understanding nitrogen transformations and …spring creek wildlife refuge motts basin floyd bennett...

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

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)

NYC Sewer System

NYC Sewer System

New York Times

Impacts of nitrogen loading

Impacts of nitrogen loading

Impacts of nitrogen loading

Impacts of nitrogen loading

Impacts of nitrogen loading

Oysters and Water Quality

• Benthic-Pelagic Coupling - Enhance coupled nitrification-denitrification?

N2

Organic N

Seston Biodeposits

NH4+

ammonification

NO3-

nitrification

denitrification

Rates of Denitrification by Habitat Piehler and Smyth 2011

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

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

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

Rebuild by Design “Living Breakwaters”

Oysters and Water Quality

• Benthic-Pelagic Coupling - Enhance coupled nitrification-denitrification?

N2

Organic N

Seston Biodeposits

NH4+

ammonification

NO3-

nitrification

denitrification

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?

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

Phytoplankton Abundance Jamaica Bay 2010-2011

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!

Sediment tray with oyster cage (high = 125 m2, medium = 75 m2 or low = 25 m2)

Response Variables – Sediment N cycling

Exchangeable NH4+

Sediment AFDM & C:N

Denitrification Enzyme Activity

Nitrification

Sediment nitrogen cycling

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

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

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

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

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

Denitrification enzyme activity • Date effect all sites

• No treatment effects

Hoellein and Zarnoch, Ecol. Appl. 2014

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

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

Oyster effect when sediment most nutrient limited

Hoellein and Zarnoch, Ecol. Appl. 2014

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-

Effects of oysters on denitrification

Kellogg et al. 2013 found higher rates of denitrification on restored oyster reefs

Piehler and Smyth 2011

Oyster Restoration Research Project

Hudson River Foundation and > 30 other partner groups

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

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!

Soundview Reef

Sediment and Reef Core Incubations CAN method

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

-)

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

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?

Oysters and Water Quality

• Benthic-Pelagic Coupling - Enhance coupled nitrification-denitrification?

N2

Organic N

Seston Biodeposits

NH4+

ammonification

NO3-

nitrification

denitrification

Response Variables – Oyster Feeding

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

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)

Phytoplankton Abundance Jamaica Bay 2010-2011

Soundview Reef

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

Phytoplankton Abundance Soundview 2011-2012

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

Oyster Feeding Rates at Soundview

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

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

Oysters and Water Quality

• Benthic-Pelagic Coupling - Enhance coupled nitrification-denitrification?

N2

Organic N

Seston Biodeposits

NH4+

ammonification

NO3-

nitrification

denitrification

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)

Denitrification higher at eutrophic oyster reef

Hoellein , Zarnoch, Grizzle, Biogeochemistry, In Press

Direct denitrification favored over coupled nitrification-denitrification

Hoellein , Zarnoch, Grizzle, Biogeochemistry, In Press

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

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

Lab experiments – Oysters x Trophic status

eutrophic oligotrophic +oystersNo oysters

Denitrification potential is enhanced by oysters under oligotrophic

conditions

Implications for NYC Restoration

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.

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

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

Summary

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

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