Reproductive Biology of Elasmobranchs Presented by: Cori Jobe & Tricia Meredith

Introduction Reproduction has proceeded along only a few paths Great diversity among congeners - Brood sz., ovarian cycle, gestation period, mating system, nursery Reproductive processes for most sharks are unknown

Introduction Primitive mode in fishes – broadcast spawning & oviparity Embryos of oviparous fishes: - Have small amt. of yolk - Hatch in undeveloped condition - Highly vulnerable - Suffer heavy mortality Reproductive adaptations contribute to evolutionary success - Diverse group with continuum of reproductive strategies

Internal Fertilization All elasmobranchs have internal fertilization Females retain fertilized eggs for varying amts. of time - Oviparous - Viviparous Bypassing larval stage: - Reduces losses to predation - Young have greater # of potential prey

Oviparity Eggs enclosed in cases & deposited No further parental care Nourished solely by yolk Slit in case allows for ventilation & oxygenation R. erinacea egg case

Oviparity Oviparous elasmobranchs are: - Benthic - Littoral or bathyal - Usually small Produce small young – limited amt. of nutrients Found only in: - Heretodontidae, Scyliorhinidae, Orectolobidae - Rajiiformes Probably ancestral condition in sharks Swell shark egg case Juvenile swell shark emerging

Viviparity Retain embryos in uterus Embryos born fully developed Aplacental viviparity - Yolk dependency - Oophagy - Placental analogue Placental viviparity

Aplacental Viviparity No placental connection between mother and offspring Previously called ovoviviparity Variation in modes of embryo nourishment Ultrasound of egg cases in nurse shark Sonogram of embryo, post-hatching

Yolk Dependency Embryos depend solely on yolk deposited in egg Do not receive supplemental nourishment from mother during gestation Retained in uterus for protection Young are relatively small at birth Nurse shark uterus

Porbeagle embryo with yolk stomach Oophagy Large ovary, small eggs Most eggs exist to nourish developing young Embryos dependent on yolk for short amt. of time, then begin to ingest other eggs C. taurus produces “feeding egg cases” C. taurus utilizes uterine cannibalism Porbeagle embryo with yolk stomach

Placental Analogues Regions of uterine epithelium that secrete “uterine milk” Embryotroph secreted by long villi, called trophonemata on uterine lining Common in rays

Placental Viviparity Nourished by yolk sac 1st few weeks Yolk sac then elongates & become vascularized Tissues of yolk sac & uterine wall grows together, forming the placenta Nutrients shunted from mother to embryo

Male Reproductive System Seminal vesicles Testes Genital ducts Efferent ducts Epididymides Ampullae epididymis Urogenital papilla Siphon sacs Claspers Testes [bonnethead] Claspers [Skate]

Testes Paired symmetrical structures where sperm is produced Vary greatly in size during the year and life cycle Vary among species in morphology and functional arrangement

Developmental process Testis Ampullae Spermatocyst Spermatoblasts Sertoli cells Germ cells Spermozeugma Spermatophores

Ductus efferens Leydig gland Epididymis Ampullae epididymis Testes Ductus deferens Liver [spiny dogfish]

[dogfish] Ductus deferens Seminal vesicle Sperm sac Marshall’s gland Urogenital sinus Cloaca Urogenital papillae Clasper [dogfish]

Claspers Paired copulatory organs Rhipidion Paired copulatory organs Form articulations with the pelvic fin upon reaching maturity During copulation, only one clasper is inserted into the female A grip on the right pectoral fin positions the female on the male’s left, and the right clasper would be used Terminal rhipidion serves to anchor the clasper within the reproductive tract of the female (hook or spine) Sperm is ejected via siphon sacs Speculation that they may serve to flush the female reproductive tract of semen from previous matings Clasper Pelvic fin Siphon sac [whitetip reef shark]

Mature male? testis Ducts deferens clasper However, the calcification and rigidity of the clasper, and the ability of the rhipidion to splay open and erect the spur are the best standards for determining maturity in male elasmobranchs. Immature male seminal vesicle Mature male

Female Reproductive System Pelvic fin Cloacal opening Ovaries Oviducts Ostium Vagina Uterus Oviducal (shell) gland Ovary Oviduct Liver [blue shark]

Ovaries Paired or single structures where ova are produced Usually both are fxnal, while in galeoid forms only the right is fxnal Vary among species in morphology and functional arrangement

Oviducal (shell) gland Elasmobranch Ova Generally large and full of yolk Oophagous lamnoid sharks Produce large #’s of small eggs 2 eggs ovulated, 1/oviduct Oviparous sharks Egg case provides protection Viviparous sharks Egg case incorporated into placenta Part of the ova not cleaved becomes the yolk sac Oviducal (shell) gland Uterus Ovary Ova [spiny dogfish]

Sperm Storage Fertilization occurs prior to encapsulation [salmon shark] Fertilization occurs prior to encapsulation Sperm stored in shell gland Storage times range from 4 wks- >1yr Lamniformes show no evidence of long-term storage Lumen

Reproductive Cycles Complex and poorly understood Ovarian cycle How often a female develops a batch of oocytes and ovulates a batch of eggs Gestation period Length of time between fertilization and parturition Concurrent or consecutive? Some species reproduce every 2 yrs (biennial) Some species have annual cycles, where females carry developing oocytes and embryos at the same time Reproductive cycles >3.5 yrs have been postulated

Mature female? Immature Mature Ovaries small Shell gland appears as slight swelling Vagina sealed by hymen Mature Ovaries large with bright yellow oocytes Shell gland several times the diameter of the oviducts [bull shark]

Mating & Reproductive Behavior Courtship bites may signal male intent Precopulatory behaviors result in male grasping female for clasper insertion Females may be selective Males may cooperate Multiple paternity may occur

Conclusion General trend from oviparity to viviparity with small #s of fully developed young Reproductive adaptations that made them successful now threaten their survival Understanding reproductive biology can help shape conservation & management

References Carrier JC. 1996. Identification and closure of nurse shark breeding grounds. The IUCN/SSC Shark Specialist Group. hark News 6: March. http://www.flmnh.ufl.edu/fish/organizations/ssg/sharknews/sn6/shark6news9.htm Carrier JC, Murru FL, Walsh MT & Pratt HL. 2003. Assessing reproductive potential and gestation in nurse sharks (Ginglymostoma cirratum) using ultrasonography and endoscopy: an example of bridging the gap between field research and captive studies. Zoo. Biol. 22: 179-187. Castro JI. 2000. The biology of the nurse shark, Ginglymostoma cirratum, off the Florida east coast and the Bahama Islands. Environ. Biol. Fish. 58: 1-22. Pratt HL & Carrier JC. 2001. A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environ. Biol. Fish. 60: 157-188.