Abstract
Forest stratification plays a crucial role in light interception and plant photosynthetic activities. However, despite the increased number of studies on biodiversity–ecosystem function, we still lack information on how stratification in tropical forests modulates biodiversity effects. Moreover, there is less investigation and argument on the role of species and functional traits in forest layers. Here, we analysed from a perspective of forest layer (sub-canopy, canopy and emergent species layers), the relationship between diversity and aboveground biomass (AGB), focusing on functional diversity and dominance, and underlying mechanisms such as niche complementarity and selection. The sub-canopy layer had the highest species richness and diversity, while the emergent layer had the highest AGB. Species richness–AGB relationship was positive for each forest layer, but stronger for sub-canopy layer than for canopy and emergent layers. Total AGB was strongly correlated with functional diversity, leaf and wood traits of species in the sub-canopy and canopy layers. This suggests that sub-canopy and canopy species are major drivers of stand diversity–AGB relationship, and that resource filtering by canopy or emergent trees may not reduce the strength of diversity–AGB relationship in the sub-canopy layer. We argue that complementary resource use by sub-canopy species that supports niche complementarity, is a key mechanism driving AGB in natural forests. Selection effects are most evident in emergent species and niche complementarity effects for sub-canopy and canopy species, supporting arguments that AGB is affected by sub-canopy species’ efficient use of limited resources despite competition from emergent species.
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References
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
Batista NDA, Bianchini E, Carvalho EDS, Pimenta JA (2014) Architecture of tree species of different strata developing in environments with the same light intensity in a semi-deciduous forest in southern Brazil. Acta Bot Brasilica 28:34–45. https://doi.org/10.1590/S0102-33062014000100004
Carroll IT, Cardinale BJ, Nisbet RM (2011) Niche and fitness differences relate the maintenance of diversity to ecosystem function. Ecology 92:1157–1165. https://doi.org/10.1890/10-0302.1
Chen HYH, Klinka K (2003) Aboveground productivity of western hemlock and western redcedar mixed-species stands in southern coastal British Columbia. For Ecol Manag 184:55–64. https://doi.org/10.1016/S0378-1127(03)00148-8
Fargione J, Tilman D, Dybzinski R, Lambers JHR, Clark C, Harpole WS, Knops JMH, Reich PB, Loreau M (2007) From selection to complementarity: shifts in the causes of biodiversity-productivity relationships in a long-term biodiversity experiment. Proc Royal Soc B 274:871–876
Forrester DI, Bauhus J (2016) A review of processes behind diversity—productivity relationships in forests. Curr For Rep 2:45–61. https://doi.org/10.1007/s40725-016-0031-2
Geldenhuys CJ (2002) Tropical secondary forest management in Africa: reality and perspectives. Food and Agriculture Organization, Rome
Grace JB, Bollen KA (2005) Interpreting the results from multiple regression and structural equation models. Bull Ecol Soc Am 86:283–295. https://doi.org/10.1890/0012-9623(2007)
Gravel D, Canham CD, Beaudet M, Messier C (2010) Shade tolerance, canopy gaps and mechanisms of coexistence of forest trees. Oikos 119:475–484. https://doi.org/10.1111/j.1600-0706.2009.17441.x
Guilherme FAG, Morellato LPC, Assis MA (2004) Horizontal and vertical tree community structure in a lowland atlantic rain forest, southeastern Brazil. Rev Bras Botânica 27:725–737. https://doi.org/10.1590/S0100-84042004000400012
Ishii H, Asano S (2010) The role of crown architecture, leaf phenology and photosynthetic activity in promoting complementary use of light among coexisting species in temperate forests. Ecol Res 25:715–722. https://doi.org/10.1007/s11284-009-0668-4
Ishii H, Azuma W, Nabeshima E (2013) The need for a canopy perspective to understand the importance of phenotypic plasticity for promoting species coexistence and light-use complementarity in forest ecosystems. Ecol Res 28:191–198. https://doi.org/10.1007/s11284-012-1025-6
Jacob M, Leuschner C, Thomas FM (2010) Productivity of temperate broad-leaved forest stands differing in tree species diversity. Ann For Sci 67:503. https://doi.org/10.1051/forest/2010005
Kattge J, Diaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright IJ, Cornelissen JHC, Violle C, Harrisson SP, Van Bodegom PM, Reichstein M, Enquist BJ, Soudzilovskaia NA, Ackerly DD, Anand M, Atkin O, Bahn M, Baker TR, Baldocchi D, Bekker R, Blanco CC, Blonder B, Bond WJ, Bradstock R, Bunker DE, Casanoves F, Cavender-Bares J, Chambers JQ, Chapin FS III, Chave J, Coomes D, Cornwell WK, Craine JM, Dobrin BH, Duarte L, Durka W, Elser J, Esser G, Estiarte M, Fagan WF, Fanf J, Fernandez-Mendez F, Fidelis A, Finegan B, Flores O, Ford H, Frank D, Freschet GT, Fyllas NM, Gallagher RV, Green WA, Gutierrez AG, Hickler T, Higgins SI, Hodgson JG, Jalili A, Jansen S, Joly CA, Kerkhoff AJ, Kirkup D, Kitajima K, Kleyer M, Klotz S, Knops JMH, Kramer K, Kühn I, Kurokawa H, Laughlin D, Lee TD, Leishman M, Lens F, Lenz T, Lewis SL, Lloyd J, Llusià J, Louault F, Ma S, Mahecha MD, Manning P, Massad T, Medlyn BE, Messier J, Moles AT, Müller SC, Nadrowski K, Naeem S, Niinemets Ü, Nöllert S, Nüske A, Ogaya R, Oleksyn J, Onipchenko VG, Onoda Y, Ordoñez J, Overbeck G, Ozinga WA, Patiño S, Paula S, Pausas JG, Peñuelas J, Phillips OL, Pillar V, Poorter H, Poorter L, Poschlod P, Prinzing A, Proulx R, Rammig A, Reinsch S, Reu B, Sack L, Salgado-Negret B, Sardans J, Shiodera S, Shipley B, Siefert A, Sosinski E, Soussana J-F, Swaine E, Swenson N, Thompson K, Thornton P, Waldram M, Weiher E, White M, White S, Wright SJ, Yguel B, Zaehle S, Zanne AE, Wirth C (2011) TRY - a global database of plant traits. Glob Chang Biol 17:2905–2935. https://doi.org/10.1111/j.1365-2486.2011.02451.x
Kelty MJ (2006) The role of species mixtures in plantation forestry. For Ecol Manag 233:195–204
King DA, Wright SJ, Connell JH (2006) The contribution of interspecific variation in maximum tree height to tropical and temperate diversity. J Trop Ecol 22:11–24. https://doi.org/10.1017/S0266467405002774
Kuznetsova A, Brockhoff PB, Christensen R (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-32
Laliberté E, Legendre P, Shipley B (2015) Measuring functional diversity (FD) from multiple traits, and other tools for functional ecology. R package version 1.0–12
Lasky JR, Uriarte M, Boukili VK, Erickson DL, John Kress W, Chazdon RL (2014) The relationship between tree biodiversity and biomass dynamics changes with tropical forest succession. Ecol Lett 17:1158–1167. https://doi.org/10.1111/ele.12322
Laughlin DC (2011) Nitrification is linked to dominant leaf traits rather than functional diversity. J Ecol 99:1091–1099. https://doi.org/10.1111/j.1365-2745.2011.01856.x
Liang J, Crowther TW, Picard N, Wiser S, Zhou M, Alberti G, Schulze E, Mcguire AD, Bozzato F, Pretzsch H, De-Miguel S, Paquette A, Hérault B, Scherer-lorenzen M, Barrett CB, Glick HB, Hengeveld GM, Nabuurs G, Pfautsch S, Viana H, Vibrans AC, Ammer C, Schall P, Verbyla D, Tchebakova N, Fischer M, Watson JV, Chen HYH, Lei X, Schelhaas M, Lu H, Gianelle D, Parfenova EI, Salas C, Lee E, Lee B, Kim HS, Bruelheide H, Coomes DA, Piotto D, Sunderland T, Schmid B, Gourlet-fleury S, Sonké B, Tavani R, Zhu J, Brandl S, Baraloto C, Frizzera L, Balazi R, Oleksyn J, Zawiła-Niedźwiecki T, Bouriaud O, Bussotti F, Finér L, Jaroszewicz B, Jucker T, Valladares F, Jagodzinski AM, Peri PL, Gonmadje C, Marthy W, O’Brien T, Martin EH, Marshall AR, Rovero F, Bitariho R, Niklaus PA, Alvarez-loayza P, Chamuya N, Valencia R, Mortier F, Wortel V, Engone-obiang NL, Ferreira LV, Odeke D, Vasquez R, Lewis SL, Reich PB (2016) Positive biodiversity-productivity relationship predominant in global forests. Science 354:aaf8957. https://doi.org/10.1126/science.aaf8957
Lin D, Anderson-teixeira KJ, Lai J, Mi X, Ren H, Ma K (2016) Traits of dominant tree species predict local scale variation in forest aboveground and topsoil carbon stocks. Plant Soil 409:435–446. https://doi.org/10.1007/s11104-016-2976-0
Lopez OR, Farris-lopez K, Montgomery RA, Givnish TJ (2008) Leaf phenology in relation to canopy closure in southern Appalachian trees. Am J Bot 95:1395–1407
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. https://doi.org/10.1038/35083573
Mason NWH, de Bello F, Dolezal J, Leps J (2011) Niche overlap reveals the effects of competition, disturbance and contrasting assembly processes in experimental grassland communities. J Ecol 99:788–796. https://doi.org/10.1111/j.1365-2745.2011.01801.x
Mensah S, Veldtman R, Assogbadjo AE, Glèlè Kakaï R, Seifert T (2016a) Tree species diversity promotes aboveground carbon storage through functional diversity and functional dominance. Ecol Evol 6:7546–7557. https://doi.org/10.1002/ece3.2525
Mensah S, Glèlè Kakaï R, Seifert T (2016b) Patterns of biomass allocation between foliage and woody structure: the effects of tree size and specific functional traits. Ann For Res 59:49–60
Mensah S, Veldtman R, du Toit B, Glèlè Kakaï R, Seifert T (2016c) Aboveground biomass and carbon in a South African Mistbelt forest and the relationships with tree species diversity and forest structures. Forests 79:1–17. https://doi.org/10.3390/f7040079
Mensah S, Pienaar OL, Kunneke A, du Toit B, Seydack A, Uhl E, Pretzsch H, Seifert T (2018) Height-diameter allometry in South Africa’s indigenous high forests: assessing generic models performance and function forms. For Ecol Manage 410:1–11. https://doi.org/10.1016/j.foreco.2017.12.030
Mittelbach GG, Steiner CF, Scheiner SM, Gross KL, Reynolds HL, Waide RB, Willig MR, Dodson SI, Gough L (2001) What is the observed relationship between species richness and productivity? Ecology 82:2381–2396. https://doi.org/10.1890/03-8021
Morin X, Fahse L, Scherer-Lorenzen M, Bugmann H (2011) Tree species richness promotes productivity in temperate forests through strong complementarity between species. Ecol Lett 14:1211–1219. https://doi.org/10.1111/j.1461-0248.2011.01691.x
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142
Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ, Cornelissen JHC, Díaz S, Dominy NJ, Elgart A, Enrico L, Fine PVA, Howard JJ, Jalili A, Kitajima K, Kurokawa H, McArthur C, Lucas PW, Markesteijn L, Pérez-Harguindeguy N, Poorter L, Richards L, Santiago LS, Sosinski EE, Van Bael SA, Warton DI, Wright IJ, Wright SJ, Yamashita N (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312. https://doi.org/10.1111/j.1461-0248.2010.01582.x
Paquette A, Messier C (2011) The effect of biodiversity on tree productivity: from temperate to boreal forests. Glob Ecol Biogeogr 20:170–180. https://doi.org/10.1111/j.1466-8238.2010.00592.x
Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87:1733–1743. https://doi.org/10.1890/0012-9658(2006)
Prado-junior JA, Schiavini I, Vale VS, Arantes CS, Van Der Sande MT, Lohbeck M, Poorter L (2016) Conservative species drive biomass productivity in tropical dry forests. J Ecol 104:817–827. https://doi.org/10.1111/1365-2745.12543
Pretzsch H (2014) Canopy space filling and tree crown morphology in mixed-species stands compared with monocultures. For Ecol Manage 327:251–264. https://doi.org/10.1016/j.foreco.2014.04.027
Reich PB, Knops J, Tilman D, Craine J, Ellsworth D, Tjoelker M, Lee T, Wedin D, Naeem S, Bahauddin D, Hendrey G, Jose S, Wrage K, Goth J, Bengston W (2001) Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410:809–810
Rosseel Y (2012) lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36
Ruiz-Benito P, Gómez-Aparicio L, Paquette A, Messier C, Kattge J, Zavala M (2014) Diversity increases carbon storage and tree productivity in Spanish forests. Glob Ecol Biogeogr 23:311–322. https://doi.org/10.1111/geb.12126
Seidel D, Leuschner C, Scherber C, Beyer F, Wommelsdorf T, Cashman MJ, Fehrmann L (2013) The relationship between tree species richness, canopy space exploration and productivity in a temperate broad-leaf mixed forest. For Ecol Manag 310:366–374. https://doi.org/10.1016/j.foreco.2013.08.058
Seifert T, Seifert S, Seydack A, Durrheim G, von Gadow K (2014) Competition effects in an afrotemperate forest. For Ecosyst 1:13. https://doi.org/10.1186/s40663-014-0013-4
Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA 94:1857–1861. https://doi.org/10.1073/pnas.94.5.1857
Vance-Chalcraft HD, Willig MR, Cox SB, Lugo AE, Scatena FN (2010) Relationship between aboveground biomass and multiple measures of biodiversity in subtropical forest of Puerto Rico. Biotropica 42:290–299. https://doi.org/10.1111/j.1744-7429.2009.00600.x
Vilà M, Vayreda J, Comas L, Ibánez JJ, Mata T, Obón B (2007) Species richness and wood production: a positive association in Mediterranean forests. Ecol Lett 10:241–250. https://doi.org/10.1111/j.1461-0248.2007.01016.x
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301. https://doi.org/10.1890/07-1206.1
Waide RB, Willig MR, Steiner CF, Mittelbach G, Gough L, Dodson SI, Juday GP, Parmenter R (1999) The relationship between productivity and species richness. Annu Rev Ecol Syst 30:257–300. https://doi.org/10.1146/annurev.ecolsys.30.1.257
Wang W, Lei X, Ma Z, Kneeshaw DD, Peng C (2011) Positive relationship between aboveground carbon stocks and structural diversity in spruce-dominated forest stands in New Brunswick, Canada. For Sci 57:506–515. https://doi.org/10.1111/oik.01525
Whittaker R, Heegaard E (2003) What is the observed relationship between species richness and productivity? Ecology 84:3384–3390. https://doi.org/10.1007/s00442-003-1343-z
Wu X, Wang X, Tang Z, Shen Z, Zheng C, Xia X, Fang J (2015) The relationship between species richness and biomass changes from boreal to subtropical forests in China. Ecography (Cop) 38:602–613. https://doi.org/10.1111/ecog.00940
Yachi S, Loreau M (2007) Does complementary resource use enhance ecosystem functioning? A model of light competition in plant communities. Ecol Lett 10:54–62. https://doi.org/10.1111/j.1461-0248.2006.00994.x
Zanne AE, Lopez-Gonzalez G, Coomes DA, Ilic J, Jansen S, Lewis SL, Miller RB, Swenson NG, Wiemann MC, Chave J (2009) Data from: towards a worldwide wood economics spectrum. Dryad Digit Repos. https://doi.org/10.5061/dryad.234
Zhang Y, Chen HYH, Taylor AR (2017) Positive species diversity and above-ground biomass relationships are ubiquitous across forest strata despite interference from overstorey trees. Funct Ecol 31:419–426. https://doi.org/10.1111/1365-2435.12699
Acknowledgements
This research was supported by the African Forest Forum through a research grant provided to the first author. We also acknowledge the “Consolidoc” financial support from the Research Division of Stellenbosch University. The authors are grateful to the two anonymous reviewers and the editor for their comments on the earlier versions of this article.
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SM and TS originally formulated the idea. SM, TS and BdT conceived the sampling design. SM collected and analysed the data. SM wrote the manuscript with editorial support from BdT and TS.
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Mensah, S., du Toit, B. & Seifert, T. Diversity–biomass relationship across forest layers: implications for niche complementarity and selection effects. Oecologia 187, 783–795 (2018). https://doi.org/10.1007/s00442-018-4144-0
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DOI: https://doi.org/10.1007/s00442-018-4144-0