Climate change in the shallows – interacting effects of diel-cycling hypoxia and acidification* Denise Breitburg Andrew Keppel Seth Miller Rebecca Burrell

*unpublished student data removed from presentation

Atmospheric CO2

Acidification Respiration

+CO2

Hypoxia/ deoxygenation

-O2 Eutrophication

Fisheries

warming

Multiple stressors – management, understanding

Atmospheric CO2

Acidification Respiration

+CO2

Hypoxia/ deoxygenation

-O2

warming

Multiple stressors – management, understanding

Breitburg et al., in press; data from Maas et al. 2014, Breitburg et al., unpublished

Costa Rica Dome 0-1000 m

Estuarine salt marsh 1 m

Chesapeake Bay

Gedan et al, unpubl

Breitburg et al., 2015

Shallow Chesapeake Bay high productivity restricted circulation nutrient enriched

high respiration seasonal & diel-cycling hypoxia

Diel-cycling hypoxia and acidification • Patterns? • Do diel-cycling acidification and hypoxia affect

native species in spite of potential adaptation and daily periods of recovery? (Experiments with oysters & fish)

Contrasting patterns at 3 sites in Chesapeake Bay ’

dis

so

lve

d o

xyg

en

(m

g/L

)

0

2

4

6

8

10

12

time of day

pH

6.5

7.0

7.5

8.0

8.5

Oxygen and pH daily cycles

MD-DNR: eyesonthebay.net

‘Classic’ diel cycling’

Bear Creek

‘Classic’ diel cycling’ d

iss

olv

ed

ox

yg

en

(m

g/L

)

0

2

4

6

8

10

12

time of day

pH

6.5

7.0

7.5

8.0

8.5

Oxygen and pH daily cycles

Daylight – Photosynthesis dominates + oxygen, -CO2

‘Classic’ diel cycling’ d

iss

olv

ed

ox

yg

en

(m

g/L

)

0

2

4

6

8

10

12

time of day

pH

6.5

7.0

7.5

8.0

8.5

Oxygen and pH daily cycles

Dark – Respiration dominates - oxygen, +CO2

R² = 0.76

6.5

6.7

6.9

7.1

7.3

7.5

7.7

7.9

8.1

8.3

0 2 4 6 8 10 12

pH

DO (mg/L)

Salt marsh Creek Rhode River, Chesapeake Bay

Strong tidal signal

0

2

4

6 D

O (

mg

/L) P ≤ 0.0002

6.4

6.6

6.8

7

7.2

7.4

L F H E

pH

Tide Stage

P ≤ 0.0005

Low Flood High Ebb

0

1

2

3

4

5

6

7

8

9

10

0:00 2:24 4:48 7:12 9:36 12:00 14:24 16:48 19:12 21:36 0:00

DO

(m

g/L

)

Time of day

DO Time Series (7/16-21 GCRW Marsh)

7/16/2014

7/17/2014

7/18/2014

7/19/2014

7/20/2014

7/21/2014

High Tide

Low Tide

High Tide

Low Tide

Dawn - 5:54-5:58

daw

n

Tide-dominated pattern: timing of minima vary among days

R² = 0.9365

6.5

7

7.5

8

8.5

9

0 2 4 6 8 10 12

pH

DO (mg/L)

DO vs. pH (7/10-8/11 SERC Dock) Dock site Rhode River, Chesapeake Bay

Mid-day minima

3

3.5

4

4.5

5

5.5

6

6.5

7

7.5

8

0:00 2:24 4:48 7:12 9:36 12:00 14:24 16:48 19:12 21:36 0:00

DO

(m

g/L

)

Time of Day

DO Time Series (8/6-11 SERC Dock)

8/8/2014

8/9/2014

8/10/2014

Dawn 6:10-6:16

High Tide Low Tide Low Tide High Tide

Stratification on sunny days – Mid-day minima

DO and pH at 2 m continue to decline after dawn

0.00

0.50

1.00

1.50

2.00

2.50

2.00 3.00 4.00 5.00 6.00

De

pth

(m

)

DO (mg/L) 7.00 7.10 7.20 7.30 7.40

pH

5:32

5:56

6:18

6:43

7:06

7:25

7:50

8:13

Sample Time

Shallow water cycles of dissolved oxygen and pH

Large spatial variation in timing and magnitude of cycles- different drivers dominate patterns Spatial variation in ways hypoxia and acidification interact with diel patterns of behavior and physiology

Disease Growth

Eastern Oyster (Crassostrea virginica)

Growth Sensitivity to hypoxia

Atlantic & inland silversides (Menidia menidia & M. beryllina)

LabVIEW program

manifold

Rep

. 1

R

ep.

2

Rep

. 3

R

ep.

4

Rep

. 5

R

ep.

6

N2 MFC

00.00 N2 system,

n=3

CO2 system, n=4

O2 system, n=3

20psi

LiqN2 with gas removal

V

V

O2 MFC

00.00

20psi

O

2

CO2 MFC

00.00

15psi

CO2

Emergency fail closed solenoid

Air system, n=5

Air compres

sor

Condensing coil in freezer

Drip leg to drain

condensate

CO2 stripper column (soda

lime filled)

drying column (indicating silica

filled) Particle filter

00.00

drain

CO2 free air

^ ^

Normally open

When energized

3-way solenoid

air

H2

O

Air MFC

15psi

V

Emergency air

compressor

Emergency fail open solenoid

Oxyguard DO probes

Durafet pH probes

Trt.

1

Tr

t.

2

Trt.

3

Tr

t.

4

Trt.

5

Sp

ar e

air

H2

O

Burrell et al., accepted pending revision

LabView program

0.00.51.01.52.02.53.03.54.04.55.05.56.06.57.07.58.08.59.09.5

10.010.511.0

Dis

solv

ed o

xyge

n (

mg/

L)

2012 dissolved oxygen trend

DO_WB_mean

DO_WP_mean

DO_GP_mean

DO_BP_mean

DO_BB_mean

6.90

7.00

7.10

7.20

7.30

7.40

7.50

7.60

7.70

7.80

7.90

8.00

7/3

1/2

012

2:2

4

7/3

1/2

012

14

:24

8/1

/20

12 2

:24

8/1

/20

12 1

4:2

4

8/2

/20

12 2

:24

8/2

/20

12 1

4:2

4

8/3

/20

12 2

:24

8/3

/20

12 1

4:2

4

8/4

/20

12 2

:24

8/4

/20

12 1

4:2

4

pH

(u

nit

s)

2012 pH trend

DO_WB_mean

DO_WP_mean

DO_GP_mean

DO_BP_mean

DO_BB_mean

Eastern Oyster (Crassostrea virginica)

Immune response/disease (Dermo – Perkinsus marinus) hemolymph pH hemocyte function prevalence and intensity of infections Juvenile growth

Mea

n pH

±SE

7.0

7.2

7.4

7.6

7.8

8.0

Time

0 2 4 6 8 10

Mea

n pH

±SE

7.0

7.2

7.4

7.6

7.8

8.0

Time

0 2 4 6 8 10

Control

Cycling pH

Cycling DO & pH

Cycling DO;

Hemolymph pH affected by water pH

water

hemolymph

Virginia Clark - 2014

Prop

ortio

n ph

agoc

ytic

hem

ocyt

es

0.00

0.05

0.10

0.15

0.20

Severe cycling hypoxia - Normcapnia Severe cycling hypoxia - Cycling pH Normoxia - Normcapnia Normoxia - Cycling pH

Cycling (DO, CO2, DO+CO2) stimulates hemocyte function

low oxygen high oxygen hi pH low pH hi pH low pH

(cycling down to DO = 0.5, pH = 7.1)

Keppel et al., in review

Infe

ctio

n In

tens

ity

(mea

n of

all

dise

ased

oys

ters

)

0.8

1.0

1.2

1.4

1.6

1.8

Severe cycling hypoxia - Normcapnia Severe cycling hypoxia - Cycling pH Moderate cycling hypoxia - Cycling pH Normoxia - Normcapnia Normoxia - Cycling pH

Stimulation of hemocytes only tends to reduce infection progression when oxygen is high

low oxygen high oxygen hi pH low pH hi pH low pH Keppel et al., in review

Low salinity year ΩCalcite =0.69

High salinity year ΩCalcite =1.87

Juvenile growth cycling down to

DO = 0.5, pH = 7.1

Keppel 2014

The effect of diel-cycling pH differed in high and low salinity/ ΩCalcite years

0

1

2

3

4

5

6

6.87.0

7.27.4

7.67.8

8.0

02

46810

Cle

aran

ce R

ate

(L h

r-1 g

-1)

pH

Dissolved Oxygen (mg L -1) at Low Plateau

p < 0.0001Adj R2 = 0.27

Low pH slightly increases oyster filtration rates

2 way ANOVA then Planar regression Clark 2014.

Atlantic and inland Silversides- Growth, Aquatic Surface Respiration & Mortality

Seth Miller

Growth of juvenile Menidia beryllina was lower relative to controls when fish were reared in diel-cycling dissolved oxygen or constant hypoxia conditions, but was not affected by cycling pH or constant low pH

© Dave Conover

Laboratory experiments indicated that simultaneous exposure to low pH can make fish more sensitive to low dissolved oxygen

Even brief daily exposures to acidification and hypoxia can negatively affect species that are native to systems with large natural fluctuations

So – Why worry about multiple stressors?

For mobile species, co-occurrence with other stressors can determine exposure to acidification

Almost all species tested behaviorally avoid low dissolved oxygen. Co-occurring hypoxia may therefore reduce exposure to respiration-driven acidification

Individual stressors can either exacerbate or reduce effects of other stressors

We can’t predict consequences or manage effectively if we don’t consider the full context in which organisms live