Below‐ground complementarity effects in a grassland biodiversity experiment are related to deep‐rooting species

Summary 1.Belowground resource partitioning is often proposed as the underlying mechanism for the positive relationship between plant species richness and productivity. For example, if species have different root distributions, a mixture of plant species may be able to use the available resources more completely than the individual species in a monoculture. However, there is little experimental evidence for differentiation in vertical root distributions among species and its contribution to biodiversity effects. 2.We determined species-specific root standing biomass over depth using molecular techniques (real time-qPCR) in a large grassland biodiversity experiment (1-8 plant species mixtures), in two years. Species-specific root biomass data were used to disentangle the effects of positive interactions between species (complementarity effects) and effects due to dominance of productive species (selection effects) on root biomass in mixtures. In a next step, these biodiversity effects were linked to the diversity of rooting depths and the averaged rooting depth of the community. 3.Root biomass increased with species richness. This was mainly due to positive interactions (the complementarity effect), which increased with species richness belowground. In contrast, the selection effect decreased with species richness. Although there was considerable variation in vertical root distribution between species in monocultures, the diversity of rooting strategies did not explain the complementarity effect. Rather, the abundance of deep-rooting species in mixtures (i.e. high community weighted mean) was significantly related to the complementarity effect. Comparing the ‘predicted’ root distribution (based on monocultures) to the actual distribution in mixtures, we found that mixtures rooted deeper than expected, but this did not better explain the complementarity effect. 4.Synthesis: This study demonstrates that vertical root distributions of species provide only subtle evidence for resource partitioning. We found no evidence that functional diversity in vertical rooting patterns was important for the complementarity effect, in contrast to our expectation that the enhancement of productivity was due to resource partitioning. Alternatively, we found significant but weak relationships between the complementarity effect and deep-rooting communities, based on the community weighted mean root distribution. This suggests that factors other than belowground resource partitioning alone may drive the biodiversity-productivity relationship. This article is protected by copyright. All rights reserved.

[1]  P. Reich,et al.  Plant diversity effects on grassland productivity are robust to both nutrient enrichment and drought , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[2]  H. de Kroon,et al.  Spatial heterogeneity of plant-soil feedback affects root interactions and interspecific competition. , 2015, The New phytologist.

[3]  S. Kembel,et al.  Plant Phenotypic Plasticity Belowground: A Phylogenetic Perspective on Root Foraging Trade‐Offs , 2005, The American Naturalist.

[4]  Michel Loreau,et al.  Niche and fitness differences relate the maintenance of diversity to ecosystem function: comment. , 2012, Ecology.

[5]  G. McNickle,et al.  The Behavioral Ecology of Nutrient Foraging by Plants , 2011 .

[6]  R. B. Jackson,et al.  A global analysis of root distributions for terrestrial biomes , 1996, Oecologia.

[7]  H. de Kroon,et al.  Unveiling below‐ground species abundance in a biodiversity experiment: a test of vertical niche differentiation among grassland species , 2010 .

[8]  Robert B. Jackson,et al.  THE GLOBAL BIOGEOGRAPHY OF ROOTS , 2002 .

[9]  N. Buchmann,et al.  No Evidence of Complementary Water Use along a Plant Species Richness Gradient in Temperate Experimental Grasslands , 2015, PloS one.

[10]  F. Bazzaz,et al.  Underground Niche Separation in Successional Plants , 1976 .

[11]  C. Wirth,et al.  A trait-based experimental approach to understand the mechanisms underlying biodiversity–ecosystem functioning relationships , 2014 .

[12]  P. Legendre,et al.  A distance-based framework for measuring functional diversity from multiple traits. , 2010, Ecology.

[13]  A. Weigelt,et al.  Positive biodiversity–productivity relationship due to increased plant density , 2009 .

[14]  F. Berendse Competition between plant populations with different rooting depths II. Pot experiments , 1981, Oecologia.

[15]  F. Chapin,et al.  EFFECTS OF BIODIVERSITY ON ECOSYSTEM FUNCTIONING: A CONSENSUS OF CURRENT KNOWLEDGE , 2005 .

[16]  F. Berendse,et al.  Long-term persistence of a positive plant diversity-productivity relationship in the absence of legumes , 2009 .

[17]  Christian Wirth,et al.  From pots to plots: hierarchical trait‐based prediction of plant performance in a mesic grassland , 2016 .

[18]  M. Pärtel,et al.  Plant species richness belowground: higher richness and new patterns revealed by next‐generation sequencing , 2012, Molecular ecology.

[19]  W. Beyschlag,et al.  Aggregative Root Placement: A Feature During Interspecific Competition in Inland Sand-Dune Habitats , 2006, Plant and Soil.

[20]  P. Reich,et al.  Increasing plant diversity effects on productivity with time due to delayed soil biota effects on plants , 2012 .

[21]  Fabien Quétier,et al.  Assessing functional diversity in the field - methodology matters! , 2007 .

[22]  M. Semchenko,et al.  Plant root exudates mediate neighbour recognition and trigger complex behavioural changes. , 2014, The New phytologist.

[23]  D. Wardle,et al.  Interspecific interactions and biomass allocation among grassland plant species , 2003 .

[24]  S. Graham,et al.  Spatial patterns of plant diversity below‐ground as revealed by DNA barcoding , 2011, Molecular ecology.

[25]  Per B. Brockhoff,et al.  lmerTest Package: Tests in Linear Mixed Effects Models , 2017 .

[26]  J. Cahill,et al.  Disentangling root system responses to neighbours: identification of novel root behavioural strategies , 2015, AoB PLANTS.

[27]  J. Fridley,et al.  Fine‐scale belowground species associations in temperate grassland , 2015, Molecular ecology.

[28]  P. Reich,et al.  Species and functional group diversity independently influence biomass accumulation and its response to CO2 and N. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  S. von Felten,et al.  Belowground nitrogen partitioning in experimental grassland plant communities of varying species richness. , 2009, Ecology.

[30]  Michel Loreau,et al.  Partitioning selection and complementarity in biodiversity experiments , 2001, Nature.

[31]  D. F. Grigal,et al.  Vertical root distributions of northern tree species in relation to successional status , 1987 .

[32]  D. Bates,et al.  Linear Mixed-Effects Models using 'Eigen' and S4 , 2015 .

[33]  A. Mamolos,et al.  Depth of Root Activity of Coexisting Grassland Species in Relation to N and P Additions, Measured Using Nonradioactive Tracers , 1995 .

[34]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[35]  Ian T. Carroll,et al.  Impacts of plant diversity on biomass production increase through time because of species complementarity , 2007, Proceedings of the National Academy of Sciences.

[36]  E. Schulze,et al.  The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community , 2004 .

[37]  Sandra Lavorel,et al.  A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services , 2013 .

[38]  H. de Kroon,et al.  Unravelling below‐ground plant distributions: a real‐time polymerase chain reaction method for quantifying species proportions in mixed root samples , 2008, Molecular ecology resources.

[39]  K. Beard,et al.  Plant–soil feedbacks provide an additional explanation for diversity–productivity relationships , 2012, Proceedings of the Royal Society B: Biological Sciences.

[40]  Janneke HilleRisLambers,et al.  The importance of niches for the maintenance of species diversity , 2009, Nature.

[41]  D. Wardle,et al.  The Overlooked Role of Facilitation in Biodiversity Experiments. , 2017, Trends in ecology & evolution.

[42]  D. Tilman,et al.  Root depth distribution and the diversity–productivity relationship in a long‐term grassland experiment , 2013 .

[43]  F. Berendse Competition between plant populations with different rooting depths , 1979, Oecologia.

[44]  Angela Hodge,et al.  The plastic plant: root responses to heterogeneous supplies of nutrients , 2004 .

[45]  Christian Wirth,et al.  Long‐term study of root biomass in a biodiversity experiment reveals shifts in diversity effects over time , 2014 .

[46]  G. Daily,et al.  Biodiversity loss and its impact on humanity , 2012, Nature.

[47]  C. Wilke Streamlined Plot Theme and Plot Annotations for 'ggplot2' , 2015 .

[48]  L. Mommer,et al.  Can root trait diversity explain complementarity effects in a grassland biodiversity experiment? , 2016 .

[49]  J. Postma,et al.  Root foraging elicits niche complementarity-dependent yield advantage in the ancient 'three sisters' (maize/bean/squash) polyculture. , 2014, Annals of botany.

[50]  Do grassland plant communities profit from N partitioning by soil depth? , 2012, Ecology.

[51]  G. McNickle,et al.  Plants Integrate Information About Nutrients and Neighbors , 2010, Science.

[52]  T. Herben,et al.  Horizontal and vertical distribution of root absorption zones of four common grass species in a mountain grassland , 2003 .

[53]  P. Reich,et al.  Diversity and Productivity in a Long-Term Grassland Experiment , 2001, Science.

[54]  R. Joffre,et al.  Quantifying species composition in root mixtures using two methods: near-infrared reflectance spectroscopy and plant wax markers. , 2006, The New phytologist.

[55]  D. Tilman,et al.  Ecological mechanisms associated with the positive diversity-productivity relationship in an N-limited grassland. , 2009, Ecology.

[56]  Bernhard Schmid,et al.  Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands. , 2008, Ecology.

[57]  Maik Bartelheimer,et al.  Should I stay or should I go? Roots segregate in response to competition intensity , 2015, Plant and Soil.

[58]  E. Schulze,et al.  Using Plant Functional Traits to Explain Diversity–Productivity Relationships , 2012, PloS one.

[59]  H. Kroon,et al.  Independent variations of plant and soil mixtures reveal soil feedback effects on plant community overyielding , 2013 .

[60]  L. Mommer,et al.  Going underground: root traits as drivers of ecosystem processes. , 2014, Trends in ecology & evolution.

[61]  L. Mommer,et al.  Plant species richness promotes soil carbon and nitrogen stocks in grasslands without legumes , 2014 .

[62]  Liesje Mommer,et al.  Root-Root Interactions: Towards A Rhizosphere Framework. , 2016, Trends in plant science.

[63]  F. Berendse,et al.  Diversity-productivity relationships: initial effects, long-term patterns, and underlying mechanisms. , 2005, Proceedings of the National Academy of Sciences of the United States of America.