Biodiversity and Ecosystem Functioning: Looking Back and Moving Forward Jiang, Lin School of Biology Georgia Institute of Technology

Outline Current knowledge on biodiversity and ecosystem functioning (BEF) Current knowledge on biodiversity and ecosystem functioning (BEF) Mechanisms: niche complementarity and positive selection effects Mechanisms: niche complementarity and positive selection effects Problems associated with current BEF studies Problems associated with current BEF studies An important mechanism that has received relatively little attention: the negative selection effect An important mechanism that has received relatively little attention: the negative selection effect Hypothesis: multiple forms of BEF relationships. Hypothesis: multiple forms of BEF relationships. My own experimental data My own experimental data Literature survey Literature survey Biodiversity and stability: Biodiversity and stability: Question: Does predation alter the relationship between biodiversity and stability? Question: Does predation alter the relationship between biodiversity and stability?

Species extinction: past, current, and future trends

Definitions Biodiversity: genetic, taxonomic, or functional diversity. Biodiversity: genetic, taxonomic, or functional diversity. Species richness: the number of species. Species richness: the number of species. Ecosystem functioning: stocks of energy and materials, fluxes of energy or material processing, and stability of stocks or rates over time Ecosystem functioning: stocks of energy and materials, fluxes of energy or material processing, and stability of stocks or rates over time Biomass, decomposition, the ability to support consumer populations, temporal stability of biomass. Biomass, decomposition, the ability to support consumer populations, temporal stability of biomass.

Type 1 Species richness Ecosystem functioning Vitousek and Hooper 1993 Hypothetical relationships between biodiversity and ecosystem functioning

Type 1 Type 2 Species richness Ecosystem functioning Vitousek and Hooper 1993

Hypothetical relationships between biodiversity and ecosystem functioning Type 1 Type 2 Type 3 Species richness Ecosystem functioning Vitousek and Hooper 1993

Cedar Creek Experiment Tilman et al. 2001

BIODEPTH Experiment Hector et al. 1999

The commonly observed relationship between biodiversity and ecosystem functioning Type 2 Species richness Ecosystem functioning

Mechanisms for the positive BEF relationship Niche Complementarity Niche Complementarity Niche differentiation among species allows diverse communities to utilize available resources more completely (Tilman et al. 1997) Niche differentiation among species allows diverse communities to utilize available resources more completely (Tilman et al. 1997) Low diversityHigh diversity No niche overlap

Mechanisms for the positive BEF relationship The positive selection (or sampling) effect The positive selection (or sampling) effect Positive correlation between species competitive ability and its contribution to ecosystem functioning. Positive correlation between species competitive ability and its contribution to ecosystem functioning. Increasing diversity increases the probability that communities are dominated by functionally important species (Aarssen 1997, Huston 1997, Tilman et al. 1997) Increasing diversity increases the probability that communities are dominated by functionally important species (Aarssen 1997, Huston 1997, Tilman et al. 1997) Low diversityHigh diversity Competitively dominant

The positive selection effect appears to be the primary mechanism behind positive relations between biodiversity and community biomass (Cardinale et al. 2006)

Problems with current BEF experiments Most BEF experiments are short-term. Most BEF experiments are short-term. Last less than one generation of experimental organisms. Last less than one generation of experimental organisms. Most BEF experiments focus on biomass production. Most BEF experiments focus on biomass production. Patterns on biomass production may not be generalized to other ecosystem variables. Patterns on biomass production may not be generalized to other ecosystem variables.

The negative selection effect No positive correlation between species competitive ability and its contribution to ecosystem functioning. No positive correlation between species competitive ability and its contribution to ecosystem functioning. Increasing diversity increases the probability that communities are dominated by functionally insignificant species. Increasing diversity increases the probability that communities are dominated by functionally insignificant species. Low diversity High diversity Competitively dominant

Strong negative selection effects can lead to no effects of biodiversity on ecosystem functioning Species richness Ecosystem functioning Type 3

Strong negative selection effects can even lead to negative effects of biodiversity on ecosystem functioning Species richness Ecosystem functioning

A simple simulation study to illustrate the negative selection effect A regional pool of 20 species A regional pool of 20 species Two ecosystem functions: community biomass and an undefined non-biomass function Two ecosystem functions: community biomass and an undefined non-biomass function For each species, its biomass and contribution to the undefined function are independently and normally distributed For each species, its biomass and contribution to the undefined function are independently and normally distributed Better competitors, which attain greater biomass, always exclude worse competitors Better competitors, which attain greater biomass, always exclude worse competitors No complementarity effects No complementarity effects Ten different species compositions at each diversity level (2, 6, 10, 14 and 18 species) were randomly drawn from the species pool Ten different species compositions at each diversity level (2, 6, 10, 14 and 18 species) were randomly drawn from the species pool 100 simulation experiments 100 simulation experiments

A positive BEF relation for community biomass vs. diverse BEF relations for the non-biomass function

Three new types of BEF relations Type 1 Type 2 Type 3 Species richness Ecosystem functioning Jiang et al., Oikos, in press

Bacterial diversity experiment: negative selection effects Two-way factorial design: Two-way factorial design: Bacterial richness: 1, 2, 3, 4 species from a four-species pool containing Bacillus cereus (Bc), Bacillus pumilus (Bp), Frigoribacterium sp. (F), and Serratia marcescens (Sm) Bacterial richness: 1, 2, 3, 4 species from a four-species pool containing Bacillus cereus (Bc), Bacillus pumilus (Bp), Frigoribacterium sp. (F), and Serratia marcescens (Sm) The presence/absence of a bacterivorous ciliate: Tetrahymena pyriformis The presence/absence of a bacterivorous ciliate: Tetrahymena pyriformis Ecosystem properties: Ecosystem properties: Total bacterial biomass Total bacterial biomass Decomposition of particulate organic matter (wheat seeds) Decomposition of particulate organic matter (wheat seeds) Consumer (Tetrahymena) abundance Consumer (Tetrahymena) abundance

Experimental Timeline Week1Week2Week3 Week 4-6 Week7 Microcosm setup Bacterial inoculation Consumer inoculation Wheat seed introduction Sampling

Four Bacterial Species Frigoribacterium sp.Serratia marcescens Bacillus pumilusBacillus cereus

Tetrahymena pyriformis

Total bacterial biovolume increased with diversity due largely to positive selection effects Jiang, Ecology, 2007

Testing the mechanisms ( Testing the mechanisms (Loreau 1998) O T : the total yield of a polyculture max(Mi) : the maximum monoculture yield of the species in the mixture D max > 0: the complementarity effect present D max = 0: the positive selection effect present D max < 0: the negative selection effect present

Bootstrapped 95% confidence intervals (CI) of Dmax Jiang, Ecology, 2007

No bacterial diversity effect on decomposition due to negative selection effects Jiang, Ecology, 2007

Bootstrapped 95% confidence intervals (CI) of Dmax Jiang, Ecology, 2007

No bacterial diversity effect on consumer abundance due to negative selection effects Jiang, Ecology, 2007

Bootstrapped 95% confidence intervals (CI) of Dmax Jiang, Ecology, 2007

Abundant evidence suggests that increasing prey diversity tends to reduce predator abundance The negative selection effect: diverse communities are more likely to contain unpalatable or inedible prey, which can become dominant in the presence of predators. Ideas in different fields: the resource concentration hypothesis in agricultural pest control (Andow 1991). the variance in edibility hypothesis in community ecology (Duffy et al. 2007) the dilution effect in disease ecology (Keesing et al. 2006)

Existing decomposer diversity- decomposition experiments Jiang et al., Oikos, in press

Summary The negative selection effect may contribute significantly to the BEF relationship. The negative selection effect may contribute significantly to the BEF relationship. The positive BEF relationship for aggregate community biomass may not be generalized to other ecosystem functions. The positive BEF relationship for aggregate community biomass may not be generalized to other ecosystem functions. Positive BEF relations should be uncommon when examining ecosystem functions for which species competitive ability is not a reliable indicator of its functional impact. Positive BEF relations should be uncommon when examining ecosystem functions for which species competitive ability is not a reliable indicator of its functional impact. Future BEF experiments should pay more attention to ecosystem functions other than biomass. Future BEF experiments should pay more attention to ecosystem functions other than biomass.

Biodiversity and stability Multiple concepts of stability (Pimm 1984, 1991) Multiple concepts of stability (Pimm 1984, 1991) Temporal stability: the reciprocal of temporal variability (i.e., how much a variable fluctuates over time) Temporal stability: the reciprocal of temporal variability (i.e., how much a variable fluctuates over time) Resistance Resistance Resilience Resilience Persistence Persistence Stability can be measured at both population and community levels. Stability can be measured at both population and community levels.

Biodiversity and stability: ideas and theories Early conceptual ideas that increasing biodiversity tends to increase stability Early conceptual ideas that increasing biodiversity tends to increase stability MacArthur (1955), Elton (1958), Odum (1959), Margalef (1969) Theoretical predictions that increasing biodiversity tends to reduce population stability May (1973), Lehman and Tilman (2000) Theoretical predictions that increasing biodiversity tends to increase community stability (e.g., stability of total community biomass) Tilman (1999), Ives and Hughes (2002)

Biodiversity and stability: empirical findings Common positive diversity-stability relationships at the community level Common positive diversity-stability relationships at the community level McNaughton 1977, Dodd et al. 1994, McGrady-Steed et al. 1997, McGrady-Steed and Morin 2000, Valone and Hoffman 2003a, Caldeira et al. 2005, Steiner 2005, Steiner et al. 2005a, b, Romanuk et al. 2006, Tilman et al. 2006, Vogt et al. 2006, Zhang and Zhang 2006 McNaughton 1977, Dodd et al. 1994, McGrady-Steed et al. 1997, McGrady-Steed and Morin 2000, Valone and Hoffman 2003a, Caldeira et al. 2005, Steiner 2005, Steiner et al. 2005a, b, Romanuk et al. 2006, Tilman et al. 2006, Vogt et al. 2006, Zhang and Zhang 2006 Various diversity-stability relationships at the population level Various diversity-stability relationships at the population level Positive: Romanuk and Kolasa 2004, Kolasa and Li 2003, Valone and Hoffman 2003b, Romanuk et al. 2006, Vogt et al Positive: Romanuk and Kolasa 2004, Kolasa and Li 2003, Valone and Hoffman 2003b, Romanuk et al. 2006, Vogt et al Neutral: McGrady-Steed and Morin 2000, Romanuk and Kolasa 2002, Steiner et al. 2005a Neutral: McGrady-Steed and Morin 2000, Romanuk and Kolasa 2002, Steiner et al. 2005a Negative: Gonzalez and Descampus-Julien 2004, Tilman et al Negative: Gonzalez and Descampus-Julien 2004, Tilman et al

Does predation affect the relationship between biodiversity and stability? Positive and neutral effects of biodiversity on population stability are typical for experiments conducted in systems involving multiple trophic levels Positive and neutral effects of biodiversity on population stability are typical for experiments conducted in systems involving multiple trophic levels Hypothesis: Increasing diversity may promote population stability in the presence of predators via the weak interaction effect. Hypothesis: Increasing diversity may promote population stability in the presence of predators via the weak interaction effect. McCann et al. (1998): large oscillations of strong-interacting predator-prey populations may be damped when additional prey species that interact weakly with predators are present. McCann et al. (1998): large oscillations of strong-interacting predator-prey populations may be damped when additional prey species that interact weakly with predators are present.

A microcosm experiment Two-way factorial design: Two-way factorial design: The presence/absence of a predatory ciliate: Lacrymaria sp. The presence/absence of a predatory ciliate: Lacrymaria sp. A prey diversity gradient (1, 2, 3 species) with three bacterivorous ciliates: Colpidium striatum (C), Halteria sp. (H), and Tetrahymena pyriformis (T). A prey diversity gradient (1, 2, 3 species) with three bacterivorous ciliates: Colpidium striatum (C), Halteria sp. (H), and Tetrahymena pyriformis (T). Experimental duration: one month Experimental duration: one month Species abundance data collected every 2-3 days Species abundance data collected every 2-3 days

The strength of predator-prey interactions differs among prey species Low Intermediate High

Predation altered the relationship between diversity and community stability

Predation altered the relationship between biodiversity and population stability

Summary The relationship between biodiversity and stability is context-dependent. The relationship between biodiversity and stability is context-dependent. In the absence of predators, increasing biodiversity reduced population stability but had little effect on community stability. In the absence of predators, increasing biodiversity reduced population stability but had little effect on community stability. In the presence of predators, weak predator-prey interactions helped stabilize population and community dynamics in more diverse communities. In the presence of predators, weak predator-prey interactions helped stabilize population and community dynamics in more diverse communities.

The take-home message Type 1 Type 2 Type 3 Species richness Ecosystem function (stability included)

Acknowledgments Georgia Institute of Technology Georgia Institute of Technology National Science Foundation National Science Foundation Shivani Patel, Hena Joshi Shivani Patel, Hena Joshi