6 j moore ensenada2012
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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
0
500
1,000
1,500
2,000
2,500
42 45 48 51 54 57 60 63 66 69 72 75 78 81 84 87 90 93 96
$0
$5
$10
$15
$20
$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
0
500
1,000
1,500
Green
0
500
1,000
Black
0
500
1,000
White
0
100
42 45 48 51 54 57 60 63 66 69 72 75 78 81 84 87 90 93 96
YEAR
Red
0
500
1,000
1,500
A B C D
Serial Depletion by Species
Slide provided by Ian Taniguchi
Pink
0
500
1,000
1,500
Green
0
500
1,000
Black
0
500
1,000
White
0
100
42 45 48 51 54 57 60 63 66 69 72 75 78 81 84 87 90 93 96
YEAR
Red
0
500
1,000
1,500
A B C D
WS
0
500
1000
1500
2000
2500
1984 1986 1988 1990 1992 1994
# b
lack a
balo
ne i
n
fixed
plo
ts
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)
0
5
10
15
20
25
30
35
0 5 10 15 20 25 30 35Weeks post-initiation
Cu
mu
lati
ve m
ort
ali
ty (
%)
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.
8
10
12
14
16
18
20
0 50 100 150 200 250 300
Day of Experiment
Tem
pe
ratu
re
C
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
0
100
200
300
400
500
6001
99
1
19
92
19
93
19
94
19
95
19
96
19
97
19
98
19
99
20
00
20
01
20
02
20
03
20
04
20
05
20
06
20
07
20
08
Pro
du
ctio
n (
10
00
po
un
ds)
$0
$1
$2
$3
$4
$5
$6
$7
$8
$9
$10
Va
lue
(m
illio
n $
)
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
0
5
10
15
20
25
30
35
40
45
MO
RTA
LIT
Y (
%)
OV
ER
10
.6 M
ON
TH
S
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
8
10
12
14
16
18
20
A S O N D J F M A M J J
Untreated
BIO
MA
SS
(kg
)
Terramycin
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
0
50,000
100,000
150,000
200,000
250,000
300,000
350,000
2002 2003 2004 2005 2006 2007 2008 2009 2010
Catc
h (
# a
balo
ne)
0
5,000
10,000
15,000
20,000
25,000
30,000
35,000
40,000
45,000
# P
art
icip
ants
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
0.10
0.15
0.20
0.25
SMI
Neg
SMI
Pos
Fara 1
Neg
Fara 1
Pos
Fara 2
Neg
Fara 2
Pos
Bodega
Neg
Bodega
Pos
Location and Infection Status
Co
nd
itio
n In
de
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
0
1,000,000
2,000,000
3,000,000
4,000,000
5,000,000
6,000,000
1940 1950 1960 1970 1980 1990 2000
Year
Com
merc
ial la
ndin
gs
(pounds)
0
50,000
100,000
150,000
200,000
1940 1950 1960 1970 1980 1990 2000
Year
Com
merc
ial la
ndin
gs
(pounds)
^
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
1
2
3
45
67
8
9
G. V
an
Bla
rico
m
45
C. Harrold
Black abalone counts by year and site, 1981-2011
0
5000
10000
15000
20000
25000
30000
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31
Tota
l ab
alo
ne
co
un
ts b
y si
te
1981 1991 2001 2011
46
0
200
400
600
800
1000
1200
1 2 3 4 5 6 7 8 9 10 11
Tota
l ab
alo
ne
co
un
ts b
y si
te
2001 2003 2005 2007 2009 2011
8
7
8
7
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
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