The IUCN/SSC Shark Specialist Group
Shark News 9: June 1997
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Reproductive Modes of Elasmobranchs
William C. Hamlett PhD, Indiana University School of Medicine, USA
Introduction
Vertebrates typically nourish their developing offspring by one of
three major methods. The first involves yolk reserves, the most familiar
example being the chicken egg. The embryo relies exclusively on yolk
for its nutrient needs during development. The second method involves
uterine secretion of a nutrient substance termed histotroph or uterine
milk, a kind of maternal milkshake. The embryo ingests and absorbs
the histotroph for growth and development. The final method is a
placenta. Fetal membranes form a connection with maternal tissues
to establish a utero-placental complex that supplies the embryo with
nutrients and oxygen and removes wastes. Generally a species utilises
only one of these methods, but placental sharks sequentially utilise all
three; progressing from reliance on yolk, to histotroph to a placenta.
The lemon shark Negaprion brevirostris is a viviparous species in which the yolk sac and stalk are converted into a placenta and umbilical cord. This pup, new-born in a shallow Caribbean lagoonal nursery ground, still has its placenta attached. The umbilical scar left after the cord drops off will heal over during the next few months. Photo: S. Gruber.
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The elasmobranch fishes (sharks, skates and stingrays) display an
enormous variety of reproductive specialisations to provision their
developing young with nutrients. Reproduction is either oviparous
(egg laying) or viviparous (live bearing, including 70% of all sharks).
All elasmobranchs undergo an initial period of development that
is reliant on yolk reserves sequestered in the yolk sac. Embryos are
either totally yolk-reliant and lay eggs enclosed in a thick egg case
(oviparity), or are only initially reliant on yolk and subsequently
receive supplemental maternal nutrients during prolonged uterine
gestation prior to live birth (viviparity). Viviparous species differ in
the manner of delivery and type of maternally derived nutrients they
supply to their embryos. Viviparity may be aplacental, in which a
definitive maternal-fetal vascular connection is lacking, or placental,
in which a vascular organ composed of both maternal and fetal tissues
mediates exchange of nutrients, gases and waste products.
The Egg
All elasmobranchs employ internal fertilisation, in which the male's
pelvic fins are modified to serve as copulatory organs termed claspers.
Following fertilisation, eggs are transmitted through specialised anterior
regions of the oviducts termed the nidamental or shell glands. These
paired glands perform the dual functions of (a) sperm storage and (b)
elaboration of mucus, albumen and egg coverings. The type of egg
covering differs with the type of reproductive
mode of a particular species. In oviparous species,
including all skates and some sharks, the initially
thick, pliable egg case hardens after being
deposited to protect the embryos from predation
and physical trauma. Egg case tendrils and sticky
filaments attach the egg to some substrate where
the eggs incubate, unguarded for several weeks
or months until hatching. (Elasmobranchs are
not known to display parental care after birth.)
The amount of yolk initially in the yolk sac limits
the size an oviparous embryo may attain, and
they are therefore relatively smaller than
aplacental species. Empty egg cases are frequently
found on the shore as 'mermaid's purses'.
Placental sharks form a thin egg covering the
consistency of plastic wrap that is incorporated
into the placenta. Egg coverings are transitory or
non-existent in stingrays.
Utilisation of yolk occurs by two methods.
Yolk is digested by enzymes in the yolk syncytium
and metabolites are absorbed by the yolk sac
endoderm and transferred to the fetal circulation. Additionally, ciliated
cells in the ductus vitellointestinalis, a patent tube in the yolk stalk
connecting the yolk sac with the fetal alimentary canal, move yolk
platelets to the fetal gut where they are digested and absorbed.
Aplacental Viviparity
Aplacental viviparous species are of three types. The first (aplacental
yolk sac variety) are those that incubate embryos in the maternal
uterus without making any other provision for supplemental
nourishment other than that originally in the yolk reserves. This is the
most common reproductive strategy employed by sharks and it affords
protection from predation. Sharks displaying this mode of
reproduction include the dogfishes, cow sharks, angel sharks, frill
sharks and tiger sharks. The second type (aplacental with uterine
villi or trophonemata) retains initially yolk-reliant embryos in the
uterus but supplements yolk stores by secretion of histotroph or
uterine milk. This method is best exemplified by the stingrays. The
final aplacental type (aplacental with oophagy and intrauterine
cannibalism) is found in the lamnoid sharks, makos, threshers and
sand tigers. The young hatch within the uterus in the first three months
and feed on ovulated eggs. The sand tiger, however, is the only
documented intrauterine cannibal. It develops functional dentition at
an early age and consumes its siblings in addition to eggs.
Viviparous species retain developing embryos and fetuses in the
dilated posterior portion of the oviduct, which serves as a functional
uterus. Physical associations between the maternal lining and the
developing young range from simple uterine retention of yolk reliant
embryos to the establishment of a vascularised placenta rivalling that
of mammals. The period of uterine retention may be from 2-3 months
in some stingrays, 9-11 months in some placental sharks to 24 months
in the aplacental spiny dogfish. The degree to which the mother
provides nutrients to supplement yolk reserves varies greatly with the
mode of reproduction. In the case of the aplacental dogfish, additional
nutrient contribution from the mother is considered nil and the term
fetus weighs 40% less than the fertilised egg. Recently the whale shark
has been shown to be aplacental viviparous. A gravid female was
examined that contained a staggering 300 uterine embryos. Many
were enclosed in the egg case and still contained a yolk sac while most
others were free in the uterus and possessed a vitelline scar, a remnant
of the resorbed yolk sac.
Uterine Milk
In some aplacental sharks, the uterus develops uterine villi that may elaborate a nutrient fluid that is absorbed and/or ingested by the embryos. The quantity and composition of the uterine secretions finds its zenith in the stingrays, where the embryo may show a weight gain in excess of 5,000%. The term 'trophonemata' was coined to refer to the highly elongate, richly vascularised uterine villi of stingrays.
Throughout gestation, as yolk reserves diminish, trophonemata increase in size and progressively elaborate uterine secretions rich in protein and lipids, termed histotroph or uterine milk. The fetuses ingest and digest the milk for further growth. The high degree of vascularity of trophonemata serves to increase the surface area available for intrauterine gas exchange.
Figure 1. Stingray embyro, with yolk stalk (st) and yolk sac (ys) still attached, resides in the uterus (ut) adorned with secretory trophonemata (t). From Hamlett et al. 1993.
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Oophagy
Among the lamnoid sharks, a particularly bizarre reproductive strategy
is employed. The maternal ovary produces thousands of relatively
small eggs about the size of a garden pea, each enclosed in an egg
case. Embryo development rapidly exhausts yolk reserves. Sand tiger
embryos precociously develop tooth buds by the time they are 30 mm
in total length and by 60 mm they have multiple rows of erupted teeth.
Embryos use their dentition to tear out of their egg case and feed on
other uterine eggs in a process called oophagy (egg eating) and (in the
sand tiger) cannibalise other smaller uterine siblings (intrauterine
cannibalism or embryophagy). At term only one fetus survives in each
uterus, achieving gigantic proportions of more than a metre in length.
Placental Viviparity
Approximately 70% of all sharks are viviparous, giving birth to living young. Of these 30% are placental and develop a placenta resembling that of mammals. Other reproductive similarities to mammals include internal fertilisation, the presence of the same suite of reproductive hormones, uterine gestation via a placenta, and a prolonged pregnancy (generally 8-12 months). At birth the babies are capable of swimming and hunting independently.
Figure 2. In placental sharks at term, the yolk stalk is transformed into an umbilical cord which may have appendiculae and the yolk sac contributes to the functional placenta. Specialized attachment sites for the distal portion of the placenta modulate metabolic exchange. From Hamlett 1993. Environ. Biol. Fishes 38: 253-267.
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Among humans, multiple births are considered unusual, whereas in placental sharks it is the rule. Placental sharks bear from four to 100 offspring, depending on the species. These impressive numbers are only modest when compared to the thousands of eggs a bony fish may lay at one time. Since shark embryos are safely harboured inside the mother's body, virtually all survive to birth. This affords protection of the embryos from predation during this early vulnerable period.
Characteristics of placental sharks include: 1) lengthy gestation
period, 2) reduced number of offspring when compared to bony fish,
3) increased degree of maternal protection during development of the
embryos and 4) increased chance of survival of the offspring due to
their large size at birth.
In placental sharks, initial development is yolk-reliant but instead of
retracting the yolk sac into the abdominal wall, placental species
convert the yolk stalk and yolk sac into an umbilical cord and placenta
respectively. The placenta is an amalgam of fetal and maternal tissues. In
most placental sharks a thin, flexible egg covering encloses each fetus
and fetal portion of the placenta, thus all metabolic exchange between
mother and fetus is effected through the intervening egg covering.
In most placental sharks the umbilical cord is smooth, but in
others it is festooned with branched, vascular extensions termed
appendiculae. These structures have been demonstrated to absorb
fluids from the uterine environment and thus may serve as a
paraplacental nutrient-absorptive site that may function while the
definitive placenta is forming.
Conclusions
Elasmobranchs are an ancient group that display an impressive variety
of reproductive modes ranging from oviparity to placental viviparity.
Viviparous development is the most diverse and includes species that
drink a uterine 'milkshake', others that eat one another within the
uterus, and others that form a placental connection similar in many
ways to that of man. All of these means of reproduction are highly
successful and are utilised by extant species.
Various reproductive characteristics of elasmobranchs, and sharks
in particular, make them sensitive to perturbation by man. They are
slow to mature sexually, have a large energy investment in relatively
few young and some sharks only breed every other year. Because of
these characteristics, rates of replacement within populations are very
slow. In the face of the increasing pressures placed on elasmobranchs
as a food source, from recreational fishing, as bycatch from other
fisheries, and the enormous price that shark fins bring on the
international market, their reproductive future must be considered
carefully. It is, therefore, vitally important to be conservative in
harvesting from these populations.
References
Hamlett, W.C. 1987. Comparative morphology of the elasmobranch placental barrier. Arch. Biol. (Bruxelles). 98:135-162.
Hamlett, W.C., and Tota, B. (Co-Editors). 1989. Evolutionary and Contemporary Biology of Elasmobranchs, J. Exp. Zool., Suppl. 2, Alan R. Liss, Inc., New York, 198 pages.
Hamlett, W.C., and Rasweiler IV, J. (Co-Editors). 1993. Comparative Gestation and Placentation in Vertebrates, Part I. Chondrichthyes, Osteichthyes, Amphibia, Reptilia and Marsupilia. J. Exp. Zool., Vol. 266, no. 5, Alan R. Liss, Inc., New York, 138 pages.
Hamlett, W.C., Eulitt, A.M., Jarrell, R.L. and Kelly, M.A. 1993. Uterogestation and Placentation in Elasmobranchs. J. Exp. Zool. 266: 347-367.
Hamlett, W.C., Musick, J.A., Eulitt, A.M., Jarrell, R.L., and Kelly, M.A. 1996. Ultrastructure of Uterine Trophonemata, Accommodation for Uterolactation and Gas Exchange in the Southern Stingray, Dasyatis americana. Can. J. Zool. 74: 1417-1430.
William C. Hamlett PhD, South Bend Center for Medical Education,
Indiana University School of Medicine,
B-10 Haggar Hall, University of Notre Dame,
Notre Dame, Indiana, 46556, USA
Fax. + 1 219-631-7821
Email: hamlett.1@nd.edu
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