reproductive biology of the blacktip shark, carcharhinus limbatus

Reproductive biology of the blacktip shark,
Carcharhinus limbatus (Chondrichthyes: Carcharhinidae)
off West and North African coasts
by
Christian CAPAPÉ (1), Amadou Abdoulaye SECK (2), Youssouph DIATTA (3)
Christian REYNAUD (1), Farid HEMIDA (4) & Jeanne ZAOUALI (1)
AbsTract. - The blacktip shark, Carcharhinus limbatus, is commonly captured along the west coast of Africa and rarely
in the Mediterranean, where it was recorded in the Gulf of Gabès (southern Tunisia). Following competition pressure from
its sympatric species, the sandbar shark, C. plumbeus and the spinner shark, C. brevipinna, it migrated northward into the
Gulf of Tunis and off the Algerian coast. Adult males and females reached over 167 cm and 178 cm total length (TL),
respectively. The largest male and the largest female were 216 cm and 245 cm TL, respectively. They were no significant
differences of relationship of mass versus TL between males and females. C. limbatus is a placental viviparous elasmobranch. Adult females had a single ovary and two functional uteri, in which encapsulated eggs and embryos were not
equally distributed. Mating occurred in Spring or in early Summer, with parturition in July. Gestation lasted approximately
one year. There is perhaps a biannual reproductive cycle. In some specimens, vitellogenesis proceeded in parallel with gestation. Diameter of the largest yellow yolked oocytes ranged from 23 to 25 mm (mean: 23.95 ± 0.80) and their mass from
5.9 to 8.4 g (mean: 7.48 ± 0.92). Both uteri were compartmentalised into chambers and a single embryo developed in each
chamber. Size and mass at birth, based on fully developed embryos, and the smallest free-swimming specimens (neonates)
were between 61-65 cm TL and 0.935-1.375 kg respectively. A chemical balance of development based on mean dry masses of the largest yellow yolked oocytes and the fully developed embryos was # 69. It was the highest value ever computed
in a viviparous elasmobranch, and confirmed that C. limbatus is a matrotrophic species. Ovarian fecundity was slightly
higher than uterine fecundity. There was a slight relationship between the two categories of fecundity and the females TL.
Litter sizes ranged from 6 to 8. Among the embryos and the free-swimming specimens the females outnumbered the males
ones. This was not the case for the adults.
résumé. - Biologie de la reproduction du requin bordé, Carcharhinus limbatus (Chondrichtyens: Carcharhinidae) au
large des côtes ouest et nord de l’Afrique.
Le requin bordé, Carcharhinus limbatus est communément capturé le long de la côte occidentale de l’Afrique mais
plus rarement en Méditerranée, où il a été signalé dans le golfe de Gabès (Tunisie méridionale). Subissant des pressions de
compétition avec les espèces sympatriques, le requin gris, C. plumbeus et le requin tisserand, C. brevipinna, il a par conséquent migré vers des régions plus septentrionales, dans le golfe de Tunis et au large de la côte algérienne. Les mâles et les
femelles sont adultes au-delà de 167 cm et 178 cm de longueur totale (LT), respectivement. Le plus grand mâle et la plus
grande femelle avaient respectivement une LT de 216 cm et 245 cm. Il n’y a pas de différence significative concernant les
relations taille-masse entre mâles et femelles. C. limbatus est une espèce vivipare placentaire. Les femelles adultes ont un
seul ovaire et deux utérus fonctionnels dans lesquels les œufs encapsulés et les embryons ne sont pas également répartis.
L’accouplement a lieu au printemps ou au début de l’été, tandis que la parturition se déroule en juillet. La gestation dure
approximativement une année. Le cycle de reproduction est bisannuel, mais chez certains spécimens, la vitellogenèse se
déroule parallèlement à la gestation. Le diamètre des plus grands ovocytes mûrs varie de 23 à 25 mm (moyenne: 23,95 ±
0,80) et la masse de 5,9 à 8,4 g (moyenne: 7,48 ± 0,92). Les deux utérus sont divisés en chambres et dans chacune d’elles se
développe un unique embryon. La taille et la masse à la naissance, fondées sur les embryons à terme et les plus petits spécimens libres, sont comprises entre 61 et 65 cm de LT et 0.935-1.375 kg, respectivement. Une balance chimique de développement fondée sur les masses sèches des plus grands ovocytes mûrs et des embryons à terme est de 69. C’est la plus grande
valeur jamais calculée chez un élasmobranche vivipare et elle confirme que l’espèce est matrotrophe. La fécondité ovarienne est légèrement plus élevée que la fécondité utérine. Il apparaît une faible relation entre les deux catégories de fécondité et la LT des femelles. Les portées vont de 6 à 8 individus. Parmi les embryons et les spécimens libres, les femelles sont
plus nombreuses que les mâles. Ce n’est pas le cas pour les adultes.
Key words. - Carcharhinidae - Carcharhinus limbatus - MED - Western African coast - Reproductive biology.
Eight species of the genus Carcharhinus are known in
the Senegalese waters (Cadenat and Blache, 1981; Séret and
Opic, 1981), of which the blacktip shark, Carcharhinus limbatus, is abundantly and regularly landed at the fishing sites
(1) Laboratoire d’Ichtyologie, Université Montpellier II, Sciences et Techniques du Languedoc, 34095 Montpellier Cedex 5, FRANCE.
[[email protected]].
(2) Musée de la Mer, Institut fondamental d’Afrique noire Cheikh Anta Diop, Gorée, SÉNÉGAL.
(3) Département de Biologie animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop, BP 5005, Dakar, SÉNÉGAL.
(4) Laboratoire Halieutique, Faculté des Sciences biologiques, Université des Sciences et Techniques Haouari Boumédienne, B.P. 32, El
Alia, 16 111 Bab Ezzouar, Alger, ALGÉRIE.
Cybium 2004, 28(4): 275-284.
Reproductive biology of Carcharhinus limbatus off African coasts
located along the coast of Senegal, especially the Cape Verde
Peninsula (Capapé et al., 1994).
Data on the reproductive biology of the blacktip shark
have been reported for specimens from Madagascar (Fourmanoir, 1961), the North-West Atlantic (Clark and Von
Schmidt, 1965), South Africa (Bass et al., 1973), North Africa (Capapé, 1974), the Gulf of Mexico (Branstetter, 1981;
Castillo-Geniz et al., 1998, the southeastern United States
(Castro, 1996) and Senegal (Cadenat and Blache, 1981;
Capapé et al., 1994). New records of C. limbatus from this
latter area and from North Africa coast allow upon the previous data to be expanded and compared. Size at sexual maturity, size at birth, reproductive cycle, fecundity and sex ratio
are detailed in this article.
MATERIAL AND METHODS
A total of 183 Carcharhinus limbatus (Valenciennes,
1841) was examined, representing 90 males and 93 females.
One hundred and sixty six specimens, 80 males and 86
females were caught by demersal gill-nets off the Senegalese
18°
17°
16°
16°
Sénégal
15°
Ouakam
Kayar
I. of Gorée
14°
N
50 km
Gambia
Capapé et al.
coast between 1993 and 2002 (Fig. 1). In addition, 17 specimens caught off the North Africa shore were observed. A
single specimen was from off the Algerian coast: a juvenile
female, 170 cm total length (TL) caught by longline during a
fishing tuna survey conducted in 2002. The capture occurred
9 miles off Boumerdes, city located 50 km east to Algiers
(Fig. 2). Sixteen specimens were captured in the Tunisian
waters by demersal trawling between 1971 and 1990. Of the
ten specimens from the Gulf of Gabès (southern Tunisia),
four were adult, two males and two females, ranging between
1600 and 180 cm TL, six were juvenile, five males and a single female, ranging between 82 and 93 cm TL. All the specimens caught in the Gulf of Tunis, northern Tunisia, were
juveniles, three males and three females, ranging between
92.5 and 100 cm TL (Fig. 2).
The monthly collection of the specimens from the three
areas is summarized in table I.
Twenty developing embryos and 14 fully developed
embryos were examined.
The specimens were measured to the nearest millimetre
for total length (TL) following Bass et al. (1973) and
weighed to the nearest gram, when possible. Measurements
comprised clasper length (CL, mm) according to Collenot
(1969), and the diameter of yellow yolked or ripe oocytes
and developing oocytes. All the oocytes, the eggs and the
embryos were weighed to the nearest decigram. They were
removed from the ovaries and the uteri and then measured
and weighed to the nearest decigram.
The onset of sexual maturity was determined by the relationship between CL versus TL. Bass et al. (1973) noted that
claspers of juveniles are short and flexible, they added that
males are adult when claspers are rigid, elongated and calcified. In addition, some aspects of the testes and the genital
organs are described. Size of females at sexual maturity was
determined from the condition of ovaries and the morphology of the reproductive tract. Two categories of specimens
were distinguished for males and females.
To investigate the embryonic development and the role
of the mother during gestation, a chemical balance of devel5°
38°
N
0°
200 km
13°
35°
Morocco
Figure 1. - Map of the coast of Senegal showing the fishing places
() where one or more Carcharhinus limbatus from the studied
sample were captured. W: west coast of Africa. S: northern coast of
Africa. [Carte des côtes du Sénégal montrant les lieux de pêche
( ) où un ou plusieurs Carcharhinus limbatus de l’échantillon
étudié ont été capturés.]
276
Ouahran
5°
10°
Boumerdes
Algiers
Algeria
Tunis
Tunisia
Gabes
Figure 2. - Map of the Mediterranean North African shore showing
the fishing places ( for the Algerian coast and * for the Tunisian
coast) where one or more Carcharhinus limbatus from the studied
sampling were captured. [Carte des côtes méditerranéennes de
l’Afrique du Nord montrant les lieux de pêche ( pour la côte
algérienne et * pour la côte tunisienne) où un ou plusieurs Carcharhinus limbatus de l’échantillon étudié ont été capturés.]
Cybium 2004, 28(4)
Capapé et al.
Reproductive biology of Carcharhinus limbatus off African coasts
Table I. - Monthly catches of Carcharhinus limbatus. W, N = West and North African coasts. [Captures mensuelles de Carcharhinus limbatus. W, N = Côtes ouest et nord de l’Afrique.]
Feb.
W N
1 1 2 - 1 1 3
Mar.
W N
- 4 4 3 - 3 7
Apr.
May
Jun.
W N W N W N
3 - 10 7 3
2 - 2 5 5 - 12 - 12 3
4 - 7 2 13 2
4 - 2 5 8 - 9 2 18 2
13
23
35
opment (CBD) was considered. CBD is based on the mean
dry mass of fertilized eggs and fully developed embryos.
CBD can be computed as the mean dry mass of fully developed embryos divided by the mean dry mass of yellow
yolked oocytes or eggs. CBD is a tentative estimate.
The comparisons of curves for the relationship mass-total
length were made by ANCOVA.
Tests for significance (p < 0.05) were performed by using
ANOVA, student t-test, chi-square test.
Jul.
Aug.
W N W N
17 4 3 3 - 8 20 4 11 18 1 3 5 - 2 23 1 5 48
16
300
Sep.
W N
4 - 2
4 2
5 1
- 2
5 3
14
Oct.
W N
- 2 2 3 1 4 6
Nov.
W N
1 3 4 - 1 1 5
Dec.
W N Total
3 58
- 32
3 90
- 63
2 30
2 93
5
183
Neonate
Juvenile
Adult
275
250
CL = 0.155 TL - 73.87; r = 0.95
n = 77 (5  + 46  + 26 )
225
200
CL (mm)
Jan.
Category W N
Juvenile
2 Adult
- Total 2 Females Juvenile
1 Adult
5 Total 6 Grand total
8
Sex
Males
175
150
125
RESULTS
100
Size at sexual maturity
Males
Two stages of male development were considered, juvenile and adult (Fig. 3). During the juvenile stage, the males
had short and flexible claspers and both testes and genital
duct were membranous and undeveloped. This stage comprised 58 males between 61 and 65 cm TL. Among the juveniles, fifteen small free-swimming specimens were collected.
They exhibited an unhealed scar on their ventral surface and
were probably neonates, ranging between 62 and 65 cm TL.
During the adult stage, the claspers were rigid, elongated
and calcified. The testes were developed, with spermatocysts
externally visible. The genital duct was conspicuously developed and the ductus deferens (sensu Hamlett et al., 1999)
clearly twisted.
The CL versus TL relationship plotted in figure 3, does
not clearly show an inflexion between juveniles and adults,
probably to sampling, maturing specimens between 130 and
150 cm were rarely found. In this category of males, close to
become adults, claspers grow the fastest, as this is generally
the case in elasmobranch species
The smallest adult male was 155 cm TL, but over 167 cm
TL, all the observed specimens were adult. Thirty-two adult
males were collected. The largest male reached 216 cm TL,
the heaviest male weighed 65 kg but it was 213 cm TL.
75
Cybium 2004, 28(4)
50
25
400
600
800
1000
1200
1400
TL (mm)
1600
1800
2000
2200
Figure 3. - Clasper-length (CL, mm) vs total length (TL, mm) in
male Carcharhinus limbatus. [Longueur des ptérygopodes (CL,
mm) en fonction de la longueur totale (TL, mm) chez les Carcharhinus mâles.]
Females
Similar to the males, two categories of females were considered: juvenile and adult. Sixty-three juveniles were
observed, ranging between 61.5 and 178 cm TL. Seven juvenile females were observed, ranging between 61.5 and 64.5
cm TL. The juveniles larger than 95 cm TL, had whitish ovaries with oocytes of microscopic size and indistinct ovi­du­
ctal glands. Females, between and 178 cm TL, had trans­
lucent oocytes and a differentiated genital duct. They probably entered a maturation stage over this size. The 30 adults
TL ranged from 163.5 to 245 cm TL. The functional ovary
exhibited batches of developing and fully yolked oocytes.
The genital tract was fully developed and in some specimens
both uteri contained egg capsules or embryos at different
stages of development. The smallest adult female with ovary
containing fully yolked oocytes ready to be ovulated, was
277
Reproductive biology of Carcharhinus limbatus off African coasts
Capapé et al.
Table II. - Reproductive cycle of female Carcharhinus limbatus. Condition of ovary and uteri during gestation. [Cycle de reproduction des
femelles de Carcharhinus limbatus. État de l’ovaire et des utérus pendant la gestation.]
Numero
of record
Month of
catch
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
Jan.
Jan.
Jan.
Jan.
Jan.
Feb.
Apr.
Apr.
Apr.
Apr.
Jun
Jun.
Jun.
Jun.
Jul.
Jul
Jul.
Jul.
Aug.
Aug.
Sep
Sep.
Oct.
Nov.
Dec.
Size of Mass of
female
female Ovarian activity
(TL, mm)
(kg)
1790
1870
1950
2150
2350
> 2000?
1700
1800
1890
1940
1635
1780
1860
2100
2220
2250
2270
2350
2300
2450
2150
2200
2100
1635
1820
50.0
49.5
56.0
63.0
68.0
?
?
?
48.0
55.0
36.0
50.0
49.5
67.0
66.0
?
?
75.0
> 60.0
?
?
?
?
36.0
45.0
Vitellogenesis
?
Vitellogenesis
Vitellogenesis
Vitellogenesis
?
Vitellogenesis?
Vitellogenesis?
Vitellogenesis
Vitellogenesis
Vitellogenesis
Vitellogenesis
Vitellogenesis
Vitellogenesis
Vitellogenesis
Vitellogenesis
Vitellogenesis
Vitellogenesis
Resting
Vitellogenesis
?
Vitellogenesis
Vitellogenesis
Vitellogenesis
163.5 cm TL and weighed 36 kg (Tab. II, record 11), and
above 178 cm TL, all the females were adult. The largest
female reached 245 cm TL, but it was not weighed; the
heaviest female weighed 75 kg and was 235 cm TL (Tab. II,
record 18).
Reproductive cycle
The results summarized in table I show that the blacktip
shark was located in the Senegalese waters between April
and September, with a peak in June, July and August for both
male and female juveniles and adults. Among the juveniles,
15 small free-swimming specimens were collected in August
and September. Most of the adult females were pregnant.
They were usually captured in June and July. Of 32 observed
adult males, 16 specimens were collected in June, July and
August. The single female collected from off the Algerian
coast was caught in May. The adult specimens from the
Tunisian waters were caught in September and the juveniles
between May and September.
278
Oocytes
Oocytes
diameter
number
(mm)
18-19
?
18-19
18-20
?
?
?
?
20-21
18-20
24
23-25
24-25
23-24
23-24
?
24
23-24
23-25
?
14-15
?
16
?
21
25
?
?
?
?
16
>6
14
16
22
14
?
16
15
?
14
?
Uterine
content
Embryos?
?
Embryos
Embryos
?
Embryos?
Embryos?
Embryos?
Embryos
Embryos
?
Embryos
Embryos
?
Embryos
Eggs
Eggs?
Embryos
Embryos
Embryos
?
Embryos
size (TL,
mm)
Embryos
mass
(gramme)
Embryos
or eggs
number
?
?
?
400-420
?
?
?
?
450-460
?
?
595-610
?
600-625
-
?
?
395-425
?
?
?
?
632-725
?
?
935-1107
?
1015-1127
?
22
340-415
-
-
?
115
335-405
-
6
6
?
6
?
8
8
?
?
8
-
In juvenile females, two ovaries were observed. Both
ovaries were small, slender and of similar size and weight.
Some morphological differences developed as the specimens
grew and reached maturity. The right one continued to
increase in length and mass and then became functional. On
the other hand, in all adults, both uteri were functional. The
ovary produced oocyte batches similar in size and in mass.
Only one of these batches developed into fully yolked or ripe
oocytes, the other degenerated. Thirty oocytes were measured
from two females containing near-term foetuses. Their diameter ranged from 23 to 25 mm (mean: 23.95 ± 0.80); their
mass from 5.9 to 8.4 g (mean: 7.48 ± 0.92). Fertilized eggs
were enveloped with a transparent and brownish capsule,
which ended on both side, by a large folded and twisted filament. The eggs were fragile and sometimes spilled during
handling. Consequently, they could not be weighed.
Table II reveals that females with developing embryos
occurred throughout the year. Females with fully developed
embryos were recorded in July (records 15 and 18). Females
Cybium 2004, 28(4)
Capapé et al.
Reproductive biology of Carcharhinus limbatus off African coasts
Table III. - Carcharhinus limbatus sex-ratio for each category of
specimens and for the total sample. [Sex-ratio de Carcharhinus limbatus pour chaque catégorie de spécimen et pour l’échantillon
total.]
Category
Uterine content Embryos
Free-swimming Neonates
specimens
Other juveniles
Total juveniles
Adults
Total
General total
Males
20
6
52
58
32
90
110
Females Females/
Males
24
1.2/1
7
1.1/1
56
1.07/1
63
1.08/1
30
1/1.03
93
1/1.03
117
1.06/1
with eggs in the uteri occurred in August (record 19 and
probably record 20), and post-partum females in August
(record 18) and September (record 23). Records 22, 23, 4, 9,
3, 15 and 18, show a regular increase in size and mass of the
embryos. They suggest that gestation period appears to be
11-12 months approximately, but not longer.
Eggs and embryos were not equally distributed in each
uterus. Embryos were more numerous in the left uterus than
in the right one. The embryos less than 11.5 cm TL were free
in the uteri and exhibited a large slightly vascularised yolksac and filaments gills (Tab. II, record 23). The other records
of pregnant females bore embryos with well-established placenta connected to the embryo by a smooth and unadorned
umbilical stalk. The filaments gills were considerably
reduced and they completely disappeared in specimens
between 33.5 and 40.5 cm TL (Tab. II, record 23) They were
at mid-term gestation and totally formed and pigmented, and
the length of the umbilical stalk measured in six embryos
was between 14 and 20.5 cm. At the end of the gestation, the
umbilical stalk presented large variations in length, between
43 and 50 cm, and in mass, between 25.1 and 31.8 g. Concomitant with the embryonic development, the uteri are
compartmentalized in chambers, and, in each chamber, a
single embryo developed. The uterine folds were developed
and very convoluted at the distal ends of both uteri. All the
observed embryos, developing or full term, were sexed.
Size and mass
Two females measuring 222 and 235 cm TL and weighing 66 kg and 75 kg (records 15 and 18) contained six and
eight full term embryos, respectively. The TL of these 14 full
term embryos ranged from 59.5 to 62.5 cm (61.25 cm ± 8.02
mm), their mass from 935 g to 1.127 kg (1.0335 kg ±
63.54 g). Eight males and six females were sexed. Thirteen
small free-swimming specimens, six males and seven
females were collected, ranging between 61.5 and 65 cm TL
(65.604 cm ± 24.75 mm) and weighed between 1.12 and
1.375 kg (1.2527 kg ± 99.40 g).
The relationship total mass versus total length did not
Cybium 2004, 28(4)
show significant differences between males and females.
The relationships are for males: log TM = 3.16 log TL - 5.76:
r = 0.94; n = 74 and for females: log TM = 3.22 log TL 5.92: r = 0.98; n = 70 (F = 2.16; p = 0.14).
Chemical balance of development
Fresh masses of 14 fully yolked oocytes ranged from 5.9
to 8.4 g (mean: 7.5 ± 0.9) and of 16 fully developed embryos
from 935 to 1127 g (1033.5 g ± 63.5). CBD based on mean
dry masses calculated for C. limbatus was # 69.
Fecundity
The ovarian fecundity was based on the number of
oocytes counted in each adult female. Considering that vitellogenesis proceeds in parallel with gestation, we counted the
yellow yolked oocytes ready to be ovulated. The ovarian
fecundity ranged from 14 to 25 (mean: 17.18 ± 3.7). There is
a slight relation between ovarian and females size. The uterine fecundity is based on the number of eggs, developing
and/or fully term embryos. It ranged from 6 to 8 (mean: 6.8
± 1.1). Uterine fecundity does not appear to be related with
females size.
Sex-ratio
Except in adults, females slightly outnumbered males for
each category of specimens as well as for the total sample.
However, whatever the category of specimens, these differences in number are not significantly different (Tab. III).
DISCUSSION
The blacktip shark is widely distributed and prone to
large migrations (Garrick, 1982; Compagno, 1984). Off Senegal, captures of blacktip sharks occurred throughout the
year but mainly in spring and summer (Tab. I). They concern
juveniles and adults of both sexes and among them large
specimens. These specimens approach the coast when the
inshore waters become warmer probably in order to find
preys (Diatta et al., 2001) and to reproduce. Off the Tunisian
coast, C. limbatus was occasionally captured and records are
rather rare (Bradaï, 2000). A competition pressure from sympatric species, C. plumbeus, C. brevipinna and C. limbatus
was suspected by Capapé (1989) and corroborated by recent
information provided by Bradaï (2000) in the Gulf of Gabès.
C. limbatus seems unable to establish definitively in southern Tunisian waters.
Hemida et al. (2002) showed that some Carcharhinus
spp. recently observed off the Algerian coast migrated from
the eastern Atlantic into the Mediterranean through the Strait
of Gibraltar. This is probably also the case for the female C.
limbatus caught off the Algerian coast. The species is more
279
Reproductive biology of Carcharhinus limbatus off African coasts
Table IV. - Sizes at sexual maturity and maximal sizes of Carcharhinus limbatus reported from different areas. [Tailles à la maturité
sexuelle et tailles maximales de
Carcharhinus limbatus relevées
dans différentes régions.]
Size at sexual maturity Maximal size (mm)
Area
Authors
(mm)
Males
Females Males
Females
1350-1630
1550
Florida
Clark and Von Schmidt (1965)
1486
1580
2125
Brazil
Sadowsky (1967)
1800
1900
2260
2470
South African
Bass et al. (1973)
1360-1600
1580
Gulf of Mexico
Branstetter (1981)
1450
1560
1743
1930
Southeastern U. S.
Castro (1996)
1250
1450
Gulf of Mexico
Castillo et al. (1998)
1670
1780
2160
2450
West-North Africa
Present study
abundant off the African western coast than in the Red Sea.
On the other hand, the captures sites of C. limbatus in the
Alborran Sea (Moreno, 1995) and off the Algerian coast suggest migration from the eastern tropical Atlantic.
Data about size at sexual maturity and maximal size of
C. limbatus reported from different areas are summarized in
table IV. Blacktip sharks from American coasts males
matured at a smaller size than those from the African coasts,
while the latter reached a larger TL than the former. Size at
maturity and maximal size are subjected to intraspecific
changes related to the area in agreement with Moreno’s opinion (1995). Similar patterns were observed for the close
related species, C. brevipinna, according to Stevens and Mc
Loughlin (1991) and Capapé et al. (2003). Furthermore, all
these reports confirmed the Branstetter’s opinion (1981) who
noted that ‘males mature at a much smaller size than females
and do not attain as great a length’. These reports suggest
that generally females are larger than males and Mellinger
(1989) noted that this is practically the rule in elasmobranch
species except for scyliorhinids.
The fully developed embryos and the neonates reported
in the present article suggest that size at birth ranged between
59.5 and 65 cm TL in Senegalese waters. Previous data are
summarized in table V. They showed that size at birth
occurred at a smaller size in specimens from the American
coast and corroborated the Garrick’s opinion (1982) who
noted a ‘considerable variation in size of young at birth is
largely geographic’.
Similar intraspecific variations in size at birth were
reported in the literature for the spinner shark (Capapé et al.,
2003). They are probably due to fact that in placental viviparous species, the uteri are compartmentalised and probably
the nutrients are not equally distributed by the mother to the
embryos, mostly as a result of variation in vascularity (see
Hamlett and Hysell, 1998; Hamlett et al., 1998b, 2002).
Variations in size at maturity and in maximal sizes are probably the consequence of variations in size at birth partially
due to the reproductive mode of the species. A comparison
of these biological parameters available to date in literature
suggests that different C. limbatus populations appear to be
distinct according to the area. Similar observations were pro280
Capapé et al.
Table V. - Sizes at birth of Carcharhinus limbatus reported from
different areas. [Tailles à la naissance de Carcharhinus limbatus
relevées dans différentes régions.]
Size at birth
Area
Authors
(mm)
600-720
Madagascar
Fourmanoir (1961)
600
Red Sea
Gohar and Mazhar (1964)
540-570
Florida
Clark and Von Schmidt (1965)
600-630 South Africa coast
Bass et al. (1973)
497
Texas
Garrick (1982)
625
Senegal
Garrick (1982)
550-600 Southeastern U. S.
Castro (1996)
460-570
Gulf of Mexico
Castillo et al. (1998)
Present study
610-650 West-North Africa
vided for the spinner shark (Capapé et al., 2003). By contrast, geographical intraspecific variations in size at sexual
maturity, maximal size and size at birth seems to be not so
evident in the sandbar shark, C. plumbeus (Garrick, 1982;
Capapé, 1984).
Off the Senegalese coast, C. limbatus mating probably
occurred between April and August, when male and female
adults were the most encountered and equally distributed
(Tab. 1). Mating occurred in November off Brazil (Sadowsky, 1967), between June and July in the northern central
Gulf of Mexico (Branstetter, 1981), from mid-May to early
June off the southeastern United States (Castro, 1996).
Generally, carcharhinid species displaying pregnancies
develop compartments or chambers, which enclose a single
embryo. The first observation was provided by Davy (1860 in
Ranzi, 1932) for the blue shark, Prionace glauca. Similar patterns were also described in C. dussumieri (Alcock, 1890;
Teshima and Mizue, 1972), in C. melanopterus (Alcock, 1890;
Lyle, 1987), in C. falciformis (Gilbert and Schlernitzauer,
1966), in Carcharhinus sp. (Teshima and Mizue (1972), C.
plumbeus (Baranes and Wendling, 1981; Capapé, 1984; Hamlett, 1989), in Rhizoprionodon terraenovae (Hamlett and
Wourms, 1984; Hamlett, 1989), in C. cautus and C. fitzroyensis (Lyle, 1987), in C. brachyurus (Chiaramonte, 1996) and in
C. brevipinna (Capapé et al., 2003). However, Castro (1993a)
Cybium 2004, 28(4)
Capapé et al.
did not mention this feature in C. isodon and Hazin et al.
(2002) in C. acronotus. Uterine chambers were also observed
in triakids (Ranzi, 1932, 1934; Teshima and Mizue, 1972;
Capapé and Quignard, 1977) and in sphyrnids (Alcock, 1890;
Schlernitzauer and Gilbert, 1966; Capapé et al., 1998).
In matrotrophic elasmobranchs, the contribution of
mother-derived organic molecules is very important
(Wourms, 1981; Hamlett and Wourms, 1984; Hamlett et al.,
1985a-e; Hamlett, 1987, 1989; Hamlett et al. 1993a, 1993b;
Fishelson and Baranes, 1998; Hamlett et al., 2002). These
species produce an egg mass that is clearly less than the mass
of fully developed embryos. Matrotrophy is characteristic of
dasyatids, gymnurids and rhinopterids (Wourms 1981;
Wourms et al., 1988; Mellinger, 1989; Capapé et al., 1992;
Seck et al., 2002). By contrast, in pure lecithotrophic species
(sensu Wourms, 1977, 1981), which produced heavier eggs,
the role of the mother during gestation is reduced to a minimum. In lecithotrophic species, the mother only protected
the embryonic development and provided inorganic nutrients to the embryos (Mellinger, 1989; Hamlett and Hysell,
1998; Hamlett et al., 1998). This was observed in squatinids
(Capapé et al., 1990, Capapé et al., 2002) and in centrophorids (Ranzi, 1932; Guallart and Vicent, 2001).
The gestation period was subdivided into three phases in
C. brevipinna by Capapé et al. (2003). During the first phase,
which lasts two months approximately, the embryos are
somewhat lecithotrophic and they are mainly nourished by
the yolk. They ranged in size between 8.6 and 10.5 cm TL.
Then, in the second phase, the concomitant development of
mother’s uterine villi and embryo gill-filaments and the
resorption of yolk increase the role of the mother during gestation and the embryo are lecitho-matrotrophic which corroborates observations by Hamlett et al. (1985a) for the
Atlantic sharpnose shark, Rhizoprionodon terraenovae. The
embryos at this phase was over 18.5 cm TL. The phase lasts
three months until the placenta is definitively established and
the yolk and the gill-filaments completely resorbed. The
embryos ranged between 33.5 and 34.5 cm TL. During the
third phase, the nutrition required for the embryonic development is exclusively supplied by the mother. The embryos
are now strictly matrotrophic. This phase probably lasts
more than six months, until parturition. The embryos are
now strictly matrotrophic. However, these three phases were
not clearly observed in the African blacktip sharks. Among
the embryos observed in pregnant females, the smallest
implanted were between 33.5 and 40.5 cm TL (Tab. II, record
23). The placenta was definitively attached and the uteri
exhibited well-developed folds. Concomitantly, the yolk was
completely absorbed while the filaments gills of the embryos
were totally resorbed. In records 4, 9, 15, 18, the embryos
were completely formed and the nutrition required for the
embryonic development was exclusively supplied by the
mother. The embryos were strictly matrotrophic. Castro
Cybium 2004, 28(4)
Reproductive biology of Carcharhinus limbatus off African coasts
(1996) noted that implantation occurred during the 10th and
11th week of gestation, when the embryos measured 17.819.4 cm TL. A comparison between data of Castro (1996)
and ours (this study) on C. limbatus, and those given by Capapé et al. (2003) on C. brevipinna, suggests that similar patterns probably occurred during embryonic development in
both species.
Females with embryos at the end of development were
observed in July and females with eggs in uterus in August
for C. limbatus from the coast of Senegal. Similar observations were given for specimens from the northwest Atlantic
(Clark and Von Schmidt, 1965), South Africa (Bass et al.,
1973) and north central Gulf of Mexico (Branstetter, 1981).
Parturition occurred from early May to early June in Bulls
Bay, South Carolina (southeastern United States) according
to Castro (1996). Vitellogenesis proceeds in parallel with
gestation and soon after parturition, fully yolked oocytes are
immediately ovulated. The reproductive cycle could last one
year approximately. However, Bass et al. (1973) suggested
that the females bore embryos in alternative year. Branstetter
(1981) reported that ‘two pos-partum females had not developing ovarian eggs, which suggested a non-gravid year in
the reproductive cycle’. Similar patterns were described by
Castro (1996) for specimens from southeastern United
States. A female caught in August (Tab. II, record 20) had
the ovary in a resting phase and the uteri were empty but
slightly distended. This female probably contained eggs that
were expelled between handling and landing. Moreover, two
adult females caught in the Gulf of Gabès exhibited developing oocytes in the ovary, the uteri were not distended and no
placental attachments sites were observed. It was speculative
to state if they were primipare females. A female (Tab. II,
record 22) aborted when landed on the deck boat and, of six
embryos, a single one was given by fishermen. The ovary of
this female did not exhibit vitellogenetic activity. A biannual
reproductive cycle remains a suitable hypothesis but needs
confirmation. This only concerns some specimens in our
sample. Castro (1996) noted that this biannual cycle is typical of sharks of genera Carcharhinus and Negaprion. By
contrast, Hamlett et al. (1993a) noted that in most placental
sharks such as C. plumbeus. Rhizoprionodon terraenovae
and Mustelus canis embryos are developing in the uteri;
another batch of eggs are enlarging and receiving yolk in the
ovary, and consequently ‘soon after parturition, the females,
will mate and conceive again’. Branstetter (1981) collected
near term females C. acronotus carrying large developing
ovarian eggs, by contrast, Hazin et al. (2002) reported that
vitellogenesis and gestation occurred consecutively in C.
acronotus. A biannual or an annual reproductive cycle is
observed in same species. Consequently, it appears that the
length of a reproductive cycle is related to fact that females
are, whether or not, energetically capable of producing both
a litter and yellow yolked oocytes in a twelve-month period,
281
Reproductive biology of Carcharhinus limbatus off African coasts
as suggested by Simpfendorfer and Unsworth (1998) with
regard to a placental elasmobranch, the whiskery shark, Furgaleus macki, from south-western Australia.
A chemical balance of development (CBD) of circa 69
calculated for C. limbatus is the highest values ever observed
in elasmobranch species, close to its related species C.
brevipinna, 65.8 (Capapé et al., 2003) and more than the c.
47 for Mediterranean Dasyatis violacea (Hemida et al.,
2003), the c. 30.6, for the butterfly ray, Gymnura altavela,
from Tunisian waters (Capapé et al., 1992), and the c. 31.12
for the bull ray, Pteromylaeus bovinus from the coast of Senegal (Seck et al., 2002). C. limbatus is a pure matrotrophic
species following the definition of Wourms et al. (1988). As
in C. brevipinna, the C. limbatus CBD value we have calculated concerns a viviparous placental species. This suggests
that the role of mother during gestation is very important,
more than this observed in viviparous aplacental species,
including dasyatids and gymnurids whose gestation is rather
short, between two and six months (Ranzi and Zezza, 1936;
Capapé, 1993; Capapé and Zaouali, 1995; Mollet et al.,
2002; Hemida et al., 2003), and the mother’s role during
embryonic development is very important (Mellinger, 1989;
Cateni et al., 2003). By contrast, the CBD of c. 0.5 obtained
for both Squatina squatina and S. oculata from the Tunisian
coasts (Capapé et al., 1990) and c. 0.73 for S. oculata from
the coast of Senegal (Capapé et al., 2002) are very low values. They are pure lecithotrophic species (sensu Wourms et
al., 1988) and the mother’s role is rather reduced to protect
the embryos during gestation.
Ovarian fecundity is higher than uterine fecundity. This
is due to the fact that some fully yolked oocytes were not
ovulated and entered atres­ia. Moreover, pregnant females
probably aborted during capture or handling, and may have
partially lost their brood. This phenomenon was observed
and is considered as a rule in viviparous elasmobranchs
(Mellinger, 1989). Both fecundities are slightly related with
females size. Similar patterns were observed in C. plumbeus
and C. brevipinna from Mediterranean areas (Capapé, 1984;
Capapé et al., 2003).
Litter sizes ranged from 6 to 8 with an average of 6.8 in
the pregnant females we have observed and they ranged from
1 to 8 according to Cadenat and Blache (1981). Off Madagascar and Comorian Islands, litter sizes ranged from 3 to 8
(Fourmanoir, 1961), off South Africa from 1 to 8, average
being 6.7 (Bass et al., 1973). Bass et al. (1973) combined the
data of Baughman and Springer (1950) and Clark and Von
Schmidt (1965) and noted that the litters ranged from 3 to 8
according to in north west Atlantic, and in this area, Bigelow
and Schroeder (1948) reported from 3 to 8 embryos per litter.
In the Gulf of Mexico, litter size ranged from 2 to 6 (Branstetter, 1981; Castro, 1996) or from 2 to 7 (Castillo et al.,
1998). Bass et al. (1973) summarizing previous data, suggested that litter size increase with mother size. However,
Springer (1960) did not show litter sizes increasing with
mother size in C. plumbeus. According to Stevens and Mc
282
Capapé et al.
Loughlin (1991), a relation between litter sizes and mother
sizes could not be considered as a rule in carcharhinids.
The sex-ratio of the embryos shows that the sexes are
approximately in equal numbers. Similar data were reported
by Stevens and Mc Loughlin (1991) on different species of
sharks from Australian waters and other sharks from different marine areas throughout the world, in a literature review
provided by the same authors. It is 1: 1 in Iago omanensis
from the northern Red Sea (Waller and Baranes, 1994), C.
limbatus from the Gulf of Mexico (Castillo et al., 1998) and
for C. brevipinna from the Tunisian waters (Capapé et al.,
2003). By contrast, among post partum population, males
outnumbered females in our sample, except in adults. Stevens and Mc Loughlin (1991) reported that the sex ratio was
about equal in seven shark species, but in 13 shark species
males significantly outnumbered females even if females
slightly predominated males in adult population. Similar patterns were reported for various shark species (Stevens and
Mc Loughlin, 1991) and with regard to C. plumbeus from
off Florida, Springer (1960) suggested that this phenomenon
was the consequence of high rate mortality in males. Reviewing previous papers, Stevens and Mc Loughlin (1991) suggested that it was rather a result of a sexual segregation.
Generally, adult females approach the shore in order to protect and/or to expel their brood in nursery areas (Castro,
1993b). Moreover, our sample comprised pregnant females
that carried fully developed embryos, parturient females and
neonates suggest that the spinner shark have probably tried
to find nursery areas along the Senegalese coast, however,
this hypothesis needs further observations in order to be confirmed.
Acknowledgments. - Jeanne Zaouali is indebted to her late husband and Christian Capapé to his late friend, Mr. Mohamed Zaouali, past-president of the “Office National des Pêches de Tunisie”,
for his interest and his assistance throughout the period of their
investigations along the Tunisian coast. All the authors are grateful
to the fishermen from the Tunisian and Algerian coasts who provided them material and they particularly thank the fishermen of
Ouakam fishing site in Senegal and especially Ms. Abdoulaye Diop
and Alioune Ndoye for providing information and material. We also
thank Dr. Bernard Séret from MNHN (Paris) for sending important
papers and constructive comments, which allowed us to improve
the manuscript. Thanks are also due to two anonymous referees for
their helpful comments on the manuscript.
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Reçu le 23 décembre 2003.
Accepté le 31 mai 2004.
Cybium 2004, 28(4)