species with great functional and evolutionary differences. In addition, interactive effects of PD and FD were more important to leaf decomposition than their isolated effects. Our results suggest that PD and FD have interactive effects on decomposition and represent different axes of ecosystem variation, indicating we should avoid using phylogenies as a proxy for functional diversity. We argue that future BEF experiments may alter their design by considering a multifaceted scenario investigating community effects on ecosystem functioning, and idiosyncratic effects of key traits which may determine community assembly and ecosystem processes.
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References
Bannar-Martin KH, Kremer CT, Ernest SM, Leibold MA, Auge H, Chase J, Decklerck SAJ, Eisenhauer N, Harpole S, Hillebrand H, Isbell F, Koffel T, Larsen S, Narwani A, Petermann J, Roscher C, Cabral JS, Supp SR (2017) Integrating community assembly and biodiversity to better understand ecosystem function: the community assembly and the functioning of ecosystems (CAFE) approach. Ecol Lett 21:167–180. https://doi.org/10.1111/ele.12895
Barbe L, Mony C, Jung V, Santonja M, Bartish I, Prinzing A (2018) Functionally or phylogenetically distinct neighbours turn antagonism among decomposing litter species into synergy. J Ecol 00:1–14. https://doi.org/10.1111/1365-2745.12944
Berg B (2014) Decomposition patterns for foliar litter—a theory for influencing factors. Soil Biol Biochem 78:222–232. https://doi.org/10.1016/j.soilbio.2014.08.005
Cadotte MW (2013) Experimental evidence that evolutionarily diverse assemblages result in higher productivity. Proc Natl Acad Sci USA 110:8996–9000. https://doi.org/10.1073/pnas.1301685110
Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. Proc Natl Acad Sci USA 105:17012–17017. https://doi.org/10.1073/pnas.0805962105
Cadotte MW, Davies TJ, Peres-Neto PR (2017) Why phylogenies do not always predict ecological differences. Ecol Monogr 87:535–551. https://doi.org/10.1002/ecm.1267
Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail Narwani A, Mace GM, Tilman D, Wardle DA, Kinzing 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. https://doi.org/10.1038/nature11148
Cardinale BJ, Venail P, Gross K, Oakley TH, Narwani A, Allan E, Flombaum P, Joshi J, Reich PB, Tilman D, van Ruijven J (2015) Further re-analyses looking for effects of phylogenetic diversity on community biomass and stability. Funct Ecol 29:1607–1610. https://doi.org/10.1111/1365-2435.12540
Cavender-Bares J, Keen A, Miles B (2006) Phylogenetic structure of Floridian plant communities depends on taxonomic and spatial scale. Ecology 87:S109–S122. https://doi.org/10.1890/0012-9658(2006)87%5b109:PSOFPC%5d2.0.CO;2
Crawley MJ (2012) The R book, 2nd edn. Wiley, Chichester
Davies TJ, Urban MC, Rayfield B, Cadotte MW, Peres-Neto PR (2016) Deconstructing the relationships between phylogenetic diversity and ecology: a case study on ecosystem functioning. Ecology 97:2212–2222. https://doi.org/10.1002/ecy.1507
de Bello F, Berg MP, Dias AT, Diniz-Filho JAF, Götzenberger L, Hortal J, Ladle RJ, Lepš J (2015) On the need for phylogenetic ‘corrections’ in functional trait-based approaches. Folia Geobot 50:349–357. https://doi.org/10.1007/s12224-015-9228-6
De Marco A, Meola A, Maisto G, Giordano M, De Santo AV (2011) Non-additive effects of litter mixtures on decomposition of leaf litters in a Mediterranean maquis. Plant Soil 344:305–317. https://doi.org/10.1007/s11104-011-0748-4
Dias AT, Berg MP, de Bello F, Oosten AR, Bílá K, Moretti M (2013) An experimental framework to identify community functional components driving ecosystem processes and services delivery. J Ecol 101:29–37. https://doi.org/10.1111/1365-2745.12024
Díaz S, Lavorel S, de Bello F, Quétier F, Grigulis K, Robson TM (2007) Incorporating plant functional diversity effects in ecosystem service assessments. Proc Natl Acad Sci USA 104:20684–20689. https://doi.org/10.1073/pnas.0704716104
Díaz S, Purvis A, Cornelissen JHC, Mace GM, Donoghue MJ, Ewers R, Jordano P, Pearse W (2013) Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecol Evol 3:2958–2975. https://doi.org/10.1002/ece3.601
Dimitrakopoulos PG (2010) Influence of evenness on the litter-species richness–decomposition relationship in Mediterranean grasslands. J Plant Ecol 3:71–78. https://doi.org/10.1093/jpe/rtq009
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Finerty GE, Bello F, Bílá K, Berg MP, Dias AT, Pezzatti GB, Moretti M (2016) Exotic or not, leaf trait dissimilarity modulates the effect of dominant species on mixed litter decomposition. J Ecol 104:1400–1409. https://doi.org/10.1111/1365-2745.12602
Flynn DF, Mirotchnick N, Jain M, Palmer MI, Naeem S (2011) Functional and phylogenetic diversity as predictors of biodiversity–ecosystem–function relationships. Ecology 92:1573–1581. https://doi.org/10.1890/10-1245.1
Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246. https://doi.org/10.1111/j.0030-1299.2004.12738.x
Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380. https://doi.org/10.1016/j.tree.2010.01.010
Gianuca AT, Pantel JH, De Meester L (2016) Disentangling the effect of body size and phylogenetic distances on zooplankton top-down control of algae. Proc R Soc B 283:20160487. https://doi.org/10.1098/rspb.2016.0487
Graça MA, Bärlocher F, Gessner MO (eds) (2005) Methods to study litter decomposition: a practical guide. Springer, Berlin
Gravel D, Bell T, Barbera C, Combe M, Pommier T, Mouquet N (2012) Phylogenetic constraints on ecosystem functioning. Nat Commun 3:1117. https://doi.org/10.1038/ncomms2123
Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910. https://doi.org/10.1046/j.1365-2745.1998.00306.x
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Laughlin D (2014) Applying trait-based models to achieve functional targets for theory-driven ecological restoration. Ecol Lett 17:771–784. https://doi.org/10.1111/ele.12288
Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. https://doi.org/10.1038/35083573
McLaren JR, Turkington R (2011) Plant identity influences decomposition through more than one mechanism. PLoS One 6:e23702. https://doi.org/10.1371/journal.pone.0023702
Mouillot D, Villéger S, Scherer-Lorenzen M, Mason NW (2011) Functional structure of biological communities predicts ecosystem multifunctionality. PLoS One 6:e17476. https://doi.org/10.1371/journal.pone.0017476
Naeem S, Loreau M, Inchausti P (2002) Biodiversity and ecosystem functioning: the emergence of a synthetic ecological framework. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning. Oxford University Press, Oxford, pp 3–11
Olden JD, Poff NL, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24. https://doi.org/10.1016/j.tree.2003.09.010
Pan X, Berg MP, Butenschoen O, Murray PJ, Bartish IV, Cornelissen JH, Dong M, Prinzing A (2015) Larger phylogenetic distances in litter mixtures: lower microbial biomass and higher C/N ratios but equal mass loss. Proc R Soc B 282:20150103. https://doi.org/10.1098/rspb.2015.0103
Paquette A, Joly S, Messier C (2015) Explaining forest productivity using tree functional traits and phylogenetic information: two sides of the same coin over evolutionary scale? Ecol Evol 5:1774–1783. https://doi.org/10.1002/ece3.1456
Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234. https://doi.org/10.1071/BT12225
Petchey OL, Gaston KJ (2002) Functional diversity (FD), species richness and community composition. Ecol Lett 5:402–411. https://doi.org/10.1046/j.1461-0248.2002.00339.x
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2017) nlme: linear and nonlinear mixed effects models. R package version 3.1-131. https://CRAN.R-project.org/package=nlme
Prescott CE (2010) Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry 101:133–149. https://doi.org/10.1007/s10533-010-9439-0
Prinzing A (2016) On the opportunity of using phylogenetic information to ask evolutionary questions in functional community ecology. Folia Geobot 51:69–74. https://doi.org/10.1007/s12224-016-9242-3
Rosado BHP, Dias ATC, Mattos EA (2013) Going back to basics: importance of ecophysiology when choosing functional traits for studying communities and ecosystems. Nat Conserv 11:15–22. https://doi.org/10.4322/natcon.2013.002
Rosado BHP, Figueiredo MSL, Mattos EA, Grelle CEV (2016) Eltonian shortfall due to the Grinnellian view: functional ecology between the mismatch of niche concepts. Ecography 39:1034–1041. https://doi.org/10.1111/ecog.01678
Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Ricther A, Eberl L, Zechmeister-Boltenstern S, Riedel K (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6:1749–1762. https://doi.org/10.1038/ismej.2012.11
Srivastava DS, Cadotte MW, MacDonald AAM, Marushia RG, Mirotchnick N (2012) Phylogenetic diversity and the functioning of ecosystems. Ecol Lett 15:637–648. https://doi.org/10.1111/j.1461-0248.2012.01795.x
Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. University of California Press, California
Tardif A, Shipley B (2015) The relationship between functional dispersion of mixed‐species leaf litter mixtures and species' interactions during decomposition. Oikos 124:1050–1057. https://doi.org/10.1111/oik.01686
Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302. https://doi.org/10.1126/science.277.5330.1300
Tobner CM, Paquette A, Gravel D, Reich PB, Williams LJ, Messier C (2016) Functional identity is the main driver of diversity effects in young tree communities. Ecol Lett 19:638–647. https://doi.org/10.1111/ele.12600
Tucker CM, Cadotte MW, Carvalho SB, Davies TJ, Ferrier S, Fritz SA, Grenyer R, Helmus MR, Jin LS, Mooers AO, Pavoine S, Purschke O, Redding DW, Rosauer DF, Winter M, Mazel F (2017) A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol Rev 92:698–715. https://doi.org/10.1111/brv.12252
Venail P, Gross K, Oakley TH, Narwani A, Allan E, Flombaum P, Isbell F, Joshi J, Reich PB, Tilman D, van Ruijven J, Cardinale B (2015) Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct Ecol 29:615–626. https://doi.org/10.1111/1365-2435.12432
Vos VC, van Ruijven J, Berg MP, Peeters ET, Berendse F (2011) Macro-detritivore identity drives leaf litter diversity effects. Oikos 120:1092–1098. https://doi.org/10.1111/j.1600-0706.2010.18650.x
Wardle DA, Bonner KI, Nicholson KS (1997) Biodiversity and plant litter: experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 79:247–258. https://doi.org/10.2307/3546010
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Acknowledgements
We would like to thank Msc. Manuela Bandeira for plant species and abundance data; Dr. Nathan Kraft (UCLA) for essential assistance in several stages of this research; Drs. André Dias (UERJ) and Antoine Tardif (Université de Sherbrooke) for advice and discussion about leaf sampling and storage; Drs. Jarcilene Cortez (UFPE), Inara Leal (UFPE) and Marcus Cianciaruso (UFG) for experimental design insights; Dr. Gustavo Souza (UFPE) for assistance in molecular phylogeny; Dr. Caroline Biondi (UFRPE) for assistance in leaf chemical analysis; Dr. Cláudio Cristino (UFRPE) for computational assistance in combination selection; Drs. Mauro de Mello (UFRPE), Paula Omena (UNICAMP), Bráulio Santos (UFPB) and André Dias (UERJ) for manuscript proof reading and language adjustments. PHAS had scholarship by Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES), and ACBLS is financed by the Brazilian Ministry of Education (MEC) as a Tutor at the Tutorial Education Program (PET) in Ecology at Universidade Federal Rural de Pernambuco. This study was partially supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/MCTIC), Biodiversity Research Program, Brazilian Rainforest Network (PPBio-MA, Research Grant 457483/2012-1).
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PHAS and TG-S conceived the study with further contribution of ACB-L-S. PHAS collected data. ACB-L-S provided field and laboratorial infrastructure and TG-S performed data analysis pre- and post-experiment. PHAS wrote the first draft; other authors provided editorial advice.
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Communicated by Brian J. Wilsey.
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Sena, P.H.A., Lins-e-Silva, A.C.B. & Gonçalves-Souza, T. Integrating trait and evolutionary differences untangles how biodiversity affects ecosystem functioning. Oecologia 188, 1121–1132 (2018). https://doi.org/10.1007/s00442-018-4269-1
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DOI: https://doi.org/10.1007/s00442-018-4269-1