AMER. ZOOL., 17:379-410 (1977).
Reproduction and Development in Chondrichthyan Fishes
JOHN P. WOURMS
Department of Zoology, Clemson University, Clemson, South Carolina 29631
SYNOPSIS Patterns of chondrichthyan reproduction and development are diverse. Species
either are reproductively active throughout the year, or have a poorly defined annual cycle
with one or two peaks of activity, or have a well defined annual or biennial cycle. Based on
embryological origin and adult morphology, their reproductive system is more similar to
tetrapods than to teleosts. Primordial germ cells are of endodermal origin. The Wolffian
ducts in males and Mullerian ducts in females become the functional urogenital ducts.
Differentiation is under hormonal control. Unusual features of the reproductive system
include an epigonal organ in males and females. It contains lymphoid and hemopoietic
tissue. Leydig's gland, a modified region of the kidney, produces seminal fluid. In some
species, sperm passing through the vas deferens, is enclosed in spermatophores. Rotating
about their long axis, helical spermatozoa can move forward or reverse direction.
Spermatogenesis often occurs in bicellular units, spermatocysts. These consist of a
spermatogonium enclosed in a Sertoh cell. Fertilization is internal. Claspers, modified
portions of the pelvic fins act as intromittent organs. In many viviparous sharks and rays,
the female reproductive system is asymmetrical. Eggs of some sharks are the largest known
cells. Yolk platelets contain lipovitellin. Oocytes have lampbrush chromosomes. Eggs
released from the ovary into the body cavity are transported by ciliary action to the ostium
of the oviduct. There they are fertilized. Physiological polyspermy is normal. The shell
gland, a specialized region of the anterior oviduct, functions both in long term sperm
storage and in egg case production. Egg cases of sharks and skates consist of unique
collagenous protein with a 400 A period, organized as a cholesteric liquid crystal.
Chimaeroid egg cases contain 550 A pseudotubules in orthogonal lattices. In small sharks,
males copulate by coiling around the female. A parallel position is assumed by large sharks.
Skates and rays copulate with ventral surfaces apposed or by a dorsal approach. Biting is a
pre-copulatory release mechanism. Parental care, except for selective oviposition, is
lacking. Heavily yolked eggs undergo meroblastic, discoidal cleavage. Development is
lengthy, shortest (2-4 months) in rays, longer in skates (3-8 months) and longest (9-22
months) in sharks and chimaeras. Most sharks and all rays are viviparous. Chimaeras,
skates, and some sharks are oviparous. Viviparity either involves a yolk sac placenta or is
aplacental. If aplacental, the embryo derives nutrients either from yolk reserves, or by
intra-uterine embryonic cannibalism, or from placental analogues which secrete "uterine
milk." Phylogenetic position, geographical distribution, benthic vs. pelagic habitat, adult
size, egg-embryo size, feeding ecology, and embryonic osmoregulation are factors in the
retention of oviparity or the evolution of viviparity.
the two groups have in common than by
the ways in which they differ. This is
The chondrichthyan or cartilaginous especially true with respect to patterns of
fishes include the sharks, skates, rays, and reproduction and development in which
chimeras. They are one of the oldest living structural and functional similarity that is
groups of jawed vertebrates. They are manifest at the anatomical level becomes
often considered to be primitive or ar- e ven more striking at the level of tissue,
chaic. Yet, when one considers that the ce ll, and molecule. These fishes almost
chondrichthyan fishes and the amniotes s e e m to constitute an experimental system
represent two extremes of vertebrate in which many of the novel structures and
evolution, one is more impressed by what processes characteristic of the vertebrates
were first developed.
I am grateful to Dr. James W. Atz of the American . Chondrichtyan fishes are of particular
Museum of Natural History for reading portions of interest to reproductive and developmental biologists since, for the first time in the
the manuscript and for many helpful suggestions.
INTRODUCTION
379
380
JOHN P. WOURMS
vertebrate line, the following processes
either make their appearance or else become well established: 1) internal fertilization; 2) viviparity; 3) placental mechanisms
for fetal maintenance; 4) patterns of genital tract development and sex differentiation, closely resembling the ones in amniotes; 5) vertebrate type of reproductive
endocrinology. The first four topics will be
reviewed as well as related areas of interest
such as: patterns of reproduction;
gametogenesis; fertilization and early development; egg case ultrastructure; the
role of the shell gland in egg case formation; and the significance of viviparity.
Reproduction and development of holocephalans (chimaeras) will be discussed in
terms of available information. The endocrinology of reproduction will not be
treated in detail since it has been extensively reviewed in recent years (Chieffi,
1967; Dodd, 1972, 1975).
which passes from the fetus through the
cloaca of the female. A placenta is not
illustrated, however. By 1673, the anatomist Steno had rediscovered and published
an illustrated account of the placenta in
Mustelus laevis.
What happens next constitutes a curious
chapter in the history of biology. It has
been generally claimed that the works of
Aristotle, Rondelet, and Steno were overlooked until the time of Johannes Muller
(1842). This does not seem to have been
the case. Review works such as that of
Bohadsch (1776, also 1761) cite all three of
these authorities. Moreover, Muller (1842)
discusses in detail the work of his immediate and distant predecessors. It is
more accurate to say that Muller, an outstanding anatomist and one of the founders of physiology, was better able to appreciate the significance of his findings
and to communicate them to a receptive
audience. His classic paper marks the beginning of modern studies of chondrichHISTORICAL REVIEW
thyan reproduction and development. Not
The earliest recorded observations on the only did he review all previous studies, but
reproductive biology of chondrichthyan he also greatly expanded on them with his
fishes are those of Aristotle. He distin- own original observations. The structure
guished between oviparous and viviparous and probable function of the placenta in
species and described the egg cases of the the dogfish M. laevis and the blue shark
former. He discovered the yolk sac Prionace glauca (Linnaeus) were treated in
placenta in Mustelus laevis Risso [= M. canis detail. A comparative approach was used
(Mitchill)] and was aware that it differed to study reproduction in non-placental
from the mammalian placenta (Aristotle, viviparous species, ovoviviparous species,
Peck translation 1965, 1970). Although and oviparous species. In the latter, not
Aristotle's observations were neglected for only were shark and skate egg cases
many centuries, it is unlikely that knowl- studied but also those of the chimaera,
edge of elasmobranch reproduction was Callorhynchus.
ever lost entirely. Since skates and dogfish
Following Muller, research has tended
have continued to be staple items of diet to progress through areas of current insince ancient time, both fishermen and terest to the developing science of biology.
cooks would undoubtedly have distin- From Miiller's time to the present, certain
guished between oviparous and viviparous papers can be recognized as landmarks. A
species and would have been familiar with few are listed here. Embryological studies
their anatomy. A revival of formal interest were firmly established by Balfour (1885).
in elasmobranch reproduction coincided Ruckert (1899) and Ziegler and Ziegler
with a revival of interest in natural history (1892) worked out the early stages of deduring the Renaissance. Rondelet (1554), velopment. Dean and his associates proone of the early zoological encyclopedists duced monographs on: the reproduction
illustrated part of the ovary and the egg and development of chimaeras (Dean,
case of a skate. He also depicts a female 1906); the frilled shark Chlamydoselachus
shark (probably M. laevis) which is con- (Smith, 1937; Gudger, 1940); and the
nected to a fetus by an elongated yolk stalk heterodontid sharks (Smith 1942). Van-
-
CHONDRICHTHYAN REPRODUCTION
^
debroek (1936) carried out the principal
study of morphogenetic movements associated with gastrulation. Needham
(1942) reviewed the physiology of development. A number of studies have dealt
with the anatomy of the reproductive system (c/., Dean 1916-1922 for early references). In this respect, Borcea's (1905)
study is outstanding. He paid particular
attention to the role of the shell gland in
egg case production. Chemical studies of
the egg case and its cellular origin originate with Faure-Fremiet and Baudoy
(1938) and Filhol and Garrault (1938).
Beginning in 1922, Leigh-Sharpe reported
on a series of investigations of secondary
sex characteristics. Viviparity has been an
area of special interest (Gudger 1912,
1951; Te Winkel, 1943, 1950). In a unique
series of papers Ranzi (1932, 1934) reported on comparative studies of adaptations for viviparity. In addition to placental
species, he also considered non-placental
species that displayed special embryonic
and maternal adaptations, viz., "placental
analogues." Intra-uterine oophagy was reported by Shann (1923) and Springer
(1948). The physiology of gestation has
attracted the attention of Daiber and his
associates (Price and Daiber, 1967;
Graham, 1967). Gilbert and his co-workers
have contributed not only to the study of
placentation (Gilbert and Schlernitzauer,
1966; Schlernitzauer and Gilbert, 1966) but
also to an understanding of clasper-siphon
sac function (Gilbert and Heath, 1972).
Reproduction and reproductive seasons
have been treated by Matthews (1950) in
the basking shark Cetorhinus, the blue
shark Prionace glauca (Tucker and Newnham, 1957), the spiny dogfish Squalus
acanthias Linnaeus (Hishaw and Albert,
1947; Jensen, 1966), and the skate Raja
erinacea Mitchill (Fitz and Daiber, 1963;
Richards et al., 1963).
REPRODUCTIVE CYCLES
On the basis of Breder and Rosen's
(1966) massive review offish reproductive
patterns and cycles, it is apparent that
chondrichthyan fishes are either oviparous
or viviparous. Information on reproduc-
381
tive cycles tends to be incomplete or fragmentary. The present state of knowledge
is unsatisfactory especially when compared
to rigorous studies of invertebrate reproductive cycles (Giese, 1959; Giese and
Pearse, 1974). Sampling is a major problem. Large samples need to be taken at
appropriate intervals over a period of several years. This has been done only for a
few small, inshore species or for larger
species which have been the subject of
commercial fisheries. Based on a limited
survey of three inshore forms, Squalus,
Mustelus, and Scyliorhinus, Dodd (1972)
postulated the existence of sophisticated
annual reproductive cycles. The situation
is more complex. Three basic types of
cycles are encountered: 1) reproduction
throughout the year; 2) a partially denned
annual cycle with one or two peaks; and 3)
a well defined annual or biennial cycle.
The first category consists of those
species which are either reproductively active throughout the year or for the major
part of the year, e.g., Scyliorhinus,
Chlamydoselachus, and Heterodontus (in
part). Ford (1921) and Metten (1939) report that a population of Scyliorhinus
canicula (L.) from the English Channel in
the vicinity of Plymouth breeds throughout the year. Although somewhat more
prolific in spring and summer, they have
no definite breeding season. Based on
2000 specimens collected in the IIfracombe region, Harris (1952) concluded
that the spawning season lasts about 8-9
months starting in November and continuing until July. Dodd's (1972) observations
that ovaries of female dogfish from areas
of the Irish Sea become quiescent during
the summer support Harris' view. Are
these differences real or due to sampling
bias? Harris (1952) raised the question of
sampling error since Ilfracombe probably
represents a spawning ground into which
females migrate at the spawning season.
Gudger (1940) reported that the frilled
shark, Chlamydoselachus anguineus Garman,
a viviparous species, breeds throughout
the year. He attributes its continuous reproductive activity to the relative constancy of a deep sea habitat. Finally, a
variety of cycles are encountered within
382
JOHN P. WOURMS
the genus Heterodontus. Barnhart (1932)
states that the California species H. francisci (Girard) spawns throughout the year.
Although the population of H. japonicus
Macleay in the vicinity of Misaki, Japan,
does deposit eggs throughout the year,
there is an apparent peak in activity in
March-April (Smith, 1942). Recent field
studies of McLaughlin and O'Gower (1971)
reveal a well defined August-September
spawning season for Australian populations of//, portusjacksoni (Meyer).
The second category includes those
species with a partially defined annual cycle. Although reproductively active
throughout the year, they tend to exhibit
one or two peaks in activity. Raja erinacea
Mitchill and Hydrolagus colliei (Lay and Bennett) exemplify this pattern. Richards et al.
(1963) reported that R. erinacea is reproductively active throughout the year.
(Their study lasted almost 10 years and
included detailed examination of 15,000
specimens per year). Once having attained
maturity, adult males produce sperm continuously. Mating, fertilization, and the
production of egg cases take place
throughout the year. The study compared
two distinct, but geographically close
populations, one in Block Island Sound
and the other in Long Island Sound. The
presence of egg cases within a female was
considered evidence of its reproductive
activity. The Block Island Sound populations displayed two peaks. During
November-January, 30-60% of the adult
females were "gravid" and during June
and July, 15-30% of the females were
"gravid." During the remainder of the
year, the per cent of "gravid" females was
under 25% and tended to average about
10%. The Long Island Sound population
had a similar pattern with peaks of 5-15%
during the November-January and JuneJuly periods as well as a low level of
"gravid" females during the rest of the
year. Similar patterns were found in a
Delaware Bay population although the
summer peak was greater than the fall
(Fitz and Daiber, 1963). In a related
species, R. eglanteria Bosc they found that
egg maturation and spawning occurred
only during the spring. Differences in re-
productive cycles between two populations
of the same species as well as differences
between species, suggest a need for careful
study and cautious generalization. Among
the chimaeroids, only Hydrolagus colliei
(Lay and Bennett) of the Pacific Coast of
North America is readily accessible for
study. Dean (1906) reported that although
it is reproductively active throughout the
year, a peak in activity probably occurs
during late summer and early fall. More
recently, Stanley (1961, cited in Johnson
and Horton, 1972) confirmed that the
summer was a period of peak reproductive
activity although 33% of the females and
all the males showed evidence of activity
throughout the year.
The third category includes those
species with a well defined annual or biennial cycle, viz.,Squalus acanthias L.,Mustelus
canis (Mitchell) and Urolophus halleri
Cooper. It may also include other migratory forms such as Eulamia milberti (Miiller
and Henle) and Cetorhinus maximus (Gunner). The spiny dogfish, Squalus acanthias,
widely distributed throughout the northern regions of the Atlantic and Pacific
oceans, shows a striking periodicity. Males
display an annual cycle. Females display a
biennial cycle which can be attributed to a
gestation period of 22 months. Parturition
usually occurs in the autumn. Shortly
thereafter copulation ensues (Hisaw and
Albert, 1947; Holden and Meadows, 1964;
Jensen, 1966). Simpson and Wardle (1967)
discovered an annual cycle of activity in
the male testes. Maximum sperm accumulation coincided with the JanuaryFebruary breeding period of the biennial
female cycle. The smooth dogfish, Mustelus
canis, has also been reported to have an
annual cycle (Hisaw and Abramowitz,
1939). The details of the cycle were established by Graham (1967) for a migratory
population in Delaware Bay. This species
is also viviparous. The gestation period,
however, is 11 months long (Te Winkel,
1950). M. canis winters off North Carolina.
Northward migration begins in early
spring. In Delaware Bay, males first appear during the last week of April and the
first week of May. Females first appear
during the next two weeks. Parturition
CHONDRICHTHYAN REPRODUCTION
occurs at this time. Ovulation occurs during the first three weeks of June. Mating is
restricted to the time after parturition and
before ovulation. Ovulation is said to be
dependent upon copulation (Hisaw and
Abramowitz, 1939). The population seems
remarkably well synchronized since all
gravid females carry embryos at the same
stage of development. In the round sting
ray of California, Urolophus halleri Cooper,
the major reproductive season occurs in
late May, June, and early July (Babel,
1967). At this time, most males are in
mating condition, and the majority of
females ovulate. Shortly thereafter small
embryos are to be found in their uteri.
Quantitative studies demonstrated an annual cycle both of spermatogenesis and
oogenesis. A small number of females are
out of synchrony with the rest of the
population and ovulate in December.
They are successfully fertilized with sperm
which has been stored for several months.
Annual cycles have also been reported in
some of the larger migratory species of
sharks, both inshore and pelagic. Available
information although fragmentary is of
interest. The primary winter range of the
sandbar shark, Eulamia (=Carcharhinus)
milberti is off the southeastern coast of the
United States. It is extended as far north as
Long Island and Cape Cod to form a
primary nursery range where from late
March to early August the young are born.
Although the period of gestation is nine
months, females only seem to reproduce
every other year. Sexes tend to be segregated, except during courtship and mating. In southeastern Florida, June is the
time of maximum mating activity
(Springer, 1960). The basking shark,
Cetorhinus maximus (Gunner), illustrates the
complications which seasonal migrations,
both vertical and horizontal, introduce
into the study of reproductive cycles. In his
definitive study, Matthews (1950) presents
circumstantial evidence that this shark is
viviparous. Direct evidence in the form of
gravid females is lacking. This is remarkable considering that this species, the second largest shark, is common and has been
the subject of commercial fisheries. Matthews (1950) is of the opinion that the re-
383
productive cycle of the basking shark is
correlated with its seasonal migration. Off
the west coast of Scotland where his studies
were conducted, these sharks begin to appear in April and become most numerous
in May and June. Similar spring inshore
movements have been reported in Norway
and British Columbia. All of the adult fish
which were examined were in breeding
condition and showed signs of recent
copulation. Based on these observations,
there appears to be a single yearly reproductive cycle which is at its peak during the
second half of May. There remains, however, the problem of the nature and duration of the female cycle. Since gravid
females have not been reported in modern
times, Matthews (1950) suggests that they
desist from basking at the surface sometime before the embryo reaches a recognizable size. One assumption is that they
migrate to deep, off shore water during
pregnancy. The period of gestation obviously is not known, hence the duration of
the female cycle is not known. Older reports, cited by Matthews, suggest that
males may be sexually active during the
entire year.
DEVELOPMENT OF THE CONADS AND GENITAL
DUCTS
On the basis of its embryological origin
and morphology, the reproductive system
of chondrichthyan fishes is more similar to
amphibia and amniotes than to teleosts. In
most vertebrates, including chondrichthyan fishes, the somatic portion of the
gonad has a dual origin, the cortex and
medulla. These two tissues, although in
close proximity, are distinct and have different developmental histories. This pattern is in contrast to cyclostomes and teleosts where the somatic tissue of the gonad
has a single origin, the peritoneal
epithelium. Hence the somatic portion of
the gonad is comprised entirely of the
cortex (Chieffi, 1967; Hoar, 1969). Chieffi
(1967) has provided a modern account of
gonad development and differentiation in
Torpedo ocellata and Scyliorhinus caniculus.
Gonads develop in the dorsolateral lining
of the peritoneal cavity in the posterior
384
JOHN P. WOURMS
half of the body. Usually there is one
gonad on each side of the dorsal mesentery. The undifferentiated gonad is derived from two sources, the cortex and the
medulla. The cortex which is more laterally located develops first. It appears as an
elongated strip of the mesodermal
epithelium which forms the peritoneal
wall. This thickening becomes a multilayered convex mass of cells which protrudes into the coelomic cavity to form the
germinal ridge. On its dorsal side, the
ridge develops a hollow which is filled by
migrating mesoderm cells. These cells
comprise the medulla. In Scyliorhinus, the
medulla is derived from the nephrogenic
cord (=interrenal blastema) while in Torpedo, it is derived from the same center of
proliferation which forms the nephrogenic
cord.
Under normal conditions, genetic factors determine whether the embryonic
gonad will differentiate into an ovary or
testes. The first step involves the migration
of primordial germ cells to the gonad.
Hoar (1969) states that there is considerable evidence for a widespread origin of the
primordial germ cells. In the elasmobranchs, however, it is well established that
the primordial germ cells segregate from
the primitive entoderm quite early in development (prior to embryo formation?)
and migrate via the mesoderm into the site
of the developing gonad (Beard, 1903-04;
Woods, 1902; Hardisty, 1967). There they
settle in the cortical region of the gonad.
At this stage, the gonad is considered indifferent. In genetic females, the primordial germ cells once having settled in the
cortex retain their cortical location. In Torpedo, a few germ cells do migrate from the
cortex to the medulla in 24-32 mm female
embryos. Transient connections are established with the mesonephric tubules, but
these soon degenerate. Formation of the
primary ovarian follicles occurs by the 75
mm stage. In genetic males, primordial
germ cells migrate from the cortex to the
medulla (at 22 mm in Torpedo; at 30-32 mm
in Scyliorhinus). Formation of the sex cords
and the seminiferous ampullae occur during the 40-60 mm stages of Torpedo
(Chieffi, 1967). Once germ cell migration
has been completed, that region, either
cortex or medulla, which will form the
definitive gonad grows rapidly while the
remaining region fails to develop. Thus,
the sex of the individual is determined
4
quite early.
Secondary sex characters also make an
early appearance. According to Chieffi
(1967), their appearance coincides with
sexual differentiation in the genital ridges.
The reproductive ducts provide the means
for conveying gametes from the gonads to
the exterior. In common with most vertebrate embryos, elasmobranchs develop two
sets of urogenital ducts, only one of which
will function as a reproductive duct. In
males, the functional duct is the mesonephric or Wolffian duct and in females, it is
the Miillerian duct. The mesonephric duct
is derived, by direct transition, from the
pronephric duct. In males, the excretory
and genital functions of the Wolffian
(mesonephric) duct become segregated. In
Squalus acanthias, mesonephric tubules establish connections between the seminiferous tubules of the testes and the Wolffian
duct. These tubules become the vasa efferentia or efferent ducts. The remainder
of the duct differentiates into an
epididymis, vas deferens, and seminal sac.
The urinary or opisthonephric duct is independent of the mesonephric duct. In
female embryos, however, the upper part
of the Wolffian duct atrophies while the
lower part serves as urinary duct (Balfour,
1885; Kerr, 1919; Goodrich, 1930; Nelsen,
1953). In female elasmobranchs a second
set of ducts, the Miillerian ducts, function
in reproduction. They become the
oviducts. Although the embryonic development of the Miillerian ducts in elasmobranchs differs from that of other vertebrates, their function and anatomical relationships in the adults are remarkably
similar. The Miillerian ducts of elasmobranchs are well developed and appear
early during the course of ontogeny. The
anterior end of each duct opens into the
coelom by a funnel, the ostium tubae. Not
infrequently, the funnels of the right and
left ducts combine to form a single median
ostium. The duct, proper, is of large size,
regionally specialized, and opens inde-
CHONDRICHTHYAN REPRODUCTION
k
pendently into the cloaca. Miillerian ducts
develop from the pronephros and the
pronephric duct. The funnel region is
derived directly from one or more pronephric nephrostomes. The main portion
of the Miillerian duct develops from the
pronephric duct. The pronephric duct
undergoes a gradual longitudinal splitting
into an anterior-posterior direction to
produce a dorsal and ventral tube. The
ventral tube is continuous with the pronephric funnel and becomes the Miillerian
duct. The dorsal tube receives the kidney
tubules. It is a true Wolffian (mesonephric)
duct which persists as the functional urinary duct of the opisthonephros. Both
ducts open separately into the cloaca
(Kerr, 1919; Goodrich, 1930). Miillerian
ducts also develop in males. In immature
males of some species, e.g., Notorynchus
maculatus Ayers, they may persist as
rudimentary right and left oviducts
(Daniel, 1928). Normally, they atrophy or
survive only as vestigal funnels (Goodrich,
1930). Chieffi (1967) reviewing the reaction of the duct systems to steriod hormone treatment presents evidence for
hormonal control of differentiation. Other
important secondary sex characters are
external and are found in males, viz., the
pelvic claspers or copulatory organ, found
in almost all Chondrichthyes; the frontal
(cephalic) clasper of the chimaeras; and
alar spines on the pectoral fins of skates.
Of these, only the pelvic claspers have
received any significant attention. The
claspers are derived from the medial margin of the pelvic fins and develop simultaneously with the sexual differentiation of
the testes. In Torpedo, growth of the clasper
is not affected by treatment with steriod
hormones. Chieffi (1967) suggests that
they are a somato-sexual character.
MALE REPRODUCTIVE SYSTEM
Functional Organization
The male reproductive system consists
of the testes, accessory glands, genital
ducts, and secondary sex organs. Its organization has been the subject of numerous studies {cf., Borcea, 1905; Dean, 1906;
385
Daniel, 1928; Matthews, 1950; Stanley,
1963) so it will not be treated in detail here.
The testes are paired organs attached to
the body wall along either side of the
vertebral column by a mesorchium. Testes
vary in size and shape and are often enlarged during the breeding season. Closely
associated or even sometimes combined
with the elasmobranch testes are the epigonal organs. These consist of lymphoid or
hemopoietic tissue (Matthews, 1950). According to Stanley (1963), the epigonal
organ and hemopoietic tissue are not pressent in the reproductive system of
holocephalans. Spermatogenesis occurs
within the testis, in units termed ampullae.
Hoar (1969) has pointed out inter-specific
variation in the basic organization of the
testis. The testis of the basking shark consists of many lobules, separated by connective tissue trabeculae (Matthews, 1950).
Each lobule is equivalent to the entire testis
of the dogfish, Scyliorhinus (Mellinger,
1965). In the dogfish testis, the spermatogenic ampullae are arranged in six
zones which correspond to stages in ampullae formation and spermatogenesis
(Mellinger, 1965). Mature sperm are discharged from the testis through the efferent ducts (vasa efferentia). In sharks, the
number of efferent ducts range from two
to six. In skates and rays, there is a single
efferent duct (Daniel, 1928; Babel, 1967).
The efferent duct(s) joins the epididymis.
The epididymis usually assumes the form
of a coiled tubule but in some species, e.g.,
Cetorhinus, it may form a compact mass of
highly convoluted tubules (Matthews,
1950). The epididymis passes into the vas
deferens. There is usually a well defined
region of demarcation between the two
structures. The anterior portion of the vas
deferens tends to be coiled while the posterior portion extends as a straight tube to
the urogenital sinus. In many elasmobranchs, "sperm sacs" arise as diverticula
from the posterior region of the vas deferens. Their size varies according to species.
Sperm passes from the vas deferens into
the urogenital sinus and from these via the
urogenital papilla into the cloaca.
Leydig's gland empties into the vas deferens. Leydig's gland is the anterior part
386
JOHN P. WOURMS
of the kidney which has lost its excretory
function in males and has acquired a secretory function. It consists of a mass of
convoluted tubules embedded in connective tissue. According to Matthews (1950),
it is responsible for secreting the greater
part of the seminal fluid.
The size of the vas deferens varies considerably among the elasmobranchs. It is
often expanded to form an ampulla which
is used for sperm storage, e.g., Urolophus
(Babel, 1967). This tendency becomes extreme in the basking shark where the expanded ampulla may contain 20-25 liters
of spermatophores. In addition to size, the
ampulla of the vas deferens in the basking
shark has been structurally modified. The
interior consists of a series of transverse
folds each of which forms a circular diaphragm with an eccentric aperture. The
ampulla is lined with an epithelium that is
made up of two cell types, viz. tall ciliated
cells and short cells. The latter occupy a
basal position between the ciliated cells.
The short cells secrete the material which
forms the cortex of the spermatophores
(Matthews, 1950). The vas deferens serves
one of two functions. In most species,
sperm diluted with seminal fluid is stored
in it. In other species, e.g., the basking
shark, sperm is packaged into spermatophores. Spermatophores of Cetorhinus
may attain a size of 30 mm. They consist of
a cortex of hyaline material which surrounds a central mass of sperm. The packaging of sperm into spermatophores varies
in different species from simple sperm
aggregation to the complex structures of
Cetorhinus (Hoar, 1969). Spermatophores
are not present in the chimaera, Hydrolagus
colliei but may occur in Chimaera monstrosa
(Stanley, 1963). The basic organization of
the male reproductive system in the
chimaera, H. colliei closely resembles other
chondrichthyans. Important differences
do exist, e.g., the complex chambered ampulla of the vas deferens whose epithelial
lining is regionally differentiated into several secretory regions (Stanley, 1963).
Spermatogenesis
The organization of chondrichthyan
spermatozoa has been reviewed by
Ginzburg (1972). Sperm are very large,
exceeding 100 /A in total length. The head
portion is also long, 30-40 \x, which is
10-20 times the length of the sperm head
*
in most teleosts. The sperm is characterized by a long, pointed, spirally twisted
head which gives it a corkscrew appearance (Retzius, 1902). The helical twisting
also includes the midpiece and tail. The
helical shape of the sperm is correlated
with its locomotion. Squalus sperm move
primarily by rotation about their long axis
rather than by a lateral lashing motion.
Rotation of the gyres of the helix apparently can be reversed, allowing the sperm
to reverse direction without turning (Stanley, 19716). Both at the microscopic and
ultrastructural levels, chondrichthyan
sperm are conservative in structure and do
not differ significantly from other vertebrate sperm (Boisson, et al., 1968; Stanley,
1971<z,i). Attempts to determine the ultrastructural basis of spiralization have not
been successful (Stanley, 19716).
A number of investigations have dealt
with spermatogenesis in elasmobranchs
(cf., Mellinger, 1965; Stanley, 1966,
I97la,b; Boisson et al., 1968 for earlier
references). Stanley's 1966 study of
Scyliorhinus will be reviewed here. In the
elasmobranch testis, spermatogenesis takes
place in spherical seminiferous follicles or
ampullae located at the termini of a highly
branched system of collecting ductules.
Follicles originate at fixed sites on the
dorsal or dorsal-lateral margins of the testis. New seminiferous follicles are formed
when one or two spermatogonia are surrounded by several epithelial cells. The
epithelial or follicle cells are considered to
be homologous with mammialian Sertoli
cells (Stanley, 1966). Both the spermatogonia and follicle cells undergo an
inital period of mitotic activity. At the end
of this period there are about 500 Sertoli
cells in a Scyliorhinus follicle and about 250
in a Torpedo follicle. Spermatogonia are
present in equal number. Within a follicle,
the two cell types segregate into two concentric single layers. Sertoli cells surround
the central lumen, while spermatogonia
are adjacent to the limiting membrane.
CHONDRICHTHYAN REPRODUCTION
Each spermatogonium is engulfed by a
single follicle cell. The result is a bicellular
unit, the spermatocyst. After this, the Sertoli cell undergoes no further division.
Within a seminiferous follicle, there are
many spermatocysts all of which differentiate synchronously. Each spermatogonium undergoes four successive
divisions to produce 16 spermatogonia.
These transform into 16 primary spermatocytes which undergo meiosis to produce 32 secondary spermatocytes and then
64 spermatids. Spermatids differentiate
into mature sperm. Differentiating sperm
cells are connected by intercellular cytoplasmic bridges. Spermiogenesis has been
described at the ultrastructural level by
Boisson et al. (1968) and Stanley (\91\a,b).
Except for details previously noted, it differs little from spermiogenesis in other
vertebrates. Spermiation takes place in mature follicles, i.e., those with fully differentiated spermatozoa, when an opening
forms in the follicle wall and continuity is
established with the attached terminal
branch of the collecting ductule system.
The bundles of mature sperm pull away
from each of the Sertoli cells and flow into
the ductules. Following this, the follicle
contracts until the Sertoli cells form a solid
mass in the interior. Then they degenerate
and are resorbed. In the chimaera, H.
colliei, the general features of spermatogenesis are similar to those in
Scyliorhinus (Stanley, 1963).
Secondary sex characters
Highly developed male secondary sex
characters are found in the Chondrichthyes. These include the claspers or
copulatory organs and the siphon sac. In
skates and rays, the siphon sac is replaced
by a clasper gland (La Marca, 1964; Babel,
1967). Fertilization is internal in the
Chondrichthyes. The claspers function as
intromittent organs during copulation
(Gilbert and Heath, 1972; Hoar, 1969).
They represent modifications of the male
pelvic fin. Their structure varies in different species (Leigh-Sharpe, 1920-1926, cited
in Hoar, 1969). The clasper is formed in
part by cartilaginous elements which sup-
387
port the medial margin of the pelvic fin
and extend beyond the posterior margin
as a rod. The clasper can be looked upon
as a part of the fin rolled up to form a tube
whose edges overlap. The proximal opening of the clasper tube is the apopyle and
its distal opening is the hypopyle (LeighSharpe, 1920). The mechanism of the
clasper-siphon sac or clasper gland function has been subject to experimental
study in rays, Urolophus (La Marca, 1964;
Babel, 1967) and in the sharks, Squalus and
Mustelus (Gilbert and Heath, 1972). During erection, the clasper in Urolophus,
bends forward to lie along the ventral
surface of the animal (Babel, 1967). La
Marca (1964) reports a medial flexure of
85°. At the same time, the clasper rotates
so the dorsally located apopyle widens and
contacts the cloaca. Sperm then passes
from the urogenital papilla through the
cloaca and into the clasper tube. Contraction of the striated muscles which sheath
the clasper gland expels a secretion into
the clasper tube. The secretion moves the
sperm through the tube and out of its
distal end (Babel, 1967; La Marca, 1964).
Although some details differ, clasper function is similar during copulation in Squalus
and Mustelus (Gilbert and Heath, 1972).
One clasper is flexed medially about 90°
and inserted into the oviduct where it is
anchored to the wall by a cartilaginous
complex at its tip. During copulation,
sperm is passed from the urogenital
papilla into the clasper groove (=tube)
where it is then washed into the oviduct by
sea water expelled from the siphon sac.
The siphon sac had previously been filled
with water by repeated flexing of the
clasper (Gilbert and Heath, 1972). In
sharks, the siphon sacs are paired, subdermal structures located in the pelvic
region on either side of the mid line between the skin and the abdominal wall.
The sacs are blind pockets, closed at their
anterior end and opening into the clasper
groove at their posterior end. Sacs are
sheathed with muscle and lined with a
secretory epithelium. Upon electrical
stimulation of the muscular wall, the sacs
contract to 85 per cent of their original
length. The relative sizes of the sacs vary. In
388
JOHN P. WOURMS
S. acanthias they measure 12 per cent of the
total body length and 30 per cent of the
body length inM. canis (Gilbert and Heath,
1972).
Secretory cells occur throughout the entire epithelium of the siphon sac of sharks
and in localized regions of the clasper
gland in skates and rays (La Marca, 1964;
Babel, 1967; Gilbert and Heath, 1972).
Mann (1960) has shown that the undiluted
siphon sac secretion of sexually mature
spiny dogfish, S. acanthias, contains a high
concentration of 5-hydroxytryptamine (5HT), 5.7-7.7% or about 16 mg/animal.
The siphons of immature males contain
200 times less 5-HT. Mann and Prosser
(1963) demonstrated that application of
either 5-HT or siphon sac fluid to spiny
dogfish uterus in vitro initiated a brief but
powerful contraction which was succeeded
by periodic contractions. They suggested
that 5-HT, introduced during copulation,
caused uterine contractions which would
aid in sperm transport. This generalization
may be premature since 5-HT could not be
found in the clasper glands of Torpedo and
Raja and was present only in traces in
Mustelus canis. The apparent discrepancy
could be explained by a possible diversity
of function. Clasper glands of skates and
rays produce a white, viscous, slightly acid
fluid which coagulates on contact with sea
water. La Marca (1964) reported that the
secretion of the stingray, Urolophus, contained a muco or glycoprotein and a phospholipid. He proposed that some of the
secretion coagulates, sealing the margins
of the clasper groove and thus converting
it into a closed tube. The remainder serves
as a vehicle for sperm suspension and
transport. One also wonders whether these
secretions participate in the formation of
"sperm plugs" found in the uteri of Raja
erinacea (Richards, et al., 1963).
FEMALE REPRODUCTIVE SYSTEM
Functional organization
The female reproductive system consists
of the ovaries and oviducts. These are in
close association but are not morphologically continuous. Oviducts display a con-
siderable degree of regional differentiation. The morphology of the reproductive
system has been well described (Borcea,
1905; Dean, 1906; Daniels, 1928; Gudger,
1940; Metten, 1939; Matthews, 1950; Stanley, 1963; Hoar, 1969). Organization of
the ovary and oviduct is highly variable
due to species diversity and a wide range
of reproductive patterns. Adaptation for
viviparity have a profound effect on the
organization of the oviduct.
Although the ovaries and oviducts begin
development as paired structures, they
often become asymmetrical in adults. In
the sharks, Scyliorhinus, Pristiophorus, Carcharhinus, Galeus, Mustelus, and Sphyrna,
the right ovary is functional and the left
ovary atrophies. Both oviducts are present
(Daniel, 1928). With the exception of
Scyliorhinus, these sharks are viviparous.
Among the viviparous rays, the right ovary
and oviduct undergo varying degrees of
reduction or loss. In Urolophus, the right
ovary is non-functional but both oviducts
are functional. In contrast, both the right
ovary and oviduct are absent in Dasyatis
bleekeri (Babel, 1967). In skates which are
oviparous, both ovaries and oviducts are
present and functional. The oviducts often
function in synchrony (Wourms, unpublished). This is also true for the chimera,
Hydrolagus colliei (Dean, 1906; Stanley,
1963).
The ovaries are paired structures, except as noted above. They are attached on
either side of the vertebral column to the
anterior-dorsal wall of the body cavity by a
mesentery, the mesovarium. Structure and
shape are variable. The ovary is usually
elongate in sharks and some rays (Metten,
1939; Babel, 1967) but may be nearly
spherical in skates (Wourms, unpublished). In most Chondrichthyes, the ovaries
are naked (gymnovarium condition). The
germinal epithelium covers the outer surface of the ovary. Ovarian follicles develop
from the germinal epithelium. Ripe follicles burst through the surface to discharge
ripe ova into the abdominal cavity. In most
instances the ovary is solid. When the
ovary is hollow, lymph spaces develop
within the ovarian stroma. Development of
the ovarian follicle has been reviewed
A
CHONDRICHTHYAN REPRODUCTION
(Hoar, 1969; Dodd, 1972). Except for several points to be considered elsewhere, it is
not noticably different from other vertebrates. Although the ovary of the basking
shark, Cetorhinus, differs considerably
from that of other elasmobranchs
(Matthew, 1950), it is often erroneously
used to illustrate the viviparous condition.
In Cetorhinus, the surface of the ovary is
invested by a fibrous coat. The germinal
epithelium invaginates from the surface to
form a network of tubules. The ovary is, in
effect, hollow. The tubules open to the
surface in a pocket on the right side. Ova
are discharged into the pocket and pass
from there, via the peritoneum, to the
oviduct. In Cetorhinus and some other
elasmobranchs, epigonal organs are associated with the ovary (Matthews, 1950).
Corpora atretica and corpora lutea have
been described for a number of species.
Their probable role in hormone production has been considered (Hoar, 1969;
Dodd, 1972).
The organization of the oviduct varies
according to function and reproductive
pattern. Hoar (1969) summarizes the functions as: 1) egg collection; 2) transport of
eggs to exterior; 3) egg case formation; 4)
site for development of young in viviparous forms; 5) site of sperm reception and
storage; and 6) dissolution of the spermatophore cortex. The oviduct ( = Mullerian duct) originates as a simple tube which
then undergoes regional differentiation.
Four regions can be distinguished: an anterior ostium tubae or funnel; the shell
gland or nidamental gland; a connecting
isthmus; and an expanded posterior
uterus. The ostium is a funnel at the
anterior end of the oviduct which serves to
collect ovulated eggs. It is formed either by
the fusion of the anterior end of the
oviducts, e.g., Cetorhinus, or by asymmetrical development of one primitive funnel,
e.g., that of the right side in Scyliorhinus
(Metten, 1939). From the ostium, a tubular
portion of the oviduct leads to the shell or
nidamental gland. This gland is best developed in oviparous species. In viviparous
species, it tends to be reduced or vestigial.
In its fully developed state, the shell gland
is a compound tubular gland. It synthe-
389
sizes and secretes albumin and mucus in all
species (Threadgold, 1957). In oviparous
species and those viviparous species which
produce egg cases, it also secretes egg case
proteins (Borcea, 1905; Filhol and Garrault, 1938). In some species, e.g.,
Scyliorhinus, it is involved in sperm storage
(Metten, 1939). An isthmus leads from the
shell gland to the posterior region of the
oviduct. The latter region can be expanded, especially in viviparous species, to
form a uterus. In oviparous species, the
uterus normally serves only as a passageway for the eggs. An apparent exception is
the chimaera, H. colliei where the uterine
epithelium participates in the morphogenesis of the egg case (Dean, 1906).
The uterus of viviparous species is highly
developed and displays various modifications for viviparity. These will be discussed
in the section on viviparity. Oviducts sometimes merge at their extreme posterior end
to form a common vagina (Daniels, 1928;
Matthews, 1950). In most species, the
oviducts either singly or as a common
vagina open into the cloaca usually dorsal
to the rectal opening. A hymen or tissue
membrane may be present near the posterior end of the oviduct (Daniels, 1928). In
the chimaera, H. colliei, both oviducts
open directly to the exterior (Dean, 1906).
Oocytes, oogenesis, egg transport
Chondrichthyan fishes produce small
quantities of large eggs. Mature eggs range
in size from one mm in Scoliodon sorrakowah
(Prasad, 1951, cited in Ginzburg, 1972) to
100 mm or more in Ginglymostoma and
Chlamydoselachus (Gudger, 1940). The eggs
of the latter two sharks are probably the
largest known cells of any living animal.
Egg size generally reflects the reproductive strategy of the species. In Scoliodon and
Gymnura (= Pteroplatea) where the egg is
much reduced in size, the developing embryo receives almost all of its nutrients
from the mother via a placenta or
trophonemata (Ranzi, 1934). Massive accumulation of yolk occurs in oviparous
species and in viviparous species such as
Ginglymostoma and Chlamydoselachus in
which the developing embryo is solely de-
390
JOHN P. WOURMS
pendent on its yolk reserves (Gudger,
1940). Mature ovarian and ovulated eggs
have a regular spherical shape. The egg
may assume an ellipsoidal shape when
enclosed in an egg case.
Yolk reserves dominate the structure of
the mature egg. They consist of granules
and platelets associated with small
amounts of cytoplasm. In section, the eggs
of some fishes, e.g., Torpedo, display concentric layers of bright and dark yolk similar to what is seen in the avian egg (Ruckert, 1899). Yolk color tends to be characteristic of a species. It is usually yellow or
orange, but may be pink or light green. A
lens shaped blastodisc is located at one
pole. The blastodisc also may have a distinctive color which differs from that of the
yolk. The egg nucleus is located within and
near the surface of the blastodisc. According to Ginzburg (1972) the nucleus is arrested at metaphase of the second maturation division. The egg is surrounded by an
extracellular egg envelope, closely apposed to the egg surface. Some confusion
exists as to the number of egg envelopes
and their origin (Ginzburg, 1972). Most of
the material is produced by the oocyte,
hence is a primary egg envelope (Balfour,
1885). Follicle cells may contribute additional material. The older literature makes
mention of a zona radiata. In teleosts,
ultrastructural studies have shown that it
consists of the egg envelope matrix and
closely spaced microvilli of the oocyte surface. The latter may interdigitate with follicle cell microvilli (Wourms, 1976). The
chondrichthyan zona radiata is probably of
similar structure.
Mature eggs contain a relatively small
amount of cytoplasm located in the blastodisc and at the peripheral. The cytoplasm contains the standard cell organelles
(Jollie and Jollie, 1967a). Most of the egg,
however, is made up of yolk inclusions.
Yolk platelets predominate together with a
diverse spectrum of inclusion bodies (Jollie
and Jollie, 1967a). The yolk platelets were
described by Riickert (1899) who pointed
out that their size and shape differed according to species. An important chemical
and morphological study of yolk platelets
in Raja batis was done by Faure-Fremiet
(1933). Re-examined in terms of current
knowledge, his results indicate that the
platelets contain livetin, lipovitellin and
probably phosvitin. Fujii (1960) used modern analytical techniques to confirm the
presence of lipovitellin. He also demonstrated that the physical and chemical
properties of the lipoproteins of the
dogfish Scyliorhinus stellaris were very much
similar to those of a frog and the hen. With
regard to structure, platelets occur in the
form of strongly birefringent, rectangular
or pyramidal polygons enclosed in a
fluid-filled vacuole. Faure-Fremiet's experiments (1933) on the platelets indicate that
yolk proteins of skates are assembled in a
paracrystalline lattice which is probably
similar to that of amphibian yolk (Wallace,
1963; Karasaki, 1963). The yolk platelets
of Mustelus canis closely resemble those of
R. batis (Grodzinski, 1958). Electron micrographs of Squalus acanthias eggs while
confirming the general structure of yolk
inclusions were not of sufficiently high
resolution to demonstrate the presence or
absence of periodicities in yolk platelets
(Jollie and Jollie, 1967a). Of the early work
on the chemical composition of eggs, reviewed by Needham (1942), that part dealing with total composition and lipid fractions is still valid. Eggs contain a significant
amount (5.9% wet weight) of urea as do
the tissues of adult fishes. Protein and fat
content varies according to species. Raja
eggs contain 28% protein and 7% fat
whereas eggs of the shark Heptranchus contain 25% protein and 23% fat. The fat
fraction contained 88% neutral fats and
12% unsaponifiable material. Oleic,
linolenic, and iwaskic acids accounted for
79% of the neutral fats. The remaining
21% was made up of isopalmitic, palmitic,
and stearic acids. The unsaponifiable fraction contained octadecyl, cetyl, selachyl alcohols, and cholesterol. Subsequent
studies have confirmed these figures,
shown squalene to be present in quantity,
and added considerably to the list of fatty
acids. Studies on the eggs of deep sea
sharks have shown an increase in the unsaponifiable fat fraction (21-44%) (Higashi
etal., 1953; Zama et al., 1955; Shimma and
Shimma, 1968).
CHONDRICHTHYAN REPRODUCTION
^
391
Although a challenging and perhaps also in the interior of the oocyte. A similar
ideal system for the study of oogenesis, follicular infolding has been observed in
there have been few modern investigations the heavily yolked eggs of cephalopods
of chondrichthyan eggs. Certainly nothing (Cowden, 1968). In addition to the infoldapproaches the combined chemical, struc- ing, cells of the follicular epithelium aptural, and endocrinological studies of am- pear to function as nutrient cells (Wallace,
phibian eggs (Wallace, 1972). A major ex- 1903). Babel (1967) has convincingly demception to this are those studies which have onstrated that enlarged follicle cells conbeen concerned with the endocrine func- tain inclusions which are structurally idention of the ovary. The general pattern of tical to the yolk granules of the oocyte. It
oogenesis does not differ appreciably from would appear that these follicle cells
that of other lower vertebrates with heavily synthesize and transport yolk as do follicle
yolked eggs. Details and further refer- and nurse cells of some invertebrates.
ences can be found in Balfour (1885),
Since a direct connection between the
Wallace (1903), Marechal (1906), Mat- ovary and the oviduct is lacking in most
thews (1950), Bertin's review (1958), and chondrichthyans, mature eggs are disBabel (1967). Oogenesis in chimaeras was charged from the ovary directly into the
described by Dean (1906) and Stanley body cavity. They are then transported to
(1963).
and enter the oviduct via the ostium or
Only two topics will be considered here, funnel at its anterior end. In some species,
lampbrush chromosomes and specialized e.g., Cetorhinus, the ostium is in close proxstructures associated with yolk formation. imity to a specialized ovarian pocket from
Riickert (1892, cited in Callan, 1957) de- which the ova are discharged. Ova pass
scribed lampbrush chromosomes in the directly into the oviduct (Matthew, 1950).
oocytes of the shark Pristiurus only ten In most species, ovulation occurs at any
years after they had been discovered by point along the surface of the ovary. Ova
Flemming. He appears to have been the released into the body cavity are then
first to use the term, lampbrush. In his transported in the oviduct. In Scyliorhinus
definitive study of lampbrush chromo- Metten (1939) has experimentally demonsomes in Pristiurus and Scyllium, Marechal strated that this is effected by continuously
(1906) described them as filaments, mostly beating cilia arranged in tracts within the
in the form of loops projecting laterally abdominal cavity. Selective orientation of
from the chromosome axis. In 1957 Callan the cilia with respect to the direction of
re-examined the lampbrush chromosomes their power strokes enables these tracts to
in the oocytes of Scyllium. He was able to act as unidirectional pathways. Cilia occur
demonstrate, for the first time, the pres- on: the peritoneal wall; outer surface of
ence of axial chromomeres and to show the oviducts; and portions of the liver, bile
that they closely resembled the classical duct, and hepatic portal vein. The absence
of cilia in males and immature females
amphibian lampbrush chromosome.
Due to yolk accumulation during (Metten, 1939) suggests that ciliation is
oogenesis, there is a massive increase in under hormonal control.
egg size. Sometimes yolk accumulation has
involved the modification of pre-existing Sperm storage
structures. Babel (1967) reported an unusual proliferation and infolding of the
Sperm storage occurs in females of sevfollicular epithelium in the oocytes of the eral species of sharks and skates. Informaray Urolophus halleri. Extensive folding car- tion on chimaeroids is insufficient to draw
ries the follicular epithelium far into the conclusions (Stanley, 1963). In addition to
egg's center. This infolding amplifies the demonstrating sperm storage in sharks
surface area of the follicular epithelium. It and skates, Metten (1939) and Richards et
also alters its spatial distribution so that the al. (1963) reviewed the previous evidence.
transport of metabolites or yolk precursors A series of observations have established
would occur not only at the surface but that female elasmobranchs maintained in
392
JOHN P. WOURMS
isolation are able to repeatedly deposit and resemble ellipsoids. There are a
fertilized eggs after an initial mating. For number of exceptions. Eggs of the
example, Clark (1922) reported that a heterodontid sharks resemble a wood
female skate, in the absence of males, auger (Smith, 1942). The ellipsoidal body
deposited fertilized eggs during a period of the egg case is surmounted by two
of five-six weeks. Metten (1939) concluded flanges which spiral around the case. The
that the shell gland is the site of sperm egg cases of chimaeras are intricate and
storage since he found sperm there but not morphologically complex {cf., Dean, 1906
in other regions of the reproductive tract. for detailed descriptions). They are spinIn freshly excised glands, clusters of active dle or tadpole-shaped and are exceptionsperm were found within the lumen of ally large (150-450 mm) both in absolute
those tubules which secrete the egg shell. and relative terms. Their shape conforms
Sperm were not found in the albumin or not only to the shape of the egg but to the
shape of the fully developed embryo
mucous secreting regions of the gland.
(Dean, 1906). They possess a series of
respiratory pores and elaborately sculpEgg cases and egg case formation
tured lateral flanges. Newly formed egg
cases
are light colored, often white. They
The eggs of all oviparous species and
rapidly
darken after oviposition (Dean,
many viviparous species are enclosed in
1906).
leathery egg cases. Chondrichthyans proModern work on the structure and
duce two types of egg cases. Oviparous
species produce permanent egg cases composition of egg cases begins with
which are usually deposited on or near the Faure-Fremiet. Working with Scyliorhinus
bottom. Embryonic development is com- and two species of Raja, he showed that the
pleted within the egg case. Both egg case egg case was made up of many layers.
and embryo are subject to physical and When examined with polarizing optics,
biological hazards. In viviparous species, alternating layers were strongly birefrindiverse reproductive strategies govern the gent. Protein was found to be the principal
fate of egg cases. In some instances, e.g., structural component. On the basis of its
the stingray Urolophus, an egg case is not relative insolubility and sulfur content, the
formed (Babel, 1967). In many species, a structural protein was considered to be a
temporary egg case is formed from which type of keratin, ovokeratin (Faurethe embryo emerges to complete de- Fremiet, 1938; Faure-Fremiet and
velopment in utero. Finally the egg case Baudouy, 1938). Subsequent chemical and
may be retained during the entire period physical studies, however, indicated that
of intra-uterine development and even in- the structural protein(s) was not keratin
corporated into the placenta, e.g., M. cams but collagen (Gross et al., 1958). Early
(Te Winkel, 1963). Size and shape of egg electron microscope studies (Gross et al.,
cases vary according to species. The egg 1958) failed to find axial periodicities.
case of the whale shark Rhincodon is 150 x Wourms and Sheldon (1971, 1972) re300 mm (Baughman, 1955) whereas that ported that shark and skate egg cases conof Scoliodon sorrakowah is 3 x 5 mm (Prasad, tain an imperfectly ordered orthogonal
1951, cited in Ginzburg, 1972). Four basic array of structural components. One comshapes are encountered (cf. Cox, 1963, for ponent displays a 400 A periodicity whose
illustrations). Egg cases of skates and some banding pattern remains in lateral register
sharks, e.g., Rhincodon, are quandrangular over long distances. The repeat units conwith horn-like processes at each corner. sists of: 1) a 90 A dense band; 2) a 125 A
The dorsal surface is usually arched while light band traversed by fine filaments in
the ventral surface is flattened. Species ladder-like fashion; 3) a second 90 A
differences which may be associated with dense band; and 4) a 90 A light band not
environmental adaptations have been de- traversed by filaments. Each dense band
scribed in skates (Ishiyama, 1958). Egg can be resolved into two dense sub-bands
cases of sharks tend to be more rounded separated by a light band. Equidistant
A
CHONDRICHTHYAN REPRODUCTION
fe
50-75 A point densities observed in transverse sections probably are sectioned filaments. The periodicity and banding pattern differs from that of most vertebrate
collagens. It closely resembles the elastoidin form of collagen found in sharks by
McGavin and Pyper (1964). The organization of egg case collagen does not appear
to be fibrillar. A cholesteric liquid crystal
model of egg case collagen best explains
both the completed structure and its mode
of assembly (Wourms, unpublished). The
same periodicities and banding patterns
have now been found in Heterodontus, Apristurus, Ginglymostoma, Galeorhinus,
Halaelurus, CephaloscyIlium, and Raja
(Wourms and Sheldon, unpublished). Recently, Knight and Hunt (1974, 1976) have
confirmed and extended these observations in the egg cases of Scyliorhinus
caniculus using biochemical, X-ray diffraction, and ultrastructural methods. Their
results were corroborated by Rusaoven et
al. (1976). While collagen is the major
structural component of shark and skate
egg cases, the question remains whether
there are other components present. Egg
case collagen may have unique physical
and chemical properties. Chemical studies
have shown that the tyrosine content is
unusually high for collagen. Tyrosine residues may provide the basis for phenolic
crosslinking. This is consistent with the
demonstration of a quinone-tanned protein in the egg case (Brown, 1955) and
phenol oxidases in the shell gland
(Threadgold, 1957; Krishnan, 1959). The
presence of sulfur in egg cases, originally
reported by Faure-Fremiet, is not inconsistent with collagen since Blanquet and
Lenhoff (1966) have found disulfidelinked collagenous proteins in nematocysts.
393
of layers and their relative positions vary.
Ultrastructural examination revealed: 1) a
granular layer smilar to the outer layer of
the dogfish egg case; 2) layers of fibrils
without banding patterns or periodicity;
and 3) a population of tubular components. Granules are of different sizes and
they seem to be aggregates of smaller
units. The tubular component forms the
egg case surface, associated sculpturing,
and the filamentous projections. The tubular component is a lattice of 550 A
pseudotubules. Lattices are arranged in
layers in which all of the pseudotubules are
oriented in one direction. Adjacent layers
are aligned at 90° angles to form an imperfect orthogonal array. The 550 A unit is a
pseudotubule since the walls of adjacent
tubules are shared in common. The walls
contain 10-15 subunits about 90 A in
diameter. The subunits appear to be hollow cylinders (Wourms and Sheldon,
1971; unpublished). Illustrations of fossil
chimaeroid egg cases (Dean, 1906) differ
little from modern egg cases. The remarkable difference in structure and the probable difference in chemical composition of
elasmobranch and holocephalan egg case
proteins is consistent with Patterson's
(1965) view that a direct relationship between the two groups cannot be demonstrated.
The chondrichthyan egg case is a tertiary egg envelope (Wilson, 1925, following Ludwig, 1875) since its structural proteins are synthesized and secreted by the
oviduct. At the time of spawning, an egg
enters the oviduct, is fertilized and is enclosed in an egg case. The shell gland, a
specialized region of the anterior oviduct
synthesizes and secretes egg case structural
proteins (Borcea, 1905; Dean, 1906; Filhol
and Garrault, 1938). It also appears to
Egg cases of chimeras display a consid- control the deposition and morphogenesis
erably different structural organization of the egg case in sharks and skates
which probably reflects a basic chemical (Borcea, 1905; Fitz and Daiber, 1963). In
difference. Egg cases of Hydrolagus, Cal- the chimaera, H. colliei, the posterior relorhynchus, and Harriotta, representing gion of the oviduct appears to participate
members of the three families of living in the moulding of the lateral flanges and
chimeras, have an identical structural or- respiratory pores (Dean, 1906). The seganization. The egg case is made up of quence of egg case formation in the skate
three structural components arranged in R. eglanteria proceeds according to the
discrete, birefringent layers. The number following sequence: 1) formation of the
394
JOHN P. WOURMS
anterior horns; 2) formation of the anterior two-thirds of the egg case; 3) fertilized egg flows into case; 4) posterior
third forms; and 5) posterior horns are
completed (Fitz and Daiber, 1963). In the
chimaera H. colliei the sequence is similar.
The egg containing capsule is formed first
and then the spindle shaped tail portion
(Dean, 1906).
The shell gland is a compound tubular
gland (Borcea, 1905; Filhol and Garrault,
1938). The epithelial cells forming the
tubules are secretory cells. Zones of specific secretory activity can be distinguished.
Although there is variation, especially in
viviparous species, three regions have been
distinguished using simple staining
techniques, viz., an anterior zone of ovalbumin synthesis, a zone of mucous synthesis, and a zone of shell protein synthesis
(Metten, 1939). Histochemical studies of
the same species of Scyliorhinus (Threadgold, 1957) showed five distinct regions.
"These zones secrete respectively a carbohydrate, a carbohydrate substance
which is metachromatic, a polyphenol
oxidase, a protein, a phenol, and perhaps a
phenolic protein and a basic protein."
Similar results were obtained by Krishnan
(1959). Combined histochemical and incorporation studies with radioactive proline suggest that two classes of cells are
present within the same shell secreting
tubules and occupy alternate positions
(Rusaouen et al., 1976). One cell secretes
collagen and the other secretes a protein
containing large amounts of tyrosine and
sulfhydryl groups. These findings would
be consistent with a collagen cross linked
by phenolic tanning and disulfide linkages.
Wourms and Sheldon (1972; unpublished)
reported on the ultrastructure of the shell
gland in Raja inornata Jordan and Gilbert.
They found that within the tubule of the
shell secreting region all of the cells in a
given region were identical. Shell secreting
cells have an abundant and well developed
rough endoplasmic reticulum. They also
contain many granules which consist of an
outer ring of light material and an inner
core of dark material. Granules are
formed within the Golgi complex from
. material derived from the rough endo-
plasmic reticulum. Granules are secreted
into the lumen where they coalesce into
fibrils. Light material within the fibrils has
a 400 A periodicity and the banding pattern of egg case collagen. It is possible that
both egg case collagen and the phenolic
tanning enzymes are packaged in the same
granule. The terminal stages of secretion
agree with Borcea's (1905) scheme. Shell
secreting tubules empty into common
ducts at the base of ciliated lamellae. Parallel rows of lamellae extend across the inner
surface of the gland. It is suggested that
nascent fibrils leaving the tubules fuse into
sheets which are sequentially extruded
from the structurally polarized lamellae.
Each lamella would control the deposition
of a single layer in the egg case. At this
point the advantages of a liquid crystal
model of collagen organization are apparent. It provides the plasticity necessary to
make rearrangements at the molecular
and supramolecular level.
MATING AND PARENTAL CARE
Mating
In chondrichthyan fishes, fertilization is
internal and obviously requires close contact between the sexes. Copulation, however, has been observed only on infrequent
occasion. Most accounts deal with small,
inshore fishes, e.g., Scyliorhinus, Heterodontus, and Raja. In spite of the paucity of
information, mating appears to follow one
of several patterns. These seem to be determined by the size and shape of the
fishes.
In small sharks and probably also
chimaeras, the male coils himself around
the female. This was first observed in
Scyliorhinus and probably also occurs in
Squalus and Mustelus (Gilbert and Heath,
1972). A more complete description of
mating behavior is available for Heterodontusfrancisci (Dempster and Herald, 1961).
Courtship commenced with the male biting the female on almost any part of the
body. Seizing the left pectoral fin of the
female in his mouth, the male manoeuvred
his tail over the back of the female immediately in front of the second dorsal fin.
m
CHONDRICHTHYAN REPRODUCTION
395
With the purchase thus afforded, he in- the pair resting ventral side down on the
serted the right clasper into the cloaca. bottom. The male bent his tail 75° beneath
Copulation lasted about a half hour during the female's, flexed one clasper medially
which the female was passive. Although 90° and inserted it into the cloaca and
copulation has not been observed in oviduct. Spines (=alar spines?) on the
chimaeras, there is circumstantial evidence upper anterior surface of the male's pecthat the series of actions involved is similar toral fin assisted in holding the female.
to that of small sharks. Male holocephalans Small species of skates mate with the venpossess a second pair of claspers, the tral surfaces apposed. Richards et al.
antero-pelvic claspers. They also possess a (1963) state that "after the male mounts
cephalic clasper. Neither organ is found in the female, she rolls her pectorals inside
elasmobranchs (Dean, 1906). The clasper his allowing him to maintain a firm hold on
is a cartilagenous rod equipped with denti- her back with his alar spines." Alar spines
cles. Movement is effected through at- are retractile, claw-like spines found in
tachments to the musculature of the lower adult male skates where they occupy one to
jaw and labial cartilage (Raikow and five rows at the outer margin of the dorsal
Swierczewski, 1975). Dean (1906) suggests surface of each pectoral fin (Bigelow and
that the cephalic clasper is used to grasp Schroeder, 1953). Although definitive evithe female since the pattern of scars found dence is lacking, rays seem to copulate as
near the dorsal fin of egg-laying females do the small skates. La Marca (1964) states
matches the arrangement of denticles on that the length and manner of flexion of
the clasper. Dean (1906) concludes that in the claspers in the stingray Urolophus rules
Hydrolagus colliei, the male wraps his body out any method of copulation except venaround the female and gains purchase by tral apposition.
attaching the cephalic clasper near the
Female sharks of a variety of species
female's dorsal fin. The antero-pelvic clas- have been reported to bear the scars of
pers which are erectile probably serve as tooth cuts on their bodies (Springer, 1960,
additional means of attachment.
1967; Stevens, 1974). In the blue shark, P.
Relatively little is known about copula- glauca, tooth cuts which are found only on
tory behavior in large sharks. Clark (1963) female sharks longer than 180 cm are
reports observations made by Brown on considered to be courtship scars (Stevens,
the lemon shark Negaprion brevirostris Poey. 1974). Somewhat earlier Springer (1967)
Copulation took place at night. The pair had reached a similar conclusion based on
assumed a parallel position with the heads the examination of a number of species of
slightly apart and the posterior half of the large sharks. Drawing on Clark's account
bodies in very close contact. The pair of copulation in the lemon shark, Stevens
moved in tandem with closely syn- (1974) concluded that the bites were not
chronized swimming motions. It is reason- made to aid the male in hanging on during
able to assume that this parallel position is copulation. Instead, biting serves as a
typical of copulation in large sharks. Their necessary pre-copulatory release mechaless flexible bodies preclude them from nism in females. Biting behavior observed
assuming the coiled position of smaller during the courtship of'Heterodontns (Dempster and Herald, 1961) and Raja eglanspecies.
taria
(Libby and Gilbert, 1960) supports
There are two main patterns of copulation in skates and rays. Smaller species of this view. Tooth sexual dimorphism reskates mate with the ventral surfaces ap- ported in some sharks (Springer, 1967)
posed while males of larger species make seems to be related to courtship behavior.
either a dorsal or ventral approach
(Richards et al., 1963). Libby and Gilbert Parental care
(I960) observed mating in Raja eglantaria.
It lasted for more than two hours. The
In the strict sense of the term, parental
male bit the caudal margin of the female's care of the young is unknown. Early repectoral fin. Copulation took place with ports of parental care based on the obser-
396
JOHN P. WOURMS
vation of family groups composed of
mother and young are misinterpretations
(Breder and Rosen, 1966). It was not parental care but rather the tendency of
small sharks to follow any large moving
object. The closest approach to parental
care appears to involve the selection of
incubation sites and the specific orientation of egg capsules within these sites.
McLaughlin and O'Gower (1971) present
circumstantial evidence for this in Port
Jackson sharks,//, portusjacksoni. Spawning
probably occurs in open areas. They
suggest that the female takes the newly
extruded egg in her mouth, swims to a
protected site, and places the egg in a
crevice. After hardening, the egg due to its
corkscrew shape is effectively anchored in
place. If confirmed, this would account for
the "nest" of H. japonicus eggs described by
Smith (1942).
EARLY DEVELOPMENT
Fertilization and polyspermy
Fertilization is internal in all chondrichthyan fishes. Gametic encounter
takes place in the upper part of the
oviduct, anterior to the shell gland when
this gland is present. Riickert (1899) demonstrated that eggs which were at the entrance of the shell gland had been fertilized
and contained spermatozoa which were
transforming into pronuclei. In some
species, e. g., Scyliorhinus where sperm
storage occurs, fertilization is believed to
occur in the shell gland (Metten, 1939).
Further study is needed. In either case, it
follows that fertilization occurs before the
egg case is fully formed.
Physiological polyspermy, as a normal
aspect of fertilization has been recognized
since the latter part of the 19th century
(Ginzburg, 1972). Chondrichthyan eggs
are heavily yolked and their development
superficially resembles that of avian and
reptilian eggs. Fertilization and early development occur within the blastodisc.
Riickert (1899), Dean (1906) and others
have shown that the blastodisc is penetrated by a number of spermatozoa (over
100 in some sharks). Monospermy does
not seem to occur. Riickert (1899) reports
that all of the spermatozoa entering the
blastodisc are transformed into pronuclei
of similar size and structure. The female
pronucleus fuses with the closest male
pronucleus. At first, supernumerary male
pronuclei are evenly distributed in the
blastodisc, but are subsequently displaced
by derivatives of the zygote nucleus. The
supernumerary pronuclei undergo mitosis, display typical metaphase figures, and
remain viable throughout the blastula
stage. Although they do not participate in
embryogeneses, their exact fate is not
known. According to Riickert (1899), they
become the periblast nuclei, a theory
which is the basis of an historical controversy (Nelsen, 1953). Although they
may persist for long periods, it is likely that
the supernumerary pronuclei degenerate.
Periblast cells probably arise from peripheral blastoderm cells.
Development
An overview of chondrichthyan development is given by Balfour (1885);
Ziegler (1902); Nelsen (1953); and Pasteels
(1957). The chondrichthyan egg is markedly telolecithal. Cleavage is meroblastic
and is usually confined to a small cap of
cytoplasm, at one pole, the blastodisc. Eggs
of the horned shark, Heterodontus, and the
chimera, Hydrolagus, also undergo a series
of cleavages within the yolk mass (Smith,
1942; Dean, 1906). Prior to the the first
cleavage, the zygote nucleus divides several times producing four or more nuclei
and establishing a temporary syncytium.
The first four cleavages are meridional or
vertical. The resulting blastoderm consists
of a central group of three or four cells
surrounded by 10-12 marginal cells. The
fifth cleavage plane is horizontal and produces an upper and lower layer of blastomeres in the central region. A cavity subsequently appears between the two layers.
Successive cleavages establish three major
cell populations: surface blastomeres, deep
blastomeres, and periblast. The surface
blastomeres, consisting of a single layer of
cells, encloses the segmentation cavity.
Deep blastomeres are numerous and lie
CHONDRICHTHYAN REPRODUCTION
m.
397
within the segmentation cavity. Only these
two populations participate in embryo
formation. The third population, the syncytial periblast, occupies a peripheral position and also extends centrally as the floor
of the segmentation cavity. The blastoderm acquires a flattened disc shape as
cleavage continues. Its upper surface is
made up of a single layer of flattened cells
beneath which is a tightly packed mass of
deep blastomeres. The segmentation cavity is present only in the caudal portion of
the blastoderm. Vandebroek (1936) has
provided a fate map of the presumptive
organ forming areas in the blastoderm of
the shark, Scyllium. Most of the future
endoderm lies on the surface in a small
sector at the caudal margin of the blastoderm. Some endodermal cells also lie
deep within the blastoderm. The epidermal ectoderm occupies almost the entire
cephalic portion of the blastoderm. Immediately behind it is a large semi-circular
region of presumptive neuroectoderm.
The prechordal plate forms a small median region on the surface immediately
cephalic to the endoderm. A thin crescent
of notochord lies between the pre-chordal
plate and the neural ectoderm. The presumptive mesoderm is found in two crescent shaped regions along the lateralcaudal margins of the blastoderm (Vandebroek, 1936; Nelsen, 1953).
doderm establishes a complete floor by
growing medially beneath the mesodermal plates and fusing below the
notochord (Vanderbroek, 1936; Nelsen,
1953). Vandebroek's (1936) fate map and
account of morphogenetic movements
should be approached with considerable
caution. The recent drastic revision of the
classical account of morphogenetic movements and the fate map of the trout (Ballard, I966a,b, 1968) calls into question
other studies of the same vintage and
employing similar methods. In point of
fact, preliminary studies by Ballard (personal communication) have shown that
Vanderbroek's account is in error and
must be redone. In this respect, it is worth
noting that there are very few experimental studies of the early development of
elasmobranchs. Vivien (1955) reported
that the pregastrula blastoderm of
Scyliorhinus could be divided into two or
four segments without affecting development. After formation of the subgerminal
cavity, sagittal section of the blastoderm
caused twin formation. Isolated marginal
regions did not form embryos. Two embryos with normal orientation were obtained by transverse section of the caudal
region of the blastoderm, i.e., over the
subgerminal cavity. Loss of regulatory ability coincided with the onset of active morphogenetic movement.
In addition to the classical accounts,
Vandebroek (1936) has provided an
analysis of the complex morphogenetic
movements which culminate in embryogenesis. During gastrulation, the presumptive epidermal and neural ectoderm
retain their surface location and expand
greatly. Notochordal, pre-chordal plate,
mesodermal and endodermal cells migrate
from the surface, over the caudal edge of
the blastodisc, into the segmentation cavity. The cells of the notochord and prechordal plate move into a median position
beneath the neural plate. As the embryo
begins to take shape, it rises above the
surface of the blastoderm. A head fold is
present at the anterior end while a
notochord has formed in the median
plane. The mesoderm and endoderm lie
on either side of it. Subsequently, the en-
The later phases of development have
been dealt with on numerous occasions
and except for the following topics will not
be considered here (cf., Balfour, 1885;
Ziegler, 1903; Dean, 1906; Nelsen, 1953;
Pasteels, 1958). Dean (1906) in his study of
the chimaeroid fish, H. colliei, states that
their development is shark-like. Several
points of difference exist and should be
re-examined. The behaviour of the yolk
during development is remarkable. By day
32, and early embryo, the yolk mass has
been partitioned into fragments of varying
size. Prior to that, it underwent a modified
total cleavage. Only a small portion of the
yolk is enclosed within the yolk sac. The
rest, an estimated 80-90%, forms a creamy
mass. Dean (1906) suggests that this yolk
either is absorbed via the external gills or is
swallowed. Dean (1906) also describes and
398
JOHN P. WOURMS
figures an open blastopore which com- in Breder and Rosen, 1966). One would
municates with an archenteron. The ar- like to know whether the rate of developchenteron is lined with several layers of ment is intrinsically more rapid in warm
cells and is distinct from the segmentation water species or is brevity due to a higher
cavity. Since Dean worked with a limited temperature.
amount of preserved material, the need
for critical re-examination is obvious.
REPRODUCTIVE PATTERNS—VIVIPARITY
Embryonic development is a lengthy
process. It is longest in sharks and
Reproductive patterns in chondrichthychimaeras, of intermediate length in an fishes have been reviewed by Breder
skates, and shortest in the rays. Develop- and Rosen (1966) and others (Ranzi, 1932,
mental rate is temperature dependent 1934; Needham, 1942; Budker 1958;
(Harris, 1952) and also species specific. Amoroso, 1960; Hoar, 1969). An overall
Development is relatively rapid in the vivip- picture emerges. All recent chondrichthyarous rays. The gestation period is 4 an fishes employ internal fertilization.
months in Myliobatis bovina, 3 months With few exceptions, e.g., Cetorhinus
in Urolophus halleri, and 2 months for (Matthews, 1960), they produce a relaDasyatis (=Trygon) violacea (Ranzi, 1934; tively small number of large, heavily
Babel 1967). Development in the ovipa- yolked eggs. These fishes are either
rous skates is of intermediate duration. In oviparous or viviparous (Tables 1, 2). If
six species of skates within the genus Raja, they are oviparous (chimaeras, skates,
Clark (1922) observed incubation times some sharks) their eggs are enclosed in an
which ranged from 4.5-5.5 months in R. egg case and deposited in the external
clavata Linnaeus to 8 months in R. naevus environment. Development is completed
Miiller and Henle. An apparent exception outside of the body of the mother. Eggs
is R. marginata Lacepede with a duration of are retained in viviparous species and emalmost 15 months. In R. eglantaria, Libby bryonic development is completed in utero.
and Gilbert (1960) found an incubation Traditionally, these fishes have been
time of 9 weeks in a Florida population. categorized as oviparous, ovoviviparous,
Whereas Fitz and Daiber (1963) reported or viviparous species. Budker (1958) and
12 weeks for northern (Delaware-New Hoar (1969) pointed out that the distincYork) populations. Among sharks and tion between ovoviviparity and viviparity is
chimaeras, especially those from temper- artificial. Ranzi (1934) has shown that in
ate waters, the longest incubation or gesta- live bearing species fetal/maternal nutrition periods occur. Dean (1906) reports tional dependency ranges from nil to alincubation times of 9-12 months for the most complete. Placental species only occhimaera, H. colliei. Similar times have cupy an intermediate position in this
been reported by McLaughlin and series. Moreover, the placenta develops
O'Gower (1971) for three species within only after a period of yolk reserve dethe oviparous shark genus Heterodontus. In pendency. Budker (1958) subdivided the
Scyliorhinus the incubation time is 6-8 viviparous fishes into placental and aplamonths (Ranzi, 1934; Harris, 1952). Gestation periods of 11 months and 8-12
months respectively have been reported TABLE 1. Reproductive patterns in chondnchthyan fishes.
for the carcharhinid sharks, Mustelus canis I. Oviparity
(Te Winkel, 1950) and C. milberti (Spring- II. Viviparity
A. Aplacental viviparity
er, 1960). The 22-24 month gestation
1. Dependent solely on yolk reserves
period of the spiny dogfish, S. acanthias is
2. Oophagy: Intrauterine embryonic canthe longest period thus far documented.
nibalism
At the other extreme, an Indian shark,
3. Placental analogues — uterine milk secretion and/or uterine trophonemata
Chiloscylium grispem Miiller and Henle lays
B. Placental viviparity
eggs that take 2.5-3.0 months to complete
1. Yolk sac placenta: Ontogenetic transition
development (Aiyar and Nalini, 1938 cited
from yolk reserve dependency
CHONDRICHTHYAN REPRODUCTION
399
TABLE 2. Modes of reproduction in chondrichthyan fishes.
Class Chondrichthyes
Subclass Elasmobranchii
Order Squaliformes
Suborder Hexanchoidei
1. Family Hexanchidae (Cow Sharks)— Viviparous
2. Family Chlamydoselachidae (Frill Sharks) —
Viviparous
Suborder Heterodontoidei
3. Family Heterodontidae (Bullhead or Horn
Sharks) — Oviparous
Suborder Lamnoidei
4. Family Odontaspidae (Sand Sharks) — Viviparous
5. Family Scapanorhynchidae (Goblin Sharks) —
Viviparous
6. Family Lamnidae (Mackerel Sharks) — Viviparous
7. Family Cetorhinidae (Basking Sharks) — Presumed viviparous
8. Family Alopiidae (Thresher Sharks) — Viviparous
9. Family Orectolobidae (Carpet or Nurse Sharks)
— Oviparous and viviparous
10. Family Rhincodontidae (Whale Sharks) —
Oviparous
11. Family Scyliorhinidae (Cat Sharks) — Oviparous, one viviparous species
12. Family Carcharhinidae (Requiem Sharks) — Viviparous
13. Family Sphyrnidae (Hammerhead Sharks) —
Viviparous
Suborder Squaloide
14. Family Squalidae (Dogfish Sharks) — Viviparous
15. Family Pristiophoridae (Saw Sharks) — Vivipa-
16. Family Squatinidae (Angel Sharks) —Viviparous
Order Rajiformes
Suborder Pristoidei
17. Family Pristidae (Sawfishes) — Viviparous
Suborder Rhinobatoidei
18. Family Rhinobatidae (Guitarfishes) — Viviparous
19. Family Rhynchobatidae (Guitarfishes) — Viviparous
Suborder Torpedinoidei
20. Family Torpedinidae (Electric Rays) —Viviparous
21. Family Narkidae (Electric Rays) — Viviparous
22. Family Temeridae (Electric Rays) — Viviparous
Suborder Rajoidei
23. Family Rajidae (Skates) — Viviparous
24. Family Arhynchobatidae (Skates) — Oviparous
25. Family Anacanthobatidae (Skates) — Oviparous
Suborder Myliobatoidei
26. Family Dasyatidae (Sting Rays) — Viviparous
27. Family Myliobatidae (Eagle Rays) — Viviparous
28. Family Mobulidae (Manta Rays) — Viviparous
Subclass Holocephali
Order Chimaeriformes
29. Family Callorhynchidae (Chimaera) — Oviparous
30. Family Chimaeridae (Chimaera) — Oviparous
31. Family Rhinochimeridae (Chimaera) — Oviparous
Modified from Breder and Rosen, 1966and Budker,
1971.
cental species. Here, the aplacental species
have been categorized as: 1) dependent
solely on yolk reserves; 2) oophagous; or 3)
possessing placental analogues (Table 1).
Table 2 summarizes the occurrence of
oviparity and viviparity within the Chondrichthyes (cf., Breder and Rosen, 1966;
Bigelow and Schroeder, 1948, 1953 for
additional detail). Viviparity, in varying
degrees, is widespread. It almost seems
characteristic of the elasmobranchs.
Oviparity, in contrast, is confined to the
three extant families of chimaeras, the
three or more families of skates in the
suborder Rajoidei, and four families of
sharks.
Knowledge of the developmental
physiology of oviparous species is derived
chiefly from studies on the sharks,
Scyliorhinus and skates, Raja. Following
oviposition, the embryo enclosed in the
egg case completes its development while
exposed to the vagaries of the surrounding
environment. Harris (1952) and Collenot
(1966) have shown that the rate of development is temperature dependent. The
egg case affords a considerable degree of
mechanical protection. Phenols contained
within it may serve as anti-microbial
agents. During the early phases of development, the embryo is sealed within the
egg case and is effectively isolated from the
outside environment (Ouang, 1931;
Smith, 1936). The egg and embryo retain
urea, even though the egg case is structurally permeable to it (Needham and
Needham, 1930). Sometime during early
development, at 20 days in Raja eglanteria
(Libby and Gilbert, 1960) and at the 35-40
mm stage in Scyliorhinus, (Collenot, 1966),
sea water is admitted into the egg. This is
brought about by the dissolution of mu-
400
JOHN P. WOURMS
cous plugs in preformed passages (Col- 55%) loss of organic material during delenot, 1966) or the opening of respiratory velopment (Ranzi, 1934; Hisaw and Alpores (Dean, 1906). Rhythmic movements bert, 1947; Amoroso, 1960). S. acanthias is
of the embryo bring about a continuous typical. One to four fertilized eggs are
flow of sea water through the egg case. enclosed in an elongated egg case. The egg
The egg contains all of the organic mate- case remains intact for about six months,
rial required for development. Although after which the embryos hatch and commostly used in forming embryonic struc- plete the remaining 12-16 months gestatures, some serves as an energy source. tion in the uterus. The processes of yolk
This accounts for the 21% loss of organic absorption and utilization are similar to
material during the development of those of oviparous species, especially
Scyliorhinus (Ranzi, 1932; Amoroso, 1960). Scyliorhinus (Te Winkel, 1943). The syncyWater and inorganic material are derived tial yolk sac cytoplasm digests and absorbs
from the environment (Amoroso, 1960).
yolk during early stages (Jollie and Jollie,
Organic material, stored in the yolk, is 1967a). During later stages, yolk platelets
transferred to the developing embryo by are moved from the external sac up the
several different processes (Beard, 1896; yolk stalk into the internal sac and from
Te Winkel, 1943; Jollie and Jollie, 1967a). there into the intestine. Movement is efIn the earliest phase, yolk is incorporated fected by ciliated epithelia. The intestine
into blastoderm cells, probably by becomes functional when the embryo is
phagocytosis, and digested intracellularly. approximately 65-70 mm long. During deIn the next phase, yolk was once believed velopment, the internal yolk sac increases
to be digested extracellularly by merocytes, in size while the external yolk sac is dii.e., extra-embryonic yolk cells. Jollie and minished. Absorption is almost complete at
Jollie (1967a) have shown that in Squalus parturition (Te Winkel, 1943). Jollie and
the merocytes are part of the peripheral Jollie (19676) describe ultrastructural
syncytial cytoplasm of the yolk sac. The changes in the mucosa of the pregnant
products of digestion pass into the vitelline uterus. It is transformed into a respiratory
circulation. Extracellular digestion by the membrane which may also regulate the
endodermal epithelium of the yolk sac and transport of water and electrolytes.
subsequent absorption of digested yolk Changes involve extensive vascularization
into the vitelline circulation may also oc- and a reduction in the quantity of tissue
cur. In the Chondrichthyes, all three germ between the maternal blood and the
layers take part in the epiboly of the blas- uterine lumen.
todisc to form a three-layered yolk sac
Oophagy, a curious adaptation for vi(Ruckert, 1922). In the later phases of viparity, has evolved in several families of
development, yolk is mainly digested shark. It is a form of intra-uterine emwithin the intestine of the embryos (Beard, bryonic cannibalism and can be said to
1896; Te Winkel, 1943). Yolk platelets are represent a final solution to sibling rivalry.
moved directly from the external yolk sac The phenomenon was first recognized and
into the gut by ciliated epithelia. In some described by Lohberger (1910) and subinstances, e.g., Scyliorhinus (Collenot, 1966), sequently confirmed by Shann (1923) in
the yolk duct or umbilical canal is enlarged embryos of porbeagle sharks, Lamna spp.
at its terminal end to form an internal yolk Porbeagle embryos are quite large and
sac which empties directly into the intes- massive, over 55 cm in length. They aptine.
pear to have an enormous yolk sac. The
The least specialized of the viviparous yolk sac, however, is absorbed at an early
fishes are those aplacental species which (6 cm) stage (Shann, 1923). What appears
depend solely on yolk reserves. This to be a yolk sac is really the cardiac
category corresponds in part to Types la stomach, enormously distended by eggs
and Ib of Ranzi (1934). Fishes exhibiting which have been ingested by the developthis pattern, e.g., Squalus acanthias, Scymnus,ing embryo. In Lamna cornubica, each
Centrophorus, display a considerable (15- oviduct may contain two embryos. Some
CHONDRICHTHYAN REPRODUCTION
authors (Gudger, 1940) have overlooked
the phenomenon of oophagy. As a result
they have concluded that the enormous
size of the porbeagle embryos is due to
eggs which are of enormous size. More
recently, Springer (1948) has reported on
oophagy in the sand shark Odontaspis
taurus (Rafinesque) (=Carcharius taurus).
Living embryos were exceedingly active in
utero. They dashed about, open mouthed,
inside the oviduct snapping at whatever
they encountered, including the investigator's hand. In this case, there was only
one embryo in each oviduct. Normally,
several fertilized ova are enclosed within
one egg capsule, but only a single active
embryo hatches. This strategy is strikingly
similar to that of some gastropods, e.g., the
Buccinidae and Muricidae. Once hatched,
the developing embryo feeds on successive
crops of ovulated eggs. Springer (1948)
suggests that oophagy offers two advantages. It produces very large embryos (up
to 105 cm) which carry an extra reserve of
nutrients. Also, as a result of its intrauterine behaviour, the fetal shark emerges
at parturition as an experienced predator.
The frequency with which oophagy occurs
is not known. Springer (1948) and Budker
(1971) suggest that additional species of
mackerel sharks (Lamnidae) and some
thresher sharks (Alopiidae) are oophagous. Even without chemical analysis, it is
obvious that oophagous embryos undergo
a great increase in organic content. Added
material is of maternal origin.
401
lipid and protein containing granules appear, mature, and are secreted. The most
highly developed placental analogues
occur in the form of villous tufts of uterine
epithelium, e.g., Dasyatis violacea and
Myliobatis bovina or trophonemata, e.g.,
Gymnura micrura (Ranzi, 1934). Trophonemata are long, flattened glandular
appendages. They enter the embryo
through the spiracles and pass into the
esophagus where they release secretory
product into the gut. Wood-Mason and
Alcock (1891) introduced the term,
trophonemata, to distinguish them from
intestinal villi. The efficiency of placental
analogues surpasses that of the yolk sac
placenta. They account for a 1700-5000%
increase in organic material during development compared to the 840% and
1050% increase in two placental species,
the blue shark, P. glauca, and the dogfish,
M. laevis (Ranzi, 1934; Needham, 1942).
The placental analogues found in these
three species of rays represent the culmination of a series of adaptations which
originate with yolk dependent species.
Stages in the evolution of placental
analogues become apparent when the electric rays, Torpedo ocellata and T. mormorata
are considered. Both show a net loss of
organic material during development,
22% and 34% respectively (Ranzi, 1934;
Amoroso, 1960). While the uterine lining
has elaborated prominent folds and lamellae, relatively few secretory cells are present (Ranzi, 1934). The uterine milk conThe final category of aplacental vivip- tains little (1.2%) organic material and less
arity includes species which have placental fat (0.1%). Weight loss occurs since the
analogues. It corresponds to Group III of quality and quantity of secreted material is
Ranzi (1934). Placental analogues are mod- inadequate for the energy requirements of
ified regions of the uterine epithelium the embryo. The comparative study of
which secrete an embryotrophe or Ranzi (1934) reveals a progressive shift in
"uterine milk" which is absorbed or in- the energy budget of development from a
gested by the embryo (Amoroso, 1960). negative to positive balance. This change
Leucocytes are sometimes found in the apparently is accomplished by an increase
secretion. Their origin is unknown. In the in efficiency of the placental analogues.
ray, Dasayatis violacea, the "milk" has an There is an increase in the total number of
organic content of 13% and a total fat secretory cells in the uterine epithelium as
content of 8% (Ranzi, 1934). The secretion well as an increase in the organic content
process in the epithelial cells of Dasayatis (5-9%) of their secretory product, e.g.,
and Myliobatis commences with the en- Mustelis vulgaris, M. antarcticus (Ranzi,
trance of a leucocyte into the cell. The 1934). Parallel evolution of efficient plaleucocyte disintegrates. Shortly thereafter cental analogues in sharks and rays proba-
402
JOHN P. WOURMS
bly reflects a basic selection for increased C. falciformis is greatly reduced while the
efficiency in maternal-fetal maintenance. maternal epithelium remains relatively
In some instances, evolution of efficient unchanged. Both maternal and fetal
placental analogues and placentae have epithelia are greatly reduced in the placenresulted in reduction of egg size, e.g., the tae of M. canis and S. tiburo. For details of
ray, Gymnura, and the shark, Scoliodon.
the histological organization of placentae,
The placental form of viviparity is reference should be made to the studies
confined to two families of sharks, the listed above.
Carcharhinidae (requiem sharks) and the
Several peculiarities are associated with
Sphyrnidae (hammerhead sharks). Within placentae in the sharp-nosed shark,
these groups, placentae are of frequent Scoliodon. In S. palasorrah, the yolk sac
occurrence and appear to have evolved established a specialized connection with a
independently. In the Carcharhinidae, trophonematous cup (Mahadevan, 1940).
species within the genera Carcharhinus, In S. sorrakowah, due perhaps to small egg
Prionace, Scoliodon, Carcharias, Hemigaleus size and the consequent need for establishParagaleus and Mustelus have placentae. ing a placental connection, the yolk sac is
Within a genus some species, e.g., Mustelus not filled with granules but with a network
canis may have a placenta while others, e.g., of cellular strands and blood vessels. In
M. antarcticus do not. In the Sphyrnidae, addition, a yolk stalk does not form. Instead
Sphyrna is the principal placental genus of an umbilical stalk, a placental cord car(Schlernitzauer and Gilbert, 1966).
rying two blood vessels connects the emPlacental structure has been described in bryo to the placenta. In Scoliodon as well as
detail for Mustelus canis (Miiller, 1840; Paragaleus and Sphyrna, the umbilical stalk
Ranzi, 1934) Prionace glauca (Miiller, 1840; or placental cord is festooned with fingerCalzoni, 1936), Carcharhinus falciformis like processes called appendiculae. An ab(Gilbert and Schlernitzauer, 1966), sorptive function is attributed to them
Scoliodon surrakowah and S. palasorrah (Budker, 1958).
(Mahadevan, 1940), and Sphyrna tiburo
The details of placenta formation are
(Schlernitzauer and Gilbert, 1966). The best known in M. canis (Te Winkel, 1950,
placenta in all instances is a yolk sac 1963; Graham, 1967). Information on
placenta. Variation exists with respect to Sphyrna and Scoliodon can be found in
the intimacy of fetal-maternal contact and Schlernitzauer and Gilbert (1966) and
the thickness and number of intervening Mahadevan (1940). In Mustelus canis, the
tissue layers. In most species, e.g., M. canis, gestation period is 10-11 months. During
P. glauca, Sphyrna tiburo, there is an inti- the first three months, the developing emmate interdigitation of the maternal and bryo is yolk dependent. It undergoes an
fetal tissues. In contrast, the placentae of ontogenetic transition during the third
Carcharhinus dussumerieri (Mahadevan, and fourth months and establishes a pla1940) and C. falciformis (Gilbert and cental connection which is retained until
Schlernitzauer, 1966) rest on a thickened, birth. This pattern is common to all plavascularizied region of the uterine wall.
cental sharks. The process begins with the
Schlernitzauer and Gilbert (1966) state fertilization of three to ten eggs. Each egg
that all exchange between the fetal and is enclosed in a thin membranous capsule
maternal blood systems involves up to five and released into the uterus at 16-24 hour
tissue layers. These are: 1) maternal en- intervals. Development proceeds for the
dothelium; 2) maternal epithelium; 3) egg next three months. During this period,
case; 4) fetal epithelium; and 5) fetal en- transverse folds grow from the endodothelium. Reduction or loss of one or metrium and form compartments around
more of these layers may occur. Only a few each embryo (Graham, 1967). Comsharks retain the egg envelope and incor- partmentalization occurs in most placentai
porate it into the placenta, e.g., M. canis species. The endometrium undergoes
and S. tiburo. Schlernitzauer and Gilbert other changes. At first, it is slippery due to
(1966) report that the fetal epithelium in secreted fluids. As placentation begins, the
CHONDRICHTHYAN REPRODUCTION
endometrium becomes "sticky." Changes
occur in the yolk sac and egg capsule.
During the second month of development,
the yolk sac begins to expand. Expansion
continues until the embryo is completely
surrounded by the sac. The yolk sac then
contracts and becomes localized in a small
area where the placenta is forming.
Changes in adhesivity are associated with
placentation. Prior to placentation, yolk
sac, egg capsule, and endometrium are
easily separated. As placentation commences, they adhere but can be separated.
They can no longer be separated after the
placenta forms. The egg capsule is incorporated into the placenta, and on the basis
of histological evidence seems to undergo
chemical changes. Placentation also involves folding of the yolk sac and uterine
epithelia and the subsequent interdigitation of the two tissues.
Structural differences between the distal
and proximal portions of the yolk sac often
occur (Gilbert and Schlernitzauer, 1966).
In most carcharhinids, connection between the yolk sac, placenta and the embryo is by a modified yolk stalk or umbilical
stalk. This contains the yolk duct (vitellointestinal duct) and the umbilical vein and
artery (Budker, 1958).
In the 40 years that have elapsed since
Ranzi's classic work, a surfeit of research
problems have been available yet have
gone untouched. Regretably, there is still
little to report on the physiology of viviparous species, especially placental ones.
An exception to this is Graham's (1967)
study of placentation in Mustelus canis.
Using 3H-glucose, he demonstrated that
low molecular weight organic substances
"filter" across the placental tissues into the
yolk sac cavities and from there are passed
up the yolk duct into the intestine. He
concluded that nutrient transfer through
the placenta of late term fetuses is nonhemotrophic. Obvious questions of embryonic nutrition and placental function
are raised. The 800-1000% increase in
organic material in the embryos of placental species indicates an efficient mode of
nutrient transfer (Ranzi, 1934). What is
involved? The uterine milk of M. canis has
a high (9%) organic content. What role
403
does it play? Alternate pathways of absorption do exist. After the establishment of
the placenta in M. canis, there is a dramatic increase in the uptake of labelled tracers from the uterine cavity (Graham,
1967). The state of knowledge is even
more unsatisfactory in other species. The
formation of a trophonematal cup at the
site of placental attachment in Scoliodon as
well as the elaboration of "absorptive" appendiculae on the placental cords of
Scoliodon, Sphyrna, and Paragaleus (Budker,
1958) suggest that intra-uterine secretions
are being absorbed. One would like to
know the balance between absorption and
placental transfer. In addition the functional difference between the occluded,
vascular placental cord of Scoliodon and the
patent yolk stalk of the carcharhinid
placenta should be pursued.
Viviparity
The reproductive strategies of chondrichthyan fishes are diverse and successful. Oviparity and placental vivparity are
the two extremes in a continuum of reproductive adaptations. Current interest centers about the retention of oviparity and
the evolution of viviparity. Both processes
are subject to the forces of selection. Since
selection operates primarily at the level of
the individual and population, the advantages or disadvantates of each pattern
must be considered in terms of the individual and the species (cf., Wourms and
Evans, 1974a,b; Wourms and Cohen,
1975, for examples in teleosts). A study
involving the 600 or more chondrichthyan
species is premature. What follows is a
prolegomena to a more detailed study of
reproductive strategies. Basic trends in
chondrichthyan reproduction and some
factors which may effect the evolution of
viviparity will be explored.
Eight factors seem to be important in the
evolution of viviparity and the retention of
oviparity (Table 3). The first of these is the
phylogenetic position of a species. Oviparity is the least specialized and primitive
pattern of chondrichthyan reproduction.
From it, viviparity has independently
evolved in several different groups.
404
J O H N P. WOURMS
TABLE 3. Factors in the evolution of viviparity.
1.
2.
3.
4.
5.
6.
7.
8.
Phylogenetic position
Geographical distribution
Habitat: Benthic vs. pelagic
Feeding ecology
Adult size
Egg/embryo size
Osmoregulation
General reproductive strategy of viviparity
Oviparity as it occurs in these fishes is a
specialized strategy since it is based on the
advantages of producing small numbers of
large eggs. As a result the fecundity of
oviparous species is low. That of viviparous species does not differ appreciably.
Holden et al. (1971) reported the
maximum egg laying rate of the skate, R.
clavata, to be one egg per day. At best, this
could account for 360 eggs per year, probably far less. Harris (1950) estimated that
the maximum production of eggs in
Scyliorhinus is 120 eggs per year. Breder
and Rosen (1966) give a figure of 108
embryos per brood for the viviparous
shark Hexanchus. These are maximum values. Production of 2 to 50 young per year
seems more likely. The initial low fecundity of oviparous species may aid in explaining the widespread occurrence of viviparity in this group. The advantages of
viviparity could be acquired without substantial loss of fecundity. A necessary feature of viviparity is internal fertilization.
This appears to have evolved early and is
found in all extant oviparous and viviparous species (Matthews, 1955; Tortonese,
1950; Breder and Rosen, 1966). Subsequent steps in the evolution of viviparity
involved retention of fertilized eggs, thinning and loss of the egg case, elaboration
of mechanisms for fetal maintenance, and
reduction in egg size. Simple egg retention
occurs in several diverse taxa, e.g.,
Ginglymostoma and Chlamydoeslachus. The
diversity of mechanisms for fetal maintenance in present day chondrichthyans
suggests that viviparity is still evolving. In
this respect, it would appear that once
viviparity has evolved, it is retained. In
terms of phylogenetic position (Table 2)
several points are of interest. All living
chimaeras and probably all fossil chimaeras
are oviparous (Dean, 1906; Bigelow and
Schroeder, 1953). Twelve of the sixteen
families of elasmobranchs are viviparous.
Placental viviparity is confined to two of
these families. Oviparity occurs only in
four families. Two of these, the Orectolobidae (carpet sharks) and the
Scyliorhinidae (cat sharks) have viviparous
species. The former includes Ginglymostoma which is considered to have recently
made the transition from an oviparous to a
viviparous condition (Gudger, 1940).
Within the Scyliorhinidae, one member of
genus Galeus, G. polli Cadenat is marginally
viviparous while other species within the
genus and family are oviparous (Breder
and Rosen, 1966). Within the order
Rajiformes, derived from sharks or sharklike ancestors, only the skates have retained oviparity whereas members of the
other four suborders are all viviparous.
The geographical distribution of the
major groups of the Rajiformes tends to be
correlated with their reproductive
strategies. Skates (suborder Rajoidei)
which are oviparous occur chiefly in temperate and polar regions. The other four
suborders, sawfishes, guitarfishes, and
rays, which are viviparous, are found in
tropical and sub-tropical regions (Bigelow
and Schroeder, 1953). A similar correlation is not found in sharks.
Tortonese (1950) was the first to call
attention to a possible relationship between habitat and reproductive strategies
in sharks. He noted that oviparous species
were benthic, littoral, and not of large size.
Viviparous species were more diverse in
habitat. Association of oviparity with a
benthic habitat is still valid in sharks and
can be extended to skates and chimeras.
Skates and chimeras also tend to be of
moderate size. Many skates and some
chimeras tend to be littoral. Many large
species of pelagic sharks, e.g., the blue
shark, are viviparous. The advantages of
viviparity to a pelagic species are readily
apparent. Oviparity in benthic species may
be opportunistic or may offer advantages.
In the case of viviparous rays many of
which are benthic, other factors may be
operable.
Feeding ecology is a function in part of
d
CHONDRICHTHYAN REPRODUCTION
size and also habitat. Large sharks and
sawfishes, active predators of fishes, tend
to be viviparous. Smaller sharks e.g.,
Heterodontidae and Scyliorhinidae, and
the skates, both of which feed on benthic
invertebrates and small fishes, are oviparous. Torpedos, sting rays, and eagle rays
which have a similar feeding ecology are
viviparous. Why? One family and two
species of chondrichthyan fishes are considered macro-plankton feeders: the whale
shark, Rhincodon; the basking shark,
Cetorhinns; and the devil rays, Mobulidae
(Bigelow and Schroeder, 1948, 1953).
They are large, pelagic fishes. The first is
oviparous (Baughman, 1955). Cetorhinus is
presumed viviparous (Matthews, 1950)
and the Mobulidae are viviparous. If any
significance can be attached to the difference, one is tempted to suggest that oviparity is less advantageous in view of the apparent rarity of the whale shark. Since
gigantism in the marine environment is
often associated with plankton feeding, size
rather than feeding ecology may be more
relevant to reproductive strategies.
Tortonese (1950) stated that viviparity
was a function of large adult size in sharks.
This generalization can be extended to the
skates, rays, and chimaeras. Viviparous
species tend to produce larger offspring.
The largest oviparous embryo is that of the
whale shark, circa 35 cm (Baughman,
1955). Most oviparous embryos tend to be
considerably smaller, under 15 cm. In contrast, viviparous embryos of 45-60 cm are
not uncommon (P. glauca, Wourms, unpublished). Embryos of about 100 cm have
been reported in Odontaspis (Springer,
1948). Absolute size is an advantage to the
large offspring of viviparous species. Embryos of 45-60 cm length are considerably
above the median size of 15-30 cm for
adult fishes (Marshall, 1971). In terms of
Hutchison and MacArthur's (1959) model
of size distribution, several advantages accrue from increased size: 1) reduction in
number of potential predators; 2) reduction in number of competitors; and 3) a
greater number of potential food organisms. Increased embryo size also results
in greater efficiency, since swimming
speed is a function of absolute size (Mar-
405
shall, 1971). Growth phenomena may be
another reason why large species tend to
be viviparous. As a generalization, early
phases of postembryonic growth tend to
almost be exponential. Embryos whose initial size is large tend to grow to a large
adult size (Marshall, 1953).
The factor of egg/embryo size is related
in part to adult size. As a rule, large adults
develop from large embryos. Post-partum
embryos of viviparous species are larger
than newly hatched oviparous embryos.
For this reason large species tend to be
viviparous. Size differences can be accounted for in terms of embryonic and
maternal energetics and upper limits to
egg size. Oviparous embryos consume 25%
or more of their organic content during
development (Ranzi, 1934). Viviparous
species suffer the same loss but in many
instances have evolved efficient means of
continuous fetal nutrition. Where
mechanisms for continuous fetal nutrition
have evolved, the fetus attains a large size.
The maternal energy budget is more
efficient since nutrients are delivered on
demand rather than sequestered in the
egg prior to demand (Wourms and Cohen,
1975). In oviparous species, the size of the
embryo is limited by the size of the egg.
The eggs of some sharks are gigantic cells.
The egg of the whale shark may represent
an upper limit in absolute size. In spite of
this, the embryo is only half the size of the
average viviparous shark embryo.
Price and Daiber (1967) suggested that
the inability of elasmobranch embryos to
regulate urea content and osmotic pressure during early development constituted
a selective disadvantage which led to the
evolution of viviparity. Read's (1968) demonstration of ornithine-urea cycle enzymes
in all stages of development appears to
contradict this. Pang, et al. (1967) reviewed
the subject but did not resolve the issue. It
would seem that even if early stage oviparous embryos can control their urea content, it can be done more efficiently and
with less expenditure of embryonic energy
in the uterine environment.
Finally, the evolution of viviparity in the
chondrichthyans cannot be divorced from
the general strategy of viviparity. A bal-
406
JOHN P. WOURMS
ance sheet of evolutionary advantages and
disadvantages shows the following. The
maternal environment offers the advantages of protection from predators and
other hazards. It also provides physiological regulation of the environment. In some
instances, supplemental mechanisms of
fetal nutrition have evolved. Viviparity
leads to increased size of full term embryos. Size increase is advantageous. An
apparent reduction in fecundity, considered a negative aspect of viviparity, does not
seem important in the Chondrichthyes.
In an overview of chondrichthyan reproductive strategies, several themes
emerge. The primitive reproductive pattern is oviparity. In the Chondrichthyes, it
is a specialized strategy since the production of a small number of large eggs has
been selected for. Reproductive success
(Richards et al, 1963) and diversity of
species in the skates attest to the advantages of this strategy. Viviparity seems to
have evolved independently, almost on a
group-specific or species-specific basis.
The repeated evolution of viviparity in
different taxa, its prevalence in the elasmobranchs, and the reproductive success
of viviparous species attest to its advantages. Eight factors are considered to affect
the retention of oviparity or the evolution
of viviparity. They probably act in concert.
The relative influence of each factor probably varies according to species.
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