Hillebrand et al. 10.1073/pnas.0701918104.

Supporting Information

Files in this Data Supplement:

SI Figure 4
SI Figure 5
SI Figure 6
SI Figure 7
SI Figure 8
SI Figure 9
SI Table 2
SI Table 3
SI Table 4
SI Text




SI Figure 4

Fig. 4. Effects of herbivory or fertilization on producer species richness as a function of ecosystem productivity, biomass effects of herbivory and fertilization, and producer community evenness. Horizontal lines are neutral effect sizes, and thick lines indicate significant regressions (P < 0.05) in the metaanalysis. Symbols represent freshwater (&#9675;), marine (D), and terrestrial (&#9632;) systems.





SI Figure 5

Fig. 5. Effects of herbivory or fertilization on producer species richness as a function of latitude, experiment duration and experiment size. Horizontal lines are neutral effect sizes, and thick lines indicate significant regressions (P < 0.05) in the metaanalysis. Symbols represent freshwater (&#9675;), marine (D), and terrestrial (&#9632;) systems.





SI Figure 6

Fig. 6. Effects of herbivory or fertilization on producer community evenness as a function of ecosystem productivity, biomass effects of herbivory and fertilization, and producer species richness. Horizontal lines are neutral effect sizes, and thick lines indicate significant regressions (P < 0.05) in the metaanalysis. Symbols represent freshwater (&#9675;), marine (D), and terrestrial (&#9632;) systems.





SI Figure 7

Fig. 7. Effects of herbivory or fertilization on producer community evenness as a function of latitude, experiment duration and experiment size. Horizontal lines are neutral effect sizes, and thick lines indicate significant regressions (P < 0.05) in the metaanalysis. Symbols represent freshwater (&#9675;), marine (D), and terrestrial (&#9632;) systems.





SI Figure 8

Fig. 8. Interaction effect sizes of herbivory and fertilization on producer community evenness and producer species richness as a function of ecosystem productivity, biomass effects of herbivory and fertilization, and producer community richness or evenness. Horizontal lines are neutral effect sizes, and thick lines indicate significant regressions (P < 0.05) in the metaanalysis. Symbols represent freshwater (&#9675;), marine (D), and terrestrial (&#9632;) systems.





SI Figure 9

Fig. 9. Interaction effect sizes of herbivory and fertilization on producer community evenness and producer species richness as a function of latitude, experiment duration and experiment size. Horizontal lines are neutral effect sizes, and thick lines indicate significant regressions (P < 0.05) in the metaanalysis. Symbols represent freshwater (&#9675;), marine (D), and terrestrial (&#9632;) systems.





Table 2. Studies included in metaanalysis with full citation, ecosystem type, the presence of factorial and nonfactorial data on evenness and richness, the study type (laboratory or field), and the number of independent studies obtained from each paper

Author

Year

System

Plant type

Study type

Factorial

No. of indep. exp.

Abe et al.

2001

Freshwater

Periphyton

Lab

No

1

Altesor et al.

2005

Terrestrial

Herb. plants

Field

No

1

Bakker et al.

2003

Terrestrial

Herb. plants

Field

No

1

Bakker et al.

2006

Terrestrial

Herb. plants

Field

No

7

Barry et al.

2004

Terrestrial

Wetland

Field

No

1

Beisner

2001

Freshwater

Phytoplankton

Field

No

3

Belsky

1992

Terrestrial

Herb. plants

Field

No

12

Bothwell

1989

Freshwater

Periphyton

Field

No

2

Bowers

1993

Terrestrial

Herb. plants

Field

No

1

Brenchley & Warington

1958

Terrestrial

Herb. plants

Field

No

1

Brown & Gange

1989

Terrestrial

Herb. plants

Field

No

1

Buckland & Grime

2000

Terrestrial

Herb. plants

Field

No

1

Buschmann et al.

2005

Terrestrial

Herb. plants

Field

No

1

Carpenter

1981

Marine

Periphyton

Field

No

1

Chalmers et al.

2005

Terrestrial

Herb. plants

Field

No

1

Collins et al.

1998

Terrestrial

Herb. plants

Field

No

2

de Bello et al.

2006

Terrestrial

Herb. plants

Field

No

5

DeNicola et al.

1990

Freshwater

Periphyton

Lab

No

2

Eskelinen & Virtanen

2005

Terrestrial

Herb. plants

Field

No

4

Fahnestock & Detling

1999

Terrestrial

Herb. plants

Field

No

2

Ford & Grace

1998

Terrestrial

Wetland

Field

No

6

Giroux & Bedard

1987

Terrestrial

Wetland

Field

No

4

Golubkov & Anokina

1992

Freshwater

Periphyton

Lab

No

1

Gordon et al.

2001

Terrestrial

Tundra

Field

No

1

Gough & Grace

1998

Terrestrial

Wetland

Field

Yes

2

Grellmann

2002

Terrestrial

Tundra

Field

Yes

1

Hagerthey et al.

2002

Marine

Periphyton

Lab

Yes

4

Hanley et al.

1995

Terrestrial

Herb. plants

Lab

No

1

Harison et al.

2003

Terrestrial

Herb. plants

Field

No

2

Hart

2001

Terrestrial

Herb. plants

Field

No

1

Hartley & Jones

2003

Terrestrial

Herb. plants

Field

Yes

1

Hartnett et al.

1996

Terrestrial

Herb. plants

Field

No

4

Hayes & Holl

2003

Terrestrial

Herb. plants

Field

No

1

Heske et al.

1993

Terrestrial

Herb. plants

Field

No

1

Hill & Knight

1987

Freshwater

Periphyton

Field

No

1

Hill & Knight

1988

Freshwater

Periphyton

Field

No

2

Hillebrand

1999

Marine

Periphyton

Field

No

9

Hillebrand

2002

Marine

Periphyton

Field

Yes

4

Hillebrand et al.

2000

Marine

Periphyton

Field

Yes/no

6

Hillebrand et al.

2004

Freshwater

Periphyton

Lab

Yes/no

2

Hillebrand & Kahlert

2001

Freshwater/ Marine

Periphyton

Field

Yes

11

Hixon & Brostoff

1983

Marine

Aquatic macrophytes

Field

No

1

Hixon & Brostoff

1996

Marine

Aquatic macrophytes

Field

No

1

Hobbs et al.

1988

Terrestrial

Herb. plants

Field

No

1

Holomuzki & Hemphill

1996

Freshwater

Periphyton

Field

No

1

Hori et al.

2006

Marine

Aquatic macrophytes

Field

No

1

Howe & Brown

2000

Terrestrial

Herb. plants

Field

No

1

Huchette et al.

2000

Freshwater

Periphyton

Field

No

1

Hunter

1980

Freshwater

Periphyton

Field

No

1

Hunter & Russell-Hunter

1983

Marine

Periphyton

Field

No

1

Huntly

1987

Terrestrial

Herb. plants

Field

No

1

Jacquemyn et al.

2003

Terrestrial

Herb. plants

Field

No

1

Jernakoff & Nielsen

1997

Marine

Epiphytes

Field

No

2

Karjalainen et al.

1998

Freshwater

Phytoplankton

Lab

Yes

1

Kehde & Wilhm

1972

Freshwater

Periphyton

Lab

No

1

Kirkham et al.

1996

Terrestrial

Herb. plants

Field

No

1

Lamberti & Resh

1983

Freshwater

Periphyton

Field

No

1

Lavrentyev et al.

1995

Freshwater

Phytoplankton

Field

No

1

Liess

2006

Freshwater

Periphyton

Lab

Yes

1

Lowe & Hunter

1988

Freshwater

Periphyton

Field

No

1

Manier & Hobbs

2006

Terrestrial

Shrubs

Field

No

1

Marcus

1980

Freshwater

Periphyton

Field

No

1

Marks & Lowe

1989

Freshwater

Periphyton

Field

Yes

1

McClatchie et al.

1982

Marine

Periphyton

Field

No

1

McCormick & Stevenson

1989

Freshwater

Periphyton

Field

Yes

1

McIntire & Hik

2005

Terrestrial

Herb. plants

Field

No

3

McIntryre et al.

2003

Terrestrial

Herb. plants

Field

No

1

McNaughton

1983

Terrestrial

Herb. plants

Field

No

4

Miller et al.

1992

Freshwater

Periphyton

Field

No

1

Moss et al.

2003

Freshwater

Phytoplankton

Lab

Yes

3

Mulholland et al.

1991

Freshwater

Periphyton

Lab

Yes

1

Munoz et al.

2000

Freshwater

Periphyton

Lab

No

1

Nicotri

1977

Marine

Periphyton

Field

No

1

Nielsen

2003

Marine

Aquatic macrophytes

Field

Yes

1

Nilsson et al.

2002

Terrestrial

Herb. plants

Field

No

1

Nomura & Kikuzawa

2005

Terrestrial

Trees

Field

No

3

Noy-Meir

1995

Terrestrial

Shrubs

Field

No

2

Olofsson et al.

2002

Terrestrial

Tundra

Field

No

2

Opsahl et al.

2003

Freshwater

Periphyton

Field

No

2

Osem et al.

2002

Terrestrial

Shrubs

Field

No

4

Ostertag & Verville

2002

Terrestrial

Herb. plants

Field

No

2

Pandey & Singh

1991

Terrestrial

Shrubs

Field

No

1

Pauli et al.

2002

Terrestrial

Herb. plants

Field

No

1

Peterson & Boulton

1999

Freshwater

Periphyton

Field

No

2

Poff & Ward

1995

Freshwater

Periphyton

Field

No

2

Pringle

1990

Freshwater

Periphyton

Field

No

2

Pringle

1996

Freshwater

Periphyton

Field

No

3

Proulx et al.

1996

Freshwater

Phytoplankton

Field

Yes

1

Ranvestel et al.

2004

Freshwater

Periphyton

Field

No

1

Romo & Villena

2005

Freshwater

Phytoplankton

Field

No

3

Royo & Carson

2005

Terrestrial

trees

Field

No

1

Safford & Harrison

2001

Terrestrial

Herb. plants

Field

No

1

Sarnelle

2005

Freshwater

Phytoplankton

Field

No

1

Smith

2003

Marine

Aquatic macrophytes

Field

Yes

1

Smith et al.

1996

Marine

Periphyton

Lab/field

No

3

Sommer

1999

Marine

Periphyton

Lab

No

4

Sommer

2000

Marine

Periphyton

Lab

No

2

Steinman et al.

1989

Freshwater

Periphyton

Lab

Yes

1

Steinman et al.

1990

Freshwater

Periphyton

Lab

Yes

1

Stevenson et al.

1991

Freshwater

Periphyton

Field

No

1

Stohlgren et al.

1999

Terrestrial

Herb. plants

Field

No

9

Suding et al.

2005

Terrestrial

Herb. plants

Field

No

31

Sullivan

1976

Marine

Periphyton

Field

No

1

Sumner & McIntire

1982

Freshwater

Periphyton

Lab

Yes

1

Sundbäck & Snoejs

1991

Marine

Periphyton

Field

No

1

Swamikannu & Hoagland

1989

Freshwater

Periphyton

Field

No

1

Taylor & Grace

1995

Terrestrial

Wetland

Field

No

3

Tilman

1987

Terrestrial

Herb. plants

Field

No

4

Turkington et al.

2002

Terrestrial

Trees

Field

Yes

1

Underwood et al.

1992

Freshwater

Periphyton

Field

No

1

Underwood & Thomas

1990

Freshwater

Periphyton

Lab

No

2

Villanueva et al.

2004

Freshwater

Periphyton

Lab

No

1

Villanueva & Modenutti

2004

Freshwater

Periphyton

Field

No

6

Walker et al.

2003

Terrestrial

Herb. plants

Field

No

1

Waser & Price

1981

Terrestrial

Herb. plants

Field

No

2

Wellnitz et al.

1996

Freshwater

Periphyton

Field

Yes

1

Willems et al.

1993

Terrestrial

Herb. plants

Field

No

1

Worm et al.

2002

Marine

Aquatic macrophytes

Field

Yes/No

2

Yin et al.

2006

Terrestrial

Herb. plants

Field

No

1

Zavaleta et al.

2003

Terrestrial

Herb. plants

Field

No

1

Yin L, Cai Z, Zhong W (2006) Crop Protection 25:910-914.

Zavaleta ES, Shaw MR, Chiariello NR, Thomas BD, Cleland EE, Field CB, Mooney HA (2003) Ecol Monog 73:585-604.





Table 3: Correlation between the integrated productivity index and the log-transformed values for each of the six resource variables

Available N

Total N

Available P

Total P

PAR

Precipitation

r

= 0.5403

r

= 0.6419

r

= 0.6350

r

= 0.7338

r

= 0.4047

r

= 0.6148

N

= 109

N

= 60

N

= 90

N

= 48

N

= 217

N

= 73

P

< 0.001

P

< 0.001

P

< 0.001

P

< 0.001

P

< 0.001

P

< 0.001





Table 4. Spearman rank correlation between the explanatory variables used for metaanalyses or general linear model

Variable

Lat

Prod

Dur

Size

Herb

Fert

Even

S

Lat

-

-0.456

-0.138

-0.438

-0.134

-0.127

-0.076

0.287

Prod

***

-

0.167

0.274

0.102

0.228

0.066

-0.187

Dur

*

**

-

0.878

0.374

0.045

0.068

-0.083

Size

***

***

***

-

0.399

0.229

-0.244

-0.010

Herb

  

***

***

-

0.099

0.103

0.062

Fert

 

*

   

-

-0.147

0.008

Even

   

*

  

-

-0.182

S

***

**

     

-

Above the diagonal, the table gives correlation coefficients, below significance levels (*, P < 0.05; **, P < 0.01; ***, P < 0.001). To enhance clarity, correlation coefficients significant at P < 0.05 are highlighted by italics. Lat, latitude; Prod, productivity; Dur, experiment duration; Herb, herbviore effects on producer biomass; Fert, fertilization effects on producer biomass; Even, producer community evenness; S, producer species richness.





SI Text

Description of Variables Obtained and Calculated from Each Study.

We defined a study as a temporally and spatially distinct experiment with treatments and corresponding controls. Multiple studies could be reported from within one publication if, for instance, the same experimental treatments were performed in multiple independent settings. When multiple measures were reported over time, we used the last temporal sample to avoid phases of transient dynamics. Exceptions were made if some unusual disturbance affected some or all of the treatments or replicates, which occurred for only three studies. In one fertilization study (Hobbs et al. 1988, see SI Table 4), the invasion of gophers destroyed the fertilization setup in the second year, so we took first year data. In a second study (Osem et al. 2002, see SI Table 4), the second to last year was used because the last year was extremely dry and not representative for the period. In one periphyton study (Hunter & Russell-Hunter 1983, see SI Table 4), data were the mean of the last three samplings. We used studies that manipulated the availability of resources or the presence of consumers or both. Almost all studies enriched mineral nutrients; three studies (Steinman et al. 1989, Wellnitz et al. 1996, and Hillebrand et al. 2004, see SI Table 4) manipulated light levels. Almost all studies manipulated herbivore presence directly; only one study used fishes to reduce herbivory by zooplankton (Moss et al. 2003, see SI Table 4).

Each study had a unique study identifier linked to the citation of the publication. We categorized the system as marine, terrestrial, or freshwater. Studies in wetlands and salt-marshes were operationally defined: studies addressing submersed or floating macrophytes or periphyton were classified as aquatic (marine or freshwater), whereas studies on above-water rooted plants were considered terrestrial. For each study site, we noted the latitude from -90 (S) to + 90 (N). We categorized the study type as factorial or nonfactorial. Main effects of herbivory and fertilization on producer richness and evenness did not differ significantly between factorial and nonfactorial experiments [group contrast metaanalysis (hereafter MA) on study type, P > 0.1], allowing us to analyze the different types of experiments and effect sizes together. We recorded three aspects of the temporal and spatial scale of the experiment: the duration of the experiment (days), and the experiment size, both as the replicate area used for fertilization manipulation (fertilization area), and the area over which consumers were manipulated (consumer area). To characterize the community structure of the plants, we also used the control (ungrazed, unfertilized) levels of evenness and ln-transformed species richness for each of the studies. Finally, treatment effects on plant biomass were calculated as ln response ratios of plant biomass to herbivory and fertilization for factorial and nonfactorial experiments in the same way as described in Methods.

We used resource availability as a proxy for ecosystem productivity. Because the studies differed in the resources they reported, it was not possible to use any single resource to characterize ecosystem productivity. Instead, we characterized productivity by calculating an integrated index of resource availability (for similar rationale, see additional refs. 1 and 2). In a first step, we retrieved as many concentrations of relevant resources as possible: We recorded the unmanipulated nutrient levels as available and/or total N as well as P (mmol g-1 for terrestrial and mmol ml-1 for aquatic studies). For terrestrial studies, we obtained a measure of water availability (precipitation in mm per year). We used the latitude and longitude of the experimental site (only field experiments) to obtain measures of ambient photosynthetically active radiation (PAR, W m-2) for all field experiments (URL: http://www.ngdc.noaa.gov/seg/cdroms/ged_iib/datasets/b05/pl.htm; see additional refs. 3 and 4). In a second step, we calculated the database-wide mean for each of the six resource variables (light, water, available P, total P, available N, total N), and expressed each value as a proportion of that mean. Finally, integrated ecosystem productivity was then expressed as the ln-transformed average of all standardized resource values obtained from that study. This aggregated index was strongly linearly correlated to the ln-transformed values for each of the six nutrient variables and thus successfully summarized the productivity of the system (see SI Table 2).

We also distinguished field and lab studies, where lab studies also include outdoor mesocosms or streamside channels or other contained experiments, which lack direct contact with the original environment. The types of consumer manipulation included exclosures, enclosures, removal, gradient, multiple, and none. Exclosures are experiments that restrict herbivore access to plants, enclosures are experiments where stocked herbivores are kept with their forage, and removal experiments exclude herbivores by means other than physical boundaries, e.g., insecticides. A few studies used a natural gradient of herbivore presence/absence, or used a "multiple" setup, representing a combination of the manipulations mentioned above or a split-plot design. Neither the type of consumer manipulation nor the distinction between field and lab studies resulted in any significant difference (metaanalysis, P > 0.05) in average effect sizes. Therefore, we used finally six continuous variables for bivariate metaanalyses (MA) and the general linear model (GLM): latitude, productivity, treatment effects on biomass, producer community evenness or richness, experiment size, and experiment duration. The variables showed very moderate levels of collinearity (see SI Table 3). Only experiment size and duration were strongly correlated (r = 0.878), others moderately (r < 0.5).

1. Hillebrand H (2005) J Ecol 93:758-769.

2. Hillebrand H (2002) J N Am Bentholog Soc 21:349-369.

2. Pinker RT, Laszlo I (1992) J Appl Meteorol 31:194-211.

3. Pinker RT, Laszlo I (1992) J Climate 5:56-65.