biodiversity and ecosystem functioning: looking back and moving forward

Biodiversity and Ecosystem Biodiversity and Ecosystem Functioning: Looking Back Functioning: Looking Back

and Moving Forwardand Moving Forward

Jiang, LinJiang, Lin

School of BiologySchool of Biology

Georgia Institute of TechnologyGeorgia Institute of Technology

Email: Email: [email protected]@biology.gatech.edu

Outline Outline Current knowledge on biodiversity and ecosystem Current knowledge on biodiversity and ecosystem

functioning (BEF)functioning (BEF) Mechanisms: niche complementarity and positive Mechanisms: niche complementarity and positive

selection effectsselection effects Problems associated with current BEF studiesProblems associated with current BEF studies

An important mechanism that has received relatively An important mechanism that has received relatively little attention: the little attention: the negative selection effectnegative selection effect

Hypothesis: multiple forms of BEF relationships.Hypothesis: multiple forms of BEF relationships. My own experimental dataMy own experimental data Literature survey Literature survey

Biodiversity and stability:Biodiversity and stability: Question: Does predation alter the relationship Question: Does predation alter the relationship

between biodiversity and stability?between biodiversity and stability?

Species extinction: past, Species extinction: past, current, and future trendscurrent, and future trends

DefinitionsDefinitions

Biodiversity: genetic, taxonomic, or Biodiversity: genetic, taxonomic, or functional diversity. functional diversity. Species richness: the number of species.Species richness: the number of species.

Ecosystem functioning: stocks of energy Ecosystem functioning: stocks of energy and materials, fluxes of energy or material and materials, fluxes of energy or material processing, and stability of stocks or rates processing, and stability of stocks or rates over timeover time Biomass, decomposition, the ability to support Biomass, decomposition, the ability to support

consumer populations, temporal stability of consumer populations, temporal stability of biomass. biomass.

Type 1

Species richness

Eco

syst

em

fu

nct

ion

ing

Vitousek and Hooper 1993

Hypothetical relationships Hypothetical relationships between biodiversity and between biodiversity and

ecosystem functioningecosystem functioning



Type 1

Type 2

Species richness

Eco

syst

em

fu

nct

ion

ing




Type 1

Type 2

Type 3

Species richness

Eco

syst

em

fu

nct

ion

ing


Cedar Creek Cedar Creek ExperimentExperiment

Tilman et al. 2001

BIODEPTH BIODEPTH ExperimentExperiment

Hector et al. 1999

The commonly observed The commonly observed relationship between biodiversity relationship between biodiversity

and ecosystem functioningand ecosystem functioning

Type 2

Species richness

Eco

syst

em

fu

nct

ion

ing

Mechanisms for the Mechanisms for the positive BEF relationshippositive BEF relationship

Niche Niche ComplementarityComplementarity Niche Niche

differentiation differentiation among species among species allows diverse allows diverse communities to communities to utilize available utilize available resources more resources more completely (Tilman completely (Tilman et al. 1997) et al. 1997)

Low diversity High diversity

No niche overlap

Mechanisms for the Mechanisms for the positive BEF relationshippositive BEF relationship

The positive selection The positive selection (or sampling) effect(or sampling) effect Positive correlation Positive correlation

between species between species competitive ability and its competitive ability and its contribution to ecosystem contribution to ecosystem functioning.functioning.

Increasing diversity Increasing diversity increases the probability increases the probability that communities are that communities are dominated by dominated by functionally important functionally important species (Aarssen 1997, species (Aarssen 1997, Huston 1997, Tilman et Huston 1997, Tilman et al. 1997)al. 1997)


Competitively dominant

The positive selection effect appears to The positive selection effect appears to be the primary mechanism behind be the primary mechanism behind

positive relations between biodiversity positive relations between biodiversity and community biomass (Cardinale et and community biomass (Cardinale et

al. 2006) al. 2006)

Problems with current BEF Problems with current BEF experimentsexperiments

Most BEF experiments are short-term.Most BEF experiments are short-term. Last less than one generation of Last less than one generation of

experimental organisms.experimental organisms.

Most BEF experiments focus on Most BEF experiments focus on biomass production.biomass production. Patterns on biomass production may Patterns on biomass production may

not be generalized to other not be generalized to other ecosystem variables.ecosystem variables.

The negative selection The negative selection effecteffect

No positive correlation No positive correlation between species between species competitive ability and competitive ability and its contribution to its contribution to ecosystem functioning. ecosystem functioning.

Increasing diversity Increasing diversity increases the increases the probability that probability that communities are communities are dominated by dominated by functionally functionally insignificant species. insignificant species.


Competitively dominant

Strong negative selection effects Strong negative selection effects can lead to no effects of can lead to no effects of

biodiversity on ecosystem biodiversity on ecosystem functioningfunctioning

Species richness

Eco

syst

em

fu

nct

ion

ing

Type 3

Strong negative selection effects Strong negative selection effects can even lead to negative effects of can even lead to negative effects of

biodiversity on ecosystem biodiversity on ecosystem functioningfunctioning

Species richness

Eco

syst

em

fu

nct

ion

ing

A simple simulation study A simple simulation study to illustrate the negative to illustrate the negative

selection effectselection effect A regional pool of 20 speciesA regional pool of 20 species Two ecosystem functions: community biomass and Two ecosystem functions: community biomass and

an undefined non-biomass functionan undefined non-biomass function For each species, its biomass and contribution to For each species, its biomass and contribution to

the undefined function are independently and the undefined function are independently and normally distributednormally distributed

Better competitors, which attain greater biomass, Better competitors, which attain greater biomass, always exclude worse competitorsalways exclude worse competitors No complementarity effects No complementarity effects

Ten different species compositions at each Ten different species compositions at each diversity level (2, 6, 10, 14 and 18 species) were diversity level (2, 6, 10, 14 and 18 species) were randomly drawn from the species poolrandomly drawn from the species pool

100 simulation experiments100 simulation experiments

A positive BEF relation for community A positive BEF relation for community biomass vs. diverse BEF relations for biomass vs. diverse BEF relations for

the non-biomass functionthe non-biomass function

negative neutral positive

Perc

enta

ge

0

20

40

60

80

100 biomass non-biomass function

Three new types of BEF Three new types of BEF relationsrelations

Type 1

Type 2

Type 3

Species richness

Eco

syst

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ing

Jiang et al., Oikos, in press

Bacterial diversity Bacterial diversity experiment: negative experiment: negative

selection effectsselection effects Two-way factorial design:Two-way factorial design:

Bacterial richness: 1, 2, 3, 4 species from a four-Bacterial richness: 1, 2, 3, 4 species from a four-species pool containing species pool containing Bacillus cereus Bacillus cereus (Bc),(Bc), Bacillus pumilus Bacillus pumilus (Bp), (Bp), Frigoribacterium Frigoribacterium sp. (F), sp. (F), and and Serratia marcescens Serratia marcescens (Sm) (Sm)

The presence/absence of a bacterivorous ciliate: The presence/absence of a bacterivorous ciliate: Tetrahymena pyriformisTetrahymena pyriformis

Ecosystem properties: Ecosystem properties: Total bacterial biomassTotal bacterial biomass Decomposition of particulate organic matter Decomposition of particulate organic matter

(wheat seeds)(wheat seeds) Consumer (Consumer (TetrahymenaTetrahymena) abundance) abundance

Experimental TimelineExperimental Timeline

Week1 Week2 Week3Week4-6 Week7

Microcosmsetup

Bacterialinoculation

Consumerinoculation

Wheat seedintroduction

Sampling

Four Bacterial Four Bacterial SpeciesSpeciesFrigoribacterium sp. Serratia marcescens

Bacillus pumilus Bacillus cereus

Tetrahymena pyriformisTetrahymena pyriformis

Total bacterial biovolume Total bacterial biovolume increased with diversity due increased with diversity due

largely to positive selection effectslargely to positive selection effects

Bacterial richness

1 2 3 4

Tota

l bacte

rial bio

volu

me (

log

10( m

3 /ml))

4

5

6

7

8

9

10

controlpredation

Bacterial composition

4

5

6

7

8

9

10

Jiang, Ecology, 2007

Testing the mechanisms (Testing the mechanisms (Loreau 1998)

)max(

)max(max

i

iT

M

MOD

OT : the total yield of a polyculture max(Mi) : the maximum monoculture yield of the species in the mixture

Dmax > 0: the complementarity effect presentDmax = 0: the positive selection effect presentDmax < 0: the negative selection effect present

Bootstrapped 95% Bootstrapped 95% confidence intervals (CI) of confidence intervals (CI) of

DmaxDmax


No bacterial diversity effect on No bacterial diversity effect on decomposition due to negative decomposition due to negative

selection effectsselection effects

Bacterial richness

1 2 3 4

Fra

ctio

n o

f w

he

at se

ed

lo

ss

0.0

0.1

0.2

0.3

0.4

0.5


0.0

0.1

0.2

0.3

0.4

0.5

controlgrazing



Dmax Dmax


No bacterial diversity effect on No bacterial diversity effect on consumer abundance due to consumer abundance due to

negative selection effectsnegative selection effects

Bacterial richness

1 2 3 4

Co

nsu

me

r p

opu

latio

n b

iovo

lum

e (

log

10(

µm

3 /ml)

)

2

3

4

5


2

3

4

5



Dmax Dmax


Abundant evidence suggests Abundant evidence suggests that increasing prey diversity that increasing prey diversity

tends to reduce predator tends to reduce predator abundanceabundance 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-Existing decomposer diversity-decomposition experimentsdecomposition experiments

Jiang et al., Oikos, in press

SummarySummary The The negative selection effectnegative selection effect may contribute may contribute

significantly to the BEF relationship.significantly to the BEF relationship. The positive BEF relationship for aggregate The positive BEF relationship for aggregate

community biomass may not be generalized community biomass may not be generalized to other ecosystem functions.to other ecosystem functions.

Positive BEF relations should be uncommon Positive BEF relations should be uncommon when examining ecosystem functions for when examining ecosystem functions for which species competitive ability is not a which species competitive ability is not a reliable indicator of its functional impact.reliable indicator of its functional impact.

Future BEF experiments should pay more Future BEF experiments should pay more attention to ecosystem functions other than attention to ecosystem functions other than biomass.biomass.

Biodiversity and stabilityBiodiversity and stability

Multiple concepts of stability (Pimm Multiple concepts of stability (Pimm 1984, 1991)1984, 1991) Temporal stabilityTemporal stability: the reciprocal of : the reciprocal of

temporal variability (i.e., how much a temporal variability (i.e., how much a variable fluctuates over time)variable fluctuates over time)

ResistanceResistance ResilienceResilience PersistencePersistence

Stability can be measured at both Stability can be measured at both population and community levels.population and community levels.

Biodiversity and stability: Biodiversity and stability: ideas and theoriesideas and theories

Early conceptual ideas that increasing Early conceptual ideas that increasing biodiversity tends to increase stabilitybiodiversity 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: Biodiversity and stability: empirical findingsempirical findings

Common positive diversity-stability relationships at Common positive diversity-stability relationships at the community levelthe community level McNaughton 1977, Dodd et al. 1994, McGrady-Steed McNaughton 1977, Dodd et al. 1994, McGrady-Steed

et al. 1997, McGrady-Steed and Morin 2000, Valone et al. 1997, McGrady-Steed and Morin 2000, Valone and Hoffman 2003a, Caldeira et al. 2005, Steiner and Hoffman 2003a, Caldeira et al. 2005, Steiner 2005, Steiner et al. 2005a, b, Romanuk et al. 2006, 2005, Steiner et al. 2005a, b, Romanuk et al. 2006, Tilman et al. 2006, Vogt et al. 2006, Zhang and Zhang Tilman et al. 2006, Vogt et al. 2006, Zhang and Zhang 20062006

Various diversity-stability relationships at the Various diversity-stability relationships at the population levelpopulation level Positive: Romanuk and Kolasa 2004, Kolasa and Li Positive: Romanuk and Kolasa 2004, Kolasa and Li

2003, Valone and Hoffman 2003b, Romanuk et al. 2003, Valone and Hoffman 2003b, Romanuk et al. 2006, Vogt et al. 20062006, Vogt et al. 2006

Neutral: McGrady-Steed and Morin 2000, Romanuk Neutral: McGrady-Steed and Morin 2000, Romanuk and Kolasa 2002, Steiner et al. 2005aand Kolasa 2002, Steiner et al. 2005a

Negative: Gonzalez and Descampus-Julien 2004, Negative: Gonzalez and Descampus-Julien 2004, Tilman et al. 2006Tilman et al. 2006. .

Does predation affect the Does predation affect the relationship between relationship between

biodiversity and stability?biodiversity and stability? Positive and neutral effects of biodiversity on Positive and neutral effects of biodiversity on

population stability are typical for experiments population stability are typical for experiments conducted in systems involving multiple conducted in systems involving multiple trophic levels trophic levels

Hypothesis: Increasing diversity may Hypothesis: Increasing diversity may promote population stability in the promote population stability in the presence of predators via the weak presence of predators via the weak interaction effect.interaction effect. McCann et al. (1998): large oscillations of strong-McCann et al. (1998): large oscillations of strong-

interacting predator-prey populations may be interacting predator-prey populations may be damped when additional prey species that interact damped when additional prey species that interact weakly with predators are present. weakly with predators are present.

A microcosm experimentA microcosm experiment

Two-way factorial design:Two-way factorial design: The presence/absence of a predatory ciliate: The presence/absence of a predatory ciliate:

LacrymariaLacrymaria sp. sp. A prey diversity gradient (1, 2, 3 species) A prey diversity gradient (1, 2, 3 species)

with three bacterivorous ciliates: with three bacterivorous ciliates: Colpidium Colpidium striatum striatum (C), (C), HalteriaHalteria sp. (H), and sp. (H), and Tetrahymena pyriformis Tetrahymena pyriformis (T).(T).

Experimental duration: one monthExperimental duration: one month Species abundance data collected every Species abundance data collected every

2-3 days2-3 days

The strength of predator-prey The strength of predator-prey interactions differs among interactions differs among

prey speciesprey species

Colpidium

Day

0 5 10 15 20 25 30

0

1

2

3

4

5Halteria

Day

0 5 10 15 20 25 30Pop

ulat

ion

dens

ity (

log 1

0(#/

ml+

1))

0

1

2

3

4

5

controlpredation

Tetrahymena

Day

0 5 10 15 20 25 30

0

1

2

3

4

5

Low Intermediate High

Predation altered the relationship Predation altered the relationship between diversity and community between diversity and community

stabilitystability

Species richness

0 1 2 3 4

SD

(lo

g 10(t

otal

com

mun

ity b

iovo

lum

e))

0.0

0.5

1.0

1.5

2.0

R2 = 0.25, P = 0.0173

controlpredation

Predation altered the relationship Predation altered the relationship between biodiversity and between biodiversity and

population stabilitypopulation stabilityColpidium

Species richness

0 1 2 3 40.0

0.2

0.4

0.6

0.8

1.0

R2 = 0.30, P = 0.035

Halteria

Species richness

0 1 2 3 4

SD

(log

10(p

opul

atio

n de

nsity

))

0.0

0.2

0.4

0.6

0.8

1.0

controlpredation

Tetrahymena

Species richness

0 1 2 3 40.0

0.5

1.0

1.5

2.0

R2 = 0.61, P = 0.0005

R2 = 0.35, P = 0.016

SummarySummary

The relationship between biodiversity The relationship between biodiversity and stability is context-dependent.and stability is context-dependent. In the absence of predators, increasing In the absence of predators, increasing

biodiversity reduced population stability biodiversity reduced population stability but had little effect on community stability.but had little effect on community stability.

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

The take-home messageThe take-home message

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(st

ab

ilit

y in

clu

ded

)

AcknowledgmentsAcknowledgments

Georgia Institute of TechnologyGeorgia Institute of Technology National Science FoundationNational Science Foundation Shivani Patel, Hena JoshiShivani Patel, Hena Joshi

biodiversity and ecosystem functioning: looking back and moving forward

Documents

ecosystem functioning

species extinction

number of species

insignificant species

effects of biodiversity

ecosystem variables

species competitive

important species aarssen