IV SIMPOSIO DE SANIDAD E INOCUIDAD CESAIBC Ponencias 19 de Septiembre

1. Impacts of Withering Syndrome
on Abalone Culture and Fisheries
in California, USA
Jim Moore
Bodega Marine Laboratory
California Department of Fish & Game
School of Veterinary Medicine
University of California, Davis
Tom McCormick

2. Outline
 Abalone commercial fisheries
 Withering syndrome
 Biology and distribution of X. californiensis
 Impact of WS on each abalone species
 Reasons for a hopeful future

3. 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

4. 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

5. California Commercial Abalone Fishery
1950s-1970 Abalone landings appeared stable.
But…
fishery moved through accessible sites and high
value species to more distant sites and less
Metric valuable species. Dollars
Tons per Kg
2,500 $25
1995 US $
2,000 $20
1,500 $15
1,000 $10
500 $5
0 $0
42 45 48 51 54 57 60 63 66 69 72 75 78 81 84 87 90 93 96
Slide provided by Ian Taniguchi, CDFG

6. Serial Depletion by Species
A B C D
1,500
Red
1,000
500
0
1,500 Pink
1,000
500
0
1,000 Green
500
0
1,000 Black
500
0
100 White
0
42 45 48 51 54 57 60 63 66 69 72 75 78 81 84 87 90 93 96
Slide provided by Ian Taniguchi YEAR

7. Serial Depletion by Species
A B C D
1,500
Red
1,000
500
0
1,500 Pink
1,000
500
0
1,000 Green WS
500
0
1,000 Black
500
0
100 White
0
42 45 48 51 54 57 60 63 66 69 72 75 78 81 84 87 90 93 96
Slide provided by Ian Taniguchi YEAR

8. 2500
Withering
# black abalone in
2000
fixed plots
Syndrome 1500
1000
500
0
1984 1986 1988 1990 1992 1994

9. Spread of WS agent in California
2010 Bodega Head
2007 Farallones 1999
1997
Mid-90s
*1985-86
Mid-90s

10. 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

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

12. 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.

13. Broad Haliotis Host Species Range
Susceptible to
X. californiensis
Species Español English 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

14. 96 16S rDNA sequence
Ehrlichia phagocytophila
100
Ehrlichia bovis
100
Anaplasma marginale
71
Cowdria ruminantium
80 Wolbachia pipientis
Xenohaliotis californiensis
Ehrlichia risticii
100
Ehrlichia sennetsu
100 Rickettsia rickettsii
78
Rickettsia prowazekii
Necrotizing hepatopancreatitus prokaryote (shrimp)
99
Caedibacter caryophila
98
Coxiella burnetti
100
Piscirickettsia salmonis (salmonids)
90 Escherichia coli

15. Healthy Withering Syndrome

17. Healthy Withering Syndrome

18. Healthy Withering Syndrome

19. Detection of X. californiensis
Tissue Histology Tissue PCR Feces PCR

20. 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

21. Proposed San Miguel Island Red Abalone
Experimental Fishery
Abundant red abalone (due to thermal refuge from WS)

22. 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)

23. Thermal Induction of WS
in Farmed Red Abalone
35
Cumulative mortality (%)
18.5°C
30
25
20
15
10
5 14.7 C
0
0 5 10 15 20 25 30 35
Weeks post-initiation
Moore et al. 2000. Journal of Aquatic Animal Health 12:26-34.

24. San Miguel Island Wild Red Abalone
El Niño Simulation
BML Ambient SMI 98-99 La Niña SMI 97-98 El Niño+1 C
AMB 11.4 C LAN 13.8 C ELN 16.5 C
20
18
16
Temperature C
14
12
10
8
0 50 100 150 200 250 300
Day of Experiment

25. San Miguel Island Wild Red Abalone
El Niño Simulation
AMB LAN ELN

26. 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.

27. California Abalone Farms
2012
•Seven farms
•Four: raceways on land
•Three: in-sea barrels or cages
•Red abalone H. rufescens
Half Moon Bay
•Fed Macrocystis pyrifera Davenport
Monterey Bay
•All present in WS endemic zone
•Severe WS impacts during 1997-1998 El Niño Cayucos
•Variable seasonal losses Santa Barbara
•Shift to domestic markets
Carlsbad Lagoon

28. Production (1000 pounds)
100
200
300
500
600
400
0
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
Pounds/1000
2001
2002
2003
2004
2005
Value/1M
2006
2007
CA Farmed Abalone Production
2008
$0
$1
$2
$3
$4
$5
$6
$7
$8
$9
$10
Value (million $)

29. 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?

30. Efficacy of a Single Oxytetracycline Treatment
on WS-related Mortality at a Red Abalone Farm
MORTALITY (%) OVER 10.6 MONTHS
45
40
35
30
25
20
15
10
5
0
1 Control
2
3 Terramycin (OTC)
4
REPLICATE 5
6
Friedman et al. 2003. Aquaculture 224:1-23.

31. Biomass Yield Following a Single Treatment with
Oxytetracycline
20
18
Terramycin
16
BIOMASS (kg)
14
12
Untreated
10
8
A S O N D J F M A M J J
Friedman et al. 2003. Aquaculture 224:1-23.

32. Oxytetracycline Bath
•500ppm
•24hrs bath, 24hrs rest x 4
•Rest one week, repeat

33. 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

34. Recent Catch History
Catch Participants
350,000 45,000
40,000
300,000
35,000
Catch (# abalone)
250,000
30,000
# Participants
200,000 25,000
150,000 20,000
15,000
100,000
10,000
50,000
5,000
0 0
2002 2003 2004 2005 2006 2007 2008 2009 2010

35. Spread of X. californiensis in California
2010 Bodega Head
2007 1999
Farallones
1997
Mid-90s
*1985-86
Mid-90s

36. X. californiensis infection has no effect
on red abalone in cold water
0.25
Condition Index, gm/cm3
0.20
0.15
0.10
0.05
0.00 SMI SMI Fara 1 Fara 1 Fara 2 Fara 2 Bodega Bodega
Neg Pos Neg Pos Neg Pos Neg Pos
Location and Infection Status

37. 2011 Sonoma County Algal Bloom-
associated Red Abalone Mortality
Jason Herum
N. Buck

38. White Abalone
Haliotis 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

39. Commercial landings
6,000,000
All abalone
5,000,000
(pounds)
4,000,000
3,000,000
2,000,000
1,000,000
0 ^
1940 1950 1960 1970 1980 1990 2000
Year
Commercial landings
200,000
White abalone
150,000
(pounds)
100,000
50,000
0
1940 1950 1960 1970 1980 1990 2000
Year

40. 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

41. 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

42. Green Abalone H. fulgens
and 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

43. Black Abalone H. cracherodii
 1985: WS discovered
 1990s: Populations collapse;
WS spreads throughout
species range
 1993: Fishery closed
 2009: Federal ESA listed G. VanBlaricom
 2010s- Evidence for WS
resistance seen at some
Channel Islands

44. Wikipedia

45. 2
1
3
9
8
4
7 5
6
C. Harrold
G. VanBlaricom
45

46. Black abalone counts by year and site, 1981-2011
Total abalone counts by site
30000
25000
20000
8
15000
7
10000
5000
0
1981 2
1 3 4 5 6 7 8 9 101991 12 13 14 15 16 17 18 19 20 200122 23 24 25 26 27 28 29 30 2011
11 21 31
1200
Total abalone counts by site
1000
8
800
600
400
7
200
0
2001
1 2 2003
3 4 2005
5 6 2007
7 8 2009
9 10 2011
11
46
10
Slide compliments of Glenn VanBlaricom

47. *
*
Slide compliments of
Carolyn Friedman

48. ISH showing binding of WS-RLP probe with both WS-RLP
and New-RLP
Slide compliments of Carolyn Friedman

49. TEM Suggests New-RLP is WS-RLP Infected
with Phage Hyperparasite
Phage hyperparasites in
New RLP
New RLP
WS-RLO
3,150x 3,150x 157,500x
Slide compliments of Carolyn Friedman

50. 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

51. Acknowledgements
 Carolyn Friedman, University of Washington
 Glenn VanBlaricom, University of Washington
 Ian Taniguchi, California Dept. Fish & Game
 David Kuschner, Channel Islands Nat’l Park