Oxygen Decline in Coastal Waters

GO2NEGlobal Ocean

Oxygen NEtwork

Denise BreitburgSmithsonian Environmental

Research Center

Hayle Estuary, UK, image: https://www.rspb.org.uk/reserves-and-

events/reserves-a-z/hayle-estuary/

Mattole River Estuary, California, USA

Image: https://en.wikipedia.org/wiki/Estuary

What am I including in coastal waters?

Estuaries, semi-enclosed seas, embayments, fjords, coastal lagoons,

etc. – Not open wave-swept coasts

Water bodies in which oxygen depletion is strongly influenced by their local watershed (catchment).

Will rely heavily on systems in the US and Europe for examples – I hope

during the discussion and the rest of the week everyone can share

observations from the rest of the world

UNITS: 1 mg/L ~ 1.4 ml/L ~ 31 μmol/L

Hypoxia definition: oxygen (concentration, saturation, partial pressures)

sufficiently low to negatively impact biological or ecological processes.

• 2 mg/L conventional cutoff, but not ideal to use

Outline:

Causes

Patterns

Ecological Effects

Jenny et al., 2016

Low oxygen occurs naturally

in many water bodies

Baltic

Sea

Black

Sea

Paleo evidence:

Instances of low

oxygen in the past in

some systems even

where nutrients have

now made oxygen

depletion more severe and extensive

1) Diaz map

• since 1950 - Over 600 coastal systems identified with <20-25% oxygen

saturationDiaz and Rosenberg 2008, Diaz

unpublished, Breitburg et al., 2018

Number of water bodies reporting hypoxia has increased

dramatically since the mid-20th century

Based on date of earliest verified

measurement of hypoxia. Probably

more unreported

‘Diaz database’

Caveate: The more we look the

more we find. Reporting lower in

developing economies

Expansion of hypoxic area

through time - Baltic Sea

Carstensen et al. (2014)

1,500 km2 65,000 km225,000 km2

Within systems oxygen depletion getting more severe and widespread

Image: www.renewableresourcescoalition.org/

overpopulation-causes-effects-solutions/

Invention of chemical fertilizers in

early 20th century:

Haber–Bosch process converts

atmospheric N2 to ammonia (NH3)

though a reaction with H2

Hot, sour and breathlessTurley et al., 2016

Underlying problems – increasing human

population, use of chemical fertilizers to

feed that population, and increasingly,

climate change

phytoplankton

zooplanktonN, P, Si

Dead cells

Fresh

water

Nutrients

(N&P)

Organic

carbon

Sediment

Modified from: https://upload.wikimedia.org/wikipedia/commons

/d/dd/Scheme_eutrophication-en.svg

Eutrophication – too much nutrients – too much production –

consequence is low oxygen

NOx, NH3/NH4+,

DON

Main nutrient sources include agriculture, sewage and burning of fossil fuels

Baltic Proper 2014 (Sources and pathways of

nutrients to the Baltic Sea

HELCOM PLC-6)

TN TP

Riverine

sources

Nutrients important but high nutrient loads not whole story

Openness~

residence time

HYPOFIN – unpublished data

Model R2= 0.72 p<0.003 Source of variation p upwelling_category 0.0392 log10 (openness) 0.0237 log10 basin+atmosTN 0.0472 warmest month mean oC 0.078

Reduced O2 introduction →

reduced ventilation (mixing)

long residence time

darkness

Balance tipped towards oxygen decline

Increased respiration →

nutrient enrichment

high biomass/oxygen demand

increased temperature

***Same basic processes as open ocean but very different

spatial & temporal scales

Fennel & Testa 2018

Cause of oxygen decline

*Aerobic respiration O2 → CO2

*Introduction of O2 (photosynthesis,

ventilation)< O2 consumption

Fennel &Testa 2018

Most important factors:

Oxygen content of source water

Respiration rate

Residence time

Nutrient loads

Untreated sewage tends to cause the most

extreme oxygen depletion

Manila Bay, 2010<20% treated

sewage,

10 million people in

watershed

River Thames , England

(raw sewage in 1800s)

Mariager Fjord, Denmark 1997 anoxia eventFallesen et al. 2000

Every year

Long residence time

High nutrient loads

High chlorophyl

1997

Warmer weather

Low wind mixing

Increased oxygen

depletion

Mussels die

Feedbacks can be important

Temporal patterns of hypoxia in nutrient-enriched systems

Persistent

(years to millennia)

Seasonal

Episodic

Diel/tidal

Chesapeake

Baltic

Black

Weeks Bay

Venice Lagoon

• year round stratification in deep basins

• Seasonal cycle in shallower water

• hypoxic/anoxic volume sensitive to inflow, warming

Persistent for years to thousands of years

(e.g. Baltic proper, Black Sea)

Black Sea

Image: https://geologycafe.com/oceans/chapter9.html

Oxygen penetration depthCapet et al., 2016

Seasonal hypoxia, NW shelf

HELCOM 2009 Conley et al., 2008

Baltic Sea

Seasonal hypoxia- stratified temperate estuary

Chesapeake Bay

dis

so

lve

d o

xyg

en

(m

g/L

)

0

2

4

6

8

10

12

Respiration dominates during dark lowest

DO around dawnTemporal patterns vary; timing as well as duration

and severity may determine which

processes/species are affected

Diel & tidally driven hypoxia

– sub-daily cycles

-natural but exacerbated by high nutrient loads

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

Daylight –

Photosynthesis dominates

+ oxygen, -CO2

Tight correlation between oxygen & pH/pCO2

Chesapeake Bay

Boynton et al., 1996

Chlorophyll important driver

Mangrove ponds in Belize & Panama

Diel-cycling hypoxia

Harness Creek,

MD

Jun Jul Aug Sep

SERC

Creates temporal & spatial variability at a

variety of scales

Affects productive refuge from deep-

water hypoxia

Affects habitat that is important predator

refuge for small & juvenile fish

Sites <

2 m

depth

Upwelling/intrusions of low oxygen water

nearshoreCrab jubileeMobile Bay (image: NOAA)

Local weather influence & decadal climate variability affect

spatial/temporal patterns and the relationship between N loads

and hypoxia extent

Chesapeake Bay hypoxia :Large-scale climate cycles and local wind

directionsMurphy et al., 2011

Altieri & Gedan 2015

Warming

Decreases oxygen introduction

• Stratification (intensity & duration)

• currents

Alters patterns of precipitation & nutrient delivery

Decreases oxygen solubility

Increases oxygen consumption

Respiration rates

Climate change will worsen oxygen depletion in most coastal systems

Meier et al., 2011

Baltic – rising temperature increases oxygen depletion, increasing precipitation

increases stratificationBusiness as usual

Effects: If you can’t breathe,

nothing else matters(American Lung Association)

• important force in evolution

•creates biologically &

ecologically important spatial and

temporal structure

• decreases biodiversity

• alters biogeochemical cycles

• direct exposure decreases

survival, growth, reproduction,

and increases disease

• alters predator-prey interactions

• effects found tropics – to – poles

• fisheries affected – location,

value, catch

• economies and human health

Declining oxygen – Important force in evolution through geological time and now

Decker et al., 2003

Robert J. Diaz, and Rutger Rosenberg Science

2008;321:926-929

Deoxygenation increases energy flow to microbes

Wright 2012

Terminal electron acceptors

Hood Canal

(Washington State, US)

Speitz et al., 2015

94 → 375 μmol/L

Hypoxia typically decreases biomass and diversity-

especially for sessile & low-mobility species

Villna s̈ et al., 2004

Benthic invertebrates – Baltic Sea

Hypoxia, and the nutrients and warming that cause deoxygenation, create

biologically, ecologically & economically relevant spatial structure- need to

consider effects both within hypoxic water and larger time & space scales

Behavior (or lack thereof) determines effects

High

oxygen

Chronic

effects

Lethal

conditionsHighly mobile species

reduced growth & reproduction

0 1 2 3 4 5 6 7 8

0.0

0.2

0.4

0.6

0.8

1.0

Bottom dissolved oxygen (mg L-1)

sea nettles

ctenophores

0 1 2 3 4 5 6 7 8

Pro

po

rtio

na

l d

en

sity

0.0

0.2

0.4

0.6

0.8

1.0

0 1 2 3 4 5 6 7 8

0.0

0.2

0.4

0.6

0.8

1.0

adult copepods and copepodites

Bottom dissolved oxygen (mg L-1)

bay anchovy larvae

naked goby larvae

0 1 2 3 4 5 6 7 8

0.0

0.2

0.4

0.6

0.8

1.0

0 1 2 3 4 5 6 7 8

0.0

0.2

0.4

0.6

0.8

1.0

random

distribution

Keister et al 1998

Breitburg et al. 1997

Reproductive to population-level effects

Normoxic Hypoxic

10

3e

gg

s fish

-1

Normoxic

sites

Hypoxic

sites

Atlantic croaker, Gulf of Mexico

Thomas & Rahmen 2011 Modified from Rose et al., 2018; croaker image: sc.dnr.gov

Low N – High O2

High N - Hypoxia

Data& images: Kevin Craig (NOAA)Total CPUE

0 - 1

1 - 2

2 - 4

> 4

Bottom Oxygen (mg l-1)

Combination of hypoxia, species behavior and fishers behavior may

increase fishing mortality & increase likelihood of overfishing

2-4

0-1

1-2

>4

DO (mg l-1)

20 m

80 m

50 km

Shrimp Vessel Sightings Shrimp abundance

Craig 2012; Purcell et al., 2017

Northern Gulf of Mexico

Data& images: Kevin Craig (NOAA)

Hypoxia creates economically relevant spatial structure

0

10

20

30

40

50

60

70

80

90

7000

9000

1100

0

1300

0

1500

0

1700

0

1900

0

2100

0

2300

0

Sp

atia

l Ov

erla

p

90-d Mean Hypoxia Area (km2)

R2=0.32

2008

2004-2016

Low oxygen exacerbates acquisition & progression of disease

Generally reduces immune response by decreasing phagocytosis and

production of reactive oxygen species

Host Pathogen

taxa

Pathogen/

disease

Dino-flagellate

Perkinsus marinus (dermo)

Keppel et al., 2016Breitburg et al., 2015b

virus White spot syndrome virus

Lehman et al., 2016

protist Amoebic gill disease Fisk et al., 2002

helminth Anguilla crassus Gollock et al., 2005

bacteria Vibrio campbelli Macey et al., 2008

bacteria Vibrio parahemolyticus

Henroth et al., 2015

bacteria Vibrio parahemolyticus

Boleza et al., 2010 Breitburg et

al., in press

}2008

2009

Patuxe

nt

julian day

160 180 200 220 240 260 280 300

Daily

min

imum

[D

O]

(mg l

-1)

0.0

2.0

4.0

6.0

8.0

10.0

HCR

HPL

LMN

MUL

SERC

Jun Jul Aug OctSep

3 mg/l

2 mg/l

1 mg/l

Even cycling low oxygen can increase susceptibility to pathogens

Breitburg et al., 2015

Mean daily minimum DO during days with salinity > 11 (mg/L)

2.0 3.0 4.0 5.0 6.0 7.0

Pe

rkin

su

s p

reva

len

ce

(%

)

40

50

60

70

80

90

100

2008

2009

Darryl Hondorp

Atlantic menhaden in Narragansett Bay

Productive Fisheries

Fish kills

Contrasting effects of

nutrient enrichment

and hypoxia

0

20

40

60

80

100

120

140

160

0 100 200 300 400 500

PRIMARY PRODUCTION, g C m-2 y-1

AN

NU

AL F

IS

HE

RY

LA

ND

IN

G, K

g H

a-1

Nixon 2002Eutrophication severity

Fis

heri

es

land

ings

Caddy 1993

hypoxia

La

ndin

gs f

ish a

nd m

obile

inve

rte

bra

tes

(lo

g1

0 k

g k

m -

2 y

ea

r -1

)

2.5 3.0 3.5 4.0 4.5 5.0 5.5

2.5

3.0

3.5

4.0

4.5

<1% hypoxia

2-9% hypoxia

10-77% hypoxia

N loadings (log10 kg km -2 surface area year -1)

Rose et al., in press; redrawn from Breitburg et al., 2009

Eutrophic coastal

systems still

function as

‘protein

factories’for

mobile catch, but

individual

important species

can be harmed,

and long-term

consequences are

uncertain

Breitburg et al., 2009

Hypoxia reduces the production efficiency of

systems: less biomass & catch/N load

•Behavior, growth and fishing

practices result in spatial and

temporal averaging by fish and

fisheries

Hypoxia direct effectsdominant

Direct and indirect effects of hypoxia and increased production

Increased production and Indirect effects of hypoxia

Increased production effects only

landland

Evidence of negative population-level

effects elusive:

Compensatory mechanisms

•turbidity as a substitute

refuge for submerged

macrophytes

Compensatory mechanisms

Abundant Solomons

Island

SAV during May 1938

compared to Summer 1999

Compensatory mechanisms

•Behavior, growth and fishing

practices

result in spatial and temporal

averaging by fish and fisheries

•overfishing keeps populations below

habitat-determined carrying capacity –

therefore little effect of decreased habitat

effects strongest when pops high and

affected habitat is critical and limited

•turbidity as a substitute refuge for

submerged macrophytes

Deoxygenation = destruction of an

ecosystem even where it does not affect

fisheries

Human dimension – dependence on local resources may

determine effects

Bolinao, PhilippinesSan Diego-McGlone et al., 2008

Finfish aquaculture

Increased fish biomass and added feed

Increased oxygen demand

Hypoxia

Fish kills

Economic losses

Human impact

Photo: http://kickerdaily.com/wp-content/uploads/2014/06/Batangas-Fish-Kill1.jpg

Laajalahti Bay, Gulf of Finland

Kauppila et al., 2005Testa et al., 2018 b

Chesapeake Bay, US

Nutrient reduction can work but will be more difficult as waters warm

Modified from Bopp et al., 2013

Low oxygen does not occur in isolation –

oxygen decline in a multiple stressor world

Oxygen change

pH changeTemperature change

1o production change

Photo: http://oceans.ubc.ca/2018/08/01/fishing-fleets-travelling-further-to-catch-fewer-fish-2/

Management & prediction requires

that we consider this

Steps to restore ocean oxygen can directly benefit people

http://7-themes.com/data_images/out/59/6971871

-big-ocean-wave.jpg

• Reduce nutrients

• Reduce greenhouse gas

emissions

• Adaptation strategies

manage resources to

acknowledge and

compensate for the

problem

Improved sanitation,

agriculture efficiency &

air quality

Avoiding the

devastation of rising

temperatures and rising

seas

Managing fisheries,

including aquaculture,

more sustainably

Take home messages:

Causes – combination of physical characteristics of system,

anthropogenic nutrients and warming

Patterns – minutes to thousands of years; meters to 10s of

thousands of km

Ecological Effects- All aspects of biology, ecology, local

fisheries

Challenge to us:

Increase Engagement with civil society and policy makers

Increase & Improve Communication

big picture

develop language to communicate importance

effects on people and on things people care about

(our children)

GO2NEGlobal Ocean Oxygen NEtwork

A major goal of GO2NE is to help

Increase research capacity and

knowledge transfer.

end

Nutrient overenrichment

We have solutions:

agriculture

wastewater treatment

reduced NOx emissions from power generation

Planning, regulations and clear goals critical

Will, $$$

Southwest River Estuary

Prince Edward Is, Canada

(explosive increase in fertilizer use;

inappropriate crop choice)

…but a combination of excess fertilizer runoff and

restricted circulation can also lead to complete

anoxia

Chesapeake Bay

Gedan et al, unpubl

Breitburg et al.,

2015

Ludsin et al., 2009

Behavior determines spatial distributions – especially vertically

Low

DOFish

avoid

bottom

Can concentrate or separate predators and their prey