Supplementary Table 1. Search terms used to identify studies using the Web of Science
database.
Stressor search terms (all used with and coral*)
Acidification or calcification
Crown of thorns or Acanthaster*
Cyclone* or hurricane* or typhoon*
Disease*
Fishery or fisheries
Irradiance
Nutrient* or eutrophication
Pollution*
Salinity
Sediment* or Turbidity
Sea level
Temperature
Ultraviolet or UV
Appendix S1: Type II error and the two-interval method
Consider the hypothetical data in Supplementary Table 2, below, which we have contrived to
make the conceptual problem associated with the two-interval method as transparent as
possible. Notice that, in every individual study, the combined effect is larger than the additive
effect (the sum of the two treatment effects when imposed separately). Thus, the evidence for
a consistent interactive effect is very strong. However, the confidence intervals on the
respective means for these treatments overlap almost completely, because the variation
among studies in the values is large, relative to the within-study differences between
treatments. Thus, using a confidence interval overlap approach is akin to using an unpaired ttest on these data (in this case yielding P=0.56), when a paired t-test (or, equivalently, a t-test
on the difference between the treatment values) is appropriate (in this case, yielding
P<0.001).
Supplementary Table 2. Table of hypothetical values illustrating the Type II error
associated with using overlapping confidence intervals as indicator of significant
differences.
Study
Additive Effect
Combined Effect
Difference
(Synergy)
1
1
2
1
2
3
5
2
3
5
8
3
4
7
10
3
5
9
10
1
6
11
13
2
7
15
16
1
8
19
20
1
10.5 ± 4.02
1.75 ± 0.61
Mean ± 95% CI
8.75 ± 4.22
Supplementary Table 3. Multiple-stressor studies with photosynthesis as the response variable. N.f.f. = not fully factorial, i.e.,
experiment not designed to detected synergistic effects. P = Gross photosynthesis. R = Gross respiration. [Chl a],[chl c2] = chlorophyll a
and chlorophyll c2 concentrations, respectively. Fv/Fm = Maximum fluorescence yield.
Response variable(s) measured
1
Reference
Stressor 1
Stressor 2
[1]
Irradiance
Acidification
[2]
Irradiance
Nutrients
[3]
[4]
[5]
[6]
[7]
[8]
[9]
[7]
[10]
[11]
Irradiance
Irradiance
Irradiance
Nutrients
Nutrients
Pollution1
Pollution2
Pollution
Pollution3
Pollution4
Sedimentation
UV
Salinity
Acidification
Sedimentation
Irradiance
Irradiance
Irradiance
Salinity
Salinity
Cyanide
Herbicide (DCMU)
3
Copper sulphate
4
Diuron
2
Fv/Fm
Fo/Fm
F/Fm'
[chl a]
[chl c2]
zoox
density
x
x
x
x
x
x
x
x
x
x
R
x
x
x
x
x
x
x
x
x
x
x
x
Other
x
x
x
x
x
x
x
P
x
x
Synergistic
effect(s)
reported
S=Synergistic
A=Antagonistic
N=None
S
N (except for
Ec, Ek)
N
n.f.f.
S
n.f.f.
n.f.f.
S
S
n.f.f.
N,A
n.f.f.
5
6
[12]
[13]
[14]
[15]
[16]
[17]
[18]
[19]
[20]
[21]
[22]
Pollution5
Sedimentation
Sedimentation
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
UV
Salinity
Temperature
Acidification
Acidification
Acidification
Pathogen
Starvation
Starvation
Starvation
Starvation
[23]
Temperature
Flow
[24]
Temperature
Irradiance
[25]
Temperature
Irradiance
x
[26]
[25]
[27]
[28]
[29]
[30]
[31]
[32]
[33]
[34]
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Fluoranthene
However, significant 3-way interaction effect of temperature, flow speed, physical injury on growth rate.
x
x
x
x
x
x
x
x
x
x
S
S
S
N
N
N
S
S
S
S
N
N6
n.f.f.
S. pistillata: S
P. ryukyuensis:
N
S
n.f.f.
S
n.f.f.
A
S
n.f.f.
S
N
n.f.f.
[35]
[36]
[37]
[38]
[39]
[40]
[41]
[42]
[43]
[44]
[45]
[46]
[47]
[48]
[49]
[50]
[51]
[52]
[53]
[5]
[54]
[55]
[56]
[57]
[58]
[59]
[60]
[61]
[62]
[63]
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
S
S
n.f.f.
n.f.f.
?
S
N
N
N
S
n.f.f.
N
A
n.f.f.
n.f.f.
n.f.f.
N,S
n.f.f.
n.f.f.
S
N
S
n.f.f.
n.f.f.
n.f.f.
S
S
S
n.f.f.
S
[64]
[65]
[66]
[67]
[68]
[67]
[69]
[70]
[71]
[72]
[14]
[73]
[74]
[75]
[76]
[77]
[78]
[79]
7
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Temperature
Irradiance
Irradiance
Irradiance
Irradiance
Irradiance
Nutrients
Nutrients
Nutrients
Nutrients
Nutrients
Nutrients
Nutrients7
Salinity
UV
UV
UV
UV
UV
“Nutrients” in this case consisted of live rotifers
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
n.f.f.
N,S
N,S
S
n.f.f.
S
N,S
S
N
A
N
A
A
N
S
S
S
S
Supplementary Table 4. Stressor-stressor interactions and direction of influence (↑ reinforcing, ↓ mitigating, ↔ mixed or no-effect).
Empty rows/columns/rows omitted. The numbers in each cell indicate the number of studies reporting that finding. Empty cells indicate
that we found no studies investigating that particular interaction.
Acidificati
on
CoTS
Fish Biomass/
Abundance
Irradiance
Nutrients
Pathogen
growth and
virulence
Pollution
Salinity
Sedimentation
UV
CoTS
Fishing
2↑
1↔
Irradiance
Nutrients
Pollution
1↑
3↓
1↔
7↓
17↑
1↔
1↔
1↔
2↑
8↑
Sedimentation
1↑
1↔
12↔
2↑
1↔
Salinity
6↑
1↔
17↑
1↑
10↑
5↑1↔
1↑
2↓
Supplementary Table 4 continued.
SLR
CoTS
Fish
Irradiance
Nutrients
Pathogen
growth and
virulence
Pollution
Salinity
Sedimentation
Storms
Temperature
UV
Storms
1↓2↔
1↓
4↑
Temperature
2↔
3↓6↔
18↑2↔
2↑
1↑
22↑1↓1↔
4↑2↔
4↓
1↑
UV
Supplementary Table 5. Summary of multiple-stressor studies as listed in Table 2. Response variable categories correspond to categories
in Figure 2. We only report the existence of interactions for studies that are designed to detect them. Studies may be listed more than
once if they measured variables in a different category and/or reported different results for different measurement variables. Zoox. =
zooxanthellae; NPQ = Non-photochemical quenching; P = Gross photosynthesis; R = Gross respiration; [chl a] = chlorophyll a
concentration; [chl c2] = chlorophyll c2; Pnet= Net photosynthesis; Fv/Fm = Variable fluorescence/Maximal fluorescence, a measure of
Photosystem II efficiency.
Reference
Stressor 1
Stressor 2
Response
Measurement
Organism
Factorial
Significant
Field
Synergistic
(O)
design
interaction
(F)
(S),
Community
or
Antagonistic
(C)
Lab
(A), or
Ecosystem
(L)
additive (+)
(E) Level
[80]
Fishing
Pathogens
Algal cover
% cover
E
N
-
F
-
[81]
Fishing
Pollution
Reef condition
Coral cover,
E
Y
Y
F
S
O
Y
Y
L
S
species richness,
colony size, fish
abundance
[1]
Irradiance
Acidification
Coral bleaching
Change in
luminance
[1]
Irradiance
Acidification
Coral calcification
Buoyant weight
O
Y
Y
L
S8
[1]
Irradiance
Acidification
Zoox.
Pnet
O
Y
Y
L
S
photosynthesis
[82]
Irradiance9
Acidification
Coral calcification
Total alkalinity
O
Y
Y
L
A
[82]
Irradiance
Acidification
Zoox.
Pnet, Pgross,R
O
Y
Y
L
A
photosynthesis
[83]
Irradiance
Acidification
Coral calcification
Buoyant weight
O
Y
N
L
+
[84]
Nutrients
Acidification
Coral calcification
Buoyant weight
O
Y
N
L
+
[85]
Nutrients
Acidification
Coral calcification
Community
C
N
-
F
-
calcification
[6]
Nutrients
Acidification
Coral calcification
Total alkalinity
O
N
-
L
-
[6]
Nutrients
Acidification
Zoox.
Pnet
O
N
-
L
-
Buoyant weight
O
Y
Y
L
A
photosynthesis
[86]
8
9
Nutrients
Acidification
Coral calcification
Species-dependent
In this case, the experimental condition for irradiance was sub-saturating
[87]
Nutrients
Acidification
Pathogenicity
Gene expression
O
N
-
L
-
[88]
Nutrients
Acidification
Pathogen growth
Growth rate
O
Y
Y
L
S
[83]
Nutrients
Acidification
Coral calcification
Buoyant weight
O
Y
N
L
-
[89]
Nutrients
Fishing
Algal cover
% cover
E
Y
Y
F
S
[90]
Nutrients
Fishing
Corallimorph cover
% cover
C
N
-
F
-
[91]
Nutrients
Fishing
Herbivory
Grazing rate
E
N
-
F
-
[92]
Nutrients
Fishing
Sea urchin density
Predation
E
N
-
F
-
[71]
Nutrients
Irradiance
Benthic microalgal
Community
C
N
-
F
-
production
production (P/R)
[93]
Nutrients
Irradiance
Coral calcification
Extension rate
O
N
-
L
-
[83]
Nutrients
Irradiance
Coral calcification
Buoyant weight
O
Y
N
L
+
[20]
Nutrients
Irradiance
Zoox.
P/R
O
Y
Y1
L
A
P/R, zoox density
O
Y
N
L
+
[chl a], colour
O
Y
Y
F/L
A
photosynthesis
[2]
Nutrients
Irradiance
Zoox.
photosynthesis
[94]
Nutrients
Irradiance
Coral pigmentation
brightness
[7]
Pollution
Irradiance
Coral mortality
% mortality
O
N
-
L
-
[7]
Pollution
Irradiance
Zoox.
Zoox. density
O
N
-
L
-
Zoox.
Fv/Fm, zoox
O
Y
Y
L
S
photosynthesis
density
Zoox.
Fv/Fm, [chl a],P
O
Y
n.r.
L
S
photosynthesis
[8]
[5]
Pollution
Salinity
Irradiance
Irradiance
photosynthesis
[95]
Salinity
Nutrients
Coral fertilization
% fertilization
O
Y
Y
L
S
[96]
Salinity
Nutrients
Coral mortality
% mortality
O
Y
Y
L
S
[10]
Salinity
Pollution
Zoox.
P/R
O
Y
Y
L
A
photosynthesis
[97]
Sedimentation
Fishing
Coral/algal cover
% cover
E
N
-
F
-
[98]
Sedimentation
Fishing
Coral/algal cover,
% cover
E
N
-
F
-
fish
abundance/diversity
[99]
Sedimentation
Irradiance
Coral mortality
Proportional
O
Y
Y
L
A
P/R
O
Y
N
L
+
hazard (relative
increase in
mortality)
[3]
Sedimentation
Irradiance
Zoox.
photosynthesis
[100]
Sedimentation
Nutrients
Coral cover
% cover
E
N
-
F
-
[101]
Sedimentation
Nutrients
Coral cover
% cover
E
N
-
F
-
[102]
Sedimentation
Nutrients
Zoox.
Fv/Fm
O
N
-
F
-
photosynthesis
[103]
Sedimentation
Nutrients
Coral mortality
% mortality
O
N
-
L
-
[104]
Sedimentation
Nutrients
Coral mortality
Juvenile
E
N
-
F
-
mortality
[105]
Sedimentation
Nutrients
Coral mortality
% cover
E
Y
n.r.
F
+
[95]
Sedimentation
Salinity
Coral fertilization
% fertilization
O
Y
Y
L
S
[106]
Sedimentation
Salinity
Growth rate
Radial growth
O
N
-
F
-
rate
[107]
Sedimentation
Salinity
Coral cover
% cover
E
N
-
F
-
[13]
Sedimentation
Salinity
Zoox.
P/R
O
Y
Y
L
S
photosynthesis
[13]
Sedimentation
Salinity
Coral mortality
% mortality
O
Y
Y
L
S
[108]
Sea level rise
Irradiance
Zoox.
P/R
O
N
-
F
-
photosynthesis
[109]
Sea level rise
Salinity
Growth rate
Stratigraphy
E
N
-
F
-
[110]
Storms
CoTS
Coral recovery
% coral cover
E
N
-
F
-
[111]
Storms
CoTS
CoTS larval
Size structure
E
N
-
F
-
recruitment
[112]
Storms
Fishing
Physical damage
Beached corals
E
N
-
F
-
[113]
Storms
Nutrients
Algal cover
% algal cover
E
N
-
F
-
[114]
Storms
Nutrients
Fish abundance
Fish species
E
N
-
F
-
C
N
-
F
-
number
[85]
Temperature
Acidification
Coral calcification
Community
calcification
[115]
Temperature
Acidification
Coral calcification
Buoyant weight
O
Y
N
L
+
[116]
Temperature
Acidification
Coral calcification
Buoyant weight
O
Y
Y
L
S
[117]
Temperature
Acidification
Coral calcification
Buoyant weight
O
Y
Y
L
S
[118]
Temperature
Acidification
Coral calcification
Linear extension,
E
N
-
F
-
density
[119]
Temperature
Acidification
Coral calcification
Buoyant weight
O
Y
N
L
+
[15]
Temperature
Acidification
Coral calcification
Alkalinity
O
Y
N
L
+
O
Y
N10
L
+
O
Y
Y
L
S
anomaly
Buoyant weight
[120]
Temperature
Acidification
Fish aerobic
Resting,
performance
maximum O2
uptake, aerobic
scope
[16]
10
Temperature
Acidification
Nutrient uptake
NH4/PO4/NO3
Interaction term was non-significant for all variables and species except for one (resting O2 uptake for O. cyanosoma)
uptake
[88]
Temperature
Acidification
Pathogenesis
Growth rate
O
Y
Y
L
S
[121]
Temperature
Acidification
Pathogenesis
Viral gene
O
N
-
L
-
O
Y
N11
L
+
O
Y
N
L
+
expression
[15]
[16]
[115]
Temperature
Temperature
Temperature
Acidification
Acidification
Acidification
Zoox.
P,R, Zoox density,
photosynthesis
F/Fm’
Zoox.
Zoox density,
photosynthesis
Fv/Fm
Zoox.
Zoox density
O
Y
N
L
+
photosynthesis
[122]
Temperature
Acidification
Bioerosion
Buoyant weight
O
N
-
L
-
[123]
Temperature
Acidification
Coral fertilization
% fertilization
O
Y
Y
L
S
[124]
Temperature
Acidification
Coral fertilization
% fertilization
O
Y
N
L
-
[124]
Temperature
Acidification
Coral larval
% mortality
O
Y
N
L
-
mortality
11
Interaction terms non-significant except for Pnet in winter
[17]
Temperature
Acidification
Zoox.
Respiration,
photosynthesis
zoox. density
O
Y
N
L
+
[17]
Temperature
Acidification
Coral mortality
% mortality
O
Y
Y
L
S
[125]
Temperature
Pathogens
Zoox.
Zoox density
O
Y
Y
L
S
SOD,ASPX,CAT
O
Y
Y
L
S
Visual
C
N
-
F
-
C
N
-
F
-
E
N
-
F
-
E
N
Y12
F
-
photosynthesis
[43]
Temperature
Irradiance
Antioxidant enzyme
activity
[126]
Temperature
Irradiance
Coral bleaching
assessment
[127]
Temperature
Irradiance
Coral bleaching
Visual
assessment, %
mortality
[128]
Temperature
Irradiance
Coral bleaching
Visual
assessment
[129]
Temperature
Irradiance
Coral bleaching
Visual
assessment
[130]
Temperature
Irradiance
Coral bleaching
Visual
E
N
-
F
-
O
N
-
F
-
O
Y
Y
L
S
assessment
[31]
Temperature
Irradiance
Coral bleaching
Visual
assessment
[39]
Temperature
Irradiance
Coral calcification
Alkalinity
anomaly
[131]
Temperature
Irradiance
Coral calcification
Growth rate
O
N
-
F
-
[99]
Temperature
Irradiance
Coral mortality
Proportional
O
Y
N
L
S
hazard
[132]
Temperature
Irradiance
Coral mortality
% mortality
E
N
-
F
-
[133]
Temperature
Irradiance
Coral disease
BBD prevalence
O
Y
Y
F
A
[133]
Temperature
Irradiance
Coral disease
BBD incidence
O
Y
Y
F
A
[133]
Temperature
Irradiance
Coral disease
BBD lesion size
O
Y
Y
F
S
BBD lesion size
O
Y
N
L
+
progression
[54]
Temperature
Irradiance
Coral disease
progression
[134]
Temperature
Irradiance
BBD lesion size
O
Y12
Y
L
A
Fatty acid
[Polyunsaturated
O
Y
Y
L
S
composition
FA]
Cora disease
progression
[48]
Temperature
Irradiance
[45]
Temperature
Irradiance
[MAA]
[MAA]
O
N
-
F
-
[135]
Temperature
Irradiance
[MAA]
[MAA]
O
N
-
L
-
[40]
Temperature
Irradiance
Zoox.
qP,qN, Fo/Fm
O
Y
Y
L
S
Zoox.
Zoox density, [chl
O
Y
N
L
+
photosynthesis
a], [chl c2]
Zoox.
Fv/Fm,Fo/Fm, [chl
O
Y
Y
L
S
photosynthesis
a], [chl c2],
O
N
-
L
-
photosynthesis
[43]
[44]
Temperature
Temperature
Irradiance
Irradiance
[MAA]
[56]
12
Temperature
Irradiance
Experiment lacked low-temperature, high-light treatment
Zoox.
Fv/Fm, zoox
photosynthesis
density
[57]
Temperature
Irradiance
Zoox.
Fv/F0
O
N
-
L
-
Fv/Fm
O
Y
Y
L
S
Zoox.
F/Fm’, [chl a],
O
N
-
F
-
photosynthesis
zoox density
Zoox.
Fv/Fm
O
Y
n.r.
L
S
Fv/Fm
O
Y
Y
L
S13
Zoox.
Fv/Fm, ETRmax,
O
N
-
L
-
photosynthesis
zoox density, [chl
O
Y14
Y
L
S
photosynthesis
[32]
Temperature
Irradiance
Zoox.
photosynthesis
[24]
[26]
Temperature
Temperature
Irradiance
Irradiance
photosynthesis
[25]
Temperature
Irradiance
Zoox.
photosynthesis
[136]
Temperature
Irradiance
a+c2]
[30]
13
14
Temperature
Irradiance
Zoox.
Fv/Fm, zoox
photosynthesis
density
Species-dependent
Differences in irradiance were due to host pigments, not experimental treatment
[63]
Temperature
Irradiance
Zoox.
Fv/Fm
O
Y
Y
F/L
S
Zoox.
Fv/Fm, [chl a],
O
Y
Y
L
S
photosynthesis
zoox density
Zoox.
[chl a], [chl c2],
O
Y
Y
L
S
photosynthesis
other pigments,
E
N
-
F
-
O
Y
Y
L
S
photosynthesis
[59]
[61]
Temperature
Temperature
Irradiance
Irradiance
zoox density
[28]
[66]
[31]
Temperature
Temperature
Temperature
Irradiance
Irradiance
Irradiance
Zoox.
[chl a], zoox
photosynthesis
density
Zoox.
Fv/Fm, ETRmax, [chl
photosynthesis
a+c2]
Zoox.
Zoox density
O
N
-
F
-
Zoox.
Fv/Fm, Zoox
O
Y
Y
F
A
photosynthesis
density, [chl a]
Zoox.
Fv/Fm, Zoox
O
Y
Y
L
S
photosynthesis
[29]
[55]
Temperature
Temperature
Irradiance
Irradiance
[39]
[54]
Temperature
Temperature
Irradiance
Irradiance
photosynthesis
density, [chl a]
Zoox.
Zoox density, net
photosynthesis
P
Zoox.
O
Y
n.r.
L
?
Fv/Fm
O
Y
N
L
+
Zoox density
O
N
-
F
-
Zoox.
Fv/Fm, [chl a],
O
N
-
L
-
photosynthesis
ETRmax
Zoox.
Fv/Fm
O
N
-
L
-
Fv/Fm
O
Y
Y
L
S
NPQ
O
Y
Y
L
S
Fv/Fm, [chl a]
O
Y
n.r.
L
S
photosynthesis
[45]
Temperature
Irradiance
Zoox.
photosynthesis
[135]
[34]
Temperature
Temperature
Irradiance
Irradiance
photosynthesis
[36]
Temperature
Irradiance
Zoox.
photosynthesis
[36]
Temperature
Irradiance
Zoox.
photosynthesis
[51]
Temperature
Irradiance
Zoox.
photosynthesis
[60]
Temperature
Irradiance
Zoox.
Fv/Fm
O
Y
Y
L
S
Fv/Fm, [chl a]
O
Y
Y
L
S15
Pmax, R
O
Y
Y
L
S11
Zoox.
Fv/Fm, Zoox
O
Y
N
F/L
+
photosynthesis
density, [chl a]
Zoox.
NPQ
O
Y
N
F/L
+
Fv/Fm
O
Y
Y
L
A
Fv/Fm, [chl a]
O
Y
n.r.
L
S
photosynthesis
[65]
Temperature
Irradiance
Zoox.
photosynthesis
[65]
Temperature
Irradiance
Zoox.
photosynthesis
[42]
[42]
Temperature
Temperature
Irradiance
Irradiance
photosynthesis
[47]
Temperature
Irradiance
Zoox.
photosynthesis
[5]
Temperature
Irradiance
Zoox.
photosynthesis
15
Responses were species-specific
[137]
Temperature
Irradiance16
Zoox.
Fv/Fm
O
N
-
F/L
-
[chl a]
O
N
-
F/L
-
Photosynthesis
[137]
Temperature
Irradiance
Zoox.
Photosynthesis
[138]
Temperature
Irradiance
Symbiont clade
Symbiont clade
E
N
n/a
F
-
[33]
Temperature
Irradiance
Coral mortality
% mortality
O
Y
N
L
-
[33]
Temperature
Irradiance
Coral Bleaching
Visual
O
Y
N
L
-
Fv/Fm
O
Y
Y
L
S
Fv/Fm
O
N
-
L
-
Visual
E
N
-
F
-
O
N
-
L
-
assessment
[33]
Temperature
Irradiance
Zoox.
photosynthesis
[68]
Temperature
Irradiance
Zoox.
photosynthesis
[139]
Temperature
Nutrients
Coral bleaching
assessment
[140]
16
Temperature
Nutrients
Coral bleaching
Zoox. expulsion
Experiment was to determine effect of irradiance history (acclimatisation) on bleaching susceptibility
[141]
Temperature
Nutrients
Coral bleaching
Visual
E
N
-
F
-
C
N
-
F
-
assessment
[85]
Temperature
Nutrients
Coral calcification
Community
calcification
[72]
Temperature
Nutrients
Coral calcification
Total alkalinity
O
Y
Y
L
A
[14]
Temperature
Nutrients
Coral calcification
Buoyant weight
O
Y
N17
L
-
[142]
Temperature
Nutrients
Coral calcification
Linear extension
O
N
-
F
-
rate
[14]
Temperature
Nutrients
Coral mortality
% Mortality
O
Y
N
L
-
[143]
Temperature
Nutrients
Coral disease
Black band
E
N
-
F
-
prevalence,
incidence
17
[143]
Temperature
Nutrients
Coral disease
Mortality
E
N
-
F
-
[69]
Temperature
Nutrients
Zoox.
Zoox density, [chl
O
Y
N
L
+
photosynthesis
a], [chl c], R
Confounded with sedimentation effects
[69]
Temperature
Nutrients
Zoox.
Pg,
O
Y
Y
L
S
Fv/Fm
O
Y
N
L
+
Zoox.
[chl a], zoox
O
Y
Y
L
A
photosynthesis
density
Zoox.
Zoox. density,
O
Y
Y
L
A
photosynthesis
[chl], NPQ
Zoox.
Fv/Fm
O
Y
N
L
-
Fv/Fm
O
Y
Y
L
S
Coral larvae
%
O
Y
Y
L
S
metamorphosis
metamorphosis
Zoox.
Fv/Fm
O
Y
Y
L
S
photosynthesis
[22]
Temperature
Nutrients18
Zoox.
photosynthesis
[22]
[72]
[14]
Temperature
Temperature
Temperature
Nutrients13
Nutrients
Nutrients
photosynthesis
[67]
Temperature
Nutrients
Zoox.
photosynthesis
[144]
[145]
18
Temperature
Temperature
Pollution
Pollution
“Nutrients” in this case consisted of feeding of Artemia salina nauplii
photosynthesis
[145]
Temperature
Pollution
Zoox.
F/Fm’
O
Y
N
L
+
Visual
E
N
-
F
-
O
N
-
F/L
-
Fv/Fm, [chl a]
O
Y
Y
L
S
Visual
E
N
-
F
-
O
Y
N
L
+
O
Y
Y
L
S
photosynthesis
[146]
Temperature
Salinity
Coral bleaching
assessment
[147]
Temperature
Salinity
Coral bleaching
Visual
assessment
[5]
Temperature
Salinity
Zoox.
photosynthesis
[148]
Temperature
Sedimentation
Coral bleaching
assessment of
bleaching
prevalence
[99]
Temperature
Sedimentation
Coral mortality
Proportional
hazard
[14]
Temperature
Sedimentation
Zoox.
Fv/Fm
photosynthesis
[149]
Temperature
Storms
Coral disease
Disease
C
N
-
F
-
O
Y
N
L
+
O
Y
Y
L
S
[chl a]
O
Y
Y
L
S
Zoox.
[chl a], zoox
O
N
-
-
-
photosynthesis
density
Productivity
Biomass
C
N
-
F
-
O
Y
n.r.
F/L
A
O
Y
Y
L
S
prevalence
[43]
[150]
Temperature
UV radiation
UV
Acidification
Zoox.
Zoox density, [chl
photosynthesis
a], [chl c2]
Coral calcification
Alkalinity
anomaly
[150]
UV radiation
Acidification
Zoox.
photosynthesis
[4]
[151]
UV radiation
UV radiation
Irradiance
Irradiance
productivity
[152]
UV radiation
Pathogen load
Coral bleaching
Visual
assessment
[12]
UV radiation
Pollution
Coral mortality
LC50
[12]
UV radiation
Pollution
Zoox.
F/Fm’
O
Y
Y
L
S
Symbiodinium
O
N
-
L
-
O
Y
Y
L
S
photosynthesis
[153]
UV radiation
Temperature
Growth rate
growth rate
[154]
UV radiation
Temperature
Coral mortality
Time to 50%
survival
[76]
UV radiation
Temperature
Coral mortality
Mortality
O
Y
Y
L
S
[155]
UV radiation
Temperature
Coral bleaching
Visual
E
N
-
F
-
Fv/Fm, [chl a]
O
Y
Y19
L
A
Zoox density
O
Y
Y
L
S
Pmax
O
N
-
L
-
assessment
[77]
UV radiation
Temperature
Zoox.
photosynthesis
[76]
UV radiation
Temperature
Zoox.
photosynthesis
[156]
UV radiation
Temperature
Zoox.
photosynthesis
19
Significant decreases occurred for all but one species.
[157]
[78]
UV radiation
UV radiation
Temperature
Temperature
Zoox.
Zoox density, [chl
O
Y
N
F
+
photosynthesis
a]
Zoox.
Fv/Fm, P:R
O
Y
n.r.
L
S20
Zoox density
O
Y
n.r.
L
S15
Fv/Fm, [chl a]
O
Y
n.r.
L
S
Zoox.
Zoox density, [chl
O
Y
N
L
+
photosynthesis
a], [chl c2]
E
N
Y21
F
-
C
N
Y22
F
-
photosynthesis
[78]
UV radiation
Temperature
Zoox.
photosynthesis
[79]
UV radiation
Temperature
Zoox.
photosynthesis
[75]
UV radiation
Temperature
Non-factorial design studies
[158]
Sedimentation
Fishing
Coral disease
Disease
prevalence
[159]
20
Temperature
Sedimentation
Coral cover
% cover
Responses were species-specific
Use of boosted regression tree analysis allowed detection of interaction effects without having a fully factorial experimental design
22
Although not strictly factorial, the range of conditions between study sites provided evidence for a synergistic effect
21
[160]
Temperature
Irradiance23
Coral bleaching
Visual
E
N
Y24
F
-
E
N
Y25
F
-
assessment
[161]
Temperature
Irradiance
Coral bleaching
Visual
assessment
1.
2.
3.
4.
5.
6.
7.
8.
9.
23
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Supplementary Table 6. Meta-regression of effect size for all photosynthetic response
variables from multiple-stressor studies that examined both temperature and irradiance
as stressors (n=26). A non-significant p-value means that a variable does not explain a
statistically significant amount of variation in effect size between studies.
Predictor
Estimate ± 95% CI
p-value
Intercept
-2.18 ± 9.78
0.66
Genus
0.113 ± 0.141
0.55
Region
-0.149 ± 1.01
0.77
Dependent variable
1.40 ± 4.21
0.18
Size of temperature treatment
-0.974 ± 1.26
0.13
Size of irradiance treatment
-0.0010 ± 0.0035
0.56
Supplementary Figure 1. Funnel plot of the light-temperature interaction term from
studies with Fv/Fm, zooxanthellae density, or [chlorophyll a] as the response variable.
Visually, the funnel plot appears to be slightly asymmetric in favour of studies reporting
synergistic effects (larger positive values), but a linear regression test of asymmetry 26
was not statistically significant (p>0.05, d.f.=24), indicating no apparent publication
bias. Also, there is no apparent hollowness to the plot (i.e., there is not a dearth of
published studies with effect sizes near zero), indicating no tendency for underreporting
where there is no significant synergistic effect. The preponderance of points on the left
side of the plot with significant effect sizes also indicates that evidence in the literature is
accumulating towards synergistic effects (at least where photosynthesis is concerned),
although the random effect model shows that this evidence is not statistically
distinguishable from a simple additive effect. The vertical dotted line represents the
mean effect size for a random effect model. The solid, dashed, and dotted curved lines
represent significant effects at the 0.01, 0.05, and 0.1 levels, respectively. Studies that
did not detect a significant interaction effect between stressors fall inside these lines.
Outside of these lines, more positive values represent larger synergistic (reinforcing)
effects and more negative values indicate larger antagonistic (mitigating) interaction
effects.
26
Sterne, J.A.C., et al., Recommendations for examining and interpreting funnel plot asymmetry in
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