Diet and trophic ecology of skates ( Raja and Bathyraja spp.) in the Gulf of Alaska

1. Diet and trophic ecology of skates (Raja and Bathyraja spp.) in the Gulf of Alaska Joseph J. Bizzarro, David A. Ebert, Simon C. Brown, Mariah D. Boyle and Gregor M. Cailliet Pacific Shark Research Center Moss Landing Marine Laboratories

2. Trophic Roles of Skates in Benthic Marine Communities Skates are common components of benthic marine communities in temperate and boreal regions (Compagno 1990). Skates consume a variety of prey taxa (e.g., polychaetes, molluscs, crustaceans, fishes), and typically occupy upper trophic levels (Ebert and Bizzarro 2007). Skates may serve as predators or competitors of groundfishes (Link and Garrison 2002; Bizzarro et al. 2007).

3. Feeding Ecology of Skates in the Gulf of Alaska: Knowledge and Need The biomass of skates in the Gulf of Alaska (GOA) appears to be increasing (Gaichas et al. 2003; Hoff 2006). There is no published food habit information on skates in the GOA. Only available data are from NMFS/AFSC reports (Yang et al. 2006; Yang 2007). Baseline, species-specific dietary information is necessary to determine the trophic roles of skates in the GOA - Development of effective, multi-species management plans - Potential impacts of exploitation and climate change on the GOA ecosystem

4. Skate Assemblage in the Gulf of Alaska Big skate (Raja binoculata) Longnose skate (Raja rhina) Aleutian skate (Bathyraja aleutica) Bering skate (Bathyraja interrupta)

5. Objectives • Determine the diets of big (Raja binoculata), longnose (R. rhina), Aleutian (Bathyraja aleutica), and Bering (B. interrupta) skates in the GOA through analysis of stomach contents • 2) Examine sources of variation in diet of each species • 3) Examine regional differences in dietary composition of big and longnose skate populations in the GOA and off central California • 4) Determine and compare trophic levels within and among species • 5) Compare interspecific diets of GOA skates to determine the degree of dietary overlap

6. C. Methods: Specimen and Sample Collection 2005 n = 237 2007 n = 1346 2006 n = 481

7. Methods: Data Collection and Analysis Data Collection Prey items identified to lowest possible taxon, weighed (0.01 g), and measured (0.1 mm) Cumulative Prey Curves Quantitative Evaluation – Regression (P > 0.05; Bizzarro et al. 2007) Dietary Indices (Single, Compound) %N, %M, %FO %IRI: %FO * (%N+%M) (Pinkas et al. 1971) %GII: (%N + %M)/21/2 (Assis 1996) Intra- and Interspecific Comparisons (%N, %M) 18 Generalized Prey Categories nmMDS – Variable Categories Permutation Tests (Manly 2007) PCA – Sources of Intraspecific Variation Cluster Analysis (UPGMA) Trophic Level Calculations (Cortes 1999; Ebert and Bizzarro 2007)

8. Results (Overall): Big skate General Dietary Information •128 of 130 contained prey items (98.5%) •68 Prey taxa identified • Trophic level = 3.67 + 0.24 •Sufficient sample size at general, but not LPT categories Dietary Composition •Crustaceans (crabs) were primary prey group (%IRI = 85.1 + 27.6) •Chionoecetes bairdi (%IRI = 62.3 + 41.3) • Crangon spp. (%IRI = 4.7 + 17.1) •Fishes (%IRI = 14.8 + 27.7; %FO = 48.4) Comparison to Literature In Alaskan waters, dietary information is limited to two specimens taken in the GOA (Yang et al. 2006) and two specimens from the Aleutian Islands (Yang 2007). Fishes and tanner crabs were the primary prey items found.

9. Results (Kodiak): Big skate %M n = 44 (2006) n = 30 (2007) Big skate dietary composition was similar between years using both %N (SIMobs = 0.639, P = 0.369) and %M (SIMobs = 0.669, P = 0.506).

10. Results (Regional): Big skate %M n = 128 n = 173 Big skate dietary composition from the GOA and off central California differed significantly by %N (SIMobs = 0.428, P = 0.005) and %M (SIMobs = 0.357, P = 0.000).Trophic level was significantly greater off CA (U = 7979.5, P < 0.001).

11. Results (Overall): Longnose skate General Dietary Information •253 of 258 contained prey items (98.1%) •68 Prey taxa identified • Trophic level = 3.68 + 0.28 •Sufficient sample size at general, but not LPT categories Dietary Composition •Crustaceans (shrimps) were primary prey group (%IRI = 82.0 + 32.2) •Crangon spp. (%IRI = 17.6 + 29.2) • Pandalus eous. (%IRI = 14.0 + 26.9) •Fishes (%IRI = 17.5 + 31.7; %FO = 46.6) Comparison to Literature In Alaskan waters, longnose skate dietary information is limited to three specimens taken in the GOA (Yang et al. 2006). Pandalid shrimps and tanner crabs dominated the diets of these specimens.

12. Results (Kodiak): Longnose skate %M n = 54 n = 94 Longnose skate dietary composition was similar between years using both %N (SIMobs = 0.639, P = 0.369) and %M (SIMobs = 0.669, P = 0.407).

13. %M n = 253 (GOA) n = 486 (CA) Results (Regional): Longnose skate Longnose skate dietary composition from the GOA and off central California differed significantly by %N (SIMobs = 0.567, P = 0.025) and %M (SIMobs = 0.411, P = 0.000).Trophic level was significantly greater off CA (U = 31,481.5, P < 0.001).

14. Results (Overall): Aleutian skate General Dietary Information •153 of 156 contained prey items (98.1%) •63 Prey taxa identified • Trophic level = 3.69 + 0.25 •Sufficient sample size at general, but not LPT categories Dietary Composition •Crustaceans (shrimps) were primary prey group (%IRI = 83.9 + 25.3) •Pandalus eous (%IRI = 34.2 + 36.4) • Chionoecetes bairdi. (%IRI = 19.9 + 29.9) •Fishes (%IRI = 13.9 + 23.6; %FO = 61.4) Comparison to Literature In Alaskan waters, dietary composition is limited to 24 specimens from the Aleutian Islands, which consumed primarily fishes, as well as crustaceans (e.g., pandalid shrimps) and, to a lesser extent, cephalopods.

15. Results (Kodiak): Aleutian skate %N n = 36 (2006) n = 60 (2007) Interannual dietary differences were evident for Aleutian skates by %N (SIMobs = 0.553, P = 0.003), but not by %M (SIMobs = 0.536, P = 0.393).

16. Results (Overall): Bering skate General Dietary Information •195 of 199 contained prey items (98.0%) •80 Prey taxa identified • Trophic level = 3.58 + 0.20 •Sufficient sample size at LPT categories Dietary Composition •Crustaceans (shrimps, euphausiids) were primary prey group (%IRI = 94.5 + 11.7) • Thysanoessa inermis/spinifera (%IRI = 31.5 + 37.9) •Eualus avinus (%IRI = 13.9 + 23.0) •Fishes (%IRI = 3.9 + 9.4; %FO = 43.1) Comparison to Literature In Alaskan waters, dietary composition consists of five specimens from the Aleutian Islands that consumed primarily crabs and polychaetes (Yang 2003; 2007), and three GOA specimens ate shrimps, crabs, and fishes (Yang et al. 2006).

17. Results (Kodiak): Bering skate %M n = 64 n = 62 Interannual dietary differences were evident for Bering skates by both %N (SIMobs = 0.229; P = 0.000)and %M (SIMobs = 0.354, P = 0.000).

18. Results: Interspecific Comparisons Overall Data Mean trophic levels ranged from 3.58 + 0.20 (Bering skate) to 3.69 + 0.25 (Aleutian skate) and differed significantly among species (Kruskal–Wallis = 14.351, P = 0.002). Post–hoc tests revealed that the difference was attributable to the comparison between Bering and Aleutian skates (Dunn’s Q = 3.630, P = 0.002); however, no other pairwise comparisons were significant (Dunn’s Q < 2.639, P > 0.05). Kodiak Data

19. Crabs Euphausiids Shrimps Results: Interspecific Comparisons

20. Conclusions •The GOA skate assemblage on the continental shelf and upper continental slope was comprised of secondary consumers with diets consisting primarily of decapod crustaceans. •Interannual dietary differences were evident for Aleutian and Bering skates. In both cases, euphausiids comprised a much greater dietary proportion during 2007, and the contribution of shrimps was relatively less substantial. •The diets of Aleutian, longnose, and Bering skates (during 2006) were quite similar, consisting primarily of shrimps, with brachyuran crabs and fishes of secondary importance. Dietary compositions differed significantly for all additional interspecific comparisons.

21. Conclusions •Several commercially important invertebrates (e.g. pandalid shrimps, tanner crabs) and fishes (e.g., walleye pollock, flatfishes) were common prey items. • Big and longnose skate populations from California consumed a greater proportion of fishes and occupied elevated trophic positions when compared to those from the Gulf of Alaska. Possible competitive release of skates in California waters as a result of decline in sympatric groundfish stocks? • Skates appeared to be generalists, consuming locally abundant fishes and invertebrates. As common generalist predators, skate diet may be a useful indicator of temporal changes in benthic prey composition (seasonal recruitment, climate change).

22. Future Work •Complete processing of all available stomach samples for each species. •Expand examination of sources of variation in skate diets. •Complete species-specific manuscripts on diet and trophic ecology, and an additional manuscript detailing the comparative feeding ecology of GOA skates. •Additional M.Sc. thesis project on diet of skates from Prince William Sound is underway using samples collected during funding for NPRB 621.

23. Specimen collection (ADFG): Kally Spalinger • Ken Goldman • Mike Byerly • Nick Sagalkin Jim Thomason • Bill Walker • Eric Hochberg Jasmine Fry • Shaara Ainsley • Diane Haas •Lewis Barnett • Priscilla Jimmeye North Pacific Research Board •NOAA/NMFS to the National Shark Research Consortium Prey Identification (NMFS–AFSC/SBNHM): PSRC Students and Interns: Funding for this research was provided by: Acknowledgements