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Biodiversity promotes primary productivity andgrowing season lengthening at the landscape scaleJacqueline Oehria,1, Bernhard Schmida, Gabriela Schaepman-Struba, and Pascal A. Niklausa,1

aDepartment of Evolutionary Biology and Environmental Studies, University of Zurich, CH-8057 Zurich, Switzerland

Edited by Shahid Naeem, Columbia University, New York, NY, and accepted by Editorial Board Member Ruth S. DeFries August 4, 2017 (received for reviewMarch 13, 2017)

Experiments have shown positive biodiversity-ecosystem func-tioning (BEF) relationships in small plots with model communitiesestablished from species pools typically comprising few dozenspecies. Whether patterns found can be extrapolated to complex,nonexperimental, real-world landscapes that provide ecosystemservices to humans remains unclear. Here, we combine speciesinventories from a large-scale network of 447 1-km2 plots with re-motely sensed indices of primary productivity (years 20002015). Weshow that landscape-scale productivity and its temporal stability in-crease with the diversity of plants and other taxa. Effects of biodiver-sity indicators on productivity were comparable in size to effects ofother important drivers related to climate, topography, and landcover. These effects occurred in plots that integrated different eco-system types (i.e., metaecosystems) and were consistent over vastenvironmental and altitudinal gradients. The BEF relations we reportare as strong or even exceed the ones found in small-scale experi-ments, despite different community assembly processes and a speciespool comprising nearly 2,000 vascular plant species. Growing seasonlength increased progressively over the observation period, and thisshift was accelerated in more diverse plots, suggesting that a largespecies pool is important for adaption to climate change. Our studyfurther implies that abiotic global-change drivers may mediate eco-system functioning through biodiversity changes.

ecosystem function and services | EVI and NDVI land surface phenology |large spatial scale | nonexperimental, real-world ecosystems | plant, bird,and butterfly species richness

Field and laboratory studies in which the diversity of plantspecies was experimentally manipulated have demonstratedthat species loss can decrease many ecosystem functions in-cluding primary productivity (1) and its temporal stability (2).These biodiversity-ecosystem functioning (BEF) studies haverevealed generally positive effects of species richness on primaryproductivity and also shed light on the mechanisms that promoteproductivity under these conditions (3). Niche differentiationamong species can enhance community-level productivity throughcomplementary resource use, decreased competition (3), and re-duced density-dependent herbivore and pathogen pressure (4).Facilitation can increase community-level productivity via positiveeffects of one species on another. For example, legumes oftensymbiotically fix atmospheric dinitrogen which subsequentlybecomes available also to nonlegume species (3). Finally, positivesampling effects occur if more diverse communities include spe-cies with high productivity and these species reach dominance (3).Although there is considerable variability among the ecosystemsinvestigated, biodiversity effects on primary productivity generallyare substantial with metaanalyses showing that they can be as largeas effects of other drivers of environmental change such as drought,fire, or eutrophication (5, 6).Field experiments in which the diversity of communities is ma-

nipulated can only address effects that occur at the scale of smallplots (typically

vegetation indices [Moderate Resolution Imaging Spectroradi-ometer enhanced vegetation index (MODIS EVI); ref. 18]. Spe-cifically, we tested whether landscape-scale biodiversity measures ofplant, bird, and butterfly communities promoted our proxy of pri-mary productivity, and its temporal stability. Capitalizing on thehigh spatial and temporal resolution of the productivity data, weanalyzed whether these effects were caused by higher momentaryvegetation activity, or by an extended growing season. We furthertested whether growing season length (GSL) increased throughoutour observation period, and whether this change depended onbiodiversity. Finally, we evaluated the magnitude of all biodiversityeffects in relation to the magnitude of effects of other drivers re-lated to climate, topography, and land cover.

ResultsPrimary Productivity. We derived two proxies of primary pro-ductivity from a remotely sensed vegetation activity index (MODISEVI; see Materials and Methods for details). EVI characterizes av-erage growing season productivity, whereas EVIGS integratesEVI over the growing season, i.e., also factors in changes inGSL (Fig. 2). We ran all analyses for both EVI and EVIGS butonly report results for EVIGS because effects were very similarfor both dependent variables. EVIGS increased strongly withthe diversity of vascular plants (Splants; Fig. 3B; F1,378 = 172,P < 0.001). A similar effect was found when using an index (S)that combined the diversity of all taxa using an ordinationtechnique (Fig. 3A; F1,379 = 240, P < 0.001). The study area wascomposed of distinct BGRs (Fig. 1). Biodiversity differed amongBGR and was negatively correlated with altitude (Pearsons productmoment correlation r = 0.48 for S and r = 0.50 for Splants),leading to a partial confounding of effects. Estimated effects ofbiodiversity became smaller when adjusted for altitude (Fig. 3 A andB; solid lines) or BGR but remained highly significant for both Sand Splants (Table S1). Biodiversity effects were independent of al-titude and BGR [interaction of S and Splants with BGR and withaltitude: not significant (n.s.)]. We also included covariates relatedto topography, climate, and land cover into our models (Table S2),but similar to BGR and altitude, effects of biodiversity remainedhighly significant even when fitted after these terms (effect sizes:Table S1).

Temporal Stability of Primary Productivity. We quantified thetemporal stability of productivity as the inverse coefficient ofvariation of EVIGS in the years 20002015 (CV1EVIGS). Thismetric increased strongly with biodiversity (S: F1,445 = 45, P

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