Impacts of Withering Syndrome on Abalone Culture and Fisheries

in California, USA

Jim MooreBodega Marine Laboratory

California Department of Fish & GameSchool of Veterinary MedicineUniversity of California, Davis

Tom McCormick

Outline

Abalone commercial fisheries

Withering syndrome

Biology and distribution of X. californiensis

Impact of WS on each abalone species

Reasons for a hopeful future

California Abalone Eco-Zones

North Coast

Red Abalone

Recreational Breath-hold Fishery

Central Coast

Red Abalone

Sea Otters & WS

South Coast & Channel Islands

5 Commercial Species

Highly Depleted- Overfishing & WS

Commercial Abalone Fisheries 1940s-present

Central mainland, then Channel Islands

Red, pink, green, black, white

1993: Black fishery closed

1996: All fisheries closed

2005: Abalone Recovery & Management Plan

• Density requirements to

re-open fisheries

California Commercial Abalone Fishery

Metric Dollars

Tons per Kg

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42 45 48 51 54 57 60 63 66 69 72 75 78 81 84 87 90 93 96

$0

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$251995 US $

1950s-1970 Abalone landings appeared stable.

But…

fishery moved through accessible sites and high

value species to more distant sites and less

valuable species.

Slide provided by Ian Taniguchi, CDFG

Serial Depletion by Species

Slide provided by Ian Taniguchi

Pink

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YEAR

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Serial Depletion by Species

Slide provided by Ian Taniguchi

Pink

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Withering Syndrome

Spread of WS agent in California

*1985-86

Mid-90s

Mid-90s

1997

19992007 Farallones

2010 Bodega Head

Withering Syndrome

Inactive, weak, shrunken animals

Foot muscle catabolism, digestive gland pathologic changes

All North American abalone species susceptible to infection, but impacts vary

Expression of disease signs is dependent upon temperature

Significant impact on abalone fisheries and aquaculture in California

Caused by a bacterium: Rickettsiales-like prokaryote, WS-RLP, Xenohaliotis californiensis

Haliotis cracherodii (wild, Channel Islands) Haliotis rufescens (farmed)

Xenohaliotis californiensis (WS-RLP)

Order Rickettsiales, Family Rickettsiaceae

Gram-negative, obligate intracellular bacterium

forming inclusions in gastrointestinal epithelium

Transmission likely fecal-oral

Not culturable on media or available cell lines

Broad Haliotis spp. host range

Friedman et al. 2000. Int. J. Systematic and Evol. Microbiol. 50:847-855.

Moore et al. 2001. Journal of Shellfish Research 20:867-874.

Broad Haliotis Host Species Range

Species Español English

Susceptible to

X. californiensis

infection

H. corrugata Amarillo Pink Yes

H. fulgens Azul Green Yes

H. cracherodii Negro Black Yes

H. rufescens Rojo Red Yes

H. sorenseni Chino White Yes

H. kamtschatkana assimilis Threaded Yes

H. kamtschatkana Pinto Yes

H. discus hannai (Ezo) (Ezo) Yes

H. tuberculata European/ormer Yes

H. diversicolor supertexta Taiwan/Variously colored Yes

Infections not observed in California limpets and other gastropods

co-cultured with infected abalone

96

100

100

71

80

100

100

78

99

98

100

90

Ehrlichia phagocytophila

Ehrlichia bovis

Cowdria ruminantium

Anaplasma marginale

Wolbachia pipientis

Xenohaliotis californiensis

Ehrlichia risticii

Ehrlichia sennetsu

Rickettsia rickettsii

Rickettsia prowazekii

Necrotizing hepatopancreatitus prokaryote (shrimp)

Caedibacter caryophila

Coxiella burnetti

Piscirickettsia salmonis (salmonids)

Escherichia coli

16S rDNA sequence

Healthy Withering Syndrome

Healthy Withering Syndrome

Healthy Withering Syndrome

Detection of X. californiensis

Tissue Histology Tissue PCR Feces PCR

Red Abalone

Present statewide, abundant in North

Highly depleted in South except San Miguel

Island

Economically most important species:

Basis for recreational fishery

Primary species farmed

Proposed experimental commercial fishery

at San Miguel Island

Proposed San Miguel Island Red Abalone Experimental Fishery

Abundant red abalone (due to thermal refuge from WS)

San Miguel Island Fishery Consideration Process

Fishers participate in resource assessment

before and during fishery

Advisory committee includes

fishers, scientists, regulators

Process is stalled since 2010 pending

quantitative risk assessment analysis for

various proposed catch levels (four

management options)

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0 5 10 15 20 25 30 35Weeks post-initiation

Cu

mu

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ve m

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ali

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%)

18.5°C

14.7 C

Thermal Induction of WS in Farmed Red Abalone

Moore et al. 2000. Journal of Aquatic Animal Health 12:26-34.

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ELN 16.5 CLAN 13.8 CAMB 11.4 C

San Miguel Island Wild Red Abalone El Niño Simulation

BML Ambient SMI 98-99 La Niña SMI 97-98 El Niño+1 C

AMB LAN ELN

San Miguel Island Wild Red Abalone El Niño Simulation

San Miguel Island Wild Red Abalone El Niño Simulation

Very strong El Niño event expected to result in significant WS outbreak & population reduction

Realistic temperature profiles show more subtle effects than previous lab studies

Data useful for fishery risk assessment modeling

Moore et al. 2011. Journal of Aquatic Animal Health 23:78-84.

Monterey Bay

Cayucos

Santa Barbara

Carlsbad Lagoon

Half Moon Bay

Davenport

•Seven farms

•Four: raceways on land

•Three: in-sea barrels or cages

•Red abalone H. rufescens

•Fed Macrocystis pyrifera

•All present in WS endemic zone

•Severe WS impacts during 1997-1998 El Niño

•Variable seasonal losses

•Shift to domestic markets

California Abalone Farms 2012

CA Farmed Abalone Production

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Pounds/1000 Value/1M

Management of WS at Abalone Farms

Cooler (deeper) intake water

Selective breeding

Shorter culture period

El Niño/La Niña forecast

No large El Niño since 1997-98 (14 years)

Oxytetracycline in artificial feed

Bacteriophage?

12

34

56

Terramycin (OTC)

Control

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REPLICATE

Efficacy of a Single Oxytetracycline Treatment on WS-related Mortality at a Red Abalone Farm

Friedman et al. 2003. Aquaculture 224:1-23.

Biomass Yield Following a Single Treatment with Oxytetracycline

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Friedman et al. 2003. Aquaculture 224:1-23.

Oxytetracycline Bath

•500ppm

•24hrs bath, 24hrs rest x 4

•Rest one week, repeat

Recreational Abalone Fishery ~1940s-present

Red abalone H. rufescens

North of San Francisco Bay

Breath-hold (snorkle) only

7” (177mm) minimum

Current limits 3/day, 24/year

$ 44.85 license + $21.34 tag

Recent Catch History

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Catch Participants

Spread of X. californiensis in California

*1985-86

Mid-90s

Mid-90s

1997

19992007

Farallones

2010 Bodega Head

X. californiensis infection has no effect on red abalone in cold water

0.00

0.05

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SMI

Neg

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Pos

Fara 1

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Location and Infection Status

Co

nd

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x, g

m/c

m3

2011 Sonoma County Algal Bloom-associated Red Abalone Mortality

Jason Herum

N. Buck

White AbaloneHaliotis sorenseni

Pt. Conception to S. Baja California

Unique deepwater habitat, ~20-65m

Highly overfished

Federal (USA) listed as ‘endangered’ in 2001

Federal recovery plan in place

Susceptible to WS in lab studies- similar to red abalone

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^

All abalone

White abalone

White Abalone Recovery Activities 2000-2008

CIMRI (Tom McCormick) facility in Oxnard

Wild broodstock collected 2000, 2003

Several spawnings

Research on

diet, temperature, disease, reproduction, behavior

Animals succumb to WS, shell lesions

White Abalone Recovery Activities 2008 Onward

Bodega Marine Laboratory

2008: Center of recovery effort

2012: First successful spawn

Future

Collect additional broodstock

• At-risk individuals in shallow water

• Deep water solitary individuals

Spawn, outplant all life stages, monitor

Green Abalone H. fulgensand Pink Abalone H. corrugata

Pt. Conception to southern Baja California

Fisheries closed in 1996

Numbers appear to be increasing without intervention- La Jolla, Catalina

Green abalone: Susceptible to WS only at high temperatures

WS may not be a significant cause of decline or barrier to recovery in southern California

Moore et al. 2009 Marine Biology 156:2325-2330.

Vilchis et al. 2005 Ecological Applications 15:469-480

Black Abalone H. cracherodii

1985: WS discovered

1990s: Populations collapse;

WS spreads throughout

species range

1993: Fishery closed

2009: Federal ESA listed

2010s- Evidence for WS

resistance seen at some

Channel Islands

G. VanBlaricom

Wikipedia

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an

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C. Harrold

Black abalone counts by year and site, 1981-2011

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10Slide compliments of Glenn VanBlaricom

*

*

Slide compliments of

Carolyn Friedman

ISH showing binding of WS-RLP probe with both WS-RLP and New-RLP

Slide compliments of Carolyn Friedman

3,150x

TEM Suggests New-RLP is WS-RLP Infected

with Phage Hyperparasite

157,500x3,150x

WS-RLO

New RLPPhage hyperparasites in

New RLP

Slide compliments of Carolyn Friedman

Future of Farms and Fisheries-Reasons for Hope

Recent signs of recovery of green, pink abalone-result of reduced fishing pressure

White abalone rapidly becoming extinct, but recovery actions are being implemented

Recent signs of recovery of black abalone-possible result of genetic selection for WS resistance

Bacteriophage may diminish pathogenicity of X. californiensis in wild and farmed abalone

Acknowledgements

Carolyn Friedman, University of Washington

Glenn VanBlaricom, University of Washington

Ian Taniguchi, California Dept. Fish & Game

David Kuschner, Channel Islands Nat’l Park