Distribution and Reproductive Ecology of Deep-Sea Catsharks

Home , Brown catshark, Cloudy catshark, Filetail catshark, Parmaturus, Swell shark

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

Brooke Elizabeth Flammang

May 2005

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. The estimate for 50% maturity for A. kampae males is based on mathematical estimate, because there was no overlap in sexual maturity among size classes in the specimens available.……………………………………………………...54

Table 8. Size at first maturity and largest immature male and female Apristurus brunneus (mm TL) by latitudinal region (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). No mature females were caught in the Washington region……………………….55

Table 9. Proportion of gravid females of total mature Apristurus brunneus, A. kampae, and Parmaturus xaniurus females by month. Apristurus kampae adult females were only caught from July through November. Parmaturus xaniurus were not caught in the month of May because of limited fishing resources………………………………………………………………………………….56

Table 10. Incubation period, size at hatching, and growth of Parmaturus xaniurus maintained in aquaria at approximately 10°C. Egg cases were collected from the Monterey Bay Aquarium (MBA), which houses adult males and females of this species……………………………………...57

ix LIST OF FIGURES

Figure 1. Total Apristurus brunneus (n = 711) collected by Northwest Fisheries Science Center (NWFSC) trawl surveys in the eastern North Pacific from June 2001 through October 2004. These specimens were arbitrarily grouped by geographic area (A = Washington (48°N to 46°N latitude), B = Oregon (46°N to 42°N latitude), C = northern California (42°N to 38°N latitude), D = central California (38°N to 34°N latitude), and E = southern California (34°N to 32°N latitude)) for further distributional analysis (Figure 2). Bathymetric contours are scaled at 500 m depths……………………………………………………………………………………….……………..58

Figure 2a. Apristurus brunneus (n = 92) collected by NWFSC trawl surveys off Washington (48°N to 46°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths…………………………………………………………………………………………...59

Figure 2b. Apristurus brunneus (n = 141) collected by NWFSC trawl surveys off Oregon (46°N to 42°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths…………………………………………………………………………………………………...60

Figure 2c. Apristurus brunneus (n = 148) collected by NWFSC trawl surveys off northern California (42°N to 38°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths………………………………………………………………………………61

Figure 2d. Apristurus brunneus (n = 52) collected by NWFSC trawl surveys off central California (38°N to 34°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths…………………………………………………………………………………………...62

Figure 2e. Apristurus brunneus (n = 71) collected by NWFSC trawl surveys off southern California (34°N to 32°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths………………………………………………………………………………63

Figure 3. Apristurus brunneus (n = 164) collected by trawl (red circles) and longline (yellow circles) surveys by the Southwest Fisheries Science Center (SWFSC) in Monterey Bay off central California from June 2002 through March 2004. Bathymetric contours are scaled at 500 m depths. Frequency of abundance for males (A; n = 72) and females (B; n = 92) caught are separated by trawl (light bars) and longline (dark bars) catches.……………………………………64

Figure 4. Total Apristurus kampae (n = 97) collected by trawl and longline surveys in the eastern North Pacific from June 2001 through October 2004, combined with catch locations of museum specimens. Specimens caught during this study are denoted by open green squares. Museum specimens are represented by squares with dark square in center. The star denotes the location of the holotype in the Gulf of California (28°N latitude). Bathymetric contours are scaled at 500 m depths…………………………………………………………………………………..65

Figure 5. Total Parmaturus xaniurus (n = 65) collected by NWFSC trawl surveys in the eastern North Pacific from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths………………………………………………………………………………………………………66

Figure 6. Parmaturus xaniurus (n = 321) collected by SWFSC trawl and longline surveys in Monterey Bay off central California from June 2002 through March 2004. Bathymetric contours are scaled at 500 m depths. Frequency of abundance for males (A; n = 117) and females (B; n = 204) caught are separated by trawl (light bars) and longline catches (dark bars).……………67

x Figure 7. Depth distribution of all maturity stages (red circle = juvenile, green triangle = adolescent, yellow square = mature, blue diamond = gravid) of Apristurus brunneus (A, n = 730), A. kampae (B, n = 97), and Parmaturus xaniurus (C, n = 376) collected by trawl and longline from 48°N to 32°N latitude……………………………………………………………………………………..68

Figure 8. Left clasper of Apristurus brunneus (A), Apristurus kampae (B), and Parmaturus xaniurus (C). CD = clasper denticles, CG = clasper groove, CR = cover rhipidion, EN = envelope, ER = exorhipidion, HP = hypopyle, PP = pseudopera, RH = rhipidion. Terminology follows Compagno (1988b) and Sato et al. (1999). Scale bar denotes 1 cm.………..……..……69

Figure 9. Inner clasper length as a percentage of total length for adult (closed triangles) and juvenile and adolescent (open triangles) male Apristurus brunneus (A; n = 317), Apristurus kampae (B; n = 54), and Parmaturus xaniurus (C; n = 140)……………………………..……….....70

Figure 10. Oviducal gland width as a percentage of total length for adult (including gravid; closed circles) and juvenile and adolescent (open circles) female Apristurus brunneus (A; n = 394), Apristurus kampae (B; n = 43), and Parmaturus xaniurus (C; n = 236)……………………...71

Figure 11. Maximum oocyte diameter versus total length of adult (including gravid; closed circles) and juvenile and adolescent (open circles) female Apristurus brunneus (A; n = 394), Apristurus kampae (B; n = 43), and Parmaturus xaniurus (C; n = 236)……………………..……..72

Figure 12. Number of mature oocytes versus total length of female Apristurus brunneus (A; n = 118), A. kampae (B; n = 11), and Parmaturus xaniurus (C; n = 89).…..…………...………..…73

Figure 13. Proportion of mature Apristurus brunneus (A), Apristurus kampae (B), and Parmaturus xaniurus (C). Solid lines designate maturity curve, dashed lines designate 95% confidence intervals. Sample sizes at proportion mature were assumed to be equal...... 74

Figure 14. Gonadosomatic (GSI) and hepatosomatic (HSI) indices for adult male (A, B) and adult female Apristurus brunneus (C, D). GSI = (G/B) x 100, where G is the total gonad mass, and B is the total body mass of the specimen; HSI = (H/B) x 100, where H is the total liver mass and B is the total body mass of the specimen. The horizontal line within each box denotes the median for the sample and the box encompasses the range of the central 50 percent of the values. Bars extending vertically from the box denote 95 percent confidence from the mean. The number of samples per month is designated above each box plot…………………………….75

Figure 15. Gonadosomatic (GSI) and hepatosomatic (HSI) indices for adult male (A, B) and adult female Parmaturus xaniurus (C, D). GSI = (G/B) x 100, where G is the total gonad mass, and B is the total body mass of the specimen; HSI = (H/B) x 100, where H is the total liver mass and B is the total body mass of the specimen. The horizontal line within each box denotes the median for the sample and the box encompasses the range of the central 50 percent of the values. Bars extending vertically from the box denote 95 percent confidence from the mean. The number of samples per month is designated above each box plot……………………………76

Figure 16. Egg case length versus female total length for Apristurus brunneus (A) and Parmaturus xaniurus (B)………………………………………………………………………..……….77

Figure 17. Egg cases of Apristurus brunneus (A), Apristurus kampae (B), and Parmaturus xaniurus (C). Scale bars are 1 cm……………………………………………………………………..78

Figure 18. Locations of Apristurus brunneus (red circles) and Parmaturus xaniurus (purple triangles) egg cases captured by trawl. The arrow points to the location at which 953 egg cases were found (n = 478, 27 October 2000; n = 475, 29 June 2001). Bathymetric contours are scaled at 500 m depths…………………………………………………………………………………………...79

xi Figure 19. Locations of Apristurus brunneus (red circles) and Parmaturus xaniurus (purple triangles) egg cases as captured by remote operated vehicle (ROV) video footage. Cruises were conducted by the Monterey Bay Aquarium Research Institute (MBARI), 1989 through 2003. Bathymetric contours are scaled at 500 m depths…………………………………………………….80

Figure 20. Apristurus brunneus and Parmaturus xaniurus egg cases captured on video footage from remote operated vehicle (ROV). Egg cases were commonly seen attached by their long fibrous tendrils to sponges (A. brunneus on Aphrocallistes vastus, A), gorgonians (A. brunneus on Euplexaura marki, B), corals (P. xaniurus on Antipathese sp., C), hydroids and compound ascideans (P. xaniurus, D), and other egg cases (P. xaniurus, E). Egg cases also provided substrate for the attachment of other filter feeders (anemone on P. xaniurus, F).………………..81

Figure 21. Apristurus brunneus and Parmaturus xaniurus egg cases captured on video footage from remote operated vehicle (ROV). Egg cases were commonly seen covered by invertebrates such as large sea stars (Rathbunaster californicus on A. brunneus, A), gastropods (Boreotrophon tripherus on A. brunneus, B), and ophiuroids (Ophiopholis longispina on P. xaniurus, C)…...…..82

Figure 22. Empty Parmaturus xaniurus egg case found in Monterey Bay Aquarium tank next to head of shortspine thornyhead (Sebastolobus alascanus). Egg case ends appear to have been bitten off……………………………………………………………………………………………………83

Figure 23. Apristurus brunneus egg case with embryo and yolk sac (A). This egg case was pulled from a bundle of 475 cases attached together by their tendrils; the bundle was caught in a National Marine Fisheries Service (NMFS) trawl on the 29 June 2001at approximately 39°N latitude. e = embryo, u = umbilicus, y = yolk sac. Photo by Elaina Jorgensen. Parmaturus xaniurus embryo (B) approximately 6 months old reared in 10°C. Photo by Allen H. Andrews....84

xii LIST OF APPENDICES

Appendix 1. Egg cases of the genus Apristurus…………………………………………………….85

xiii INTRODUCTION

Catsharks (Chondrichthyes: Scyliorhinidae) are the largest and the most diverse family of living sharks, totaling 15 genera and approximately 106 species distributed worldwide (Ebert 2003).

Two scyliorhinid genera, Apristurus and Parmaturus, are predominant fishes of the deep-water slope region that typifies the eastern North Pacific. Because these genera are typically found in deep waters, little is known about their life history or systematics. Sharks in both genera are relatively small and soft-bodied. There are approximately 35 species of Apristurus, most of which are black, dark brown, or dark grey in color and have conspicuous ampullae of Lorenzini visible on their long, compressed snouts (Springer 1979, Nakaya and Sato 1999). Of the five species of Parmaturus, only one is reported from the eastern North Pacific (Compagno 1984).

This genus can be distinguished from Apristurus species by the prominent crest of enlarged modified dermal denticles on the dorsal margin of the caudal fin and by its light ventral coloration

(Springer 1979, Compagno 1988a). Three deep-sea scyliorhinids have been reported in the eastern North Pacific: the brown catshark, A. brunneus, the long-nose catshark, A. kampae, and the filetail catshark, P. xaniurus (Eschmeyer et al. 1983, Ebert 2003).

Apristurus brunneus

The brown catshark, Apristurus brunneus (Gilbert 1892), occurs in the eastern North Pacific

Ocean, ranging from the eastern Gulf of Alaska off Icy Point, Alaska (56°N latitude) to Baja

California, Mexico (28°N latitude; Compagno 1984, Mecklenburg et al. 2002). Apristurus brunneus are 70 to 90 mm total length (TL) at birth and grow to 690 mm TL (Ebert 2003). In a northern portion of their range, off British Columbia, A. brunneus was found between 33 and 564 m depth, at a mean depth of 208 m (Jones and Geen 1977). In southern California, this species was caught in bottom trawls and on longlines at 290 to 625 m depth (Cross 1988). Roedel

(1951) reported A. brunneus to 933 m depth in bottom trawls off southern California.

The reproductive biology of A. brunneus has been examined in the northern and southern extent of its range by previous studies off British Columbia and southern California. In southern California, males were determined to mature between 450 and 500 mm TL and females between

425 and 475 mm TL (Cross 1988). Female A. brunneus > 450 mm total length (TL) off British

Columbia were gravid (carrying egg cases) in February and March (Jones and Geen 1977).

Cross (1988) found gravid females in all months except February and August. The egg case of

this species was described by DeLacy and Chapman (1935) and Cox (1964) as having a vase-

like shape and a rounded flange running the entire length of the lateral edges and terminating in

long tendrils; the egg cases are approximately 50 mm in length, excluding tendrils (Ebert 2003).

Jones and Geen (1977) speculated that the incubation period of A. brunneus egg cases in situ

was approximately a year. Incubation in captivity is reported to last 24 to 27 months in 5 to 6°C

seawater (Gilbert van Dykhuizen, Monterey Bay Aquarium, pers. comm.).

Apristurus kampae

The white-edge catshark, Apristurus kampae Taylor 1972, also occurs in the eastern North

Pacific Ocean, ranging from Cape Blanco, Oregon to the Gulf of California, Mexico, between

46°N and 26°N latitude, along the upper continental shelf to a depth of 1888 m (Compagno 1984,

Ebert 2003). Apristurus kampae is known only from the holotype, which was caught in an otter

trawl on a soft mud bottom (Taylor 1972). The holotype was an immature female, 355 mm TL,

and contained ova of varying sizes (Taylor 1972). This species may grow to a maximum of 570

mm TL (Ebert 2003). The egg case of A. kampae is approximately 70 mm long and has been

illustrated but not described (Ebert 2003).

Parmaturus xaniurus

Found from Cape Foulweather, Oregon to the Gulf of California, between 46°N and 26°N latitude,

the filetail catshark, Parmaturus xaniurus (Gilbert 1892), is brownish to black with a paler ventral

side and distinguished by enlarged dermal denticles on the anterior edge of the caudal fin (Miller

and Lea 1972, Compagno 1984, Ebert 2003). It is often found at depths between 91 and 1251 m,

usually near the bottom (Castro 1983) or within 490 m of the bottom (Compagno 1984).

Juvenile P. xaniurus are described as pelagic, living in the water column, whereas the adults are considered benthic (Lee 1969, Ebeling et al. 1970). Ebert (2003) reported that this species may hatch at a size of 70 to 90 mm TL from an egg case 70 to 110 mm long, and grow to a maximum length of 610 mm TL.

In southern California, P. xaniurus males reached reproductive maturity between 375 and 425 mm TL and females between 425 and 475 mm TL (Cross 1988). Off Baja California Sur,

Mexico, Balart et al. (2000) found no mature females, but suggested that males matured at approximately 340 mm TL. Oocyte production may be seasonal in this species, but copulation may take place year-round (Cross 1988). Cox (1964) described the egg case of P. xaniurus,

which can be distinguished from the egg case of A. brunneus as having a flange along the lateral

edges that resembles a “T” in cross-section.

Knowledge is extremely limited concerning the life history of all three of these catsharks. Cross

(1988) investigated the abundance, reproductive cycle, and food habits of A. brunneus and P.

xaniurus from the upper continental slope south of Point Dume, California (34ºN latitude). The

reproductive biology of P. xaniurus off the west coast of Baja California Sur, Mexico was

compared to the findings of Cross (1988) by Balart et al. (2000). There have been no life history

studies of A. brunneus, A. kampae, or P. xaniurus off Washington, Oregon, or California north of

Point Conception, and the occurrence of these scyliorhinids as incidental catch in commercial

fishing operations (Steve Todd, Pacific States Marine Fisheries Commission, pers. comm.)

warrants research into their biology and distribution to gauge the need for fisheries management.

Also, there is no data on these species between Washington and Point Dume, California for

comparison with the studies conducted in more northern and southern regions. By examining

the biology of these species throughout the extent of their range, it may be possible to devise new

theoretical-based hypotheses about the life history of these deep-sea elasmobranchs. The

purpose of this project is to describe the distribution and reproductive biology of A. brunneus, A.

kampae and P. xaniurus in the eastern North Pacific, between 48°N and 32°N latitude.

METHODS

FIELD SAMPLING

Samples were obtained from fishery-independent bottom trawl survey cruises conducted by the

National Marine Fisheries Service (NMFS) Northwest Fisheries Science Center (NWFSC) laboratories in Newport, OR and Seattle, WA. Samples contributed by Pacific States Marine

Fisheries Commission (PSMFC) were collected by bottom trawl in Monterey Bay and off Big Sur,

California, and were dependent upon cooperation of individual commercial fishing operations and observer availability. Additionally, specimens in collections at the University of Washington

(UW), California Academy of Sciences (CAS), Museum of Comparative Zoology (MCZ), Scripps

Institute of Oceanography (SIO), Los Angeles County Museum (LACM), Smithsonian National

Museum of Natural History (USNM), and the Commonwealth Scientific and Industrial Research

Organization (CSIRO) Hobart, Tasmania were examined to augment field samples. Institutional codes are as designated in Leviton et al. (1985).

The NWFSC provided samples from their annual slope and shelf Fisheries Research and

Monitoring (FRAM) cruises during the months of June through October from 2001 to 2004, between Cape Flattery, Washington (48°N latitude) and San Diego, California(32°N latitude). Six hundred sample locations were randomly chosen each year from a map of the survey area divided into grids 2 nautical miles by 1.5 nautical miles in length. The NWFSC survey was designed to cover three depth strata, shelf (20 to 183 m), shallow slope (184 to 549 m), and deep slope (550 to 1350 m), with the goal of sampling as many different habitat types as possible while minimizing damage to trawl gear.

The NMFS Southwest Fisheries Science Center (SWFSC) laboratory in Santa Cruz, CA provided samples obtained by fishery-independent bottom trawl and longline survey cruises targeting commercial groundfish species between Davenport, CA (approximately 37°N latitude) and

Monterey, CA (approximately 36°N latitude) from June 2002 to March 2004. Using a depth- stratified sampling method, five stations at arbitrarily designated depth gradients were surveyed monthly off central California, dependent on weather. Bottom trawls were conducted from 170 to

667 m depth. Longlines had between 750 and 7,250 hooks per haul; longline haul depths ranged from 373 to 503 m. No sampling was done in the month of May of any year because

SWFSC resources were focused towards the annual California Cooperative Oceanic Fisheries

Investigations (CalCOFI) larval fish survey.

DISTRIBUTIONAL DATA

The latitudinal and bathymetric patterns of abundance, sex ratios, and maturity of Apristurus

brunneus, A. kampae, and Parmaturus xaniurus were investigated using the catch records.

Species were arbitrarily grouped into five geographic areas, 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). Histograms detailing size and sex of

catsharks caught were plotted for each species by region. A two-way ANOVA was used to

determine if there was any difference in catches among latitudinal regions (Platell et al. 1998).

Bathymetric distribution of each species at different reproductive maturity stages was analyzed using geographic information system (GIS) mapping and graphical representation.

Egg case deposition sites were determined by catch records from NWFSC historic cruise data for which photographs were available for species identification and from observations of remotely operated vehicle (ROV) video footage from the Monterey Bay Aquarium Research Institute

(MBARI) digital library. Locations of known egg case deposition sites identified as essential fish habitat (EFH), based on repeated utilization for egg case deposition, were mapped using GIS.

Essential fish habitat was defined by the United States Congress in the 1996 amended

Magnuson-Stevens Fishery Conservation and Management Act as "those waters and substrate necessary to fish for spawning, breeding, feeding, or growth to maturity." Egg case deposition sites were described to detail the depth, temperature, and habitat characteristics of the locations utilized as nursery grounds for these deep-sea catsharks.

BIOLOGICAL DATA

Field samples were frozen upon capture and returned to Moss Landing Marine Laboratories

(MLML) for examination. Specimens were thawed, measured, and weighed. Total length was measured to the nearest millimeter (mm), with the specimen in the “natural” position.

Geometric weight-length regressions were calculated for males and females of each species using the equation W = aLb, where W is the weight in grams, L is the total length in mm, and a and b are fitted constants (Ricker 1979). Analysis of variance (ANOVA) was used to determine difference in weight-length regressions among species, sex, and geographical region.

Sex ratio of specimens caught by latitudinal region was evaluated for A. brunneus and P.

2 2 xaniurus. Using a χ test with Yates correction for continuity (χ 0.05,1 = 3.841, Zar 1999), sex

ratios were tested to determine if they were significantly different from a 1:1 (female : male) ratio.

Sexual maturity of specimens was determined by visual analysis of gonads and reproductive

organs (Table 1). In males, sexual maturity was determined by clasper development and

calcification; the terminal clasper elements are fully calcified in mature individuals. Clasper

length was measured to the nearest mm along the median, or inner, length of the clasper, from

the clasper origin at the apex of the cloaca, to the distal tip of the clasper.

Clasper morphology is distinct in many scyliorhinid species and may be useful for taxonomic

identification, especially among species of the genus Apristurus (Compagno 1988b, Compagno

and Stevens 1993). Clasper morphology was described for and compared among adult males of

each species. Clasper terminology used follows Compagno (1988b) and Sato et al. (1999).

Clasper denticles (CD) are enlarged dermal denticles with anteriorly directed cusps on the ventral

and lateral sides of the clasper. The clasper groove (CG) is the hollow through which spermatozoa is passed along the length of the clasper during copulation. The cover rhipidion

(CR) is anterior and medial to the rhipidion, and covers the clasper glans. The envelope (EN) covers the hypopyle and the anterior portion of the clasper glans. The exorhipidion (ER) is a

longitudinally elongated, external blade or flap with its base attached to the dorsolateral edge of

the clasper, with its free edge directed medially. The hypopyle (HP) is the posterior opening of

the clasper groove onto the clasper. The pseudopera (PP) is a dorsally-opening enclosed

pocket along the lateral edge of the clasper, and is located about opposite the anterior edge of

the clasper glans. The rhipidion (RH) is distal opening of the CG. It is fan-shaped for dispersing

sperm during copulation.

Maturity status in females was determined by vascularization of the ovary and development of the

oviducal gland, which produces the egg case (Table 1). The widths of the uterus, the left

oviducal gland, and mature oocytes greater than 14 mm in diameter (Cross 1988) were measured

to the nearest mm. In these scyliorhinids, only the right ovary is developed and reproductively

functional. The left ovary is vestigial (Springer 1966). Ovary mass was measured to the nearest

tenth of a gram. Changes in gonad mass, mature oocyte diameter and number, and liver mass

were analyzed for developmental and seasonal variation.

Size at first, 50 %, and 100 % maturity was determined for males and females of all species.

Size at 50 percent maturity was determined using the logistic equation detailed in Roa et al.

β + β L (1999), P(L) = α / (1 + e 0 1 ), where P(L) is the proportion of mature individuals at length L, α is the asymptote, β0 is the intercept, and β1 is the slope parameter. This logistic model provided

the best fit to the biological data. Significant differences between male and female maturity sizes

were determined by plotting 95% confidence intervals (CI) around the logistic regression; overlap

of 95% CI indicated the values were not significantly different (P > 0.05). Size of the smallest

mature and largest immature male and female were evaluated for significant difference by

geographical region using an ANOVA.

Seasonal variability of reproductive ability in adults was quantified using the gonadosomatic index

(GSI): GSI = (G/B) x 100, where G is the total gonad mass and B is the total body mass of the specimen. Gonadosomatic index was determined using testis mass in males and ovary mass

(including oocytes) in females and compared throughout the year to see if there was a seasonal fluctuation in gonad mass. Changes in liver mass were analyzed using the hepatosomatic index

(HSI): HSI = (H/B) x 100, where H is the total liver mass and B is the total body mass of the

specimen. Hepatic lipids are used in vitellogenesis, the formation of oocyte yolk (Craik 1978,

Hamlett and Koob 1999), and it was expected that any seasonal variability in HSI would coincide

with inverse fluctuations in GSI. Gonadosomatic and hepatosomatic indices were compared by

month, with significant difference determined by plotting 95% CI around the mean index value.

Egg case size and fecundity were evaluated for each species. Egg case length relative to

female TL was compared to determine if a relationship exists, as purported in Cross (1988). The

proportion of gravid females was calculated for each month to investigate reproductive

seasonality.

There is species-specific morphologic variability in egg case structure that may be useful in

determining phylogenetic and taxonomic relationships (Ishiyama and Ishihara 1977, Gomes and

de Carvalho 1995). The egg case of Apristurus kampae was described and compared to those

of A. brunneus and Parmaturus xaniurus, as well as other egg cases of the genus Apristurus

acquired from museum collections. All of the described egg cases were fully formed and located

in the posterior end of the oviduct. Egg cases were removed directly from gravid females to

ensure proper species identification.

Remotely operated vehicle (ROV) video footage taken by the Monterey Bay Aquarium Research

Institute (MBARI) during exploratory cruises of the Monterey Bay region off central California.

Footage from cruises conducted between November 1990 and February 2002 was examined for

egg case location sites. The egg case sites were described as the essential fish habitat (EFH)

used as nursery areas for these catsharks.

Association of other organisms with catshark egg cases was also observed from ROV video, to isolate possible predation events on embryonic catsharks. Teleost fishes, marine mammals, and some invertebrates, such as large sea stars and gastropods, are known to feed on embryos (Cox and Koob, 1993, Long 1996, Bor and Santos 2003, Lucifora and Garcia 2004).

Parmaturus xaniurus have been held in captivity at the Monterey Bay Aquarium (MBA) and were housed with organisms that share their habitat in nature, such as the shortspine thornyhead

(Sebastolobus alascanus), urchins (Allocentratus fragilis), and large sea stars (Rathbunaster californicus). Egg cases deposited in the tank by gravid females were observed for intraspecific and interspecific predation.

Egg cases of P. xaniurus were also collected from the MBA and returned to aquaria at MLML to

observe incubation time (time until hatching) in 10°C seawater and external changes in the egg

cases over time. Sizes at hatching and periodic size measurements were recorded to evaluate

growth of juvenile P. xaniurus in captivity. RESULTS

LATITUDINAL DISTRIBUTION

A combined total of 1,044 scyliorhinids was caught on NWFSC and SWFSC surveys from June

2001 through October 2004 (Table 2). An additional 140 specimens obtained from museums

and commercial fishing operations were also studied. Six hundred forty seven trawls conducted

by the NWFSC produced 557 catshark specimens. In the central California region, the SWFSC

provided 102 catsharks from 115 trawls and 385 catsharks from 129 longlines. Trawl catches

were composed primarily of Apristurus spp., whereas longline catches were almost exclusively P.

xaniurus. Longline surveys were performed over untrawlable grounds.

Apristurus brunneus

Of the 711 A. brunneus studied, 650 were caught by the NWFSC and SWFSC surveys between

northern Washington (48°N latitude) and San Diego, California (32°N latitude; Table 2, Figure 1).

These specimens ranged in size from 122 to 693 mm TL. The remaining 61 specimens were

commercially caught and museum specimens from this same latitudinal range but were not

included in distributional analysis because some location information could not be confirmed.

The NWFSC caught 486 A. brunneus by bottom trawl between northern Washington (48°N latitude) and San Diego, California (32°N latitude) and these catches were arbitrarily subdivided by geographic location for regional analysis (Figures 2 a through e). A normal distribution of 92 male (n = 39) and female (n = 53) specimens approximately 300 to 550 mm TL was caught off

Washington (48°N to 46°N latitude; Figure 2a). One hundred forty one A. brunneus were caught off Oregon (46°N to 42°N latitude); TL of males (n = 72) was normally distributed around 375 mm

TL and female median length (n = 69) was approximately 450 mm TL in this area (Figure 2b).

Off northern California (42°N to 38°N latitude), 136 of 148 of specimens were caught between

42°N to 40°N latitude (Figure 2c). The distribution of males in this area was bimodal (n = 61), with peaks at approximately 300 and 400 mm TL, and females were relatively even distributed between 200 and 600 mm TL (n = 87). Males (n = 24) and females (n = 28) both exhibited a bimodal distribution in frequency by TL in central California (38°N to 34°N latitude), where males peaked around 375 and 625 mm TL and females peaked at approximately 400 and 575 mm TL

(Figure 2d). Catches of A. brunneus in southern California (34°N to 32°N latitude) were scattered, and males (n = 35) and females (n = 36) ranged between 120 and 600 mm TL (Figure

2e).

In the Monterey Bay region of central California (approximately 37°N to 36°N latitude), 164 A.

brunneus were collected by the SWFSC, of which 83 were caught by longline and 81 by trawls

(Figure 3). Frequency of males by TL (n = 72) exhibited a bimodal distribution regardless of

fishing method in the central California region (Figure 3a). The greatest number of females (n =

92) caught on the longline was approximately 450 mm TL, whereas females approximately 500

mm TL were the most common of those in the trawls (Figure 3b). Fifty seven percent of A.

brunneus caught on the longline were mature or gravid females. This species was commonly

found at canyon heads in this region and at the outer continental shelf and upper slope.

Apristurus kampae

A total of 97 A. kampae was studied, of these 23 were caught in trawls during this study and the

remainder were from museum collections (Table 2). The NWFSC, which fished at greater

depths than the SWFSC, caught 21 of the 23 A. kampae. The SWFSC did not collect any A.

kampae. Two specimens were caught as bycatch during commercial sablefish fishing, and

collected for this study by PSMFC observers. Apristurus kampae were never caught on a

longline.

All of the A. kampae studied (n = 97), including museum specimens, were included in

distributional analysis to best represent what is known about the geographic distribution of this

catshark (Figure 4). These specimens extended from the northern California border (42°N) to

the holotype in the Gulf of California (28°N latitude). Twenty of the 23 specimens caught during this study were caught between 38°N and 34°N latitude. Apristurus kampae studied ranged from

74 to 647 mm TL, most of which where between 500 and 600 mm TL.

Parmaturus xaniurus

Of the 371 P. xaniurus caught from NMFS surveys, 302 were caught on SWFSC longlines (Table

2). An additional 5 specimens were obtained from commercial fishery observers.

All P. xaniurus were caught between 40°N and 32°N latitude (Figure 5). Size distribution of

males (n = 28) was skewed to the left and most males were between 400 and 475 mm TL.

Females (n = 37) were more normally distributed with most between 425 and 575 mm TL.

Parmaturus xaniurus as small as 130 mm TL was caught in bottom trawls in southern California.

The majority of P. xaniurus studied (321 of 371) were collected by the SWFSC from Monterey

Bay (37°N to 36°N latitude; Figure 6). Males (n = 117; Figure 6a) and females (n = 204; Figure

6b) in this area were caught primarily on longline surveys. The smallest catshark caught on

longlines was a P. xaniurus measured at 308 mm TL. These specimens were typically found

along the outer continental shelf and upper slope.

BATHYMETRIC DISTRIBUTION

All life stages of A. brunneus were found between 300 and 1,100 m depth (Figure 7a). However,

89% of adolescents were ≥ 600 m depth. Gravid females were caught between 300 and 500 m

depth. This species was typically caught over mud or silt bottom or rocky areas with high vertical

relief.

Apristurus kampae was typically found deeper than 1,005 m, to a maximum depth of 1,888 m

(Figure 7b), along the continental slope in areas with mud or silt bottom habitat. Juvenile A.

kampae were caught in bottom trawls from 400 to 1,800 m depth. The location of adolescents,

adults, and gravid females, was concentrated between 1,000 and 1,200 m depth.

Parmaturus xaniurus usually was found over mud or silt bottom or areas of rocky vertical relief between 300 and 550 m depth (Figure 7c). Only one juvenile P. xaniurus was caught below 500 m. Adolescents were between 300 and 600 m depth. Almost all P. xaniurus deeper than 600 m were mature. Gravid females were generally between 300 and 500 m depth. In October 2004, more than 200 juvenile P. xaniurus 130 to 200 mm TL were caught in one bottom trawl just south of Santa Cruz Island (approximately 34°N latitude), at 475 m depth.

WEIGHT-LENGTH RELATIONSHIPS

Geometric mean weight-length relationships were determined by linear regression for male and female A. brunneus, A. kampae, and P. xaniurus (Table 3). There was a significant difference in regression coefficients of weight-length relationships among species (df = 2, P = 0.030) but not between sexes of any species from the eastern North Pacific combined (df = 1, P = 0.399).

Geometric mean weight-length relationships were also determined for male and female A. brunneus when subdivided by geographic location (Table 4). Regression coefficients of the weight-length relationship were not significant by region (df = 4, P = 0.648) or sex (df = 1, P =

0.958).

SEX RATIOS

There were a greater proportion of females to males in those geographic locations where the sex ratio was significantly different from a 1:1 relationship (Table 5). For A. brunneus, the male to female ratio was significantly different from a 1:1 relationship, with females > males in northern

California (P < 0.05) and central California (P < 0.01); other regions were not significantly different.

Apristurus kampae in central California (38°N to 34°N latitude) had a sex ratio that was not significantly different from 1:1. There were not enough specimens to determine male:female ratios for this species in other regions.

The sex ratio for P. xaniurus was also significantly different from a 1:1 relationship in central

California, with a greater proportion of females (P < 0.001). Parmaturus xaniurus was rarely

caught in other regions; therefore, it was not possible to determine sex ratios in other locations.

MATURITY STAGES

Specimens representative of each maturity class (juvenile, adolescent, adult, and gravid female)

were obtained for all species (Table 6). Of the 711 A. brunneus studied, 62% were juvenile

males (n = 224) and females (n = 218). Of the remainder, 10% were adolescents and 27% were adults, including gravid females.

Sixty four percent of A. kampae specimens available were adults (n = 43 males and 28 females, including gravid females; Table 6). The remainder was 13% juveniles and 23% adolescents.

Parmaturus xaniurus males were evenly distributed among maturity classes, but females collected consisted mostly of adolescents (109 of 236 specimens). The number of adolescent females collected was twice the number of adolescent males (n = 49). Of the rest of the P. xaniurus, juveniles comprised 22%, and the remaining 36% was adults and gravid females.

REPRODUCTIVE DEVELOPMENT

Clasper Morphology

Apristurus brunneus claspers are relatively long with a broad base, tapering on the lateral edge towards the tip (Figure 8a). Claspers extend past the posterior edge of the pelvic fins, but do not reach the anterior edge of the anal fin. The ventral and lateral surfaces of the claspers, as well as the exorhipidion, are covered in numerous enlarged clasper denticles with anteriorly directed cusps. The clasper groove, through which spermatozoa are passed, is covered almost entirely by the lobate cover rhipidion and exorhipidion. The pseudopera is well developed under the anterior end of the exorhipidion. A large envelope covers the hypopyle. The rhipidion is long and flat, and not covered posteriorly by the exorhipidion. The cover rhipidion is a well-formed lobe, anterior to the rhipidion. The clasper groove is covered by its dorsal margins.

The claspers of Apristurus kampae are stout at the base and taper posteriorly along the lateral edge towards the tip (Figure 8b). Claspers extend past the posterior edge of the pelvic fins, but do not reach the anterior edge of the anal fin. The ventral and lateral surfaces of the claspers, as well as the exorhipidion, are covered in numerous enlarged clasper denticles with anteriorly directed cusps. The pseudopera is well developed under the anterior end of the exorhipidion. A

large envelope covers the hypopyle. The cover rhipidion is a well-formed lobe, anterior to the

rhipidion. The cover rhipidion and rhipidion are partially covered by exorhipidions which have

multiple dermal folds. The clasper groove is covered by its dorsal margins.

Parmaturus xaniurus claspers are very long, nearly cylindrical with slight tapering posteriorly

towards the tip (Figure 8c). Claspers extend past the posterior edge of the pelvic fins and extend

almost to the anterior edge of the anal fin. The ventral and lateral surfaces of the claspers, as

well as the exorhipidion, are covered in numerous enlarged clasper denticles with anteriorly directed cusps. The pseudopera is poorly developed. The exorhipidion is poorly differentiated along the lateral edge. The rhipidion is long and large, and is conspicuous being uncovered by

exorhipidion. The cover rhipidion is a well-defined large bulbous lobe, anterior to the rhipidion.

No envelope is present.

Claspers of the three species were morphologically and taxonomically distinct from one another.

In A. brunneus, the rhipidion at the posterior end of the clasper is exposed, whereas in A.

kampae, the rhipidion is covered by the exorhipidion. The clasper groove of P. xaniurus was exposed throughout most of the length of the clasper, and there was no envelope covering the hypopyle.

Clasper Development

Clasper length increased curvilinearly with TL in all three species (Figure 9). Clasper length in A. brunneus males began to increase at approximately 400 mm TL, reached a maximum inner clasper length of 10% TL between 490 and 540 mm TL, and did not increase further in relative length > 540 mm TL (Figure 9a). Specimens > 550 mm TL showed negative allometry in the ratio of clasper length to TL. Therefore, some A. brunneus males had fully calcified terminal clasper cartilages and were considered mature with an inner clasper length 6% TL.

Apristurus kampae adult males also had an inner clasper length 6 to 10% TL, which was reached at ≥ 500 mm TL (Figure 9b). The sample size was insufficient to determine the change in clasper length ratio in A. kampae juveniles and adolescents as compared to adults.

Parmaturus xaniurus adult males had an inner clasper length 10 to 16% of their TL (Figure 9c).

Clasper length increased rapidly after 375 mm TL and maximum clasper length occurred at approximately 400 mm TL. However, calcification of the terminal clasper elements was not always present in specimens 400 to 450 mm TL. There was no evidence of negative allometry in the clasper ratio of P. xaniurus.

Oviducal Gland Development

Oviducal gland width increased with TL in all three species but remained within 4 to 6% TL

(Figure 10). At approximately 400 mm TL, A. brunneus oviducal gland width began to increase from 1% TL to between 2.75 and 5% TL in adult and gravid female specimens ≥ 475 mm TL

(Figure 10a). The oviducal gland width percentage of TL remained in the 2.75 to 5% TL range for mature females, even as TL continued to increase.

Apristurus kampae adult females (including gravid individuals) had an oviducal gland width 2.5 to

4% TL (Figure 10b). These adult females were ≥ 500 mm TL. Oviducal gland measurements were available for only 5 immature (juvenile and adolescent) females. The remainder was museum specimens that could not be dissected.

Parmaturus xaniurus adult and gravid females had an oviducal gland width between 2.5 and 6%

TL (Figure 10c). Some adolescent females had an oviducal gland width in this range and an

oviducal gland that appeared to be fully developed, but were determined to be immature based

upon oocyte size and ovary development.

Oocyte Development

Oocyte diameter increased with TL during reproductive development in all species, and continued

to increase with size after reproductive maturity was reached (Figure 11). The smallest adult A.

brunneus females (approximately 480 mm TL) had oocyte diameters 12 to 17 mm and the largest

females (≥ 680 mm TL) had oocytes 15 to 20 mm in diameter (Figure 11a).

Apristurus kampae females had mature oocytes between 15 and 20 mm diameter (Figure 11b).

These females with mature oocytes were ≥ 475 mm TL. Three juvenile and adolescent females

had immature oocytes 3 to 4 mm diameter.

In P. xaniurus, oocyte diameter first began to increase at approximately 400 mm TL (Figure 11c).

The smallest adult females (approximately 425 to 450 mm TL) had mature oocytes 10 to 15 mm

diameter. The largest P. xaniurus females (≥ 525 mm TL) had 20 to 25 mm diameter oocytes.

There was no relationship between the number of mature oocytes and adult female TL for any

species (Figure 12). Adult A. brunneus females had between 1 and 16 mature oocytes (Figure

12a). Apristurus kampae adult females had 4 to 8 mature oocytes (Figure 12b). Parmaturus xaniurus adult females had between 1 and 11 mature oocytes (Figure 12c). Some adolescent female P. xaniurus had fully developed, vascularized ovaries before their oviducal glands were

fully developed or they were reproductively mature. This was not observed for either species of

Apristurus.

SIZE AT MATURITY

Apristurus brunneus

Size at first, 50% and 100% maturity was based on study of 317 males and 394 females (Table 7,

Figure 13a). The smallest mature male, which was determined to be size at first maturity, was

488 mm TL. Using logistic regression, it was determined that fifty percent of males were mature at 514 mm TL. All A. brunneus males were mature at 547 mm TL. The largest male was 693 mm TL. The smallest mature female was 485 mm TL. Fifty percent of females were mature at

501 mm TL. All female A. brunneus females were mature at 581 mm TL. The largest female was 660 mm TL. Male and female size at fifty percent maturity estimates were significantly different from each other based upon 95% CI (P < 0.05).

Size of the smallest mature and largest immature male and female A. brunneus varied by latitudinal region (Table 8). The smallest mature male (520 mm TL) was from central California and the largest immature male was from Washington (546 mm TL). Size at first maturity was not significantly different by latitudinal region (df = 5, P > 0.25). Size of the largest immature male increased with latitude but was not statistically different among regions (df = 5, P > 0.25). The smallest mature female (485 mm TL) was from central California and the largest immature female was from northern California (581 mm TL). No mature females were found in the Washington region. Size at first maturity varied between 46°N to 38°N latitude (mean = 540.5) and 38°N to

32°N latitude (mean = 485.5) but was not significantly different by latitudinal region (df = 4, P >

0.25). Sizes of the largest immature females were not statistically different among regions (df =

5, P > 0.25).

Apristurus kampae

First, 50% and 100% maturity estimates were based on 52 male and 45 female A. kampae, including museum specimens (Table 7, Figure 13b). The smallest mature male was 486 mm TL and the largest immature male was 484 mm TL. Fifty percent maturity of males was reached at approximately 485 mm TL. This estimate was based on the average between the largest immature and smallest mature individuals, because there was no overlap in sexual maturity among size classes in the male specimens available. All A. kampae males were mature at 486 mm TL. The largest male was 647 mm TL. The smallest mature female was 484 mm TL and all females were mature at 539 mm TL. The largest immature female was 537 mm TL. Fifty percent maturity of females was reached at 490 mm TL. Maximum length of females was 590 mm TL. Male and female sizes at fifty percent maturity estimates were not significantly different from each other based upon 95% CI (P > 0.05).

Parmaturus xaniurus

Size at first, 50%, and 100% maturity was determined from 140 male and 236 female specimens

(Table 7, Figure 13c). The smallest mature male was 409 mm TL and all males were mature at

478 mm TL. The largest male was 512 mm TL. Fifty percent maturity of males was reached at

444 mm TL. The smallest mature female was 369 mm TL and all females were mature at 543 m

TL. The largest immature female was 542 mm TL. Fifty percent maturity of females was reached at 501 mm TL. The largest female was 579 mm TL. Male and female sizes at fifty percent maturity estimates were significantly different from each other based upon 95% CI (P <

0.05).

REPRODUCTIVE SEASONALITY AND FECUNDITY

Adult male and female A. brunneus had some months in which GSI was significantly elevated, but there was no corresponding decrease in HSI, based on 95% CI bars (Figure 14). Adult A. brunneus males had an increase in GSI in May (n = 2; Figure 14a). However, the associated change in HSI in May was not significant (n = 6; Figure 14b). Females had a significant increase in GSI in May (n = 1) and June (n = 4) as compared to all other months except July and August

(Figure 14c). As with the males, there was no significant associated seasonal variability in HSI values based on overlap of 95% CI bars (Figure 14d).

The majority of A. kampae specimens were obtained from preserved museum collections (37 of

52 males and 35 of 45 females examined); therefore GSI’s and HSI’s could not be measured or calculated for this species.

Gonadosomatic indices and HSI for adult P. xaniurus males and females did not reflect a relationship between gonad and liver mass (Figure 15). Parmaturus xaniurus males exhibited an increased trend in GSI in April through July (Figure 15a). However, this was not significant based on 95% CI. Male HSI values remained relatively consistent throughout the year and were not significantly different (Figure 15b). Adult females had a significant an increase in GSI in June

(n = 7; Figure 15c). There was no significant associated seasonal variability in HSI values

(Figure 15d).

Gravid females were found in all months of the year in A. brunneus, but not in A. kampae or P. xaniurus (Table 9). From March through August, ≥ 48% of all adult female A. brunneus had egg cases (n = 113). Apristurus kampae adult females were only collected in July through

November, and gravid females were found in all months except August. In September and

October, ≥ 50% of adult A. kampae females were gravid. The greatest proportion (44 to 50%) of gravid P. xaniurus was found from July through August, and no gravid females were found

January through March or November (n = 89).

Egg case length was not significantly correlated with female total length for A. brunneus or P. xaniurus (Figure 16). Egg case lengths of A. brunneus remained consistent (n = 39 females, mean = 63.0 mm ± 4.7 mm), and were not significantly related to female total lengths (R2 = 0.08,

Figure 16a). An insufficient number of A. kampae egg cases (n = 7 gravid females) were found to identify any relationship with female total length. There was a trend of increasing P. xaniurus

egg case length with female total length, but it was not significantly correlated (R2 = 0.34, n = 22

females, Figure 16b).

ONTOGENY

Egg Case Morphology

The egg case of A. brunneus is approximately 52 to 72 mm long and 22 to 30 mm maximum

width (Figure 17a). It has long tendrils projecting from either end. The tendrils on the anterior

end are thin and fibrous, whereas the posterior tendrils are thicker and tightly coiled, tapering at

the ends. The body of the case exhibits the characteristic vase-shape of scyliorhinid egg cases,

and was a golden-yellow color when removed from the female. The egg case maintained this

color although becoming slightly more opaque through fixation in 10% formalin and preservation

in 70% ethanol. In seawater, after approximately one month, the egg case turned a dark brown

color. The surface of the egg case appears smooth. No anterior horns are present, as the

lateral ridges of the keel (the lateral flange) do not continue distal to the anterior edge. The

lateral ridges of the keel continue just slightly past the posterior edge and taper sharply medially,

in close proximity with one another. Approximately 6 to 8 small hair-like filaments, 2 to 4 mm in

length, protrude from the posterior edge. The lateral keels are more squarely shaped with

rounded edges in cross-section and run the length of the egg case.

The egg case of A. kampae is small in size, approximately 61 to 69 mm long and 23 to 24 mm

maximum width (Figure 17b). It has a rounded vase-like shape, narrowing about 25% of the

length from the anterior end. This narrow section is the point of the minimum width of the egg

case, approximately 18 mm. The surface is smooth and lustrous in appearance. The egg case

was honey-yellow in utero and turned light olive-brown after fixation in 10% formalin and

preservation in 70% ethanol. No anterior horns were present, as the lateral ridges of the keel did

not continue distal to the anterior edge. There is a very thin filamentous sheet along the anterior

edge of the egg case, extending not more than 2 to 3 millimeters, which was often found torn. The lateral ridges of the keel continue just slightly past the posterior edge and taper sharply medially, in close proximity with one another. There are no fibrous tendrils on the anterior or posterior ends of the eggcase. Approximately 8 to 10 small hair-like filaments, 2 to 3 millimeters in length, protrude from the posterior edge and fill in the area between the posterior keel ends. A similar thin filament of 4 to 6 mm in length also protrudes off each of the posterior keel ends.

The lateral keels are gently sloped in cross-section and run the length of the egg case.

In P. xaniurus, the egg case is long, 67 to 100 mm, and wide, 26 to 39 mm maximum width, with

long tendrils projecting from either end (Figure 17c). Like A. brunneus, the tendrils on the

anterior end are thin and fibrous, whereas the posterior tendrils are thicker and tightly coiled,

tapering at the ends. This egg case also exhibits the characteristic vase-shape appearance but

is less narrow near the anterior end than the A. brunneus and A. kampae cases. The egg case

was golden-yellow when removed from the female, but became dark olive-brown after fixation in

10% formalin and preservation in 70% ethanol. In seawater, the egg case became dark brown-

black after approximately one month. The lateral ridges of the keel continue just slightly past the

anterior and posterior edges, creating short horns that extend into tendrils. The lateral keels are

T- shaped in cross-section and run the length of the egg case. One egg capsule was found in

each oviduct with one egg present in each capsule. Three of twenty four gravid females (13%)

were observed to contain only one egg case, all of which were located in the left oviduct.

Egg Case Distribution

Historic NMFS trawl data showed that egg cases of A. brunneus were found from 1995 through

2001 between 46°N and 34°N latitude (Figure 18). Egg cases were located between 300 and

400 m depth (n = 131 locations, mean depth = 340 ± 65 m) in areas of rocky vertical relief, at an

average water temperature of approximately 5°C. Egg cases caught in trawls were either fully

tanned bundles of several cases, or were single, untanned cases expelled from a gravid female

during capture. Egg cases are originally translucent yellow (untanned) and turn a darker color

after being in seawater for at least a month (tanned). Bundles of egg cases consisted of two or more cases attached together by entangled tendrils. On two occasions, eight months apart, single bundles of approximately 475 A. brunneus egg cases were trawled from the same location

off northern California, at 39°N latitude.

Large bundles of A. brunneus egg cases were also identified in Monterey Bay, CA (Figure 19) using archived annotated ROV footage from MBARI cruises from 1989 through 2003. Bundles of egg cases were species specific, with Apristurus brunneus and P. xaniurus egg cases often

observed within 12 to 18 centimeters of each other but were never attached to the same bundle.

Translucent yellow, untanned egg cases, indicating recent oviposition, were visible in video

footage captured year-round. Adult catsharks were never seen in the same video footage as

egg cases.

Egg Case Habitat

Apristurus brunneus and P. xaniurus egg cases were observed in situ by ROV camera and were

associated with specific habitats in areas of rocky vertical relief in the Monterey Bay region

(Figure 20). Egg cases were located typically found between 300 and 500 m depth (n = 124

locations, mean depth = 427 ± 234 m). In central California, average water temperature at this

depth was approximately 5°C. Egg cases were attached to the substrate by long, fibrous

tendrils. Apristurus brunneus cases were observed attached to filter feeding invertebrates such as sponges (Aphrocallistes vastus; Figure 20a) and gorgonians (Euplexaura marki; Figure 20b).

Parmaturus xaniurus egg cases were also attached by their long tendrils to substrates such as corals (Antipathese sp.; Figure 20c), hydroids and compound ascideans (Figure 20d), and other egg cases (Figure 20e). In turn, a P. xaniurus egg case provided substrate for the attachment of other sessile invertebrates, such as a filter-feeding anemone (Figure 20f). It was not possible to determine the substrate type to which all egg cases were attached in the video footage available.

Therefore, it was also not possible to determine if the substrate or invertebrates associated with the different species of egg cases was species-specific.

Predation on Egg Cases

Some possible predation of egg cases was observed in situ on video footage captured by ROV, where egg cases were in contact with invertebrates capable of boring through the hard case

(Figure 21). Apristurus brunneus egg cases were covered by invertebrates such as large sea stars (Rathbunaster californicus, Figure 21a) and gastropods (Boreotrophon tripherus, Figure

21b). It was not possible to determine if bore holes were present in any of the egg cases observed in ROV video footage because of the poor resolution and low magnification of many of the still frames taken from the video footage.

Potential predation events were also observed while collecting P. xaniurus egg cases from the

Monterey Bay Aquarium (MBA). On three occasions, the tendrils of egg cases were pulled from the oral disc of large sea stars and urchins (A. fragilis) to remove the egg case from the tank.

Also, three recently-deposited egg cases were found with the anterior and posterior ends bitten off (Figure 22). This egg case was lying next to the head of a shortspine thornyhead,

Sebastolobus alascanus, which was approximately 60 cm TL.

Embryonic Development

Egg case bundles typically consisted of cases in varying stages of development, from recently deposited cases on the surface of the bundle to hatched, empty cases underneath. In many of the more recently deposited egg cases, those closer to the surface of the bundle, it was possible to observe the developing embryo by candling the case (Figure 23a). As the egg case tanned and became darker from exposure to seawater, it became increasingly difficult to see the embryo within the egg case. Embryos were not observed to be very active during development (Figure

23b) and were often resting on top of their egg yolks.

Parmaturus xaniurus egg cases were collected weekly from adults maintained at the MBA and incubated in 10°C seawater until hatching (Table 10). Parturition of the egg case from the female was known to be within a seven day period. Five juveniles (3 females and 2 males) hatched after 9 to 12 months of incubation at this temperature (100 to 122 mm TL). Hatchlings from eggcase pairs deposited by a single female hatched 2 to 6 days apart. All hatchlings lived at least one month and showed no signs of developmental deficits. Hatchlings were not measured on a regular basis because handling induced petechiae of the fins, a sign of stress in elasmobranchs. One female lived a year and grew 30 mm in length during that time. However, growth rate was extremely variable and another female grew 28 mm in approximately 6 months. This second female was observed to eat every time food (Artemia) was offered, usually two to three times a week, whereas the first female usually ate only once a week. Hatchlings that expired were observed to feed only intermittently (once every week to two weeks) or not at all. DISCUSSION

DISTRIBUTION

As with all fishing surveys, distribution and frequency of abundance information here may be biased by coverage area and gear selectivity (Compagno et al. 1991). Both trawl and longline methods of fishing introduce additional biases: bottom trawls cannot be completed over rough bottom and longlines only reflect the distribution of fishes that fed on the baited hooks. Many demersal fishes may successfully evade a bottom trawl. Longlines, which were set over untrawlable grounds, may target larger fish and those fishes more closely associated with rugged topography. In the central California region, where both bottom trawl and longline fishing was conducted, there was a conspicuous difference in species composition by fishing gear type.

Apristurus brunneus (with the exception of gravid females) was more frequently encountered in bottom trawls and P. xaniurus was primarily found on longlines. This could be due to the life histories of these species (Bass et al. 1975, Richardson et al. 2000). The uniform dark color of

A. brunneus may be a camouflage adaptation indicative of association with deep water or rocky benthic substrate, whereas the dorso-ventral counter-shading of P. xaniurus suggests more midwater habitat utilization. Gravid A. brunneus females may have been caught more on longlines than in bottom trawls because of their association with rocky vertical relief areas for oviposition. Gravid females may also have fed on baited hooks due to increased metabolic needs incurred through reproduction. All of these factors may have influenced the latitudinal and bathymetric distribution results for the species in this study.

Latitudinal Distribution

The three catshark species were sympatric in latitudinal distribution for the central California region but did not encompass exactly the same geographic areas. Apristurus brunneus was the most wide-ranging scyliorhinid collected, and the only species caught north of 42°N latitude. It was abundant in all latitudinal regions sampled between 48°N and 32°N latitude. Reported to

46°N latitude (Ebert 2003), A. kampae was only found as far as 42°N latitude. However, this is not to say that this species range is only between 32°N and 42°N latitude. Apristurus kampae was rarely encountered and found only at great depths. An increased sample size may yield specimens outside of this range. Parmaturus xaniurus was found only as far north as 40°N latitude, although this species has previously been reported as far as 46°N latitude (Ebert 2003).

Historic NWFSC survey data from 1995 through 2000 indicated that P. xaniurus was not found

north of 40ºN latitude during previous annual shelf and slope trawl surveys. Scyliorhinid

distribution can be limited by oceanographic features such as temperature, elevated ridges, and abyssal trenches that are difficult for some of them to traverse as benthic, sluggish swimmers

(Nakaya and Shirai 1992). The Mendocino Ridge and Gorda Escarpment, which lie at approximately 40.5°N latitude, are also the site of diffuse cold seeps and elevated currents

(Drazen et al. 2003). The temperature change and geologic structure of this area may act as a

barrier to habitat utilization for some catsharks. However, the presence of geologic obstacles

does not adequately explain the limits of P. xaniurus distribution, as the juveniles of this species

inhabit the midwater (Lee 1969), or why the range of A. brunneus is not limited at the same

latitudes.

Bathymetric Distribution

The bathymetric distributions of A. brunneus, A. kampae, and P. xaniurus are distinctive but do exhibit spatial overlap. Apristurus brunneus, which had the largest bathymetric range, had broad

latitudinal sympatry, but a narrow bathymetric allopatry with A. kampae within the central

California region. Apristurus brunneus and P. xaniurus were commonly caught together in

central California. A similar situation of narrow bathymetric and latitudinal sympatry is found in

scyliorhinids off southern Africa (Compagno et al. 1991). However, P. xaniurus was never

caught in the same haul as A. kampae, and the two may be considered bathymetrically allopatric.

Deep-sea benthic elasmobranchs may exhibit depth segregation to reduce competition for

resources (Carrasson et al. 1992). Apristurus brunneus, A. kampae, and P. xaniurus may be in

competition for food sources, either interspecifically or intraspecifically, because their distributions

overlap and they have similar diets among all size classes (Jones and Geen 1977, Cross 1988, Ebert 2003). The ecological consequences of bathymetric overlap of these three species, such as competition for food resources, are unknown at this time. These catshark species have

overlapping but different distribution patterns.

Bathymetric distribution also revealed depth segregation within species. Juvenile P. xaniurus are

primarily mesopelagic, and utilize the midwater region as a nursery ground (Lee 1969, Cross

1988, Nakaya and Shirai 1992). Ebeling et al. (1970) reported depth segregation of juvenile and adult P. xaniurus in the Santa Barbara Basin in southern California in their study using opening and closing Isaacs-Kidd midwater trawls. Cross (1988) determined that juveniles of A. brunneus and P. xaniurus were conspicuously absent in southern California when fishing by both bottom trawl and longline. Bottom trawls conducted in southern California by the NWFSC yielded a larger proportion of juvenile P. xaniurus (34%) than the more northerly trawls reported here. The juveniles in this southern region were also smaller in size. These tows were conducted in shallower waters than those to the north. Therefore, the paucity of newly hatched and young of the year P. xaniurus (smaller than 250 mm TL) in the north could be due to their inhabiting more shallow, midwater regions than the adults (Lee 1969).

WEIGHT-LENGTH RELATIONSHIPS

Weight-length relationships among all species from the entire study range were similar and were only significantly different among species with sexes combined, but not by species or sexes alone. The regression coefficients in female and male Apristurus brunneus appeared greater in

southern California than in Washington, but there was no significant difference or clear gradient in

change of regression coefficients latitudinally. When compared to weight-length relationships

determined by Cross (1988) and Balart et al. (2000), there was no significant difference in weight-

length relationship regression coefficients among latitudinal regions of P. xaniurus (df = 2, P >

0.25).

SEX RATIOS

Sex ratios of A. brunneus were approximately equal to 1:1 in Washington, Oregon, and southern

California, but the number of females was approximately 30% greater than that of males in northern and central California. Parmaturus xaniurus females were caught 41% more frequently than males in central California. Greater frequencies of females to males have been observed in other scyliorhinid sharks, including the swellshark, Cephaloscyllium umbratile (Taniuchi 1988), the redspotted catshark, Schroederichthyes chilensis (Fariña and Ojeda 1993), and the lesser spotted dogfish, Scyliorhinus canicula, (Ellis and Shackley 1997). Disparity in sex ratios in sharks may be a factor of sexual segregation due to bathymetric distribution (Bullis 1967) or in sampling bias.

SEXUAL DIMORPHISM

In most shark species, males reach sexual maturity at a smaller size than females of the same species (Taniuchi 1988, Ellis and Shackley 1997, Cortés 2000, Ebert 2003). One benefit of

females maturing at larger sizes is that females that are larger in size tend to have larger or more

numerous young, which are less susceptible to predation (Branstetter 1990). Cortés (2000)

stated that the number and size of offspring of A. brunneus may increase with female TL and that the number of offspring produced by P. xaniurus may increase with female TL. Size at 50% maturity in P. xaniurus males was 57 mm shorter than female size at 50% maturity, whereas sexual maturity was reached at approximately the same lengths for males and females in both A.

brunneus and A. kampae. Within the family Scyliorhinidae, male reproductive maturity occurred

at an equal or larger size than females in 10 of 17 oviparous species (Cortés 2000).

Male scyliorhinids may grow to an equal or longer maximum TL than females of the same

species, whereas females often attain the larger maximum size in most other shark families

(Compagno 1984, 1988a; Cortés 2000; Ebert 2005). In both A. brunneus and A. kampae, males

reached greater maximum TL than females. However, in P. xaniurus, the male maximum TL

was smaller than the maximum TL for females. Males in both Apristurus species were approximately the same size as females at 50% maturity, and grew to a longer maximum TL.

Cortés (2000) suggested that the males of some elasmobranch species may grow at a faster rate than females of the same species.

VARIABILITY IN SIZE AT MATURITY AND REPRODUCTIVE DEVELOPMENT

Males

Sizes at maturity determined in this study were different from those determined at lower latitudes by Cross (1988) and Balart et al. (2000). In southern California, Cross (1988) determined that A. brunneus males reached sexual maturity between 450 and 500 mm TL and P. xaniurus between

375 and 425 mm TL. Balart et al. (2000) determined reproductive maturity in P. xaniurus to occur at 340 mm TL off Baja California Sur. These estimated sizes are substantially less than values for 50 percent maturity determined in this study for A. brunneus and P. xaniurus, although the estimate by Cross (1988) for A. brunneus falls within the range of the smallest mature and largest immature males found in southern California. Size at sexual maturity can vary over time, as a result of changes in population size, environmental conditions, or geographic clines (Horie and Tanaka 2000). The studies by Cross (1988) and Balart et al. may have provided different size at maturity results because of fluctuation in population structure or temperature since the time of their research.

Maturity estimates may also be biased by the technique used to determine maturity. Cross

(1988) used relative change in clasper length and gonad weight, while Balart et al. (2000) used clasper length alone. Balart et al. (2000) examined male individuals 117 to 380 mm TL, which were smaller than the first mature P. xaniurus in central California. Adolescent P. xaniurus males exhibited asynchronous development of reproductive structures; these small individuals had claspers that were not calcified, although of equal lengths as adult claspers, and smaller testes than the adult males. The estimate by Balart et al. (2000) was based only on clasper length, and did not mention calcification of clasper elements. Therefore, it is possible that those individuals were not actually reproductively competent.

Females

As with the males, female A. brunneus and P. xaniurus also reached a size at 50 % maturity at a

greater total length than females in previous studies. In British Columbia coastal waters, all

females over 450 mm TL were determined to be mature and had vascularized eggs; some also

had egg cases (Jones and Geen 1977). These mature females are considerably smaller than

the smallest mature A. brunneus found from Washington to San Diego (477 mm TL). The largest

A. brunneus female found in Washington was immature at 544 mm TL. Apristurus brunneus

studied by Jones and Geen (1977) were collected in shallower waters, to 369 m depth, where

water temperature was approximately 8°C. Elevated seawater temperatures in this shallower

region may facilitate faster growth and maturation rates in scyliorhinids, as it does in other

elasmobranchs (Parsons 1993). Size at first maturity for female A. brunneus tended to be larger

above and smaller below 38°N latitude, although this difference was not significant. All female P.

xaniurus studied by Balart et al. (2000) in Baja California Sur (n = 22) were between 108 to 350

mm TL and sexually immature.

Cross (1988) estimated maturity of female A. brunneus and P. xaniurus between 425 and 475

mm TL in southern California, using oocyte number and diameter to determine maturity, whereas

this study used oviducal gland development. Using oocyte diameter in the case of P. xaniurus is inadequate because females of this species also develop asynchronously and exhibit fully developed and vascularized oocytes while still juveniles. The oocytes in immature P. xaniurus females reach diameters comparable with mature females well before the oviducal gland is fully formed.

There may be distinctions in reproductive maturity and seasonality based upon variations in bathymetric distribution (Bullis 1967, Carrassón et al. 1992), latitude (Parsons 1993, Horie and

Tanaka 2002), or isolation by environmental variables (Horie and Tanaka 2000). Smaller size at maturity estimates could be a factor of the lower latitude of the study areas in Cross (1988) and Balart et al. (2000). Differences in maturity estimates could also be an artifact of the smaller sample sizes in previous studies. It was not possible to determine 50 percent maturity by regional distribution throughout the entire eastern North Pacific because the sample sizes were too small when subdivided by geographic location.

REPRODUCTIVE SEASONALITY AND FECUNDITY

Gonadosomatic and hepatosomatic indices may fluctuate as a result of the production of gametes and the metabolic costs incurred through reproduction. An increase in GSI implies reproductive readiness, which may occur at first reproductive maturity or at peak times of reproductive activity.

Hepatosomatic index values may vary because of the use of hepatic lipids in the formation of gametes or because of metabolic costs incurred during the processes of mate location and copulation. There is an inverse GSI-HSI relationship in some scyliorhinids at the onset of reproductive maturity (Craik 1978, Richardson et al. 2000). In S. canicula, GSI increases as HSI

decreases during mating seasons, presumably because hepatic lipids are involved in formation of

the egg yolk during vitellogenesis (Craik 1978, Sumpter and Dodd 1979, Hamlett and Koob 1999,

Koob and Callard 1999). Therefore, variation in the HSI was investigated as an indicator of

mating period, because coincident trends of the GSI and HSI should illustrate a seasonal trend of reproductive productivity and metabolic effort.

Disparity in the GSI-HSI relationship and the presence of gravid females year-round suggest that

A. brunneus and P. xaniurus do not have well-defined reproductive seasons. The HSI for these species did not fluctuate seasonally in association with GSI. Thus, either changes in HSI and

GSI may not be a reliable measure for gauging increase in seasonal reproductive effort in these species or else they do not exhibit seasonality in their reproductive cycles. An increase in GSI does not necessarily imply reproductive activity or fertilization (Maruska et al. 1996). Other

scyliorhinids, including C. umbratile (Taniuchi 1988), blacktip sawtail catshark, Galeus sauteri

(Chen et al. 1996), and S. canicula (Ellis and Shackley 1997), exhibit a peak in GSI but deposit

egg cases year round.

An increase in GSI may actually be indicative of the mating period for these species. Apristurus brunneus had an increase in GSI in May through June, but this did not necessarily coincide with an increase in gravid females, as the highest proportion of gravid females was found in the months both preceding and following the increase in GSI. The presence of egg cases in A. brunneus year-round coincides with the findings of Cross (1988). Parmaturus xaniurus females had in increase in GSI in June and were gravid in subsequent months. However, P. xaniurus in captivity at the Monterey Bay Aquarium, Monterey, California, did deposit fertile egg cases in all months during the time in which egg cases were collected for this study. Cross (1988) reported gravid female P. xaniurus in January, August, November, and December. Gravid females of all species had fully developed, mature oocytes; therefore, exhibit continuous oviposition and would be capable of reproducing again after egg case deposition.

The most congruent conclusion is that these species reproduce throughout the year and do not have a well-defined reproductive season. Mature females were either gravid or had mature oocytes throughout the year. Egg vitellogenesis is controlled by the pituitary gland which is in turn controlled by the hypothalamus (Dodd 1972, 1983). Seasonal cues that might stimulate hypothalamus activity and incite reproductive periodicity, such as light or temperature, may not fluctuate seasonally in the deep sea. Therefore it may be that these catsharks are less affected by seasonal reproductive cues.

Apristurus brunneus and P. xaniurus egg case length was not correlated to female TL, contradictory to Cross’s (1988) findings in southern California. This was most likely a coincidence of smaller sample sizes used in the southern California study. In fact, A. brunneus egg cases were almost the same size regardless of female TL. Increase in egg case size is assumed to allow embryos to attain larger sizes before hatching, which would be beneficial in avoiding predation.

Deposition of the right egg case before the left may be a reproductive characteristic for these fishes, as it is in some skates (Templeman 1982). A few females of each species had only one egg case, in the left oviduct, presumably the egg case from the right oviduct had already been deposited before capture. In most scyliorhinids only the right ovary is functional (Hamlett and

Koob 1999), and egg cases on the right side were always more developed and farther down the uterus than the left.

ONTOGENY

Implications of Egg Case Morphology

The egg case of A. kampae is distinctive because it lacks both the anterior and posterior tendrils found on many other egg cases of the genus Apristurus (DeLacy and Chapman 1935, Cox 1964,

Springer 1979, Iglesias et al. 2002). A reproductively-isolated population of swell sharks

(Cephaloscyllium ventriosum) off Santa Catalina Island in southern California produces an egg case without tendrils, while all other populations of this species produce egg cases with long

tendrils (Grover 1972a). Many scyliorhinids exhibit some form of long tendril or fibrous filament

extending from the anterior or posterior ends, and it has long been thought that these tendrils

may help to secure the egg case to some form of substrate (Springer 1979, Castro et al. 1988,

Able and Flescher 1991, Ellis and Shackley 1997, Hamlett and Koob 1999). In both aquaria and

ROV video footage, egg case tendrils were securely wrapped around erect sessile invertebrates,

thus anchoring the case. Egg case tendrils were soft and pliable immediately following

oviposition, and became hardened after exposure to seawater. Tendrils hardened around the

substrate on which they were entangled, which made them difficult to pull off their attachment

site.

Egg-laying by a scyliorhinid has been observed in aquaria, the onset of which can be marked by

protrusion of the posterior tendrils through the cloaca (Castro et al. 1988). The female circles the attachment point of a vertical structure and the anterior tendrils of the eggcase become entangled on the substrate. Anchorage of the egg case allows the female to pull against resistance, which may facilitate parturition of the egg case (Springer 1979, Castro et al. 1988).

In the genus Apristurus, the egg cases of only 12 of the recognized 35 species have been

described previously (Appendix 1). Of these, seven are known to have long fibrous tendrils: A.

brunneus, A. exsanguis, A. laurussoni, A. longicephalus, A. macrorhynchus, A. maderensis, and

A. melanoasper. All of these species, except A. longicephalus, are described as being

“brunneus-like.” Nakaya and Sato (1999) distinguished this “brunneus-like” group based on high spiral valve count, long upper labial furrow length, and discontinuous supraorbital sensory canals.

In addition, these species are generally elongate and slender, have small teeth, and are often found shallower than 1000 m depth.

The “spongiceps-like” group of Apristurus consists of A. aphyodes, A. fedorovi, A. kampae, A.

manis, A. microps, A. pinguis, A. profundorum, A. riveri, A. spongiceps, and A. stenseni, and is

characterized by lower spiral valve counts, upper labial furrows that are equal or shorter than

lower labial furrows, and continuous supraorbital canals (Nakaya and Sato 1999). These

species also tend to be robust, heavy bodied sharks, with large teeth, large rough dermal

denticles and placoid scales, and are typically found below 1000 m depth. The egg cases of A.

aphyodes (Iglesias et al. 2002), A. kampae, A. manis, A. microps, A. riveri, A. spongiceps, and

Apristurus sp. D (Last and Stevens 1994), which fits the adult spongiceps-group morphotype, all

lack fibrous tendrils. The remaining egg cases in this group are unknown.

As evident by ROV video footage, the tendrils of A. brunneus and P. xaniurus egg cases are

essential for attaching the egg case to benthic substrate. It has been assumed that egg case

suspension above the substrate was advantageous to avoid sediment obstructing the flow of

seawater through the case. The egg cases of the spongiceps-group catsharks studied all lacked

both tendrils and fibrous filaments. The oviposition sites of these cases within the environment

are unknown, but presumably the egg case is deposited directly onto the substrate. The horn shark, Heterodontus francisci, and the Port Jackson shark, H. portusjacksoni have been observed placing their egg cases into rocky crevices with their mouths (McLaughlin and O’Gower 1971,

Ebert 2003). It is unknown whether or not any scyliorhinids exhibit the same behavior.

The tendrils of egg cases also appear to be advantageous in anchoring the case to ease parturition from the female (Castro et al. 1988). This is an opportunity not afforded to those species of the spongiceps-group whose egg cases lack tendrils. Springer (1966, 1979) described a ring of firm white tissue surrounding the cloaca in adult female A. riveri and A. parvipinnis (both gravid and not), and postulated that this flat ring was useful in rubbing against the substrate to help dislodge the egg case from the cloaca. This ring of firm tissue was not observed in A. kampae specimens.

Variable egg case morphologies may have biological and ecological effects on oviposition. This is especially a concern for spongiceps-group catsharks, the egg cases of which lack tendrils that

might facilitate anchorage. Different egg case morphologies indicate that these catsharks might

differ phylogenetically, in life histories, or habitat utilization. The ecological implications of the

lack of tendrils on the egg cases of this group of scyliorhinids are unknown at this time.

Egg Case Distribution, Habitat, and Nursery Grounds

Use of nursery grounds is common among elasmobranch species (Branstetter 1990,

Simpfendorfer and Milward 1993, Ellis and Shackly 1997), enabling neonates to survive without

risk of predation by larger conspecifics (Morrissey and Gruber 1993). In Monterey Bay, adult A.

brunneus and P. xaniurus were not caught in the same locations that egg cases were observed in

ROV video. Conversely, egg cases were not caught in the central California trawls where adults

of these species were found. Juvenile P. xaniurus exhibit a mesopelagic stage and utilize the

midwater region as a nursery ground (Lee 1969, Cross 1988, Nakaya and Shirai 1992). A

similar situation was reported for the blackmouth catshark, Galeus melastomus, which exhibits depth segregation by size and maturity class, where juveniles utilizing shallower habitat areas than mature adults (Tursi et al. 1993).

Egg case deposition sites identified by ROV video footage taken in the Monterey Bay area provided information on the precise locations used for nursery sites. Specific attributes to those areas acting as nursery grounds for A. brunneus and P. xaniurus egg cases include location at the shelf-slope break and upper continental slope, high vertical relief with substrate rugosity, and circulating water currents. Egg cases were often seen being moved by the current in ROV video footage. High vertical relief and increased water currents are important aspects of reproductive aggregation sites in Scyliorhinus retifer (Able and Flescher 1991) and some deep-sea teleosts and cephalopods (Drazen et al. 2003). Water circulation may be especially important for providing adequate oxygenation for embryogenesis when egg cases are clumped together in large aggregates. It was observed that egg cases are deposited on massive bundles of older cases that have long since hatched and started to degrade. Continued oviposition in specific locations characterizes these areas with high vertical relief and circulating currents as essential fish habitat.

Predation on Egg Cases

Embryonic catsharks are at risk of interspecific predation as a result of their sessile nature.

Boring by marine gastropods is a common cause of elasmobranch embryo mortality (Grover

1972b, Cox and Koob 1993, Smith and Griffiths 1997, Lucifora and Garcia 2004). The muricid

gastropod, Boreotrophon tripherus, which was observed on an A. brunneus egg case by ROV

video, leaves characteristic circular bore-holes in its prey. Large sea stars, brittle stars, and sea

urchins may also prey upon elasmobranch egg cases (Cox and Koob 1991). Elasmobranch

eggs have been found in the stomachs of other elasmobranch species (Ebert 1991, Long 1996,

Barrull and Mate 2001), teleosts (Grover 1972b, Long 1996), and a number of marine mammals, including sperm whales, elephant seals, and sea lions (Bor and Santos 2003). It is possible that these mammals consumed the egg cases by capturing a gravid female and that the egg cases were inadvertently ingested.

Egg cases offer protection to the developing embryo, in the form of the durable structure of the case itself. Some benthic invertebrates release anti-biofouling toxins that might help reduce predation, and these toxins may be transferred to the egg case surface (Ellis and Shackley 1997).

Alternatively, the egg cases of S. canicula produce antifouling heterogeneous microbial biofilms

(Thomason et al. 1994). If anti-fouling properties are absent in the three species studied, and bacterial or algal matter accumulates on the egg case, invertebrates on the outside of the egg cases may be grazing and not preying on the embryos. Egg cases may also be protected by being deposited in large bundles by decreasing the likelihood of predation on any one case when enclosed in a large group. Alternatively, a large aggregation of egg cases may attract potential predators.

Embryonic Development

The rate of embryonic development of A. brunneus and P. xaniurus in situ has not yet been determined. Temperature instrumentation on the ROV recorded incubation temperature of A. brunneus and P. xaniurus egg cases in situ to be approximately 5 to 7°C. Incubation time for A. brunneus under captive conditions is about 24 to 27 months in 5°C water (G. van Dykhuizen, pers. comm.). Jones and Geen (1977) reported an accelerated embryonic growth rate of A. brunneus in aquaria at approximately 10°C seawater and speculated that time to hatching under natural conditions was approximately one year. Under elevated temperature conditions in aquaria, P. xaniurus incubation time was approximately 9 to 12 months; this may represent

accelerated embryonic development. It is probable that increased water temperature

accelerates growth and development in both A. brunneus and P. xaniurus embryonic catsharks.

Apristurus brunneus, A. kampae, and P. xaniurus are found along the continental slope of the

eastern North Pacific. Previous studies of their life histories were limited to the northern and southern extent of their ranges. Trawl sets caught greater numbers of A. brunneus and longline

sets were comprised mostly of P. xaniurus. Depth segregation occurs among species, and in the

case of P. xaniurus among maturity classes. Sexual maturity was reached at larger sizes in

catsharks at higher latitudes than those previously studied. Reproduction occurs throughout the

year, without a defined breeding season. Egg cases are deposited in specific areas of vertical

relief. These nursery sites are revisited by females, as evidenced by embryos of varying

developmental stages and hatched cases in egg case bundles. Variations in egg case

morphology may have phylogenetic and ecological implications that have not yet been studied.

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Appendices.

47 Table 1. Criteria used to determine sexual maturity stages (embryonic, juvenile, adolescent,

adult and gravid female) of male and female scyliorhinids.

Maturity stage Males Females Embryo In egg case In egg case Juvenile Claspers not extending past posterior No discernible oviducal gland formed, no end of pelvic fins, testes white development of ovary in Apristurus and flaccid, epididymis not visible spp., ova ≤ 1 mm diameter in Parmaturus Adolescent Claspers extending past posterior Early oviducal gland small and heart- end of pelvic fins but not calcified, shaped, ova < 2 mm, vascularization epididymis partially coiled, testes of ovary pale pink and flaccid Adult Claspers calcified, epididymis very Oviducal gland large and bulbous, eggs coiled, testes red, firm and robust ≥ 14 mm diameter Gravid adult n/a Gravid or having a stretched uterus indicating recent parturition of egg case(s)

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.

# of Depth Sets with A. A. P. Source Sets (m) Catsharks brunneus Depth (m) kampae Depth (m) xaniurus Depth (m) NWFSC Trawls 647 24 - 1341 108 486 177- 1209 21 738 - 1233 50 269 - 563 SWFSC Trawls 115 170 - 667 11 81 178 - 656 0 211 - 564 19 178 - 564 SWFSC Longlines 129 327 - 800 22 83 361 - 800 0 302 327 - 800 TOTAL 891 141 650 21 371

49 Table 3. Geometric mean weight-length relationships for Apristurus brunneus, Apristurus kampae, and Parmaturus xaniurus for all specimens from the eastern North Pacific.

Species Sex n W = aLb R2 Source Apristurus brunneus M 318 W = 2.444 x 10-6 L3.027 0.950 This study M 90 W = 3.577 x 10-6 L2.971 0.966 Cross (1988) F 410 W = 3.679 x 10-7 L3.341 0.949 This study F 149 W = 2.379 x 10-6 L3.059 0.899 Cross (1988) Apristurus kampae M 16 W = 1.140 x 10-3 L2.090 0.831 This study F 8 W = 1.849 x 10-4 L2.421 0.830 This study Parmaturus xaniurus M 157 W = 4.538 x10-5 L2.600 0.905 This study M 29 W = 6.76 x 10-7 L3.31 not given Balart et al. (2000) M 89 W = 3.163 x 10-6 L3.427 0.934 Cross (1988) F 243 W = 1.076 x 10-5 L2.845 0.831 This study F 22 W = 9.53 x 10-7 L3.22 not given Balart et al. (2000) F 76 W = 9.377 x 10-6 L3.242 0.965 Cross (1988)

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).

Location Sex n W = aLb R2

Washington M 37 W = 1.033 x 10-6 L3.163 0.969

F 48 W = 2.562 x 10-6 L3.039 0.960

Oregon M 72 W = 9.697 x 10-7 L3.173 0.974

F 68 W = 8.966 x 10-8 L3.557 0.946

northern California M 59 W = 1.827 x 10-6 L3.077 0.980

F 87 W = 7.807 x 10-6 L2.854 0.965

central California M 101 W = 1.400 x 10-6 L3.109 0.958

F 149 W = 7.030 x 10-7 L3.239 0.931

southern California M 35 W = 2.139 x 10-7 L3.446 0.932

F 37 W = 4.376 x10-6 L2.957 0.987

51 Table 5. Sex ratios of male and female Apristurus brunneus, A. kampae, 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

2 2 χ 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.

Species Region Sex Ratio (F:M) Significance Apristurus brunneus Washington 1 : 0.74 ns Oregon 1 : 1.04 ns northern California 1 : 0.70 * central California 1 : 0.68 ** southern California 1 : 0.97 ns A. kampae central California 1 : 1.20 ns Parmaturus xaniurus central California 1 : 0.59 ***

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.

Maturity Apristurus brunneus Apristurus kampae Parmaturus xaniurus Stage Males Females Males Females Males Females Juvenile 224 218 6 7 43 38 Adolescent 16 58 5 8 49 109 Adult 77 55 43 19 48 65 Gravid n/a 63 n/a 9 n/a 24 TOTAL 711 97 376

53 Table 7. Size at first, 50% and 100% maturities (mm TL), for all 3 species of scyliorhinids collected in the eastern North Pacific combined. The estimate for 50% maturity for A. kampae males is based on mathematical estimate, because there was no overlap in sexual maturity among size classes in the specimens available.

Species Sex n First (mm TL) 50% (mm TL) 100% (mm TL) Apristurus brunneus male 317 488 514 547 female 394 485 501 581 Apristurus kampae male 52 486 c. 485 486 female 45 484 490 539 Parmaturus xaniurus male 140 409 444 478 female 236 369 501 543

54 Table 8. Size at first maturity and largest immature male and female Apristurus brunneus (mm

TL) by latitudinal region (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)). No mature females were caught in the Washington region.

Males (mm TL) Females (mm TL) Smallest Largest Smallest Largest n mature n Immature n mature n Immature Washington 3 550 36546 0 none 53 544 Oregon 6 587 66 522 14 540 55 566 northern California 6 520 55 507 15 541 72 581 central California 50 547 54 492 97 485 55 527 southern California 8 488 28 408 7 486 29 501

55 Table 9. Proportion of gravid females of total mature Apristurus brunneus, A. kampae, and

Parmaturus xaniurus females by month. Apristurus kampae adult females were only caught from

July through November. Parmaturus xaniurus were not caught in the month of May because of limited fishing resources.

Apristurus brunneus A. kampae Parmaturus xaniurus

Proportion Proportion Proportion Month n Gravid n Gravid n Gravid January 4 0.50 1 0.00 February 6 0.33 9 0.00 March 17 0.85 6 0.00 April 15 0.67 15 0.20 May 4 0.50 June 6 0.67 7 0.14 July 21 0.48 3 0.33 17 0.47 August 15 0.80 2 0.00 10 0.44 September 12 0.17 8 0.50 9 0.50 October 12 0.25 3 0.67 7 0.14 November 1 1.00 5 0.20 6 0.00 December 3 0.33 2 1.00

56 Table 10. Incubation period, size at hatching, and growth of Parmaturus xaniurus maintained in aquaria at approximately 10°C. Egg cases were collected from the Monterey Bay Aquarium

(MBA), which houses adult males and females of this species.

Size at Total Expiration/ Date of Date of Hatching Growth Last Sex Oviposition Hatching (mm) (mm) Measurement female 04 Feb 03 06 Nov 03 107 30 01 Nov 04 male 04 Feb 03 08 Nov 03 103 2 21 Feb 04 female 10 Dec 03 24 Sep 04 122 28 14 Mar 05 female 10 Dec 03 30 Sep 04 121 2 17 Oct 04 male 25 Mar 04 14 Mar 05 100 n/a 14 Mar 05

57 Figure 1. Total Apristurus brunneus (n = 650) collected by Northwest Fisheries Science Center (NWFSC) trawl surveys in the eastern North Pacific from June 2001 through October 2004. These specimens were arbitrarily grouped by geographic area (A = Washington (48°N to 46°N latitude), B = Oregon (46°N to 42°N latitude), C = northern California (42°N to 38°N latitude), D = central California (38°N to 34°N latitude), and E = southern California (34°N to 32°N latitude)) for further distributional analysis (Figure 2). Bathymetric contours are scaled at 500 m depths.

58 Figure 2a. Apristurus brunneus (n = 92) collected by NWFSC trawl surveys off Washington (48°N to 46°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths.

59 Figure 2b. Apristurus brunneus (n = 141) collected by NWFSC trawl surveys off Oregon (46°N to 42°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths.

60 Figure 2c. Apristurus brunneus (n = 148) collected by NWFSC trawl surveys off northern California (42°N to 38°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths.

61 Figure 2d. Apristurus brunneus (n = 52) collected by NWFSC trawl surveys off central California (38°N to 34°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths.

62 Figure 2e. Apristurus brunneus (n = 71) collected by NWFSC trawl surveys off southern California (34°N to 32°N latitude) from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths.

63 Figure 3. Apristurus brunneus (n = 164) collected by trawl (red circles) and longline (yellow circles) surveys by the Southwest Fisheries Science Center (SWFSC) Santa Cruz lab in Monterey Bay off central California from June 2002 through March 2004. Bathymetric contours are scaled at 500 m depths. Frequency of abundance for males (A; n = 72) and females (B; n = 92) caught are separated by trawl (light bars) and longline (dark bars) catches.

64 Figure 4. Total Apristurus kampae (n = 97) collected by all surveys in the eastern North Pacific from June 2001 through October 2004, combined with catch locations of museum specimens. Specimens caught during this study are denoted by open green squares. Museum specimens are represented by squares with dark square in center. The star denotes the location of the holotype in the Gulf of California (28°N latitude). Bathymetric contours are scaled at 500 m depths.

65 Figure 5. Total Parmaturus xaniurus (n = 65) collected by NWFSC trawl surveys in the eastern North Pacific from June 2001 through October 2004. Bathymetric contours are scaled at 500 m depths.

66 Figure 6. Parmaturus xaniurus (n = 321) collected by trawl and longline surveys by the SWFSC Santa Cruz lab in Monterey Bay off central California from June 2002 through March 2004. Bathymetric contours are scaled at 500 m depths. Frequency of abundance for males (A; n = 117) and females (B; n = 204) caught are separated by trawl (light bars) and longline catches (dark bars).

67 0

200

400

600

800 Depth (m) Depth

1000

1200 A 1400 0 100 200 300 400 500 600 700 800 Total Length (mm)

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400

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800

1000

1200 Depth (m)Depth

1400

1600 1800 B 2000 0 100 200 300 400 500 600 700 Total Length (mm)

200

400

Depth (m) Depth 600

800 C 1000 100 200 300 400 500 600 Total Length (mm) Figure 7. Depth distribution of all maturity stages (red circle = juvenile, green triangle = adolescent, yellow square = mature, blue diamond = gravid) of Apristurus brunneus (A, n = 730), A. kampae (B, n = 97), and Parmaturus xaniurus (C, n = 376) collected by trawl and longline from 48°N to 32°N latitude. 68 A B C

EN CG

PP HP EN CR PP CR CR ER ER ER

RH RH RH CD CD

69 12

2 Inner Clasper Length (% TL) (% Length Clasper Inner 0 A

100 200 300 400 500 600 700 800 Total Length (mm)

4 InnerClasper LengthTL) (% 2 B 0 100 200 300 400 500 600 700 Total Length (mm)

4 Inner Clasper Length (% TL) (% Length Clasper Inner 2 C 0 100 200 300 400 500 600 Total Length (mm)

Oviducal Gland WidthOviducal TL) (% 1 A 0 100 200 300 400 500 600 700 Total Length (mm)

4.5

4.0

3.5

3.0

2.5 Oviducal Gland Width Gland TL) (% Oviducal 2.0 B 1.5 100 200 300 400 500 600 700 Total Length (mm)

2 Oviducal Gland Width Gland TL) (% Oviducal 1 C 0 100 200 300 400 500 600 Total Length (mm)

5 Oocyte Diameter (mm) Diameter Oocyte

100 200 300 400 500 600 700 Total Length (mm)

25 B

10 Oocyte Diameter (mm) Diameter Oocyte

0 100 200 300 400 500 600 700 Total Length (mm) 30 C 25

Oocyte Diameter (mm) 5

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16 A

Number of Mature Oocytes 4

0 460 480 500 520 540 560 580 600 620 640 660 680 Total Length (mm)

16 B

Number of Mature Oocytes 4

0 460 480 500 520 540 560 580 600 Total Length (mm)

16 C

Number of Mature Oocytes 4

0 350 400 450 500 550 600 Total Length (mm)

Figure 12. Number of mature oocytes versus total length of adult female Apristurus brunneus (A; n = 118), A. kampae (B; n = 11), and Parmaturus xaniurus (C; n = 89).

73 1.0 A. brunneus males (n = 319)317) A. brunneus females (n = 411)394) 0.8

0.6

0.4 Proportion Mature 0.2

0.0 A

200 400 600 800

1.0 A. kampae males (n = 53)52) A. kampae females (n = 46)45) 0.8

0.6

0.4 Proportion Mature Proportion 0.2

0.0 B

0 100 200 300 400 500 600 700

1.0 P. xaniurus males (n = 141)140) P. xaniurus females (n = 237)236) 0.8

0.6

0.4 Proportion Mature Proportion 0.2

0.0 C

100 200 300 400 500 600 Total Length (mm) Figure 13. Proportion of mature Apristurus brunneus (A), Apristurus kampae (B), and Parmaturus xaniurus (C). Solid lines designate maturity curve, dashed lines designate 95% confidence intervals. Sample sizes at proportion mature were assumed to be equal.

74 Adult Male Apristurus brunneus Adult Female Apristurus brunneus

6 15 2 A C 5

4 10 4 (% 11 ) I 1 S 3

G 13 6 21 2 5 11 4 16 10 8 10 4 3 7 2 14 7 1 1 1 1

0 0 01 02 03 04 05 06 07 08 09 10 11 12 01 02 03 04 05 06 07 08 09 10 11 12

40 40 B D 30 30 14 14 14 6 4 10 9 6 16 12 (% 1 2 3 7 4 17 6 21 4 12 4 ) I 1 S 20 20

10 10

0 0 01 02 03 04 05 06 07 08 09 10 11 12 01 02 03 04 05 06 07 08 09 10 11 12 Month Month

75 Adult Male Parmaturus xaniurus Adult Female Parmaturus xaniurus

6 15 4 A 1 C 5 7 3 4 10 (% 5 14

) I 4 S 3 4 8 G 2 9 6 4 16 2 7 6 2 5 2 6 1 1 7

0 0 01 02 03 04 05 06 07 08 09 10 11 12 01 02 03 04 05 06 07 08 09 10 11 12

40 40 B D 7 30 30 3 8 4 6 4 4 8 9 2 (% 4 9 2 1 7 16 7 6 6 2 14

) I

S 20 20

10 10

0 0 01 02 03 04 05 06 07 08 09 10 11 12 01 02 03 04 05 06 07 08 09 10 11 12 Month Month

76 75 A

60 Egg Case Length (mm)Egg 55

50 480 500 520 540 560 580 600 620 640 660 Total Length (mm)

105 B 100

Egg Case Length (mm) Length Case Egg 75

65 460 480 500 520 540 560 580 Total Length (mm)

Figure 16. Egg case length versus female total length for Apristurus brunneus (A) and Parmaturus xaniurus (B).

A B C

Figure 17. Egg cases of Apristurus brunneus (A), Apristurus kampae (B), and Parmaturus xaniurus (C). Scale bars are 1 cm.

78 Figure 18. Locations of Apristurus brunneus (red circles) and Parmaturus xaniurus (purple triangles) egg cases captured by trawl. The arrow points to the location at which 953 egg cases were found (n = 478, 27 October 2000; n = 475, 29 June 2001). Bathymetric contours are scaled at 500 m depths.

79 Figure 19. Locations of Apristurus brunneus (red circles) and Parmaturus xaniurus (purple triangles) egg cases as captured by remote operated vehicle (ROV) video footage. Cruises were conducted by the Monterey Bay Aquarium Research Institute (MBARI), 1989 through 2003. Bathymetric contours are scaled at 500 m depths.

80 A B

C D

E F

81 A

Figure 21. Apristurus brunneus egg cases captured on video footage from remote operated vehicle (ROV). Egg cases were commonly seen covered by invertebrates such as large sea stars (Rathbunaster californicus on A. brunneus, A) and gastropods (Boreotrophon tripherus on A. brunneus, B).

82 Figure 22. Empty Parmaturus xaniurus egg case found in Monterey Bay Aquarium tank next to head of shortspine thornyhead (Sebastolobus alascanus). Egg case ends appear to have been bitten off.

84 APPENDIX 1. Egg cases of the genus Apristurus. Apristurus grouping as per Nakaya and Sato (1999).

Apristurus group Species Depth (m) Tendrils Egg case description brunneus A. acanutus A. atlanticus 1365 A. brunneus 300-800 yes DeLacy & Chapman (1935), Cox (1963) A. canutus 687 A. exsanguis yes Sato et al . (1999) A. gibbosus A. indicus 1289 A. internatus A. investigatoris 1040 A. japonicus 820-915 A. laurussoni 100-1250 yes Nakaya & Sato (1998), Iglesias et al . (2002) A. macrorhynchus 220-1140 yes Nakaya (1975) A. macrostomus A. maderensis yes Springer (1979), Nakaya & Sato (1998) A. micropterygeus A. melanoasper 512-1520 yes Iglesias et al. (2004) A. nasutus 400 A. parvipinnis 1115 A. platyrhynchus no Nakaya (1975), Springer (1979), Nakaya & Sato (2000) A. saldanha 914 A. sibogae 655 A. sinensis A. verweyi

longicephalus A. herklotsi 520-910 half Ivanov (1987), Nakaya (1991), posterior end only A. longicephalus 600-1140 half Ivanov (1987), posterior end only

spongiceps A. albisoma 935-1564 A. aphyodes >1000 no Igles ias et al . (2002) A. fedorovi 810-1430 A. kampae >1000 no Illustration in Ebert (2003); This study A. manis >1000 no Flammang & Ebert (in preparation) A. microps >1000 no Ebert, Compagno, & Cow ley (in preparation) A. pinguis A. profundorum >1000 A. riveri >1000 no Springer (1966, 1979), filamentous A. spongiceps >1000 no Flammang & Ebert (in preparation) A. stenseni Apristurus sp. D >1000 no Flammang & Ebert (in preparation)