Reproductive Biology of
Elasmobranchs
Chip Baumberger & Jeff Guertin
10/16/07
Introduction

Great diversity

Brood sizes, ovarian cycles, gestation periods,
mating systems, etc

Oviparity is common in the bony fishes (large
number of eggs and sperm released into
water for fertilization)
 All elasmos have internal fertilization (less
energy expenditure)

Improve efficiency of fertilization, avoid wastage
Reproductive Biology

Primarily studied from commercial fishery
landings
 Data from captive Elasmobranchs limited to
smaller species
Data collected typically includes:
• Age/size at onset of sexual maturity
• Size and mass relationships between males and females
• Estimates of reproductive cycle length
• Sex ratio of male pups to female pups
• Size, development time of embryos (if possible)
• Reproductive system anatomy (when we’re lucky)
Internal Fertilization

All elasmobranchs have internal
fertilization
 Improves
likelihood and efficiency of
fertilization

Two main groups
 Oviparous
(egg-laying)
 Viviparous (live-bearing)
Oviparous Forms
 Lay
eggs on substrate or attach to bottom
structures
 Nourished solely by yolk sac
 Small slit in egg case for ventilation &
oxygenation
 Primarily small, benthic, and bathyal
 Found only in three families and the skates
(primitive/ancestral condition)
Oviparous Forms

Found only in Heterondontidae, Scyliorhinidae,
Orectolobidae and Rajiformes
 Mainly bottom dwellers, many shallow water and
small species
 Commonly observed in aquarium specimens
 For instance (in captivity):
The chain dogfish, S. retifer:
• Sexually mature at 500-520 mm (M-F)
•Sperm can be stored over 800 days
•2 eggs laid every 15 days
• Eggs released at 18 mm length
• Hatch at 106 mm, ~256 days
Oviparous Forms
Cat shark
egg case
Cat shark eggs on
coral
Cat shark
open egg
case closeup
Oviparity






Females store sperm, fertilization occurs in shell gland
Secrete egg case in shell gland
Paired eggs or multiple eggs, depending on species
Eggs in tough cases, attached to substrate, vegetation
Slit in egg case for water/O2 circulation
External yolk sac for gestation, becomes internal in late
stages
David Doubilet
Swell shark, Cephaloscyllium
ventriosum: retained oviparity
Egg cases split open at 3 stages of development:
1.Immediately after egg-laying, 2. 3-4 months, yolk begins to be used,
3. 6-7 months, yolk absorbed internally, 4. Immediately post-hatch
1
2
3
4
Viviparity
Retain embryos in the uterus during
entire period of development
 Can be divided into placental and
aplacental

Aplacental Viviparity



Also called ovoviviparous
No placental connection
Three types
 Depend soley on yolk reserves
 Oophagous
 Nourished through placental analogues
Black dogfish embryos
Porbeagle embryo (oophagous)
Aplacental Viviparity - Yolk
Dependency
Embryos depend solely on yolk
 Embryos still in the uterus (protection)
 Relatively small at birth

Aplacental Viviparity - Oophagy
Ovary is huge, many small eggs
 Uses yolk at first, then ingests other
eggs

 Fertilized
and unfertilized
Intrauterine cannibalism
 Large size at birth

Placental Analogues
More efficient than just yolk-sac
 Trophonemata structure grows from uterine
lining - for nutrient supply, once embryo has absorbed all

yolk

Trophonemata envelop anterior of embryo


Uterine milk (histotroph)


enter gills/mouth, provide O2, waste removal and milk
secreted by uterine epithelium, consists of lipids, proteins
Found mainly in Batoids

Rhinoptera bonasus, Dasyatis sabina, Urolophus lobatus
Placental Viviparity





Most advanced form
Yolk-sac attach to uterine wall
Provides high growth potential
Found in about 30% of sharks
Order Carchariniformes,

Triakidae, Hemigalidae,
Carcharhinidae, Sphyrnidae
Placental Viviparity
Stage 1: Preimplantation
• Uterine wall unmodified
• Embryo utilizing yolk sac
• Vascularization present in mucosa
Stage 2: Early implantation
• Occurs at 70-85 mm in
Rhizoprionodon terraenovae
• Egg
envelope, ee, loosely attached
Uterine wall has become modified with
villi, V
Stage 3: Later Gestation
• Yolk sac and Villi vascularly
connected, exchange is two way
• Embryonic wastes taken up, unlimited
maternal nutrients flow into embryo
ys- yolk sac, V – uterine villi, Lp – Lamina propria
LA - lymphoid aggregates, Ve – vascular elements,
Male Reproductive System
Consists of testes, genital ducts,
urogenital papilla, siphon sacs,
claspers
 Testes are paired, anterior end of
coelom

 Vary
in size during the year
 Three main morphologies
 Radial,
Diametric, Compound
Male Reproductive System
Male Reproductive System
Spermatogenesis occurs in testes in the
ampullae
 Spermatocyst is made up of many
spermatoblasts, composed of Sertoli
cells and their germ cells
 Spermatocyst bursts, Sertoli cells
fragment, spermatozoa released and
conveyed through epididymis and into
the ductus deferens

Male Reproductive System
Male Reproductive System
Male Reproductive System
Morphological differences in both the
epididymis and claspers between
mature and immature males
 Most species only insert one clasper

 Sharp

hook/spur
Rotate clasper to form a connection
between clasper apopyle and urogenital
papilla
Male Reproductive System
Male Reproductive System

Sperm are packed in rounded or tubular
matrices
 Spermatophores
- sperm encapsulated in a
matrix (protection, etc)
 Spermozeugma - sperm embedded but
unencapsulated
Leydig gland
 Marshall’s gland

Female Reproductive System
Ovaries at anterior end of system
 Oviducts run the length of body
 Shell gland within oviducts

 secrete egg membranes/shells and stores
sperm

Uterus at posterior end of oviducts,
houses developing embyros

Develop villi for gas/waste/nutrient
exchange
Female Reproductive System
Female Anatomy
Female Reproductive Anatomy
Dogfish shark
• Visible under left lobe of liver
• Yolk-sac viviparous, 3-4 embryos/uterus
– create a “candle” containing embyros
• Ova and Shell glands visible
• Large developing Ova
Ova

External oocytes found on epigonal
organ in gymnovarium type ovary, large
ova

Internal ova (Lamnid sharks) release
oocytes through ostium into oviducts,
small ova
Elasmobranch Sperm Storage
Sperm stored in shell
glands
 Three types




Non-storage: Alopias
vulpinus, Lamna nasus
Short Term: Prionace
glauca
Long Term: Carcharinus
obscurus, Sphyrna lewini
Non-storage sperm
Packed in lumen or shallow tubes
 For immediate use in oviduct

Long Term Storage
Densely packed
sperm
 Deep in glands
 Not highly visible in
stains
 Found in nomadic
sharks
 Stored for 10-15
months

Reproductive Cycles
Poorly understood
 Consist of ovarian cycle and gestation
period

 May
run consecutively or concurrently
Mating and Reproductive
Behavior

Behavioral and biological changes
 Biting
of females pectoral fins, peduncle
 Aggregations of mature adults
 Changes in tooth morphology with the onset
of mating season

Large variations in reproductive season,
gestation period, frequency of mating

gestation periods range 3 months to over 3
years
Courtship Behaviors
Pre-coupling behaviors documented in
Ginglymostoma cirratum included:
 Type 1: occurred w/stationary female, shallow depth
Short duration, females either avoided or accepted
coupling behavior
 Type 2: Occurred w/swimming females, Following
behavior, multiple males, Longer duration from 1 to 90
minutes
 Type 3: Pectoral fin grasped by male, initiates
coupling behavior
Courtship Behavior
Lemon Sharks:
Schooling, following behavior
Nurse Sharks:
Pectoral Grasp
Jeffrey C. Carrier
Manta Rays:
The waltz
Mantaray.com
Samuel Gruber
Mating Behaviors
Once competition and courtship are over
 Many methods of mating

 Smaller
sharks- wrap around female with tail,
bringing clasper ventrally
 Larger, less flexible sharks – put ventral
surfaces together, clasper is flexed toward
cloaca
 Batoids – belly to belly, on the sea floor in
benthic species, in water column for pelagic
rays
Mating Behavior on film
Manta Mating http://www.youtube.com/watch?v=W_rQAmPQBV8
Conclusion

General trend from oviparity to viviparity
 Small

number of young
Reproductive adaptations now threaten
survival
 Delayed
maturity, long reproductive cycles,
small broods
References:
Cavaliere, A. 1955. Embrione di Trygon violacea. Boll. Pesca e Idrobiol. 9:197-200.
Chen, W.K. and K.M. Liu. 2006. Reproductive biology of whitespotted bamboo shark
Chiloscyllium plagiosum in northern waters off Taiwan. Fisheries Science 72: 1215–1224.
Pratt, H.L. Jr. 1993. The storage of spermatozoa in the oviducal glands of western North Atlantic
sharks. Environmental Biology of Fishes 38: 139-149
Hamlett, W. C., A.M. Eulitt, R.L. Jarrell and M.A. Kelly. 1993. Uterogestation and placentation in
elasmobranchs. J Exp Zoo. 266, No. 5, pp. 347-367.
J. C. Carrier, H. L. Pratt, Jr. and L. K. Martin. 1994. Group Reproductive Behaviors in Free-Living
Nurse Sharks, Ginglymostoma Cirratum. Copeia, No. 3, pp. 646-656.
M.P. Francis and J.D. Stevens. 2000. Reproduction, embryonic development, and growth of the
porbeagle shark, Lamna nasus, in the southwest Pacific Ocean. Fish. Bull. 98, pp. 41–63.
S.J. Joungand H.H. Hsu. 2005. Reproduction and Embryonic Development of the Shortfin Mako,
Isurus oxyrinchus Rafinesque, 1810, in the Northwestern Pacific. Zoological Studies 44, no. 4,
pp. 487-496.