Reduced ecosystem functions associated with species loss and climate change Han Y. H. Chen Faculty of Natural Resources Management Lakehead University

Research in Chen’s lab Function Biomass (C), production, Nutrients Dynamics Succession, disturbance regimes Diversity Why plants co-exist Disturbance Species interaction Climate change

Why understanding diversity function relationships is important? Continuous loss of biodiversity at the global scale “Earth loses more than three-quarters of its species in a geologically short interval (1k years), as has happened only five times in the past 540 million years… a sixth mass extinction may be under way, given the known species losses over the past few centuries and millennia” Barnosky et al. 2011, Nature 471:51-57 AgricultureForestry Urbanization Drought

Fundamental question in BEF How might loss of the world's biodiversity alter ecological function? Net primary production Nutrient cycling Outbreaks of insects and diseases?

The original hypothesis Darwin’s (1859): the presence of a “divergence of characters” is essential for reduced interspecific competition as a result of different demands for resources, and in turn, improves productivity Tilman et al. (1997) Science 277:

Diversity and productivity relationships Despite being the most published topic in ecology Debate persists about diversity effects in natural vs. planted grasslands (Adler et al. 2011, Science 333, ) Evenness Heterogeneity of life-history traits The impacts of these factors on DPRs in forest ecosystems are more poorly understood

. Hypotheses Richness & evenness The extent of life-history variation Biomes Stand origin Stand age

Methods Tropical 22 Temperate 19 Boreal 13 Each selected original study was designed to test diversity effects, i.e., similar sites and disturbance history

Net diversity effect, effect size (ES) P ij = the observed productivity of the jth observation in the ith study = the mean productivity of monocultures Evenness H’ = observed Shannon’s index S = species richness Pielou (1969)

Trait-based approach 10 Contrasting shade tolerance Contrasting nitrogen-fixing Fast-slow growth

Boosted regression trees De’ath 2007 Elith et al Regression trees + boosting Machine learning Model averaging Statistical analysis

Global average effect of diversity Ln(ES) = ES = 1.24 At a global scale, the polycultures have 24% higher productivity than monocultures

Predicted ln(ES) 34%13%15% 29% <3% <2% Zhang et al J Ecol

Niche differentiation/partitioning and/or facilitation Grasslands (Tilman and many others) Algae in fresh water systems (Cardinale BJ, Biodiversity improves water quality through niche partitioning, Nature 472, 86-89) Reduced Janzen–Connell effects Positive diversity effects on productivity are realized by reduced plant disease (Schnitzer et al. 2011, Ecology 92, ) Known mechanisms for positive DPRs

Diversity effects in belowground Few studies examined diversity effects on belowground productivity of forest ecosystems (although belowground accounts for ≈ 50% of total NPP; fine roots, <2 mm in diameter alone accounts for 33% of total NPP) Potential mechanisms are poorly understood in natural environment Greater soil volume filling in natural environments?

Methods Pb+Late-successional Picea mariana, Picea glauca, and Abies balsamea (LSC)=Pb+LSC Pinus banksiana (Pb) Populus tremuloides (Pt) Pb + Pt deep- vs. shallow-rooted conifers gymnosperm vs. angiosperm

Seasonal biomass variation Brassard et al J. Ecol.

Fine root production 19% to 83% higher in mixed- species stands than single- species stands

Vertical distribution of fine roots May June July Aug Sept Oct

Seasonal biomass heterogeneity 1 SD of biomass among 3 layers 1 SD of biomass among 7 cores

Relationships between fine root biomass and heterogeneity

Conclusion Evenness and trait diversity increase productivity both above- and belowground Exploiting resources more completely in space and time Implications Conserving species and trait diversity Diversity effects are more pronounced in old forests

Research in Chen’s lab Function Biomass (C), production, N & P resorption Dynamics Succession, disturbance regimes Diversity Plants Disturbance Species interaction Climate change

Climate change and forest dynamics Biome shift Reduced ecosystem function, NPP, carbon sink to source Forest compositional change Studied 76 old-growth (>200 years old) stands Assume an equilibrium state, thus all changes in mortality are exogenous (climate change) Widespread temporal increases in tree mortality have been attributed to climate change

Studied 96 old stands (>80 years old)

Two underlying assumptions: 1. Endogenous effects on tree mortality in old forests are weak, and thus temporal variation in tree mortality can be solely attributed to climate change 2. Climate change effects are the same in young and old forests Connell and Slatyer (1977): "We have found no example of a community of sexually reproducing individuals…… reached a steady-state equilibrium"

Others attributed temporal increases in mortality to stand development Thorpe & Daniels Can. J. For. Res. 42: Luo & Chen J. Ecol. 99: Lutz & Halpern Ecol. Monogr. 76: Competition Negative density dependence Tree ageing Unsuitable statistical methods that marginalize either climate or non-climate drivers for longitudinal data in which these drivers are highly correlated (Brown et al GCB: 17: 3697)

887 plots Measured: Stand age: 17 to 243 yr

Use Bayesian logistic models Endogenous mechanisms Asymmetric competition Stand crowding Interspecific interaction Tree ageing Exogenous mechanisms Year or Annual temperature anomaly or Drought index (PDSI or CMI)

What is Bayesian statistics? --vs. frequentist statistics Frequentist Parameters are fixed quantities Bayesian The true value of a parameter is thought of as being a random variable to which we assign a probability distribution, known specifically as prior information

Analyzed by young forests (≤ 80 years) and old (>80 years) Luo and Chen Nature Comm. 4:16554:1655

Tree mortality in young and old forests Luo and Chen Nature Comm. 4:16554:1655

Multiple climate change drivers Higher growth rates Higher NPP Higher turnover rates = high mortality? Alternatively, more food (CO2) improves tree health, thus low mortality?

Surface temperature anomalies relative to 1951–1980 from surface air measurements at meteorological stations and ship and satellite SST measurements. Hansen J et al. PNAS 2006;103: ©2006 by National Academy of Sciences

Spatially heterogeneous N deposition Recay et al Nat Geosci 7:430

Global drought trends for past 60 years Sheffied et al Nature 491: 435

Increased mortality is positively associated with temperature anomaly Negatively associated with drought index (ACMIA)

Climate change effects on tree mortality The increased mortality is also higher in Pure than mixed forests More crowded forests Among species Higher for Populus balsamifera among pioneers Higher Picea spp. than Populus tremuloides and Pinus banksiana Undergoing forest compositional shift that is independent of endogenous forest succession —an important conservation challenge!

Current and future research in Chen’s lab Function Productivity & stability Dynamics Diversity Disturbance Species interaction Climate change Why/how species co-exist? Biogeography of diversity and function of Canada’s forest Long-(>8,000 years) and short-term fire regime and forest dynamics

Acknowledgements Funding NSERC Discovery Grant NSERC Strategic Project National Centre of Excellence Network of Sustainable Forest Management Ontario Early Research Award program Northern Ontario Heritage Fund Cooperation Partners and collaborators Resolute Inc. Tembec Inc. Louisiana-Pacific Canada Ltd. Ontario Forest Ecosystem Science Co-operative Inc. Provincial Governments Canadian Forest Service