Biodiversity and Ecosystem Functioning: Looking Back and Moving Forward

1. Biodiversity and Ecosystem Functioning: Looking Back and Moving Forward Jiang, Lin School of Biology Georgia Institute of Technology Email: lin.jiang@biology.gatech.edu

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

3. Species extinction: past, current, and future trends

4. Definitions • Biodiversity: genetic, taxonomic, or functional diversity. • 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 • Biomass, decomposition, the ability to support consumer populations, temporal stability of biomass.

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

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

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

8. Cedar Creek Experiment Tilman et al. 2001

9. BIODEPTH Experiment Hector et al. 1999

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

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

12. Mechanisms for the positive BEF relationship • The positive selection (or sampling) effect • 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) Competitively dominant Low diversity High diversity

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

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

15. The negative selection effect • 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. Competitively dominant Low diversity High diversity

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

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

18. A simple simulation study to illustrate the negative selection effect • A regional pool of 20 species • 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 • Better competitors, which attain greater biomass, always exclude worse competitors • 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 • 100 simulation experiments

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

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

21. Bacterial diversity experiment: negative selection effects • 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) • The presence/absence of a bacterivorous ciliate: Tetrahymena pyriformis • Ecosystem properties: • Total bacterial biomass • Decomposition of particulate organic matter (wheat seeds) • Consumer (Tetrahymena) abundance

22. Experimental Timeline Microcosm setup Consumer inoculation Sampling Week 4-6 Week1 Week2 Week3 Week7 Bacterial inoculation Wheat seed introduction

23. Four Bacterial Species Frigoribacterium sp. Serratia marcescens Bacillus pumilus Bacillus cereus

24. Tetrahymena pyriformis

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

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

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

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

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

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

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

32. 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)

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

34. Summary • 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. • 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.

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

36. Biodiversity and stability: ideas and theories • 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)

37. Biodiversity and stability: empirical findings • 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 • 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. 2006 • Neutral: McGrady-Steed and Morin 2000, Romanuk and Kolasa 2002, Steiner et al. 2005a • Negative: Gonzalez and Descampus-Julien 2004, Tilman et al. 2006.

38. 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 • 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.

39. A microcosm experiment • Two-way factorial design: • 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). • Experimental duration: one month • Species abundance data collected every 2-3 days

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

41. Predation altered the relationship between diversity and community stability

42. Predation altered the relationship between biodiversity and population stability

43. Summary • 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 presence of predators, weak predator-prey interactions helped stabilize population and community dynamics in more diverse communities.

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

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