DISTRIBUTION AND REPRODUCTIVE ECOLOGY OF DEEP-SEA CATSHARKS (CHONDRICHTHYES: SCYLIORHINIDAE) OF THE EASTERN NORTH PACIFIC A Thesis Presented to The Faculty of Moss Landing Marine Laboratories And the Institute of Earth Systems Science and Policy California State University, Monterey Bay In Partial Fulfillment Of the Requirements for the Degree Master of Science In Marine Science by Brooke Elizabeth Flammang May 2005 © 2005 Brooke Elizabeth Flammang ALL RIGHTS RESERVED ABSTRACT Information on the distribution and reproduction of the catsharks Apristurus brunneus, A. kampae and Parmaturus xaniurus was generated from specimens collected by fishery independent survey cruises from June 2001 through October 2004 between northern Washington to San Diego, California. Longline catches consisted mainly of P. xaniurus, with occasional catch of gravid female A. brunneus. Conversely, trawl catches consisted mainly of Apristurus species. Apristurus brunneus was typically found between 300 and 942 m, while A. kampae occurred > 1,000 m depth. Parmaturus xaniurus was caught between 300 and 550 m depth. Egg cases of A. brunneus and P. xaniurus were collected in trawl surveys and observed in video footage taken by remotely operated vehicle. These egg cases were located in specific sites on areas of high vertical relief at 300 to 400 m depth. Total length at first, 50% and 100% maturity were determined for males and females of all three species. At higher latitudes, A. brunneus and P. xaniurus reached sexual maturity at larger sizes. Apristurus brunneus and P. xaniurus reproduce year-round based on the occurrence of gravid females and the lack of seasonal variation in gonadosomatic (GSI) and hepatosomatic indices (HSI) for both males and females. Gravid A. kampae females were found from July through December. The egg case of A. kampae is described and its morphology compared to the egg cases of A. brunneus, P. xaniurus, and other Apristurus species. ACKNOWLEDGEMENTS All animals were handled ethically in accordance with Institutional Animal Care and Use Committee standards under San Jose State University (SJSU) protocols 801 and 838. Equipment used in this study and funding provided to present the results of this research came from National Oceanographic and Aeronautic Administration/National Marine Fisheries Service to the National Shark Research Consortium Pacific Shark Research Center, SJSU Foundation, Myers Trust, Packard Foundation, Western Society of Naturalists Student Poster award, American Elasmobranch Society Student Travel award, Kim Peppard Memorial Scholarship fund, and SJSU lottery funds. Mahalo to D. Ardizzone, A. Carlisle, the Cruz trio, C. Davis, S. D’itullio, G. Evans, D. Irwin, L. McConnell, C. Perez, K. Quaranta, H. Robinson, W. Smith, D. Tanner, and T. Trejo, who graciously donated their time to assist in the necropsy of all the specimens used in this study. The collection of samples was made possible by C. Schnitzler, S. Haddock, and G. Matsumoto (MBARI); K. Cross, M. Ezcurra, V. Franklin, S. Greenwald, and K. Lewand (MBA); S. Todd (PSMFC); D. Pearson (NMFS-SCL (SWFSC); B. Lea (CDF&G); the NWFSC FRAM team, especially K. Bosely, E. Fruh, D. Kamikawa, V. Simon, T. Wick, and the crews of the B.J. Thomas, Miss Julie, Excalibur, Blue Horizon and Captain Jack (Captain B. Fletcher, Joe and Kevin). Museum collection access and photographs were attained by the help of K. Hartel and C. Kenaley (MCZ); D. Catania, and W. Eschmeyer (CAS); P. Hastings and H. Walker (SIO); K. Maslenikov (UW), E. Jorgensen (AFSC), S. Jewett (USNM), P. Last (CSIRO), and J. Connors and S. von Thun (MBARI). J. Bizzarro and M. Levey provided wise tutelage in Arcview GIS. Technical support was made available by J. Arlt and B. Rose. Invaluable insight and discussion that greatly improved the quality of this thesis were given by W. Smith, L. Compagno, L. Ferry-Graham, J. Orr, and my esteemed committee members, D. Ebert, G. Cailliet, and R. Larson. I have been fortunate to experience their professional brilliance firsthand. I am forever indebted to L. McConnell, J. Grebel Reinhardt, A. Bonnema, J. Schuytema, W. Smith, T. Trejo, and J. Parker, for thoughtful discussion and encouragement in a multitude of different ways, which greatly improved the disposition of the author. I also would like to thank my friends at American Medical Response, especially C. Irwin, S. Nocita, M. Garcia, and S. Hamilton, who have been outstandingly supportive of “my other life”. Most importantly, I would like to thank my family and friends for their unwavering support and faith in me; they never questioned my move across the country to try to get into graduate school. They gave me the strength and confidence to follow my aspirations farther than I thought they would lead me. Namasté. Τόσο πολύ, και ευχαριστίες για όλα τα ψάρια. TABLE OF CONTENTS List of Tables…………………………………………………………………………..…………………..ix List of Figures………………………………………………………………………..………………….....x List of Appendices…………………………………………………………………..……………………xiii Introduction………………………………………………………………………..………………………...1 Apristurus brunneus………………………………………………………………………………1 Apristurus kampae………………………………………………………………………………..2 Parmaturus xaniurus……………………………………………………………………………..2 Methods…………………………………………………………………………..…………………………4 Field Sampling….……………………………………………………..………………………….4 Distributional Data…………………………………………………..……………………………5 Biological Data……………………………………………………..……………………………..6 Results……………………………………………………………………..………………………………10 Distribution……………………………………………………………………………………….10 Latitudinal Distribution………..……………………..………………………………...10 Bathymetric Distribution…………………………..…………………………………..12 Weight-Length Relationships..……………………………..……………………………...…..13 Sex Ratios…………………………………………………..……………………………………13 Maturity Stages…………………………………………….……………………………………14 Reproductive Development…………………………………………………………………….14 Clasper Morphology…………………………….……………………………………..14 Clasper Development……………………………………..…………………………..16 Oviducal Gland Development………………………….……………………………..16 Oocyte Development…………………………………..……………………………...17 Size at Maturity..……………………………………..………………………………………….18 Reproductive Seasonality and Fecundity..……….…………………………………………..19 Ontogeny…………………………………………………………………………………………21 Egg Case Morphology……………...……………………………………..…………..21 vii Egg Case Distribution…………………………..…………………………..………...22 Egg Case Habitat……………….…………………………...………………..……….23 Predation on Egg Cases………………………………………………………….…..24 Embryonic Development………………………………………………………..…….24 Discussion…………………………………………………………………………………………………26 Distribution………………….....…………………………………………………………………26 Latitudinal Distribution…………………………………………………………………26 Bathymetric Distribution……………………………………………………………….27 Weight-Length Relationships..………………………………………………………………....28 Sex Ratios………………………………………………………………………………………..29 Sexual Dimorphism……………………………………………………………………………..29 Variability in Size at Maturity and Reproductive Development…………………………….30 Reproductive Seasonality and Fecundity.…………………………………………………….32 Ontogeny…………………………………………………………………………………………34 Implications of Egg Case Morphology……………………………………………….34 Egg Case Distribution, Habitat, and Nursery Grounds………………..…………..36 Predation on Egg Cases………………………………………………………………37 Embryonic Development………………………………………..…………………….38 References……………………………………………………………………………………………......40 Tables…………………………………………………………………………………………………......48 Figures………………...………………………………………………………………………………......58 Appendix………………………………………………………………………………………………......85 viii LIST OF TABLES Table 1. Criteria used to determine sexual maturity stages (embryonic, juvenile, adolescent, adult and gravid female) of male and female scyliorhinids ………………………………………….48 Table 2. Trawl and longline survey catches of Apristurus brunneus, A. kampae, and Parmaturus xaniurus from June 2001 through October 2004(n = 1,044). Specimens obtained from commercial fishing operations or museum holdings (n = 142) are not included in this table…....49 Table 3. Geometric mean weight-length relationships for Apristurus brunneus, Apristurus kampae, and Parmaturus xaniurus for all specimens from the eastern North Pacific.……………50 Table 4. Geometric mean weight-length relationships for male and female Apristurus brunneus specimens from off Washington (48°N to 46°N latitude), Oregon (46°N to 42°N latitude), and northern (42°N to 38°N latitude), central (38°N to 34°N latitude), and southern California (34°N to 32°N latitude)…………………………………………………………….……………………………….51 Table 5. Sex ratios of male and female Apristurus brunneus and Parmaturus xaniurus off Washington (48°N to 46°N latitude), Oregon (46°N to 42°N latitude), and northern (42°N to 38°N latitude), central (38°N to 34°N latitude), and southern California (34°N to 32°N latitude). Museum specimens caught in the central California region are included for A. kampae. Sex ratios in bold type were determined to be significantly different from a 1:1 relationship using a χ2 2 test with Yates correction for continuity (χ 0.05,1 = 3.841, Zar 1999). ***, P < 0.001; **, P < 0.01; *, P < 0.05; ns, not significant……………………………………………………………………………..52 Table 6. Combined total of Apristurus brunneus, A. kampae, and Parmaturus xaniurus specimens examined of each maturity class (juvenile, adolescent, adult, and gravid female. Included are samples from all trawl and longline surveys June 2001 through October 2004, as well as museum specimens and specimens obtained from commercial fishery observers………53 Table 7. Size at first, 50 and 100 percent maturities (mm TL), for all 3 species of scyliorhinids collected in the eastern North Pacific combined.