west side story the context, causes, and consequences of the pacific oyster introduction to...

West Side Story the context, causes, and consequences of the Pacific oyster introduction to Washington State

Jennifer Ruesink

University of Washington

• Context– Ruesink, Lenihan, Trimble, Heiman, Micheli, Byers, Kay. 2005.

Introduction of non-native oysters: ecosystem effects and restoration implications. Annu Rev Ecol Evol Syst 36:643-689

• Causes– White, Ruesink, Trimble. History and management of native oysters

(Ostrea conchaphila) in Washington State. In preparation for special issue of J Shellfish Res

• Consequences– Ruesink, Feist, Harvey, Hong, Trimble, Wisehart. 2006. Changes in

productivity associated with four introduced species: Ecosystem transformation of a “pristine” estuary. Mar Ecol Prog Ser 311:203-215

– Trimble, Ruesink, Dumbauld. Factors preventing recovery of a historically overexploited shellfish species. In preparation.

Outline

Context

• Oyster introductions have occurred frequently

• High establishment rate

• Vector for numerous other species

• Nearly complete replacement of native oyster production

Compilation of oyster introductions

• Introduction = movement of species from one country/ region to another where it was not previously present

• Sources = UN FAO, several earlier reviews (Eldredge 1994, NRC 2004), published papers, personal communications

• Number of introductions = _____• Number of recipient locations = ____• Number of species = ____

Compilation of oyster introductions

• Introduction = movement of species from one country/ region to another where it was not previously present

• Sources = UN FAO, several earlier reviews (Eldredge 1994, NRC 2004), published papers, personal communications

• Number of introductions = _164_• Number of recipient locations = _73_• Number of species = _16_

When did oyster introductions occur?

0

20

40

60

80

100

120

1850 1870 1890 1910 1930 1950 1970 1990 2010

Cumulative number of transfers

Charles Elton fingered oyster introductions as the “greatest agency of all that spreads marine animals to new corners of the world”

Where have oysters been introduced?

18

61

6

19

9

6

41

3

4

Which oyster species have been introduced?

O’Foighil & Taylor 2000 Molecular Phylogenetics & Evolution 15:301

C. virginica = 16C. rhizophorae = 3

C. gigas = 64 + 6C. ariakensis = 3S. commercialis = 6S. cucullata = 3

O. edulis = 11

T. chilensis = 3C. densalamellosa = 1

O. conchaphila = 1O. puelchana = 1

C. echinata = 5C. sikamea = 3

C. iredalei = 2C. belcheri = 1

C. cortezensis = 1

How well did they do?

0

10

20

30

40

50

60

70

C. gigasC. virginica

O. edulisC. angulata

S. commercialis

C. echinataC. ariakensisC. rhizophoraeC. sikameaS. cucullataT. chilensis

Frequency of locations

Unknown

Failed

Established

Why were new oysters introduced?

• Replace native species

• Begin new product (Pacific islands)

• Research (12)

• Range expansion (4)

• By-product (3)

Introduced oysters have replaced native oyster production

Africa W USA E USA CanadaS AmericaAustralia/NZEurope

Asia

10-year production 1993-2002(metric tons shucked)

0

1e+6

2e+6

3e+7

Introduced Native Uncertain

Introduced oysters have

vectored many other

species

Context

• Oyster introductions have occurred frequently• High establishment rate• Vector for numerous other species• Nearly complete replacement of native oyster production

However, ecological impacts of introduced oysters are poorly studied:•To what extent do introduced oysters replace “ecosystem function”?•Is recovery of native oysters improved or impaired?

Causes

• Why were Pacific oysters (Crassostrea gigas) introduced to Washington State?– Harvesting native oysters was no longer

economical… but therein lies a story

VANCOUVER

SEATTLE

PORTLAND

Willapa Bay

Puget Sound

Native oyster

Baker 1995

Ostreola conchaphila (Carpenter, 1857)

•Historic Range: Sitka, AK to Mexico

•Maximum 6 cm

•Protandrous Hermaphrodite

•Brooding Females: ~250,000 larvae/adult

•Spawning above 12C for 3+ months/yr.

•Subtidal accumulations of shell

The way it used to be? Willapa Bay at low water, late 1800s

Willapa Bay – current population between 0 and -2’ MLLW is sparse in eelgrass

North Bay, Puget Sound – ~25 million oysters between 0 and -4’, newly recovered

Washington Ostreola conchaphila Harvest

0.0E+00

2.0E+04

4.0E+04

6.0E+04

8.0E+04

1.0E+05

1.2E+05

1.4E+05

1850 1860 1870 1880 1890 1900 1910 1920 1930 1940 1950 1960

Sacks

Willapa Bay

Puget Sound

Trimble, unpubl.

1840 1850 1860 1870 1880 1890 1900 1910

White population exploiting oysters0

50

100

150

200

250

Price $/basket

0

5

10

15

20

25

30

35

White fishers Price/basket

Willapa Bay timeline

1840 1850 1860 1870 1880 1890 1900 1910

White population exploiting oysters0

50

100

150

200

250

Price $/basket

0

5

10

15

20

25

30

35

White fishers Price/basket

First harvest restrictions

1840 1850 1860 1870 1880 1890 1900 1910

White population exploiting oysters0

50

100

150

200

250

Price $/basket

0

5

10

15

20

25

30

35

White fishers Price/basket

Native oysters described scientifically

1840 1850 1860 1870 1880 1890 1900 1910

White population exploiting oysters0

50

100

150

200

250

Price $/basket

0

5

10

15

20

25

30

35

White fishers Price/basket

Tideflat privatization

1840 1850 1860 1870 1880 1890 1900 1910

White population exploiting oysters0

50

100

150

200

250

Price $/basket

0

5

10

15

20

25

30

35

White fishers Price/basket

Marine Reserves

Collins, 1888

Oyster Reserves: •Legislated ~1900•Almost perfect overlap with original native oyster beds

1840 1850 1860 1870 1880 1890 1900 1910

White population exploiting oysters0

50

100

150

200

250

Price $/basket

0

5

10

15

20

25

30

35

White fishers Price/basket

C. virginica introductionSubsequent introductions:

C. gigas - establishedO. edulisC. sikameaC. ariakensis

Commercial interest shifted to Crassostrea gigas: Imports of spat to the west coast

1920 1930 1940 1950 1960 1970 1980

Cases

0

20000

40000

60000

80000

100000

120000

White, Ruesink, Trimble, unpubl.

Secondary production in Willapa Bay shifted from native to non-native shellfish (filtration too)

Ruesink, Feist, Harvey, Hong, Trimble, Wisehart. 2006. Mar Ecol Prog Ser

Research efforts also shifted

• Number of holdings in the University of Washington library referring to each species

• Scientific literature includes <15 modern papers on O. conchaphila – but this will soon change!

0

5

10

15

20

25

30

35

<1930 1930-60 1960-80

Publications

Native

Introduced

Has C. gigas functionally replaced O. conchaphila?

• Native oyster– Brooding– Slow growth– Subtidal– Loose shell

• New oyster– Broadcasting– Rapid growth– Intertidal– Reef-building

Consequences

• What are the ecological impacts of Pacific oysters (Crassostrea gigas)?– Interactions with native oysters – directly and

indirectly– Effects of shellfish and aquaculture practices

on sediment properties, eelgrass, epibiota, fish and crabs are the focus of targeted research funded in part by the shellfish industry

Potential Factors Limiting Population Recovery

- Reproductive Failure (no)

-----------------------

- Settlement Habitat Change (yes)

- Pollution and Sedimentation (yes)

- Competition (space- yes)

- Predation (yes)

- Disease (limited)

Middle Sands Reserve

Long Island Reserve

Spatfall onCinder Block Anchors

(-10m)

Native oyster recruitment

remains high

Quantitative recruitment time series

• Weekly records of spatfall from 1947-1987, 2002-2006

• Native oyster usually > Pacific oyster

0

10

20

30

40

50

60

70

80

90

100

1945 1965 1985 2005

Spat Per Shellface

1947-2006 Spatfall: O. conchaphila and C. gigas

O.conchaphilaC. gigas

But where do those larvae now settle?

What native oyster beds used to be… maybe… perhaps?

Settlement Habitat Change

C. gigas intertidal reefs

Settlement Habitat Change

Increased sedimentation from logging in watershed

Quantitative assessment of recruitment across habitats

Recruitment rate across habitatsOstreola conchaphila

Habitat

Shell Bare Eelgrass

Recruits per 10 shellfaces

0

50

100

150

200

250

300

Above MLLW Below MLLW

Mos

t av

aila

ble

habi

tat

2-factor experiment: 3 elevations, +/- competitors

Tiles on mooring

Day 0 (1 month old) Day 63 Day 304

MLLW

(- 30cm)

(+ 30cm)“HIGH”

“LOW”

“MOORING” (-1 m)

F8,112 = 2.8, P = 0.007

Survival declines when not submerged

Impacts of competitors

• Ectopleura crocea• Botryllus spp.• >45 introduced species

reported in Willapa Bay

Wonham & Carlton 2005 Biol Inv

F1,112 = 42.4, P < 0.001

Competitors Reduce Survival

F4,61 = 5.5, P = 0.001

Competitors Reduce Growth

Interactions between Washington’s native and non-native oysters

Recruitment “sink”:Intertidal aquacultureNaturalized intertidal reefs

Historical vector of non-native predators and competitors

Recruitment, but poor intertidal survival

-

Overgrowth?

High sustained recruitment indicates presence of core reproductive population

Bare Gravel Pacific shell

Crushed Pacific shell Native shell Live natives

May 2004

Recruitment improved at

lower elevations

and on natives

A

Elevation (m MLLW)

-0.6 -0.4 -0.2 0.0 0.2 0.4 0.6

Recruit density (number per 0.0125 m

2)

0

2

4

6

8

10

12

14

16

18

Total October live April live

B

Substrate type

O.c. live O.c. shell C.g. crushed C.g. shell Gravel Bare

Recruit density (number per 0.0125 m

2)

0

5

10

15

20

25

A

Rosette Bag Ground Shell

Count per shell

0

2

4

6

8

10

12

14

16

18

20

B

Density: Low High Low High Stable Unstable

Rosette Bag Ground Shell

Shell length (mm)

25

30

35

40

RogersNemahLong IslandMill Channel

Unstable treatments washed away at most sites

Stable treatments were heavily fouled at most sites

Rosettes – natives grew and survived

Rosettes – buried at other sites

Shell on ground – not a functional replacement for natives