THE EGG-CASES OF.THE SWELL SHARK, CEPHAL0SCYLLIUM VENTRIOSUM: •FORMATION,- FUNCTION, AND POPULATION DIFFERENCES. by CHARLES A. GROVER B.Sc. California State College at, Long Beach 1967 A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in the Department of Zoology We accept this thesis as conforming to the required standard The University of British Columbia August, 1970. In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the Head of my Department or by his representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department The University of British Columbia Vancouver 8, Canada ii ABSTRACT • , The swell shark, CephaloscyIlium ventriosum Garman (Scyliorhinidae), is an inshore, reef-dwelling, nocturnal species of the Eastern Pacific rim. Reproduction is oviparous. One ovary is developed. Ova are transported through the coelom by cilia, to a single ostium, which serves both oviducts. Egg formation is usually synchronous in both oviducts, and proceeds generally as in other elasmobranchs, but published and new data are combined in a new description of the egg-forming sequence. Photomicrographs show sperm stored in the shell-secreting tubules of the shell gland. This storage allows the production of fertile eggs in the absence of males for some months after mating. A membrane surrounds the embryo and yolk during the early stages of development, contrary to prior descriptions of related species. A chalaza-like structure is attached to this membrane. The young of this and several other oviparous species of sharks posess two dorso-lateral rows of enlarged denticles. In the swell shark, these appear to function in the emergence of the shark from the egg-case. Eggs are preyed upon in nature, possibly by a Stenoglossid gastropod. The sharks form at least two different populations, separated by as little as 30 km. The egg-cases of one population have no tendrils over 2cm.; the other population has long tendrils, to 2 m. Differences are also found in egg size and in the morpho• metries of the adult sharks. TABLE OF CONTENTS PAGE ABSTRACT ii LIST OF TABLES iii LIST OF FIGURES iv ACKNOWLEDGEMENTS v INTRODUCTION 1 MATERIALS AND METHODS 4 RESULTS 8 1. Descriptive Anatomy of the Female Reproductive System. 8 a. Ovary, ova, and peritoneal ciliation functioning in ovum transport. b. Ostium and oviducts. 9 c. Circulatory system. 11 d. Shell gland structure, secretions, and sperm storage. 12 2. Egg-case Structure. 16 3. Mechanics and Sequence of Egg-case Formation. 26 4. Development of the Embryo and Egg-case Changes. 35 5. Emergence of the Shark from the Egg-case. 40 6. Predation on Egg-case. 43 7. Population Differences. 45 DISCUSSION 52 SUMMARY 61 REFERENCES 64 LIST OP TABLES Page Comparisons by two-tailed t-test of measurements of egg- case samples from sharks captured at Isthmus Cove, Santa CataJLina Island, and the mainland near Los Angeles. 49 Comparisons by two-tailed t-test of morphometric ratios of samples of sharks from Isthmus Cove, Santa Catalina Island, and Point Dume, California. 51 iv LIST OP FIGURES Page 1. Diagramatic section drawings of a shell gland. 15 2. Oblique section of a keratin secretory tubule. 17 3. Section at base of laamellae of a shell gland. 18 4. Egg-case showing tendrils. 20 5. Typical pair of egg-cases. 21 6. Typical quartet of egg-cases. 22 7. Egg-case containing an embryo. 23 8. Diagramatic sections of egg-cases. 24 9. Two incomplete eggs laid by a swell shark. 31 10. Active and inactive shell glands. 32 11 . Backlit photograph of an embryo in its case. , 38 12. A newly-hatched swell shark. 41 13. Source locations of egg-cases. 48 V ACKNOWLEDGEMENTS I wish to dedicate this work to the memory of the late Arthur S.Lockley, formerly of the Biology Department, Calif• ornia State College at Long Beach. He was a dedicated teacher and a good friend. I wish to thank Dr. R. Fay, of Pacific Bio-Marine Supply, Messrs. F.Brocato, F.Calendrino, and B. Falcone, collectors at Marineland of the Pacific, andJ. Prescott, Curator? without their assistance, this work would not have begun. Dr. S. Applegate, Los Angeles County Museum of Natural History, Mr. S. Springer, U.S. Bureau of Commercial Fisheries, Dr. C. Hubbs and Dr. R. Rosenblatt, Scripps Institution of Oceanography, and Mr. J. Fitch, California Department of Fish and Game, have all contributed assistance and valuable discus• sion of the work in progress. Drs. J. McPhail, N. VJilimovsky, and R. Liley, Depart• ment of Zoology, U.B.C, have provided helpful criticism of the manuscript. Mr. L. Sharman ably handled the preparation of the histological material. Finally, my thanks to Mr. and Mrs. I. Neish, for their assistance in preparation of figures, and typing the manuscipt. INTRODUCTION The swell shark, Cephaloscyllium ventriosum Garman (= C_. uter) . of the family Scyliorhinidae, is common in the waters of California from Monterey Bay south. It is occasion• ally found as far south as Acapulco, Mexico, and is found in Chilean waters (Kato, Springer, and Wagner, 1967). It also inhabits the waters of at least some of the offshore islands. The natural history of this shark has not been described, so I have included some of my own observations. Around Santa Catalina Island, California, trapping data and direct observation using SCUBA diving gear indicate that the sharks are normally found in depths of twenty to forty meters, both day and night, and are less abundant in greater and shallower depths. Two specimens have been taken in deep trap sets; one from about 160 meters (pers. comm., Brocato), and one from about .560 meters (pers. comm., 3. Applegate). These sharks are predominantly nocturnal, and are found during the day in the crevices of rocky reefs. The members of this genus have the pe culiar ability to inflate their stomachs with water, greatly increasing their body size. The anatomy of this mechanism has been described (Clark, 1947). When disturb• ed, they use this ability to wedge themselves into the reef crevices generating an internal pressure sufficient to make it quite difficult for a diver (and, presumably, any other potential predator) to remove them from the rocks, once they - 2 - are fully inflated. V/hen removed from the water, the sharks will often inflate themselves with air, and, if returned to the water in this condition, they will float, upside down and helpless, for some time. However, this latter behavior plays no part in the natural ecology of the animal, as they are bottom dwellers (see Herald, 1962). The femaJ.es reach a maximum length of about 1.1 meters; the largest males found with them are slightly smaller. Their feeding behavior has not been studied in detail, but fish are evidently an important part of their diet. Pish are among the best baits for trapping. Laboratory observa• tions of feedings of whole fish show that even a quite small, freshly caught she.rk will quickly manipulate a fish in its mouth so that it may be swallowed head first, no matter where the fish is initially grasped. The small teeth are not used to chew or bite pieces from the prey; if it is too large to swallow whole, it is rejected. However, the large mouth and gullet and the highly distensible stomach can accomodate fish which are quite large in proportion to the shark. A shark of about 40 cm. can eventually swallow a Pacit^ic mackerel some 30 cm. long. Vision plays little or no part in feeding. Pish juices introduced into lab tanks induce active swimming and snapping in quiescent sharks during the day (recall that they are noc• turnal J. When food is introduced, its detection seems hit- - 3 - or-miss; dependant upon the shark actually running into the food, rather than orienting to it visually. This study is concerned with the egg-case of the swell shark. While the various sections of the thesis are all rel• ated • in this respect, they are also relatively independent of one another. Consequently, the pertinent historical background and the results of my own work have been grouped together within each section. The work falls into the following sec• tions. 1. Descriptive Anatomy of the female Reproductive System. a. Ovary, ova, and peritoneal ciliation functioning in ovum transport. b. Ostium and oviducts. c. Circulatory system. d. Shell gland structure, secretions, and sperm storage. 2. Egg-case structure. 3. Mechanics and Sequence of Egg-case Eormation. 4. Development of the Embryo and Egg-case Changes. 5. Emergence of the Shark from the Egg-case. 6. Predation on Egg-cases. 7. Population Differences. MATERIALS AND METHODS Sharks were captured by cage trap and while SCUBA diving at various locations off the California coast in the vicinity of Los Angeles, and at Santa Catalina Island, California. Some of the sharks and eggs examined are in the Scripps Institution of Oceanography Museum, and are so designated. With the exception of four live eggs taken while diving at Santa Catalina Island, and one from the mainland which was brought to the laboratory, all live eggs were obtained from sharks held in running sea water tanks at the Marineland of the Pacific laboratory. The eggs were removed to smaller tanks. No continuous temperature records were available. Because of fluctuations in water supply and room temperature, periodic temperature readings could not provide an accurate picture of the temperature fluctuations in the tanks, but I would estimate the absolute limits of seasonal and short-term fluctuations to be between 13° and 22° C.