J. Mar. Biol. Ass. U.K. (2005), 85, 1185^1192
Printed in the United Kingdom
Reproductive biology of Centrophorus cf. uyato from the
Cayman Trench, Jamaica
Donna M. McLaughlin* and John F. Morrissey
Department of Biology, 114 Hofstra University, Hempstead, NY 11549, USA.
*Corresponding author, e-mail: [email protected]
The taxonomy of the genus Centrophorus (Squaliformes: Squalidae) is currently in a great deal of
uncertainty. The characteristics of the species subject to the present study most closely resemble those
of Centrophorus uyato, hence the use of Centrophorus cf. uyato, though the species in question may be a species
of Centrophorus that has not been described previously. Specimens were obtained via vertical and horizontal
longline at depths of 250^913 m. The reproductive biology of 51 female and 8 male Centrophorus cf. uyato were
examined. This species is sexually dimorphic, with females attaining a larger size than males. The smallest
mature male was 81.2 cm total length whereas the smallest mature female was 91.5 cm total length. Females
are aplacentally viviparous, with the pups acquiring nutrition via large external yolk sacs, and there was a
maximum of two pups per litter. Oocytes continued to develop throughout gestation. Most females
carrying developing embryos had two large (43.3 cm), equally developed ovarian oocytes, which leads us
to believe that they ovulate soon after parturition. This species seems to exhibit complete sexual segregation during the non-breeding season, with mature males absent from the study site during summer months.
Centrophorus cf. uyato may have one of the lowest fecundities among sharks, giving birth to a maximum of
two pups every three years. All species in genus Centrophorus have small litters (56) making them vulnerable to over-exploitation.
INTRODUCTION
The reproductive biology of a few species of deep-sea
sharks has been studied, such as Centrophorus granulosus
(Guallart & Vicent, 2001), Centroscymnus coelolepis
and Centrophorus squamosus (Girard & Du Buit, 1999),
Centroscyllium fabricii (Yano, 1995), Chlamydoselachus anguineus
(Tanaka et al., 1990), and Centroscymnus owstoni and
Centroscymnus coelolepis (Yano & Tanaka, 1988). Considering
the decline of many commercial ¢sheries on the continental shelf, ¢sheries in deep-waters have expanded in
recent years, and so an improved knowledge about the
sharks inhabiting the deep sea is particularly important.
Nevertheless, there are many species of deep-water shark
for which there is little published information.
Because Jamaica is a comparatively underdeveloped
country with limited resources, it is not surprising that
there is little information regarding the deep-sea ¢sh that
live there. Therefore, it also is not surprising that the
organism examined in this study may be a species of
Centrophorus that has not been described previously (Buch,
2003). Centrophorus is a genus in the Family Squalidae
(Order Squaliformes) and the taxonomy for the genus
Centrophorus is currently in a great deal of uncertainty
(Compagno, 1984). The characteristics of this species
most closely resemble those of Centrophorus uyato
(Ra¢nesque, 1810), as such, it will be referred to as
Centrophorus cf. uyato throughout our study.
Our objectives in this study were to provide a detailed
description of the reproductive organs of both male and
female Centrophorus cf. uyato, determine the mode of
reproduction utilized, estimate the gestation period, and
Journal of the Marine Biological Association of the United Kingdom (2005)
ascertain whether or not there is a distinct breeding
season. Though there is little immediate threat of overexploitation to the deep-sea shark population of Jamaica,
because most ¢sheries operate inshore, deep-sea sharks are
being increasingly targeted in commercial ¢sheries in
other areas (e.g. Davenport & Deprez, 1989). Thus, given
that Centrophorus occurs globally, it is likely that our
research will provide reproductive data useful for the
management of other Centrophorus species currently being
harvested.
MATERIALS AND METHODS
The Cayman Trench has a maximum depth of 7686 m,
is 1700 km long and greater than 100 km wide, and extends
from the Gulf of Honduras to the Gulf of Gonave in
Hispaniola. The eastern end of the Cayman Trench’s £oor
is dominated by three deeps. One of these, the Barlett
Deep, separates Cuba from the Nicaragua Rise (Uchupi,
1975). The present crest of the Nicaragua Rise is marked
by the island of Jamaica (Arden, 1975), situated between
178300 N and 198000 N latitude and 768000 W and 788300 W
longitude. The study site (Figure 1) was located on the
north coast of Jamaica between 18827.540 N and 18879.710N
latitude, 77810.110W and 77816.370 W longitude. Sharks were
caught with vertical and horizontal longline gear using a
variety of circle hooks. Each set was soaked for 3^12 h at
depths of 250^913 m. Chum buckets and cyalumes were
used to aid attraction of animals.
Total length (TL) was measured from the tip of the nose
to the tip of the tail to the nearest 0.1cm using a standard
1186
D.M. McLaughlin and J.F. Morrissey
Reproduction in Centrophorus cf. uyato
Table 1. Categories used to describe the reproductive stage of
mature female Centrophorus cf. uyato. Stages modi¢ed from
Yano (1995).
Figure 1. Bathymetric map of Jamaica, West Indies. The
study site is located o¡ the north coast of Jamaica between
18827.540 N and 18879.710 N latitude and 77810.110 W and
77816.370 W longitude (directly o¡shore from the Hofstra
University Marine Laboratory, which is indicated by a solid
star).
tape measure. Gonad weight and embryo weight were
measured to the nearest 0.1g using an electronic balance.
All embryo weights included the external and internal yolk
sacs. All weight measurements taken were wet weight.
Clasper length was measured to the nearest 0.1cm using a
standard ruler. Clasper length was measured from the
anterior margin of the cloaca to the tip of the clasper.
The mean and standard deviation were calculated only if
the sample size was greater than two.
The specimens used for histological examination were
necropsied upon return to the laboratory. The tissues were
¢xed in 10% neutral-bu¡ered formalin for at least 48 h.
After ¢xation, the tissues were washed in running tap
water to remove the ¢xative and then serially dehydrated
in ethanol. The tissues then were perfused with Histo-X
histological clearing agent and, ¢nally, para⁄n wax. The
perfused tissues were embedded in para⁄n wax and stored
in the refrigerator to be sectioned at a later date. After at
least 24 h in the refrigerator, the tissues were sectioned at
8^10 mm using an American Optical 820 Spencer Microtome and mounted on superfrost microscope slides. The
slides were stained with Harris haematoxylin and
counter-stained with acidi¢ed eosin y. Cover slips were
a⁄xed to the slides with permount mounting medium
and allowed to dry for a minimum of 30 min. The slides
were examined under an ausJENA compound light microscope. Photographs of the slides were taken through the
microscope with an Olympus DPII digital camera.
Morphological features were used for assessing maturity
status of males. Males were considered mature if the claspers were highly calci¢ed, the distal end of the clasper
could be spread open, the base of the clasper rotated
easily, the epididymes and ductus deferens were coiled,
and there was sperm present in the reproductive tract
(Pratt, 1979). Sperm smears were taken from the ampullae
of the ductus deferens to con¢rm the presence or absence
of sperm. A clean scalpel blade was used to cut the
ampullae of the ductus deferens. The £uid inside was
removed with the tip of the scalpel blade and a thin ¢lm
was smeared across the slide. The slides were allowed to
Journal of the Marine Biological Association of the United Kingdom (2005)
Category
Abbreviation
Developing ova
DO
Ripe ova
RO
Fertilized ova
FO
Developing
embryos
DE
Near-term
embryos
NE
Post-partum
PP
Not available
NA
Description
Non-gravid females with
developing ovarian
oocytes and expanded
uteri
Non-gravid females with
ripe ovarian oocytes and
expanded uteri
Post-ovulatory females with
only fertilized ova in the
uteri
Gravid females carrying
embryos with external
yolk sacs
Gravid females carrying
embryos with no external
yolk sacs
Non-gravid females with
£accid uteri
The reproductive stage
could not be determined
Figure 2. (A) Testes of an immature male Centrophorus cf.
uyato. The testes are slender and have a smooth appearance;
(B) testes of a mature male C. cf. uyato. The testes are large and
very lobular.
Reproduction in Centrophorus cf. uyato
dry and were ¢xed and stained using the Hema 3 quickstaining system. The slides were examined under an
ausJENA compound light microscope. Photographs of the
slides were taken through the microscope with an
Olympus DPII digital camera.
Female reproductive status was evaluated based on the
stages of reproduction suggested by Yano (1995). Females
were considered immature (IM) if they had small
ovarian oocytes containing no yolk and their reproductive
tract was undi¡erentiated. Mature females were divided
into seven categories, which are described in Table 1. We
included a category for females for which the reproductive
stage could not be determined, with the most common
cause for indeterminate reproductive stage being premature abortion of embryos before the necropsy could be
performed. Because multiple specimens were stored in the
same cooler, it was impossible to determine to which
females the aborted embryos belonged.
Sperm smears were used to determine if sperm was
present in the oviducal glands. We followed the procedure
used by Pratt (1979). The oviducal gland was removed,
leaving a few centimetres of oviduct attached. The
posterior 1/3 of the gland then was removed with a clean
scalpel. The £uid from the anterior 2/3 of the gland was
squeezed out onto a microscope slide and allowed to dry.
The slides were ¢xed and stained using the Hema 3 quickstaining system.
RESULTS
Male reproductive system
The two IM males examined were 65.2 cm and 86.6 cm
TL, respectively. The mature males ranged from 81.2 to
84.7 cm TL (mean¼82.7 cm, SD¼1.57, N¼5).
Immature (N¼2) and mature (N¼5) males had two
equally developed testes. The testes of the smaller of the
two IM males were cylindrical with a smooth appearance
(Figure 2A), whereas the testes of the larger IM male and
the mature males were elongate and di¡erentiated into
multiple lobes (Figure 2B). Although the testes of the
small IM specimen were small and had a di¡erent
morphology than that of the other specimens, microscopic
examination revealed spermatocysts in various stages of
spermatogenesis. The testis of the larger IM male and the
mature males appeared very similar microscopically. We
were able to observe the seven distinct zones of spermatocyst development, as described by Maruska et al. (1996),
across the sectioned lobes of the testis.
The epididymes of the small IM specimen were highly
coiled (Figure 2A), whereas those of the large IM
specimen were straight, but neither contained sperm. The
ampullae of the ductus deferens appeared to be fused
together in the posterior region of the peritoneal cavity.
The ampullae of the ductus deferens of the small IM
male were undi¡erentiated and less than 0.5 cm in
diameter. Thick, white £uid £owed from the severed
ampullae of the ductus deferens of all mature specimens.
Thick, clear £uid £owed from the severed ampullae of
the ductus deferens of the large IM specimen. Microscopic
examination of the £uid from the ampullae of the ductus
deferens of the mature specimens con¢rmed the presence
of sperm. A smear taken from the ampullae of the ductus
deferens of the IM specimen had no sperm present.
Journal of the Marine Biological Association of the United Kingdom (2005)
D.M. McLaughlin and J.F. Morrissey 1187
Clasper length for the IM specimens were 3.9 cm and
6.6 cm. Clasper length of mature males ranged from 5.7
to 7.7 cm (mean¼6.56, SD¼1.00, N¼5). There was no
signi¢cant increase in clasper length with TL. The small
IM specimen had small claspers that lacked any calci¢cation. The large IM specimen appeared mature upon
examination of external anatomical features and hence
shared the characteristics described for the claspers of
mature males. All mature specimens had calci¢ed claspers
with spurs and the distal cartilages could be easily spread
open. The claspers were easily rotated 908 from their
relaxed position on the ventral side of the body.
Female reproductive system
All specimens less than 80 cmTL were IM (Table 2). All
specimens greater than 100 cmTL were mature. Immature
females ranged from 63.0 to 99.4 cm TL (mean¼86.2,
SD¼11.93, N¼10), and mature females ranged from 91.2
to 102.3 cm TL (mean¼ 96.2, SD¼2.85, N¼41). Size at
50% maturity was estimated at 80 to 90 cm TL.
Immature (N¼10) and mature (N¼41) females had
two equally developed ovaries. The ovaries of IM females
were elongate with a lumpy appearance (Figure 3A). The
shape of the ovaries of mature females varied with reproductive stage. Figure 3B shows one example of the variation of the shape of the ovaries seen in mature females.
The paired ovary weights for IM females were 0.6^9.1g
(mean¼4.2 g, SD¼3.5, N¼7). The paired ovary weights
for developing oocytes (DO) females were 1.5^181.7 g
(mean¼61.5 g, SD¼55.4, N¼9), 137.7 g for the single ripe
oocytes (RO) female, 19.9^47.2 g (mean¼32.7 g, SD¼8.4,
N¼10) for fertilized ova (FO) females, 16^342.8 g
(mean¼147.2 g, SD¼100.9, N¼15) for developing embryo
(DE) females, 305.8 g for the single post-partum (PP)
female, and 33.6 g, 110.8 g, and 283.10 g for the three not
available (NA) females. Figure 4 shows the relationship
between paired ovary weight and TL among mature
female Centrophorus cf. uyato. Although there was no signi¢cant correlation between paired ovary weight and TL
among all mature females, this shows the e¡ect of reproductive stage on paired ovary weight. Ovarian weights
were smallest for mature females at stages DO and FO,
Table 2. Number of Centrophorus cf. uyato in each
reproductive stage per month.
Males
Month
March
July
August
December
Total
IM
1
1
2
Reproductive stage of female
M IM DO RO FO DE NE PP NA Total
5
5
1
3
5 2
5 4
10 10
1
1
1
7 12
3 2
10 15
3
0
1
1
3
1
4
31
21
57
IM, immature; M, mature; DO, non-gravid females with developing ovarian eggs; RO, non-gravid females with ripe ovarian
eggs; FO, fertilized ova; DE, females with carrying embryos
with external yolk sacs; NE, females carrying embryos with no
external yolk sac; PP, post-partum females with £accid uteri;
NA, reproductive stage indeterminable.
1188
D.M. McLaughlin and J.F. Morrissey
Reproduction in Centrophorus cf. uyato
that constricted the anterior opening to the uterus. Posteriorly, each uterus opened into the urogenital sinus. Uteri of
DO females were not vascularized or folded and some
contained a gelatinous substance. The uteri of the RO
female were not vascularized or folded. Uteri of FO
females showed signs of increased vascularization and
folds were beginning to appear. Uteri of DE females were
highly vascularized and folded. The uteri of the PP female
were £accid and the right uterus contained brown £uid.
Oocytes, ova and embryos
Figure 3. (A) Ovaries of an immature female Centrophorus cf.
uyato; (B) ovaries of a mature female Centrophorus cf. uyato. The
shape of the ovaries of mature females varies with reproductive
stage. This particular female has two large oocytes developing
in the left ovary.
Figure 4. Relationship between paired ovary weight and total
length of mature female Centrophorus cf. uyato. DO, developing
oocytes; RO, ripe oocytes; FO, fertilized ova; DE, developing
embryo; PP, post-partum; NA, not available.
and were broadly similar. Those ¢sh at stage DE had
greater ovarian weights, as did RO and PP stages, though
sample sizes were low for the latter stages.
The remainder of the reproductive tract of IM specimens was undi¡erentiated. All mature specimens had a
single ostium leading to paired oviducts. The oviducts
continued to the right and left oviducal glands that were
heart-shaped and equally developed. Following the
oviducal glands, the isthmus led to a muscular sphincter
Journal of the Marine Biological Association of the United Kingdom (2005)
The ovaries of the IM females contained numerous
small oocytes (51cm). For mature ¢sh, the number of
RO ranged from 0^3, with one specimen having no RO
and most specimens having two RO. Among the 41
mature females, less than half (41%) had one ripe oocyte
in each ovary. The remaining mature females had equally
developed RO arranged as follows: 7.3% had one oocyte
in the left ovary, 7.3% had one oocyte in the right ovary,
7.3% had two oocytes in the left ovary, 19.5% had two
oocytes in the right ovary, 7.3% had two oocytes in the
left ovary and one oocyte in the right ovary, and 7.3%
had one oocyte in the left ovary and two oocytes in the
right ovary.
Immature oocytes were very ¢rm and held their round
shape when removed from the ovary. Ripe oocytes were
soft and the outer layers of the follicle became highly
vascularized prior to ovulation. After ovulation, the
oocytes passed through the oviducal gland to become fertilized and enclosed in a gelatinous capsule (candle). A
small orange disc was visible on the surface of each fertilized egg. At this stage the embryonic membranes were
very delicate and tore very easily. There also was very
little vascularization of the external yolk sac at this stage.
Most females with fertilized ova (90%, N¼10) had one
ovum in each uterus and small ovarian oocytes
(52.4 cm). The number of fertilized ova and embryos
within each uterus never exceeded one.
Most females with developing embryos had one embryo
per uterus (68.8%, N¼16), 6.2% only had an embryo in
the left uterus, and 25% only had an embryo in the right
uterus. Embryos remained inside the candle sac until they
reached approximately 5.5 cm TL. At this point, vascularization of the external yolk sac began to increase and the
yolk sac became more ¢rm. External gill ¢laments were
apparent until the embryos reached approximately
14.5 cm TL. All embryos were oriented with their head
facing posteriorly. At no time during gestation did the
embryos form a connection with the mother. However,
there was a signi¢cant increase in embryo weight with
embryo TL (Spearman’s rho¼0.747, P50.0005, N¼19;
Figure 5).
Centrophorus cf. uyato embryos derive nourishment from
their large external yolk sac. The external yolk sac was
connected to an internal yolk sac. The smallest embryo
with an internal yolk sac was 28.6 cm. All embryos
greater than 28.6 cm had internal yolk sacs. The internal
yolk sac was connected directly to the spiral valve intestine. We did not ¢nd yolk in the stomachs of any of the
embryos.
No near-term embryos were observed during this study.
The embryos closest to near-term had small (50.8 cm)
Reproduction in Centrophorus cf. uyato
D.M. McLaughlin and J.F. Morrissey 1189
mature males during this month. Greater than 83.3% of
males captured in December were mature.
Females were collected during all months sampled
(Table 2). Immature and FO females were collected in
August and December. Females with developing ova were
collected during all months sampled. The single RO
female was collected in August. Females with developing
embryos were collected in July, August and December.
The single PP female was collected in December.
Although females with near-term embryos were not
collected during any of the months sampled, specimens
with the largest embryos were observed in December.
DISCUSSION
Figure 5. Relationship between embryo weight and embryo
total length of developing Centrophorus cf. uyato embryos
(Spearman’s rho¼0.747, P50.0005, N¼19). Embryo weight
includes the external yolk sac.
Figure 6. Relationship between weight and total length (TL)
of developing Centrophorus cf. uyato embryos. The graph has
been divided into six sections depicting our hypothesized
occurrences of embryos in di¡erent size-classes with season.
The left margin of the graph represents time zero which
includes eggs that have been recently fertilized. Time S-1 (¢rst
summer) includes eggs with no visible embryos and small
(56.5 cm TL) embryos, time W-1 (¢rst winter) includes
embryos 6.5^10 cm TL, S-2 (second summer) includes embryos
10^18 cm TL, W-2 (second winter) includes embryos 18^28 cm
TL, S-3 (third summer) includes embryos 28^34 cm TL, and
W-3 (third winter) includes close to near-term embryos
approximately 34 cm TL.
external yolk sacs remaining. The TL of these embryos was
33.5^34.7 cm (mean¼34.1, SD¼0.57, N¼4).
Seasonal reproductive activity
With the exception of one IM male captured in August,
males were only collected in December (Table 2). Sperm
was found in the ampullae of the ductus deferens of all
Journal of the Marine Biological Association of the United Kingdom (2005)
Centrophorus cf. uyato are sexually dimorphic, with
females maturing at a larger size than males. The smallest
mature female was 91.2 cmTL, whereas the largest mature
male measured 84.7 cm TL. The largest mature female we
examined measured 102.3 cm TL, only slightly larger than
the largest IM female observed (99.4 cm TL). These data
suggest that females may mature close to their maximum
size. However, because we did not observe any females
that measured 80^90 cm TL, it is possible that the onset
of sexual maturity may occur in smaller females.
The large IM male that we examined measured
86.6 cm TL, which was larger than all of the mature
specimens. The smallest mature male was 81.2 cm TL, but
because our sample size for males was so low (N¼7), we
are unable to support any predictions about size at
maturity.
The microscopic anatomy of the testis of mature male
Centrophorus cf. uyato is similar to that of other elasmobranchs. The seven stages of spermatocyst development,
as described by Maruska et al. (1996), were obvious in all
of the testes examined. Because mature male specimens
were only collected in December, we were unable to make
any temporal comparisons of spermatocyst development
throughout the year. Spermatocyst development can be a
useful tool for predicting the seasonal production of sperm
in elasmobranchs, as the proportion of spermatocysts in
each stage of spermatogenesis provides information about
peak sperm production as well as testicular inactivity
(Maruska et al., 1996). Other studies have indicated that
a degenerate zone forms as a result of the cessation of spermatogenesis during the season. When spermatogenesis
begins again, the generation of new spermatocysts pushes
the degenerate zone across the lobe of the testis. Therefore,
documentation of the movement of the degenerate zone
across the testis can provide further information about
the incidence of spermatogenesis throughout the year
(Simpson & Wardle, 1967).
Examination of the testis of the small IM specimen
yielded some unusual results. The small specimen, which
measured 65.2 cm TL, had small cylindrical testes (Figure
2A), the reproductive tract was not completely di¡erentiated, and the claspers were underdeveloped. However,
the microscopic appearance of the IM testis was identical
to that of the mature testis. All of the stages of spermatocyst development were present in the IM testis, including
the presence of spermatocysts containing fully mature
sperm. This may indicate that sexual maturity of males
begins with development of the testis. Given that high
1190
D.M. McLaughlin and J.F. Morrissey
Reproduction in Centrophorus cf. uyato
concentrations of 3b-hydroxysteroid dehydrogenase, an
indicator for the site of steroid synthesis, occur in the cytoplasm of Sertoli cells (Simpson & Wardle, 1967), it is
possible that development of the testis, and therefore
steroid hormones, triggers development of secondary
sexual characteristics.
The larger IM male that we observed had lobular
testes, a fully developed reproductive tract, and claspers
that were morphologically mature, but there was no
sperm in the reproductive tract. The microscopic appearance of the testis of this specimen also was identical to that
of the mature males. Because sperm was being produced in
the testes of both IM males but was not present in the
remainder of the reproductive tract, it is presumably
resorbed.
In addition to our unusual ¢ndings associated with the
microscopic anatomy of the testis of the small IM male,
the epididymis was already tightly coiled. This was not
the case in the larger of the IM males. The coiling of the
epididymis is often used as an indication of maturity in
male elasmobranchs. A series of stages of maturity for
males of the species Centroscymnus coelolepis and Centrophorus
squamosus developed by Girard & Du Buit (1999) suggests
that the sperm ducts do not become tightly coiled until the
animals reach the adult stage. Our ¢ndings suggest that
the order of development of sexual characteristics in
males may not proceed in a well-de¢ned pattern. Alternatively, the larger IM male may have had a congenital
defect that prevented the sperm ducts from coiling.
Smears of the £uid taken from the ampullae of the
ductus deferens proved to be the most accurate method
for diagnosing complete sexual maturity in males. The
mature male smears contained sperm, whereas the smear
taken from the ampullae of the ductus deferens of the large
IM specimen revealed no sperm. The inconsistencies
among the sexual characteristics of the males in this study
lead us to suggest that the presence of sperm within the
distal portion of the reproductive tract is the only indisputable evidence of sexual maturity. Unfortunately, as sperm
production ceases at the end of the breeding season in
many male elasmobranchs (Maruska et al., 1996), it may
be very di⁄cult to determine stage of maturity during
the non-breeding season for male Centrophorus cf. uyato
if they too stop producing sperm during periods of
inactivity.
Female Centrophorus cf. uyato are aplacentally viviparous
with a maximum of two pups per litter. There was never
more than one embryo per uterus and some females were
only carrying one egg or embryo. All females had two
equally developed ovaries. The size of the female did not
appear to have an e¡ect on the size of oocytes developing
in the ovaries (Figure 4). Females with developing embryos
and the post-partum female had the greatest ovary
weights among mature females. The female listed as RO
had one ripe oocyte in the left ovary, but one oocyte had
already ovulated and therefore was not included in the
paired ovary weight for that specimen. It is likely that the
RO female would have been at the high end of the range of
paired ovary weights among mature females, had the
other oocyte still been in the ovary. The NA specimen
with the greatest paired ovary weight was located in the
range of females with developing embryos. It is probable
that her embryos were aborted during capture. The other
Journal of the Marine Biological Association of the United Kingdom (2005)
two NA females had fairly low paired ovary weights and
may be either DO or DE.
The fact that most females with developing embryos
also had oocytes developing in the ovaries suggests that
mating occurs soon after parturition. Furthermore,
because all pregnant females had either recently fertilized
ova in their uteri (FO) or had developing embryos and
developing ovarian oocytes (DE), we suspect that the DO
females may be sub-adults. We considered them mature
because their reproductive tracts were fully developed
and they had developing oocytes that were greater than
1cm, but we think it is unlikely that they had ever been
pregnant.
Oocytes continued to develop throughout gestation, and
most females with developing oocytes in their ovaries had
a pair of oocytes that were similar in size. Many female
elasmobranchs have only one functional ovary that
produces oocytes (Hamlett & Koob, 1999). Although
nearly half of the mature females (41%) had a similarly
sized oocyte developing in each ovary, there was a slightly
greater incidence of females with two equally developed
oocytes in the right ovary (19.5%), than females with two
equally developed oocytes in the left ovary (7.3%). It also
is surprising that the number of embryos per uterus never
exceeded one because 14.6% of the females had three
equally developed ovarian oocytes. Some female elasmobranchs continue to produce and ovulate unfertilized
oocytes as a source of nutrition for the embryos developing
within their uteri (Hamlett & Koob, 1999), but that does
not seem to be the case here, as we never observed unfertilized oocytes in the uteri containing developing embryos.
It is probable that the super£uous oocytes become atretic
and are resorbed. Nevertheless, it seems ine⁄cient to
expend energy to produce such enormous oocytes that
cannot be used. One possible explanation may be that
they produce additional oocytes to ensure maximum
reproductive output, in the event that one of the oocytes
does not fully develop.
We did not observe sperm in the oviducal glands of
any of the females. Sperm storage is a well-documented
phenomenon in many elasmobranch species. The
ability to store sperm varies widely among elasmobranchs,
but does appear to be related to phylogeny (Pratt, 1993).
Because Centrophorus probably has a long gestation, one
might predict that the length of time would cause sperm
storage to be unfeasible. However, Castro et al. (1988)
determined that the chain dog¢sh (Scyliorhinus retifer
[Garman, 1881]) was able to store sperm for as long as
three years. Therefore, a long gestation period may not
necessarily exclude a species from storing sperm. Because
there have not been any documented cases of sperm
storage in squaliform sharks, it is more likely that
sperm storage is linked to phylogeny as suggested by Pratt
(1993).
Embryos of Centrophorus cf. uyato derived nourishment
from their large external yolk sac. We saw no indication
that additional nourishment was provided through modi¢cations of the uterine lining or continuous ovulation of
unfertilized eggs. Nevertheless, there was a signi¢cant
increase in embryo weight with TL (Figure 5). Increases
in total weight of elasmobranch embryos are not
uncommon (Guallart & Vincent, 2001). The increase is
usually due to water absorption during development.
Reproduction in Centrophorus cf. uyato
Sexual segregation in sharks is a well-known phenomenon. Therefore, it is not surprising that mature male
Centrophorus cf. uyato were completely absent from the
study site during the summer months. In addition, the
only post-partum female in the study was collected in
December. This leads us to believe that this species
congregates during the winter months for parturition and
subsequent mating. There also was no evidence that
Centrophorus cf. uyato females store sperm, further
supporting a de¢ned breeding season.
The majority of females collected in August had either
recently fertilized ova in their uteri or developing embryos
of distinct size-ranges. Recent studies of deep-sea shark
populations have shown such sharks may segregate by
reproductive stage (Tanaka et al., 1990; Yano & Tanaka,
1988), and females of the coastal squaliform shark Squalus
acanthias Linnaeus, 1758 also have been documented to
segregate by reproductive stage, occurring in shallower
waters during the 1st to 6th and 19th to 24th months of
pregnancy, and in deeper waters in the 7th to 18th
months of gestation (Holden, 1974). The lack of
Centrophorus cf. uyato females carrying embryos of certain
sizes may indicate that they also segregate by reproductive
stage.
Given that the single post-partum female, the embryos
closest to near-term, and the only mature males were
collected in December, it is probable that Centrophorus cf.
uyato utilizes a well-de¢ned breeding season. In addition,
the absence of embryos of various size-ranges further
supports a de¢ned breeding season. One would expect to
¢nd embryos of all sizes at any given point during the year
if the species breeds continuously. Figure 6 shows the relationship between embryo TL and embryo weight. The six
sections of the graph show our predicted stages of development for a three-year gestation. Time zero begins during
the winter months, when males have been found at the
study site. It is at this time that fertilization takes place.
During the ¢rst summer (S-1) following time zero the
embryos range from macroscopically invisible to 6.5 cm
TL. The ¢rst winter (W-1), for which we have no data,
would include embryos ranging from 6.5 cm TL to 10 cm
TL. The hypothetical second summer (S-2) consists of
embryos ranging from 10 cm TL to 18 cm TL. The
hypothetical second winter (W-2), again containing no
data, would include embryos ranging from 18 cm TL to
28 cm TL. The hypothetical third summer (S-3) consists
of embryos ranging from 28 cm TL to 34 cm TL. The
third winter (W-3) includes embryos 434 cm TL. It is
not surprising that the embryos that are close to nearterm in W-3 have lower body weights than those from the
previous summer because the yolk reserves are being
depleted. Considering that there appears to be six distinct
size-ranges for the embryos, we suggest that gestation lasts
for three years.
Unfortunately, there have been few studies on the reproductive biology of squaliform and deep-water sharks,
though those that have been studied are known to have
long gestation periods, with Squalus acanthias and
Centrophorus granulosus having two-year gestation
periods (Holden, 1974; Guallart & Vicent, 2001), and
Chlamydoselachus anguineus having a three-year gestation
(Tanaka et al., 1990). Although C. anguineus is a member
of the Order Hexanchiformes, it is a deep-water species
Journal of the Marine Biological Association of the United Kingdom (2005)
D.M. McLaughlin and J.F. Morrissey 1191
and it is likely that the low temperature of this habitat
contributes to the extended gestation periods exhibited by
many deep-water species. Considering that most of the
aforementioned species inhabit the deep sea and utilize a
similar mode of reproduction to Centrophorus cf. uyato, it is
likely that C. cf. uyato has a long gestation period as well.
In addition, the low temperatures of the deep sea probably
cause maturity of deep-sea elasmobranchs to occur at a
fairly high age. Though age data are unavailable for most
squaloids, it has been suggested that the median age at
maturity of female Squalus acanthias in the North Paci¢c is
35.5 y (Saunders & McFarlane, 1993).
Given the poor status of many traditional ¢sh stocks on
the continental shelf, commercial ¢sheries in many areas
have expanded to target species along the continental
slope, with increased exploitation of species such as Greenland halibut (Reinhardtius hippoglossoides [Walbaum, 1792]),
orange roughy (Hoplostethus atlanticus Collett, 1889), and
Chilean sea bass (Dissostichus eleginoides Smitt, 1898) (e.g.
Haedrich et al., 2001).
Many deep-sea teleosts exhibit life-history traits more
comparable to elasmobranchs (e.g. slow grow, high age of
maturity, and low fecundity) than their shallow-water
relatives. This has resulted in rapid declines in many populations due to directed ¢shing e¡orts (Haedrich et al.,
2001).
The threats to elasmobranch populations from commercial ¢sheries are well documented (e.g. Baum et al., 2003).
Data regarding the impact of commercial ¢sheries on
shark populations is primarily based upon the faster
growing carcharhinid sharks that are more fecund and
inhabit shallower water. All species in genus Centrophorus
have small litters (56) (Compagno, 1984), making them
all vulnerable to over-exploitation. Centrophorus cf. uyato
may have one of the lowest fecundities among sharks,
giving birth to a maximum of two pups every three years.
Several species of Centrophorus are currently being
harvested for high quantities of diacylglyceryl ethers,
which are of major interest to pharmaceutical companies
(Davenport & Deprez, 1989). Given that Centrophorus
occurs globally, it is likely that our current and future
research will provide reproductive data useful for the
management of other Centrophorus species currently being
harvested. Deep-sea elasmobranchs tend to exhibit slower
growth and lower fecundity than most other elasmobranchs and may be especially prone to over-exploitation.
Hence, improved knowledge of the life history of such
species is required to ensure the e¡ective management
and sustainability of these resources.
We thank Sigma Xi Grants-In-Aid of Research and Hofstra
University for research funds, D. Burke for logistic assistance,
and the Hofstra University Marine Laboratory (HUML) sta¡,
D. Bidwell, R. Buch, C. Buchman, G. Burgess, B. Capitano,
N. Carroll, P. Daniel, I. Davenport, T. Gardner, C. Leigh,
T. Leigh, S. Macia¤, J. Olin, M. Robinson, and G. Sancho for
¢eld assistance. This is publication no. 8 of the HUML.
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