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Evolutionary diversity is associated with wood productivity in Amazonian forests

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Higher levels of taxonomic and evolutionary diversity are expected to maximize ecosystem function, yet their relative importance in driving variation in ecosystem function at large scales in diverse forests is unknown. Using 90 inventory plots across intact, lowland, terra firme, Amazonian forests and a new phylogeny including 526 angiosperm genera, we investigated the association between taxonomic and evolutionary metrics of diversity and two key measures of ecosystem function: aboveground wood productivity and biomass storage. While taxonomic and phylogenetic diversity were not important predictors of variation in biomass, both emerged as independent predictors of wood productivity. Amazon forests that contain greater evolutionary diversity and a higher proportion of rare species have higher productivity. While climatic and edaphic variables are together the strongest predictors of productivity, our results show that the evolutionary diversity of tree species in diverse forest stands also influences productivity. As our models accounted for wood density and tree size, they also suggest that additional, unstudied, evolutionarily correlated traits have significant effects on ecosystem function in tropical forests. Overall, our pan-Amazonian analysis shows that greater phylogenetic diversity translates into higher levels of ecosystem function: tropical forest communities with more distantly related taxa have greater wood productivity. Inventory data from 90 lowland Amazonian forest plots and a phylogeny of 526 angiosperm genera were used to show that taxonomic and phylogenetic diversity are both predictive of wood productivity but not of biomass variation.
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Articles
https://doi.org/10.1038/s41559-019-1007-y
Higher levels of taxonomic and phylogenetic diversity play
important and independent roles in determining ecosys-
tem function13. In experimental studies of temperate grass-
lands, higher levels of taxonomic and evolutionary diversity were
associated with greater biomass and productivity and variability in
the amount of evolutionary history shared within a group of spe-
cies was often a better predictor of productivity than the number of
species24, consistent with the hypothesis that evolutionary dissimi-
larity is related to niche complementarity15. However, although the
results of a range of biodiversity experiments27 suggest that com-
munities with distantly related lineages have greater carbon stocks
and productivity, the effect of phylogenetic diversity on measures
of ecosystem function remains controversial. Positive relationships
are common, but not a rule, and negligible effects of evolutionary
diversity on productivity and biomass have been reported in some
cases8,9. Therefore, it is still unclear whether these relationships can
be generalized, and the extent to which evolutionarily diverse com-
munities maximize function is unknown, particularly at large scales
relevant to conservation planning.
The total amount of phylogenetic diversity represented by spe-
cies within a community may be valuable for understanding how
diversity affects ecosystem function, because these properties
Evolutionary diversity is associated with wood
productivity in Amazonian forests
Fernanda Coelho de Souza  1*, Kyle G. Dexter2,3, Oliver L. Phillips  1, R. Toby Pennington3,4,
Danilo Neves  5, Martin J. P. Sullivan  1, Esteban Alvarez-Davila6, Átila Alves7, Ieda Amaral7,
Ana Andrade8, Luis E. O. C. Aragao4,9, Alejandro Araujo-Murakami10, Eric J. M. M. Arets  11,
Luzmilla Arroyo10, Gerardo A. Aymard C.12, Olaf Bánki13, Christopher Baraloto  14, Jorcely G. Barroso15,
Rene G. A. Boot16, Roel J. W. Brienen  1, Foster Brown17, José Luís C. Camargo8, Wendeson Castro  18,
Jerome Chave19, Alvaro Cogollo20, James A. Comiskey  21,22, Fernando Cornejo-Valverde23,
Antonio Lola da Costa24, Plínio B. de Camargo25, Anthony Di Fiore  26, Ted R. Feldpausch  4,
David R. Galbraith1, Emanuel Gloor1, Rosa C. Goodman27, Martin Gilpin1, Rafael Herrera28,29,
Niro Higuchi30, Eurídice N. Honorio Coronado31, Eliana Jimenez-Rojas32, Timothy J. Killeen33,
Susan Laurance34, William F. Laurance34, Gabriela Lopez-Gonzalez1, Thomas E. Lovejoy35,
Yadvinder Malhi  36, Beatriz S. Marimon37, Ben Hur Marimon-Junior37, Casimiro Mendoza38,
Abel Monteagudo-Mendoza39, David A. Neill40, Percy Núñez Vargas41, Maria C. Peñuela Mora42,
Georgia C. Pickavance1, John J. Pipoly III43, Nigel C. A. Pitman44, Lourens Poorter  45, Adriana Prieto46,
Freddy Ramirez47, Anand Roopsind48, Agustin Rudas46, Rafael P. Salomão  49,50, Natalino Silva50,
Marcos Silveira51, James Singh52, Juliana Stropp53, Hans ter Steege  13,54, John Terborgh55,56,
Raquel Thomas-Caesar57, Ricardo K. Umetsu  37, Rodolfo V. Vasquez39, Ima Célia-Vieira49,
Simone A. Vieira  58, Vincent A. Vos  59,60, Roderick J. Zagt16 and Timothy R. Baker1
Higher levels of taxonomic and evolutionary diversity are expected to maximize ecosystem function, yet their relative impor-
tance in driving variation in ecosystem function at large scales in diverse forests is unknown. Using 90 inventory plots across
intact, lowland, terra firme, Amazonian forests and a new phylogeny including 526 angiosperm genera, we investigated the
association between taxonomic and evolutionary metrics of diversity and two key measures of ecosystem function: above-
ground wood productivity and biomass storage. While taxonomic and phylogenetic diversity were not important predictors
of variation in biomass, both emerged as independent predictors of wood productivity. Amazon forests that contain greater
evolutionary diversity and a higher proportion of rare species have higher productivity. While climatic and edaphic variables
are together the strongest predictors of productivity, our results show that the evolutionary diversity of tree species in diverse
forest stands also influences productivity. As our models accounted for wood density and tree size, they also suggest that addi-
tional, unstudied, evolutionarily correlated traits have significant effects on ecosystem function in tropical forests. Overall, our
pan-Amazonian analysis shows that greater phylogenetic diversity translates into higher levels of ecosystem function: tropical
forest communities with more distantly related taxa have greater wood productivity.
A full list of affiliations appears at the end of the paper.
NATURE ECOLOGY & EVOLUTION | VOL 3 | DECEMBER 2019 | 1754–1761 | www.nature.com/natecolevol
1754
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... Current global environmental change is causing increasing interest in the role of abiotic factors in the long-term sustainability of ecosystems (De Laender et al., 2016;Mazzochini et al., 2019;Wu et al., 2021). Recent studies have indicated that abiotic drivers (e.g., environmental conditions, such as climate, soil and topography) might obscure the true magnitude and direction of biodiversity on the functioning and stability of ecosystems (Coelho de Souza et al., 2019;Gross et al., 2017;Wang et al., 2020). Environmental heterogeneity is also an important abiotic factor affecting biodiversity and stability (Oliver et al., 2010;. ...
... The χ 2 test was adopted to evaluate the goodness- Table S1.2). We specified a Gaussian spatial autocorrelation structure to account for spatial autocorrelation in structural equation model analyses, which is consistent with the shape of the semivariograms for stability in our study (Coelho de Souza et al., 2019). The explanatory variables were standardized (average = 0 and SD = 1) at each spatial extent (Cadotte, 2015). ...
... Linear mixed-effects models were used to examine the relative effects of individual driving factors on alpha stability, spatial asynchrony and gamma stability. To avoid multicollinearity effects, we made sure that the variance inflation factor of all predictive variables was less than five (Coelho de Souza et al., 2019). The best predictors of alpha stability and spatial asynchrony were selected based on Akaike's information criterion (AIC; ∆AIC < 2) (Burnham & Anderson, 2002;MuMIn, 2018). ...
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... In this sense, biomass accumulation is determined by the presence of highly productive species and not by their variety (Cardinale et al., 2007). Variation in wood density has been considered the most important species-variable in controlling patterns of biomass in tropical forests, being also a key functional trait in reflecting a trade-off between resource acquisition and conservation during forest successional change (Coelho de Souza et al., 2019;Finegan et al., 2015;Pradojunior et al., 2016;Pyles et al., 2018;Fauset et al., 2015;Sullivan et al., 2017;Poorter et al., 2019). Abiotic factors also influence tree biomass, with climate acting as an overriding force, with water availability being the key factor in the tropics . ...
... If so, evolutionary relationships among species can produce comparable estimates of niche space (Tucker et al., 2018). Recent studies have found positive relationships between evolutionary diversity metrics and biomass or wood productivity (Ali and Yan, 2018;Coelho de Souza et al., 2019;Yuan et al., 2016), meaning that forest communities with more distantly related taxa have higher levels of ecosystem function (Coelho de Souza et al., 2019). However, it remains unclear whether diversitybiomass relationships become stronger in the course of succession (Cardinale et al., 2007;Lennox et al., 2018;Yuan et al., 2016) or weaker (Lasky et al., 2014;Satdichanh et al., 2018), and how they are affected by disturbance (Osuri et al., 2020). ...
... If so, evolutionary relationships among species can produce comparable estimates of niche space (Tucker et al., 2018). Recent studies have found positive relationships between evolutionary diversity metrics and biomass or wood productivity (Ali and Yan, 2018;Coelho de Souza et al., 2019;Yuan et al., 2016), meaning that forest communities with more distantly related taxa have higher levels of ecosystem function (Coelho de Souza et al., 2019). However, it remains unclear whether diversitybiomass relationships become stronger in the course of succession (Cardinale et al., 2007;Lennox et al., 2018;Yuan et al., 2016) or weaker (Lasky et al., 2014;Satdichanh et al., 2018), and how they are affected by disturbance (Osuri et al., 2020). ...
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... For example, two communities with the same taxonomic diversity (TD) may be composed of species with highly different phylogenetic or functional traits (Webb, 2000). Taxonomic diversity has been the main measure of biodiversity all the time (Begon et al., 1986;Coelho de Souza et al., 2019). However, it should be noted that taxonomic diversity cannot explain ecological functions of the species that make up communities (Coelho de Souza et al., 2019;Jarzyna & Jetz, 2018), arising doubts regarding whether it can explain the impact of biodiversity on ecosystem functions (Cadotte et al., 2008;Devictor et al., 2010;Jarzyna & Jetz, 2018). ...
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Lineages tend to retain ecological characteristics of their ancestors through time. However, for some traits, selection during evolutionary history may have also played a role in determining trait values. To address the relative importance of these processes requires large-scale quantification of traits and evolutionary relationships among species. The Amazonian tree flora comprises a high diversity of angio-sperm lineages and species with widely differing life-history characteristics, providing an excellent system to investigate the combined influences of evolutionary heritage and selection in determining trait variation. We used trait data related to the major axes of life-history variation among tropical trees (e.g. growth and mortality rates) from 577 inventory plots in closed-canopy forest, mapped onto a phylogenetic hypothesis spanning more than 300 genera including all major angiosperm clades to test for evolutionary constraints on traits. We found significant phylogenetic signal (PS) for all traits, consistent with evolu-tionarily related genera having more similar characteristics than expected by chance. Although there is also evidence for repeated evolution of pioneer and shade tolerant life-history strategies within independent lineages, the existence of significant PS allows clearer predictions of the links between evolutionary diversity, ecosystem function and the response of tropical forests to global change.
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