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Understanding Nitrogen Transformations and Removal at Oyster Restoration Sites in the
Hudson-Raritan Estuary
Chester B. Zarnoch, Baruch College City University of New York
Michael Hassett, Loyola University Chicago Denise A. Bruesewitz, Colby College Brett F. Branco, Brooklyn College Allison Fitzgerald, New Jersey City U. Wayne Gardner, U. of Texas Ray Grizzle, U. of New Hampshire
Timothy J. Hoellein, Loyola University Chicago
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Eutrophication is a major environmental concern
• Common in estuaries globally (Kennish 2002)
• Coastal ecosystems are typically N-limited (Howarth and Marino 2006)
• Hudson River estuary among highest N load in the world (Howarth et al. 2006)
N load to various estuaries (g N m‐2yr‐1) Hudson River estuary 290 Scheldt River estuary 190 Boston Harbor (pre‐diversion) 130 Ochlockonee Bay 84 N. Gulf of Mexico (“dead zone”) 32 Narragansett Bay 28 Delaware Bay 27 San Francisco Bay 25 Long Island Sound 17 Chesapeake Bay 14 Baltic Sea 3
(Howarth et al. 2006)
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NYC Sewer System
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NYC Sewer System
New York Times
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Impacts of nitrogen loading
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Impacts of nitrogen loading
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Impacts of nitrogen loading
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Impacts of nitrogen loading
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Impacts of nitrogen loading
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Oysters and Water Quality
• Benthic-Pelagic Coupling - Enhance coupled nitrification-denitrification?
N2
Organic N
Seston Biodeposits
NH4+
ammonification
NO3-
nitrification
denitrification
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Rates of Denitrification by Habitat Piehler and Smyth 2011
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Effects of oysters on denitrification are mixed
Kellogg et al. 2013 found higher rates of denitrification on restored oyster reefs
Higgins et al. 2013 found no effect of oysters on denitrification
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Decline of oysters in NY harbor
• Fishery gone by 1920s
– Overfishing
– Habitat loss
• Dredge and fill
• Hydrological modifications
– Pollution
• Eutrophication and oxygen minima (sewage) Oyster companies under Manhattan Bridge
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Gov’t agencies now promote oyster restoration
• Studies on oyster growth,
reproduction, and survival (Levinton et al. 2011, Zarnoch and Schreibman 2012, Levinton et al. 2013, Mass-Fitzgerald 2013)
• Current management plans
include oyster restoration – 500 acres of oyster reefs by
2015 and 5,000 acres by 2050
• Oyster Restoration Research Project to determine feasibility of oyster restoration. – Over 30 partner institutions
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Rebuild by Design “Living Breakwaters”
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Oysters and Water Quality
• Benthic-Pelagic Coupling - Enhance coupled nitrification-denitrification?
N2
Organic N
Seston Biodeposits
NH4+
ammonification
NO3-
nitrification
denitrification
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Research Questions
Overarching question:
What is the influence of oysters on
sediment N cycling in an urban estuary?
Q1: Does the influence of oysters
on N cycling change across a
gradient of N loading?
Q2: Does the influence of oysters
on N cycling change across a
gradient of oyster density?
Management
implications:
At what locations and
densities within an
urban estuary could
oysters most
effectively alleviate N
pollution?
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Jamaica Bay: eutrophic coastal environment in NYC • 4 major WWTP, many CSOs
– 15,800 kg d-1 total N
– 99% of the freshwater to the bay
– 92% N load
• Mean depth 5m
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Phytoplankton Abundance Jamaica Bay 2010-2011
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N2
NH4+
ammonification
NO3-
nitrification
denitrification
Ben
thic
up
take
Microphyto- benthos
and sediment microbes
N-loading
excretion
a
b
c
e
g
Adapted from: Newell 2004
a b c
d
e
g
h
Phytoplankton: TPM, Chl a, C:N
Oyster feeding: filtration, ingestion, absorption, condition
Oyster biodeposition feces, pseudofeces, C:N
Sediment AFDM, C:N
Exchangeable NH4+
Nitrification rate
(nitrapyrin inhibition)
Denitrification enzyme activity (DEA) (chloram-phenicol amended, acetylene block)
Monthly (except winter) July ‘10-Sept ‘11
Bi-monthly (winter incl.)
2 1 Nutrient gradient (N= 4 locations)
Oyster density (ctl, low, med, high)
Experimental factors
Net ammonification f
f
Organic matter
d
h
1
2
Objective is to explain mechanisms!
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Sediment tray with oyster cage (high = 125 m2, medium = 75 m2 or low = 25 m2)
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Response Variables – Sediment N cycling
Exchangeable NH4+
Sediment AFDM & C:N
Denitrification Enzyme Activity
Nitrification
Sediment nitrogen cycling
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N2
NH4+
ammonification
NO3-
nitrification
denitrification
Ben
thic
up
take
Microphyto- benthos
and sediment microbes
N-loading
excretion
a
b
c
e
Adapted from: Newell 2004
a b c
d
e
g
h
Phytoplankton: Mass, Chl a, C:N
Oyster feeding: filtration, ingestion, absorption, condition
Oyster biodeposition feces, pseudofeces, C:N
Sediment AFDM, C:N
Exchangeable NH4+
Nitrification rate
(nitrapyrin inhibition)
Denitrification enzyme activity (DEA) (chloram-phenicol amended, acetylene block)
Monthly (except winter) July ‘10-Sept‘11
Bi-monthly (winter incl.)
2 1 Nutrient gradient (N= 4 locations)
Oyster density (ctl, low, med, high)
Experimental factors
Net ammonification f
f
Organic matter
d
g
h
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Sediment AFDM • Date effect all sites
• Treatment effect as predicted (except at Mott’s Basin)
Hoellein and Zarnoch, Ecol. Appl. 2014
N2
Organic N
Seston Biodeposits
NH4+
ammonification
NO3-
nitrification
denitrification
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Sediment AFDM and exchangeable NH4+ related across sites and seasons
AFDM (g)
0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8
exchangeable
NH
4
+ (
g N
g s
edim
ent-1
)
100
1000
10000
100000
r2=0.126
p<0.001
Spring Creek
Wildlife Refuge
Motts Basin
Floyd Bennett Field
Hoellein and Zarnoch, Ecol. Appl. 2014
N2
Organic N
Seston Biodeposits
NH4+
ammonification
NO3-
nitrification
denitrification
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Nitrification and NH4+ were not related
Exchangeable NH4
+ (g N g sediment
-1)
2000 4000 6000 8000 10000 12000 14000 16000 18000
Exchangeable NH4
+ (ug N g sediment-1)
0 2000 4000 6000 8000 10000 12000 14000 16000
Nitrification r
ate
(
g N
gA
FD
M-1 h
-1)
0.1
1
10
100
r2=0.045p=0.0002
Water column NH4+
(g L-1
)
0 100 200 300 400 500
Nitrification r
ate
(
g N
gA
FD
M-1
h-1
)
0
5
10
15
20
25
30
Spring Creek
Wildlife Refuge
Motts Basin
Floyd Bennett Field
Hoellein and Zarnoch, Ecol. Appl. 2014
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10 100 1000 10000 100000
Nitrification (
g N
m-2
h-1
)
10
100
1000
10000
100000
Net immobilization
(g N m-2 h-1)
Net ammonification
(g N m-2 h-1)
r2=0.301p<0.001
-20000 -10000 0 10000 20000 30000 40000
Nitrification (
g N
m-2
h-1
)
0
2000
4000
6000
8000
10000
12000
14000
Nitrification strongly related to ammonification
R2=0.444 p<0.001
Net ammonification (µg N m-2 h-1)
Spring Creek
Wildlife Refuge
Motts Basin
Floyd Bennett Field
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Denitrification enzyme activity • Date effect all sites
• No treatment effects
Hoellein and Zarnoch, Ecol. Appl. 2014
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DEA and nitrification weakly related
Nitrification (g N gAFDM-1
h-1
)
1 10 100
Nitrification (g N gAFDM-1 h-1)
0.1 1 10 100
Denitrification r
ate
enyzm
e a
ctivity
(g N
gA
FD
M-1 h
-1)
0
100
200
300
400
500
600
r2=0.053p=0.0002
Spring Creek
Wildlife Refuge
Motts Basin
Floyd Bennett Field
Hoellein and Zarnoch, Ecol. Appl. 2014
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Water column NO3
- (ug L
-1)
0 50 100 150 200 250 300
Dentirification e
nzym
e a
ctivity
(g N
gA
FD
M-1
h-1
)
0
100
200
300
400
500
Floyd Bennet Field
Motts Basin
Wildlife Refuge
Spring Creek
July 2010
DEA related to organic matter and water column nitrate
r2=0.334 p=0.048
Hoellein and Zarnoch, Ecol. Appl. 2014
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Oyster effect when sediment most nutrient limited
Hoellein and Zarnoch, Ecol. Appl. 2014
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N2
NH4+
ammonification
NO3-
nitrification
denitrification
Ben
thic
up
take
Microphyto- benthos
and sediment microbes
N-loading
excretion
To connect oyster waste N denitrification • Promote coupled ammonification - nitrification – denitrification • Our results suggest oysters increase organic matter • Then, see internal NH4
+ uptake favored over nitrification • Potential use of water column NO3
-, rather than nitrification derived NO3
-, for denitrification
Organic matter
immobilization immobilization
NO3-
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Effects of oysters on denitrification
Kellogg et al. 2013 found higher rates of denitrification on restored oyster reefs
Piehler and Smyth 2011
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Oyster Restoration Research Project
Hudson River Foundation and > 30 other partner groups
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Sediment N cycle adjacent to reef
A: Phytoplankton primary production, community respiration, and C:N B: Oyster excretion C: Hydrology D: Sediment organic matter E: Porewater ammonium
F: Nitrification G: Denitrification H: N2O emission I: Dissimilatory nitrate reduction to ammonium (DNRA) J: Ammonium oxidation (Annamox)
B
Sediment N cycle farther from reef
C
A
The influence of oyster reef restoration on nitrogen cycling in the Hudson-Raritan estuary
NH4+ NO2
- NO3- N2O N2
F G
H I
E
J
D
Org-N
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Intake water
Pump
Inflow Outflow
Intact core
Overlying water
Vinyl cap
O-ring
Sample collection vessel
Near Far Spat CAN Method Control = no isotope added; to measure net N2 flux Ammonium = +10 µM 15NH4
+; to measure annamox Nitrate = +10 µM 15NO3
-; to measure DN, DNRA, and NO3- source for denitrification
Objective is to explain mechanisms!
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Soundview Reef
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Sediment and Reef Core Incubations CAN method
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Sediment Denitrification at Soundview D
NF
mol N
m-2
h-1
)
0
200
400
600
800
1000
0
200
400
600
800
1000
Near Far Near Far Near Far Summer Fall Spring
Near Far Near Far Near Far Summer Fall Spring
A B
a a
b
Denitrification Potential Denitrification (+15NO3
-)
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15D
NF
(
mo
l 2
9,3
0N
2 m
-2 h
-1)
0
10
20
30
40
50
0
10
20
30
40
50
Near Far Near Far Near Far Summer Fall Spring
Near Far Near Far Near Far Summer Fall Spring
B.D.
a a b
a ab b
A B
Nitrification-Denitrification Direct denitrification
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Reef Denitrification at Soundview
Spat Shell
DN
F
mo
l N
m-2
h-1
)
0
50
100
150
200
250
300
350
Spat Shell
Y D
ata
0
50
100
150
200
250
300
350
A B
Denitrification Potential Denitrification (+15NO3-)
Carbon limitation?
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Oysters and Water Quality
• Benthic-Pelagic Coupling - Enhance coupled nitrification-denitrification?
N2
Organic N
Seston Biodeposits
NH4+
ammonification
NO3-
nitrification
denitrification
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Response Variables – Oyster Feeding
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Clearance rates in Jamaica Bay 2010-2011
Total particulate matter (mg l-1
)
0 20 40 60 80 100
Cle
ara
nce
ra
te (
l h
-1 g
DW
-1)
0
1
2
3
4
5
FBF
JBWR
MB
SC
R2 = 0.48
p < 0.001
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High organic matter in seston
Total particulate matter (mg l-1
)
0 10 20 30 40 50 60 70 80 90
Org
anic
conte
nt
of
TP
M (
fraction
)
0.0
0.2
0.4
0.6
0.8Jamaica Bay (this study)
Cape Cod estuaries (Carmichael et al. 2004 )
Bay of Marennes-Oleron (Hawkins et al. 1996)
Merbok mangrove estuary (Hawkins et al. 1998)
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Phytoplankton Abundance Jamaica Bay 2010-2011
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Soundview Reef
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Soundview Seston
Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct
To
tal p
art
icu
late
ma
tte
r (m
g l
-1)
0
10
20
30
40
50
60 Soundview
2011 2012
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Phytoplankton Abundance Soundview 2011-2012
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Low organic content in seston
Total particulate matter (mg l-1
)
0 10 20 30 40 50 60
% o
rganic
conte
nt
of
the s
esto
n
10
15
20
25
30
35
40
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Oyster Feeding Rates at Soundview
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Seston characteristics explain high clearance rates
Jun'11 Jul'11 Aug'11 Sept'11 May'12
Tota
l part
icula
te m
atter
(mg l
-1)
0
5
10
15
20
25
30
% o
rganic
conte
nt of th
e s
esto
n
10
15
20
25
30
35
40
TPM
TPMOC
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Clearance rates – July’11
FBF JBWR MB SC HOH SV
Cle
ara
nce
ra
te (
l h
-1 g
DW
-1)
0
2
4
6
8
10
To
tal p
art
icu
late
ma
tte
r (m
g l
-1)
0
5
10
15
20
25
30
35
Jamaica Bay
HR
BX
* Temporal and spatial replication of feeding physiology is required due to seston dynamics
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Oysters and Water Quality
• Benthic-Pelagic Coupling - Enhance coupled nitrification-denitrification?
N2
Organic N
Seston Biodeposits
NH4+
ammonification
NO3-
nitrification
denitrification
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Eastern oyster (Crassostrea virginica) filtration, biodeposition, and sediment nitrogen cycling at two oyster reefs with contrasting water quality in Great
Bay Estuary(New Hampshire, USA)
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Denitrification higher at eutrophic oyster reef
Hoellein , Zarnoch, Grizzle, Biogeochemistry, In Press
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Direct denitrification favored over coupled nitrification-denitrification
Hoellein , Zarnoch, Grizzle, Biogeochemistry, In Press
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1) Why was denitrification enhanced at the eutrophic
site and not at the oligotrophic site? T
ota
l b
iod
ep
ositio
n r
ate
(m
g g
-1 h
-1)
0
20
40
60
80
100
120
% o
rga
nic
co
nte
nt
of
bio
de
po
sits
0
10
20
30
40
p < 0.001 p = 0.085
Feces Pseudofeces
C:N
0
2
4
6
8
10
12
Nannie Isl.
Squamscott
Carbon Nitrogen
Ca
rbo
n b
iod
ep
ositio
n r
ate
(m
g g
-1 h
-1)
0
1
2
3
4
5
Nitro
ge
n b
iod
ep
ositio
n r
ate
(m
g g
-1 h
-1)
0.0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
A)
B)
C)
Total %OC
p = 0.002 p = 0.007
p < 0.001
p = 0.01
Hoellein , Zarnoch, Grizzle, Biogeochemistry, In Press
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2) How do we explain the oyster reef effect on denitrification potential?
Denitrification potential correlated with larger sediment particles Organic C substrate and enhanced NO3
- diffusion
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Lab experiments – Oysters x Trophic status
eutrophic oligotrophic +oystersNo oysters
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Denitrification potential is enhanced by oysters under oligotrophic
conditions
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Implications for NYC Restoration
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Implications for NYC Restoration
1. Oyster filtration most effective at less turbid sites. Long term monitoring required.
2. Mechanism for oyster mediated denitrification will likely be through enhanced C biodeposition where C is limited.
3. Sediments around reef/breakwater structures may have enhanced NO3
- diffusion.
4. Measurements of intact living structures using isotopes is needed to understand site-specific mechanisms.
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Acknowledgements: Funding: • National Science Foundation Awards: DEB-0918952 & MRI 0959876 • Hudson River Foundation • CUNY
Partners: • Gateway National Recreation Area • NYS Department of Environmental Conservation • New York City Parks – NRG • Lehman College/ SUNY- Maritime
Students: Allison Mass – CUNY Graduate Center Narendra Paramanand – Baruch College Doris Law – Baruch College Swathi Mummini- Hunter College Gena Israel – Hunter College Angela David – Loyola University Chicago S Morgan – Loyola University Chicago Steve Polaskey – Loyola University Chicago Vitaly Zaharov – Baruch College Hanen Yan – Baruch College Kevin Kucher – Penn State University Damien Christopher – NY Harbor School Jemi Jacob – Hunter College Sanne Lynham – Baruch College Corinna Singleman – CUNY Graduate Center
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Summer 2012 Soundview
May Jun Jul Aug Sep Oct
Mean D
issolv
ed O
xygen (
mg l
-1)
1
2
3
4
5
6
7
Day
Night
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Summary
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Jun'11 Jul'11 Aug'11 Sept'11 May'12
Filt
ratio
n r
ate
(m
g h
-1 g
DW
-1)
0
10
20
30
40
50
60 Cultured
Native 2-way ANOVADate; p < 0.0005Strain; p = 0.744D x S; p = 0.454
Jun'11 Jul'11 Aug'11 Sept'11 May'12
Cle
ara
nce
ra
te (
l h
-1 g
DW
-1)
0
2
4
6
8
10
Cultured
Native
2-way ANOVADate; p < 0.0005Strain; p = 0.956D x S; p = 0.986
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Jun'11 Jul'11 Aug'11 Sept'11 May'12
Org
an
ic c
arb
on
bio
de
po
sitio
n (
mg
h-1
gD
W-1
)
0.0
0.5
1.0
1.5
2.0
2.5
3.0 Cultured
Native
Jun'11 Jul'11 Aug'11 Sept'11 May'12Org
an
ic n
itro
ge
n b
iod
ep
ositio
n (
mg
h-1
gD
W-1
)
0.0
0.1
0.2
0.3
0.4Cultured
Native
2-way ANOVADate; p = 0.008Strain; p = 0.822D x S; p = 0.637
2-way ANOVADate; p = 0.003Strain; p = 0.828D x S; p = 0.65