Effects of Oil Exposure on Submerged Aquatic Vegetation Growth, Reproduction, and Herbivory

Charles W. MartinUniversity of Florida/IFAS

Nature Coast Biological Station

• Estuaries in the Gulf of Mexico provide much of the nation’s supply of fisheries, wetlands, & numerous desirable natural resources

From Lellis-Dibble et al. 2008

Deepwater Horizon Oil Spill

http://gomex.erma.noaa.gov/

Photo: Coxworth

Photo: Beinecke

• Effects of Oil on Submerged Aquatic Vegetation• Growth

• Reproduction

• Root Morphology

• Food Web Effects of Plant Oiling• Herbivory of oil-affected

plant tissue

• Future food web work

• Coastal vegetation provides numerous ecosystem services• Refuge for nekton

• Forage base for organisms

• Buffer from storms

• Water filtration

Cocodrie, LA

Lacombe, LA

Widgeon grass, Ruppia maritima

Port Sulphur, LA

From Pezeshki et al. 2000

Studies have focused on oil effects to emergent vegetation, while much less is known about

submerged vegetation

1. What are the effects of oil on Ruppiamaritima?

2. Are there food web implications from this oil exposure?

• Ruppia grown in 19L tanks at 10 psu for 31-33 days

• 4 randomized treatments:

(0mL)

(5mL)

(10mL)

(20mL)

• Tanks contained 2L of sediment and n=12/treatment

• In tanks containing oil, a layer was buried ~3cm deep before planting

Growth

Root Characteristics

Fruiting Bodies

Flowers

Reproduction

1. Growth (proportional change in weight, number of shoots)

Number of Shoots

Ch

an

ge/d

ay (

+1S

E)

0.00

0.05

0.10

0.15

0.20

0.25

0.30

None Low Medium High

p=0.737

Wet Weight

0.00

0.02

0.04

0.06

0.08

0.10

None Low Medium High

Ch

an

ge

/da

y (

+1

SE

)

p=0.494

1. Growth

2. Reproduction (proportional change in number of flowers, fruits)

Fruiting Bodies

Flowers

Fruiting Bodies

Flowers

Fruit

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

None Low Medium High

Ch

an

ge/d

ay (

+1S

E)

p=0.015A

A,B

BB

2. ReproductionFlowers

0.0

0.1

0.2

0.3

0.4

0.5

None Low Medium High

Ch

an

ge/d

ay (

+1S

E)

p=0.008

A,B

A

A,B

B

3. Root Characteristics (mass, length, diameter, area, uprooting strength)

Root Length

Le

ng

th (

mm

+1S

E)

0

20

40

60

80

100

120

None Low Med High

p=0.05A

A,B

A,B

B

Root Mass

Ma

ss (

mg

+1S

E)

0

2

4

6

8

None Low Medium High

p=0.686 Root Area

Are

a (

mm

2+

1S

E)

0.00

0.05

0.10

0.15

0.20

None Low Medium High

p=0.015

A

A,B

A,B

B

Root Diameter

Dia

mete

r (m

m+

1S

E)

0.0

0.1

0.2

0.3

0.4

0.5

None Low Medium High

p=0.021

A

A,B

A,B

B

NO OIL HIGH OIL

Uprooting Strength

Gra

ms o

f F

orc

e (

+1S

E)

0

50

100

150

200

250

None Low Medium High

A

A

B

B

p<0.001

Silliman et al. 2012

Turner et al. 2016

C:N Ratio

Treatment

C:N

Ra

tio

(+

1S

E)

20

22

24

26

28

30

None Low Medium High

A

A,B

A,B

B

p= 0.006Citation Plant Herbivore

Kraft & Denno 1982 Shrub Insects

Coley 1983 Terrestrial trees Insects

Schroeder 1983 Terrestrial tree Insects

Onuf et al. 1977 Mangroves Insects

Lilly 1975Various marine plants

Urchins

Bjorndal 1980 Seagrass Green turtle

Zieman et al. 1984 Seagrass Green turtle

Williams 1988 Seagrass Green turtle

McGlathery 1995 Seagrass Fishes

Preen 1995 Seagrass Dugong

Valentine & Heck 2001 Seagrass Urchins

Goecker et al. 2005 Seagrass Fishes

Oil Exposure = Lower C:N!

The link between C:N and Herbivory

Herbivores preferplants with highnitrogen content

• Laboratory herbivory assays

• Leaf tissue imbedded in agar matrix (Hay et al. 1984, Valentine & Heck 2001, Goecker et al. 2005, Prado & Heck 2011)

• Herbivores:• Grass shrimp (x5)

(Paleomonetes pugio)

• Amphipods (x10)(Gammarus mucronatus)

Experiment 1

Paired Choice Experiment

Experiment 2

Foraging Rate Experiment

Nonevs

Low

Nonevs

Medium

Nonevs

High

Lowvs

Medium

Lowvs

High

Mediumvs

High

None

Low

Medium

High

0.0

0.1

0.2

0.3

0.4

0.5

None Low

0.0

0.1

0.2

0.3

0.4

0.5

None Medium

-0.1

0.0

0.1

0.2

0.3

0.4

0.5

None High

-0.1

0.0

0.1

0.2

0.3

0.4

0.5

Low Medium

0.0

0.1

0.2

0.3

0.4

0.5

Low High

0.0

0.1

0.2

0.3

0.4

0.5

Medium High

Pro

po

rtio

n L

oss * *

**

p=0.19 p=0.49

p=0.04 p<0.01

p<0.01 p<0.01Treatment

Pro

po

rtio

n L

oss

0.00

0.05

0.10

0.15

0.20 A A

BB

None Low Medium High

p<0.01

All Comparisons n=12

Treatment

0.00

0.02

0.04

0.06

0.08

0.10

A

A

A

A

None Low Medium High

Experiment 1

Paired Choice Experiment

Experiment 2

Foraging Rate Experiment

-0.02

0.00

0.02

0.04

0.06

0.08

0.10

0.12

None Low

-0.02

0.00

0.02

0.04

0.06

0.08

0.10

0.12

None Medium

-0.02

0.00

0.02

0.04

0.06

0.08

0.10

0.12

None High

-0.02

0.00

0.02

0.04

0.06

0.08

0.10

0.12

Low Medium

-0.02

0.00

0.02

0.04

0.06

0.08

0.10

0.12

Low High

-0.02

0.00

0.02

0.04

0.06

0.08

0.10

0.12

Medium High

Pro

po

rtio

n L

oss

p=0.074 p=0.79

p=0.017

p=0.03p=0.012

p=0.071

p=0.0724 Hours

Treatment

0.00

0.02

0.04

0.06

0.08

0.10

0.12

A

B B B

None Low Medium High

p=0.01

48 Hours

*

**

All Comparisons n=12

+- no effect

Variable effects of DWH on populations

Small fish Large fishInsects

McCall & Pennings 2012 Able et al. 2015 Fodrie & Heck 2011

Food Web Resilience to Oil

McCann et al. 2017. Frontiers in Ecology and the Environment. 15(3): 142-149.

Food Web Resilience to OilLiterature Synthesis

McCann et al. 2017. Frontiers in Ecology and the Environment. 15(3): 142-149.

Extirpation of most sensitive nodes

oil

Unoiled Oiled

51 # Nodes 39

343 # Links 210

6.72 Link density 5.38

0.13 Connectance 0.14

oil

Extirpation of most sensitive nodes

1. What are the effects of oil on Ruppia maritima?

2. Are there food web implications from this oil exposure?

Reduced flowering, changes to root morphology, decreased uprooting force

Martin, C.W., L.C. Hollis, R.E. Turner. 2015. Effects of oil-contaminated sediments on submerged vegetation: an experimental assessment of Ruppia maritima. PLoS ONE 10(10): e0138797.

Martin, C.W., E.M Swenson. 2018. Herbivory of submerged aquatic vegetation Ruppia maritima. PLoS ONE 13(12): e0208463.

Because of changes to plant chemical composition, foraging trends were altered

• Funding: – This research was made possible in part by a grant from The Gulf of

Mexico Research Initiative. Data are publicly available through the

Gulf of Mexico Research Initiative Information & Data Cooperative

(GRIIDC) at https://data.gulfresearchinitiative.org.

– Northern Gulf Institute. The funders had no role in the design,

execution, or analyses of this project.

• Louisiana: G. Turner, K. Able, J. Fodrie, O. Jensen, P.

Lopez-Duarte, M. McCann, K. Oken, J. Olin, M. Polito, B.

Roberts, N. Rabalais, E. Swenson, J. Lee, C. Milan, G.

Peterson, R. Shaw

• Alabama: J. Valentine, K. Heck, S. Powers, S. Alford, K.

Blankenhorn, T. Kauffman, L. Steele, R. Puntila, S.

Sklenar, S. Madsen, M. Dueker, L. Lee

Acknowledgements

Questions?Email: charles.martin@ufl.edu

Fis

h p

red

ato

rs

Mars

h f

ish

Ma

rsh

Pla

nts

Pla

nk

tivo

res

Zo

op

lan

kto

nP

hyto

pla

nk

ton

Inve

rts

Alter food web structure & resilience

Food w

eb im

port

ance

Oil sensitivity2017. Frontiers in Ecology and the Environment. 15(3): 142-149.

Food w

eb im

port

ance

Critically

sensitive

species

Critical

for

resilience

Few

indirect

effects

Oil sensitivity2017. Frontiers in Ecology and the Environment. 15(3): 142-149.

Oil sensitivityF

oo

d w

eb

im

po

rta

nce

Literature Synthesis

Critically

sensitive

species

Critical

for

resilience

Few indirect

effects

2017. Frontiers in Ecology and the Environment. 15(3): 142-149.

Ecological

Network

Analysis

Oil sensitivityF

oo

d w

eb

im

po

rta

nce

1 0 1 0 1 1 0 1

0 0 0 0 0 1 1 1

0 1 0 0 0 0 0 0

0 0 0 1 0 0 0 1

0 0 0 0 0 1 0 0

0 1 0 0 0 0 0 0

0 1 0 0 0 0 0 0

0 0 0 0 0 0 0 0

Diet Matrix

Literature Synthesis

Critically

sensitive

species

Few indirect

effects

Critical

for

resilience

2017. Frontiers in Ecology and the Environment. 15(3): 142-149.

Ecological

Network

Analysis

Oil sensitivityF

oo

d w

eb

im

po

rta

nce

1 0 1 0 1 1 0 1

0 0 0 0 0 1 1 1

0 1 0 0 0 0 0 0

0 0 0 1 0 0 0 1

0 0 0 0 0 1 0 0

0 1 0 0 0 0 0 0

0 1 0 0 0 0 0 0

0 0 0 0 0 0 0 0

Taxa Oil Sensitivity

Diet Matrix

Oil Sensitivity Data

Literature Synthesis

Critically

sensitive

species

Few indirect

effects

Critical

for

resilience

2017. Frontiers in Ecology and the Environment. 15(3): 142-149.

52 nodes376 links

Phytoplankton

Spartina alterniflora

Omnivorous snailsLittoraria irrorata

Piscivorous fish

No data (13)

0: none (16)

1: weak (10)

2: strong (12)

Oil Sensitivity

Food w

eb im

port

ance

Critically

sensitive

species

Critical

for

resilience

Few

indirect

effects

Oil sensitivity2017. Frontiers in Ecology and the Environment. 15(3): 142-149.

2017. Frontiers in Ecology and the Environment. 15(3): 142-149.

• Biomarker approach to food web effects• Bulk Stable Isotopes

• Fatty Acids

• Compound specific isotopes

Food Web Resilience to Oil

• Biomarker approach to food web effects• Bulk Stable Isotopes

• Fatty Acids

• Compound specific isotopes

Food Web Resilience to Oil

Fish Stomach Contents

• Biomarker approach to food web effects• Bulk Stable Isotopes

• Fatty Acids

• Compound specific isotopes

Food Web Resilience to Oil

Terrestrial plants are the primary carbon source for most terrestrial arthropods

Estuarine inverts mostly derive carbon from algae