1. Gary D. Marty 1, Peter-John F. Hulson 2, Sara E. Miller 2, Terrance J. Quinn II 2, Steve D. Moffitt 3, Richard A. Merizon 3 1 School of Veterinary Medicine, University of California, Davis, CA, 2 Juneau Center, School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Juneau AK 3 Alaska Department of Fish and Game, Cordova AK Acknowledgments: NSF, EVOS Trustees, ADF&G Failure of Population Recovery in Relation to Disease for Pacific Herring in Prince William Sound

2. Recent history Population crashed in 1993, 4 years after the EVOS. Brief population increase: fishery reopened in 1997. Spawning population declined below threshold (20,000 mt) in 1999, fishery closed since then. Disease prevalence has been collected in Prince William Sound since 1994. mesomycetozoean Ichthyophonus hoferi (fungus-like) viral hemorrhagic septicemia virus (VHSV) Filamentous-bacteria (FB, ulcers)

3. Publications Quinn et al. 2001, data through 1998; VHSV Marty et al. 2003, data through 2000; VHSV+FB Hulson et al. 2008, data through 2004; added hydroacoustic data, concentrated on decline in early 1990’s Marty et al., in review, data through 2006; this presentation, new conclusion

4. Objectives 1.With more recent information, to see how natural mortality M is related to disease prevalence information on VHSV, FB, and Ichthyophonus, using an age-structured model. 2.To see if recruitment (age 3) is related to disease information.

5. Model Details  Estimated parameters: Recruitment and starting abundance, maturity, seine selectivity, milt calibration coefficient, hydroacoustic calibration coefficient, disease coefficients  Data: weight-at-age, seine age composition and total catch, other fisheries’ catch-at-age, spawning age composition, egg survey biomass, acoustic survey biomass, mile-days of milt, disease indices (covariates)  Natural mortality from non-disease M 0 = 0.25.  Objective function: minimize weighted sums of squares of the seine, spawning, egg survey, acoustic survey, and milt information

6. Model extension for disease Let natural mortality be a linear function of disease prevalence: Total natural mortality M = M 0 +   x i t, in which: M 0 = natural mortality from other sources, treated as a constant, x i t = ith disease prevalence index, year t   = ith disease coefficient

7. Prevalence Higher for younger ages; Outbreaks in 1994 and 1998 Higher for older ages Higher since 2001

8. Model Scenarios Base: M = 0.25 in all years Base: M = 0.25 in all years Disease: Combinations of one or both disease sources affecting one or both age groups (3-4, 5-8) after 1993 Disease: Combinations of one or both disease sources affecting one or both age groups (3-4, 5-8) after 1993 30 scenarios in all 30 scenarios in all Model selection based on AICc Model selection based on AICc Base model was much worse than all the others Base model was much worse than all the others Best model: VHSV+FB affecting ages 3-4; I. hoferi affecting all ages. Best model: VHSV+FB affecting ages 3-4; I. hoferi affecting all ages.

9. Spawning Biomass

10. Recruitment

11. Correlations of log recruitment Ages 3 – 4Ages 5+Pooled ages VHSV +FB I. hoferi VHSV +FB I. hoferi VHSV +FBI. hoferi Correlation (no lag) 0.22-0.260.41-0.210.37-0.64 P- value 0.460.390.170.490.210.02 Correlation (lag 1) 0.100.15-0.14-0.24-0.20-0.06 P- value 0.770.650.660.45 0.530.85

12. Estimated Natural Mortality White: Background Orange: 1993 Red: VHSV+FB Yellow: I. hoferi Ages 5-8 Ages 3-4

13. What If?

14. Summary Disease information is relevant and necessary in population modeling and assessment of PWS herring. Spawning biomass has not recovered after the crash of 1992-1993. Recruitment has been somewhat below normal since 1992. VHSV+FB affects younger herring (ages 3-4). High VHSV+FB prevalence in 1992-1993 and 1997-1998 appears to have increased herring mortality. ) I. hoferi affects both younger and older herring (ages 3+). It appears to have increased herring mortality continually after 2000. Neither disease is strongly correlated with recruitment.

15. Why the continued failure? Things are not now well with herring in PWS. Things are not now well with herring in PWS. Disease continues to be a major factor. Disease continues to be a major factor. Low recruitment is less important. Low recruitment is less important. Other factors may be playing a role Other factors may be playing a role Steller sea lion predation (Thorne and Thomas 2008) Steller sea lion predation (Thorne and Thomas 2008) Winter whale predation (Heintz et al.: AMSS herring session) Winter whale predation (Heintz et al.: AMSS herring session) Hatchery salmon (Deriso et al. 2008) Hatchery salmon (Deriso et al. 2008)

16. Conclusions Unprecedented study: 13 years of disease information Unprecedented study: 13 years of disease information New insight: Disease may have continual effects on a population over a long-time period, rather than just an outbreak. New insight: Disease may have continual effects on a population over a long-time period, rather than just an outbreak. Thus a new population phenomenon: the “disease regime” hypothesis. Thus a new population phenomenon: the “disease regime” hypothesis. Natural mortality may vary significantly over time for many fish populations. Natural mortality may vary significantly over time for many fish populations. Covariate information (disease, predation) will become increasingly necessary for confident stock assessment. Covariate information (disease, predation) will become increasingly necessary for confident stock assessment.

17. Extra slides not presented

18. Research needs for modeling Continued collection of disease information Development of time series of predation on herring by birds, fish, mammals Analyses of herring recruitment in relation to environmental variables Analyses comparing PWS herring with other populations Additional data collection and analyses of adult and juvenile herring (acoustics) in space and by season (fish movement) Studies on early life history of herring in PWS Relationship between growth and disease (are herring in poor condition?)

19. Sample size and Weighting Sample Size Weighting Seine AC 881 Ricker240.03 Spawning AC 1721 Hyd120.5 Egg100.5 Mile-days270.5 Total333