ICES Journal of Marine Science, 63: 1053e1065 (2006)
doi:10.1016/j.icesjms.2006.04.016
Reproductive biology of catsharks (Chondrichthyes:
Scyliorhinidae) off the west coast of southern Africa
David A. Ebert, Leonard J. V. Compagno,
and Paul D. Cowley
Ebert, D. A., Compagno, L. J. V., and Cowley, P. D. 2006. Reproductive biology of
catsharks (Chondichthyes: Scyliorhinidae) off the west coast of southern Africa. e ICES
Journal of Marine Science, 63: 1053e1065.
This study presents information on the reproductive biology of five southern African catshark species: Apristurus microps, A. saldanha, Apristurus sp., Galeus polli, and Scyliorhinus capensis. They were caught between Walvis Bay, Namibia, and Cape Agulhas, South
Africa, from 50 to 1016 m deep. The reproductive mode of four species was oviparous,
whereas G. polli exhibited aplacental viviparity. Males of all species attained first maturity
slightly larger than females, and males of the four oviparous species attained a larger LTmax
than females. The length at 50% maturity was similar for males and females in most species. All species matured at an LT > 75% of LTmax except for male Apristurus spp. and female G. polli, which matured at 71.2% and 68.8%, respectively, of LTmax. The egg case of
A. microps has minute tendrils, whereas those of S. capensis were quite long, suggesting
different egg-laying habitats. Fecundity in G. polli ranged from 5 to 13, and litter size increased in relation to increased female length. Embryos of G. polli were large, each measuring approximately 30% of female LT. Neonates of G. polli were common and appear to
have a demersal lifestyle; those of the four oviparous species were entirely absent from the
study. Gravid A. microps were found in summer and winter, indicating a protracted breeding cycle, but reproductively active S. capensis were caught only in winter. Prior to this
study, reproductive information on these catsharks was largely lacking.
Ó 2006 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Keywords: egg cases, maturity, reproduction, Scyliorhinidae, southern Africa.
Received 30 November 2005; accepted 19 April 2006.
D. A. Ebert: Pacific Shark Research Center, Moss Landing Marine Laboratories, 8272
Moss Landing Road, Moss Landing, CA 95039, USA. L. J. V. Compagno: Shark Research
Center, Iziko e South African Museum, PO Box 91, Cape Town 8000, South Africa.
P. D. Cowley: South African Institute for Aquatic Biodiversity, Private Bag 1015, Grahamstown
6140, South Africa. Correspondence to D. A. Ebert: tel: þ1 831 771 4427; fax: þ1 831 632
4403; e-mail: [email protected].
Introduction
Southern Africa has one of the most diverse chondrichthyan
faunas in the world, consisting of some 46 families, 106
genera, and more than 210 species (Compagno, 1999). Of
this total, the catsharks (Scyliorhinidae) are one of the
most diverse groups, with 8.6% of the known species;
only requiem sharks (Carcharhinidae) and skates (Rajidae)
have larger percentages, 11.0% and 10.0%, respectively
(Compagno, 1999). This figure does not include several
new scyliorhinid species and subspecies, awaiting formal
description (Human, 2004; unpublished data). At least 16
catshark species are endemic to southern Africa, and it is
expected that this number will increase as new species
are identified and described (Compagno, 1999). Despite
1054-3139/$32.00
the abundance and diversity of these sharks, their biology
is generally poorly known. The biology of five nearshore
(Dainty, 2002) and six offshore (Ebert et al., 1996; Richardson et al., 2000) southern African catsharks has been studied, but much is still unknown about their reproductive
biology. The predation rate on the egg cases of four South
African catshark species by boring gastropods is considerable (Smith and Griffiths, 1997).
South Africa’s Marine and Coastal Management (MCM;
formerly the Sea Fisheries Research Institute) research ship
FRS ‘‘Africana’’ has, since 1983, conducted cruises along
the west coast of southern Africa aimed at determining the
biomass and recruitment of Cape hake Merluccius capensis
and M. paradoxus. Those two species are the target of a
major demersal fishery. Since 1986, chondrichthyan samples
Ó 2006 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
1054
D. A. Ebert et al.
for life history and systematic studies have been collected as
a matter of course during these routine hake biomass surveys. Results published to date include an extensive overview on the distribution of the chondrichthyan fauna
(Compagno et al., 1991), and information on the feeding
ecology of the three major elasmobranch groups, including
the skates, dogfish sharks, and catsharks (Ebert et al., 1991,
1992, 1996). Several species collected and examined during
the study were previously undescribed and have since either
been described, such as the paddlenose chimaera (Rhinochimaera africana; Compagno et al., 1990) and the tiger-tail
skate (Leucoraja compagnoi; Stehmann, 1995), or are currently under investigation by the authors. This paper is
one in a series on the biology of the cartilaginous fish off
the west coast of southern Africa. Here we report on the
reproductive biology of five species of catshark collected
during the research cruises of FRS ‘‘Africana’’.
Material and methods
Field sampling
The survey area between 1985 and 1990 extended from
Walvis Bay, Namibia (23(S 14(E), to Cape Agulhas,
South Africa (36(S 20(E), between 50 and 1016 m deep,
though most trawls were <500 m (Figure 1). Inclusive of
these years, annual summer and winter surveys were conducted. Starting in 1991, the survey area ranged from the
international border of Namibia and South Africa (ca.
29(S) to Cape Agulhas, but only a summer cruise was
undertaken annually.
A random, stratified sampling design of the area was
made, and in all some 2000 pre-determined stations were
occupied, this number including some more than once; of
Figure 1. The study area off the south coast of Namibia and the
west coast of South Africa. FRS ‘‘Africana’’ bottom trawl stations
that collected cartilaginous fish are indicated by open circles.
these, at least 1030 stations had cartilaginous fish, including
scyliorhinids. The gear used was a 60-m German bottom
trawl. Payne et al. (1984, 1985) provide a detailed description of the gear deployment and the basic methodology for station selection. Although most trawling was down to 500-m
bottom depth, up to six exploratory deep trawls were
conducted per cruise to investigate the resource potential
down to ca. 1000 m. All trawls took place during daylight
with the exception of the experimental deepwater trawls,
which were conducted after dark. The entire catch of all
vertebrate species at each station was identified, weighed,
and counted (subsamples were sometimes taken when the
catch was large, but the results raised to total trawl data);
invertebrate species were identified and weighed. In all,
637 catsharks comprising five species, smalleyed catshark,
Apristurus microps (Gilchrist, 1922), Saldanha catshark,
A. saldanha (Barnard, 1925), grey wonder catshark (Apristurus sp.), African sawtail catshark, Galeus polli (Cadenat,
1959), and yellowspotted catshark, Scyliorhinus capensis
(Smith, 1838), were collected in sufficient numbers to report on their reproductive biology. The reproductive biology of the Izak catshark (Holohalaelurus regani), a sixth
catshark species, the most abundant of all collected during
the surveys, has already been documented by Richardson
et al. (2000).
Biological data
On capture the sex of each catshark was determined, total
length (LT) measured to the nearest mm, and maturity status
determined as adult, adolescent, or juvenile. LT was measured in a straight line with the shark lying in its natural position. Inner clasper length of males, as measured from the
apex of the cloaca to clasper tip, and the width of the shell
gland of females were measured for each fish. The number
and proportion of adults, adolescents, and juveniles of each
sex were analysed using a c2 test with Yates correction to
evaluate differences in sex ratios (Zar, 1996). Weights (W )
were taken on a calibrated spring balance reading to the
nearest 0.1 g. The relationships between LT and W are given
in Table 1. To evaluate differences in the relationships between LT and W between males and females, the geometric
mean regressions were calculated from logarithmic transformations of the equation W ¼ aLTb, where W is the
weight in kg, LT is the total length in cm, and a and
b are fitted constants (Ricker, 1973). The regression coefficients for males and females were compared using
ANCOVA to determine whether there was any difference
between the coefficients for each sex (Ricker, 1973).
Maturity was assessed by visually inspecting the reproductive organs following a modification of the method of
Ellis and Shackley (1997). Males were considered to be
mature when the claspers were elongated and calcified. Adolescents included those whose claspers extended beyond
the posterior edge of the pelvic fins, but lacked calcification. Juveniles had short, flexible claspers that did not
Reproductive biology of catsharks off southern Africa
1055
Table 1. Life history parameters for five species of southern African catsharks.
Species
Smalleye
catshark
Apristurus
microps
Male
Female
0.94
73 W ¼ (5 1007)L3.5026
T
40 W ¼ (2 1007)L3.799
0.89
T
49.5
46.8
81.1
82.5
50.8
48.3
61.0
56.7
Saldanha
catshark
Apristurus
saldanha
Male
Female
0.98
45 W ¼ (8 1005)L2.249
T
0.97
40 W ¼ (2 1005)L2.5941
T
74.0
70.0
83.6
90.6
69.2
69.5
88.5
77.3
Black wonder
catshark
Apristurus sp. Male
Female
0.97
20 W ¼ (2 1006)L3.1371
T
32 W ¼ (1 1006)L2.9163
0.94
T
48.8
48.5
71.2
77.6
47.9
47.5
68.5
62.5
African sawtail Galeus polli
catshark
0.87
Male
94 W ¼ (1 1006)L3.1866
T
Female 101 W ¼ (4 1006)L2.7971
0.66
T
30.2
29.5
83.7
68.8
30.3
29.6
36.2
43.0
Yellowspotted
catshark
Male
Female
0.96
95 W ¼ (4 1006)L2.9441
T
0.96
97 W ¼ (1 1006)L3.2423
T
84.0
75.0
82.4
85.2
82.9
75.6
102.0
88.0
Scyliorhinus
capensis
n
LTeW
relationship
LT at first
maturity
LT at first
maturity (cm) relative LTmax (%) LT50 (cm) LTmax (cm)
Common
name
extend beyond the posterior edge of the pelvic fins. The inner clasper length was measured and plotted as a ratio
against LT. An abrupt change in the ratio between clasper
length and LT was considered to indicate maturity. Internally, coiling of the epididymides and development of the
testes were good indicators of maturation. Females were assessed as mature in the presence of large, mature oocytes,
a shell gland that was distinctly differentiated from the
uterus, and a pendulous posterior portion of the uterus. Adolescent females had smaller ovaries, with some differentiation, but lacked mature oocytes. The shell gland was
undeveloped and the uteri were narrow and constricted.
Juveniles lacked any differentiation of the ovaries, and the
shell gland was not differentiated from the uterus. Shell
gland width was measured and plotted as a ratio against
LT. An abrupt change in the ratio between shell gland width
and LT was taken to indicate maturity. Length at 50% (LT50)
maturity was calculated for each sex by means of a logistic
regression (Roa et al., 1999; Mollet et al., 2000; Neer and
Cailliet, 2001).
The egg cases of oviparous species were removed from
the uterus of fresh or alcohol-preserved specimens. Fresh
egg cases were fixed in 10% buffered formaldehyde and
preserved in alcohol. Egg cases were described and measured following Compagno (1988) and Gomes and de
Carvalho (1995), with some modifications and additions,
including a system of abbreviations similar to those in
Compagno (1984, 2001), given below.
The scyliorhinid egg case or capsule (Figure 2) is a more
or less flattened, spindle-shaped (fusiform) sheath for eggs
with an anterior or vestibular end (AVE) through which the
hatchling shark exits the case, and a posterior or terminal
end (PTE). It is bilaterally symmetrical and somewhat depressed. The lateral edges (LED) of the case extend from
anterior to posterior and often are expanded as paired lateral flanges (LFL), anterior and posterior horns (AHN and
r2
PHN), and anterior and posterior tendrils (ATD and
PTD). The lateral flanges vary from thin and flat to thickened, with a T-shaped section. The horns vary from very
short, small and nearly vestigial to long, slender, and stout.
Tendrils vary from rudimentary to very long on both
Figure 2. A scyliorhinid egg case showing terminology and
measurements.
1056
D. A. Ebert et al.
anterior and posterior horns, and can be highly convoluted,
coiled, wiry, and highly capable of tangling with one another, with tendrils of other catshark egg cases, and with
the substratum. Some egg cases may have long, soft, and
narrow fibrous sheets of byssus-like material present on
the ventral surface of the base of each anterior horn, which
may be part of the egg case structure.
The edges of the egg case between the anterior and posterior horns are the anterior and posterior borders (ABO and
PBO). An anterolateral plane of orientation can be defined
for the egg case between the anterior and posterior ends on
both sides, and between the four bases of the horns and the
anterior and posterior borders. It is asymmetrical in a dorsoventral plane transverse to the lateral plane, with the anterior end and anterior and posterior appendages (horns and
tendrils) bent in the same direction out of the anterolateral
plane and in the dorsoventral plane. We are not aware
whether the cases are laid consistently with specific orientation apart from their being more or less parallel to the
body axis of the shark and in the axis of the lumen of the
oviduct and with the posterior end exiting the cloaca first.
However, from mechanical considerations and for consistent description of egg case structures, we consider that
the capsule surface in the direction of the asymmetrical appendages and bent anterior end is the ventral surface
(VCS), and the opposite is the dorsal surface (DCS).
In species with long, convoluted posterior tendrils (and in
some species anterior tendrils) that can snag on the bottom
and help eject the case, it would seem more functional for
the extensive tendrils to be directed ventrally away from the
shark, towards the seabed, rather than being shielded dorsally and directed towards the longitudinal axis of the
mother shark. Dorsoventral orientation of the case at ejection might be unimportant in species that have vestigial
posterior tendrils. Definition of anterolateral and dorsoventral planes allows us to define a left and right side to the egg
cases in dorsal view. In dorsoventral view, egg cases often
have a distinct constriction or waist (WAI) behind the anterior border, well in front of the posterior border. The dorsal
and ventral surfaces of the capsule can be smooth and
glossy or covered by longitudinal ridges or striations
(LRS) that can be straight or undulated, and smooth or papillose, and can give the surface a rough texture and matte
appearance. The anterior border of the egg case is closed
before hatching, but scyliorhinid eggs have two pairs of respiratory fissures, short longitudinal slits with raised ridges
surrounding them, that allow access of oxygenated water to
the embryo, a pair of anterior respiratory fissures (ARF) just
behind the anterior horn bases, and a pair of posterior respiratory fissures (PRF) just in front of the posterior horn
bases. The egg cases of the southern African species examined here, and also those of Cephaloscyllium ventriosum
and Apristurus kampae from California, have the anterior
and posterior respiratory fissures of the left side on the dorsal surface, and those of the right side on the ventral surface
of the egg case. This asymmetry needs further study.
Egg case length (ECL) is used as an independent variable
for proportional dimensions of other egg case structures and
measured longitudinally between the anterior and posterior
borders: anterior border width (ABW) between the bases of
the anterior horns; anterior respiratory fissure length (AFL),
the anteroposterior length of the right anteroventral fissure;
anterior case width (ACW), the transverse width of the case
in its anterolateral plane at its widest part anterior to the
waist; egg case height (CHI), the depth of the case at its
widest part in the sagittal dorsoventral plane; posterior border width (PBW) between the bases of the posterior horns;
posterior respiratory fissure length (PFL); anteroposterior
length of the right posteroventral fissure; posterior case
width (PCW), the transverse width of the case in its anterolateral plane at its widest part posterior to the case; waist
width (WCW), the transverse width of the case in its anterolateral plane at the waist.
Unlike most catsharks that deposit egg cases in situ,
Galeus polli is an aplacental viviparous species, giving
birth to live young. Therefore, when gravid females of
this species were found, the number of embryos in each
uterus was counted and the total number plotted against
LT to determine whether there is an increase in litter number with size. The number of embryos or uterine eggs in the
left and right uterus was recorded, and a paired-sample
t-test was used to test the null hypothesis of no difference
between the mean number of right and left uterine embryos.
Finally, to evaluate difference in sex ratios, the number and
the proportion of embryos were analysed using a c2 test
with Yates correction (Zar, 1996).
Results
Apristurus microps
In all, 113 A. microps (40 females and 73 males) were
caught in the surveys, making this the most common of
the three Apristurus species collected. The overall female:
male (F:M) sex ratio was 1:1.83, significantly different
from the expected 1:1 ratio (c2 ¼ 9.06, d.f. ¼ 1, p < 0.05).
A comparison of maturity status showed a significant difference in the sex ratio of adults, 1:2.04 (c2 ¼ 8.22, d.f. ¼ 1,
p < 0.05), but no significant difference in the sex ratios of
adolescents and juveniles ( p > 0.05). There were no significant differences in the relationship between LT and W of
males and females ( p > 0.05; Table 1).
Males ranged from 34.8 to 61.0 cm LT, 51 of the 73
caught (69.9%) being determined mature. The smallest mature male measured 49.5 cm LT and the largest immature
catshark was 50.9 cm LT. Clasper length increased between
46.0 and 50.0 LT (Figure 3a). All males >51.0 cm LT were
mature. First maturity occurred at 81.1% of maximum
length (LTmax), and LT50 was estimated to be 50.8 cm LT
(Table 1). Females ranged from 32.2 to 56.7 cm LT. Of
the 40 examined, 25 (62.5%) were determined to be mature.
The smallest mature female measured 46.8 cm LT and the
Reproductive biology of catsharks off southern Africa
(a)
11.0
Clasper length (%)
10.0
Adult
Adolescent
Juvenile
9.0
8.0
7.0
6.0
5.0
4.0
30
35
40
45
50
55
60
65
LT (cm)
Oviducal gland width (%)
(b)
5.0
Adult
Adolescent
Juvenile
4.0
3.0
2.0
1.0
0.0
30
35
40
45
50
55
60
LT (cm)
(c)
1057
largest immature one was 48.1 cm LT. Shell gland width
increased between 45.0 and 48.0 cm LT (Figure 3b). All
females >48.5 cm LT were mature. First maturity was
at 82.5% of LTmax, and LT50 was estimated to be 48.3 cm
LT (Table 1).
The adult female sample size (n ¼ 25) was too small to
determine with any certainty a seasonality to the breeding
cycle, but mature oocytes and egg cases in utero were observed in catsharks caught in both summer and winter, indicating a protracted breeding season. Four of 25 adult
females (16%) contained a single egg case in each uterus.
One summer- and one winter-caught specimen each had
a single developing egg case, while two additional summer-caught catsharks each had a single, fully developed
egg case in each uterus. Only the right ovary of A. microps
is functional. The total number of mature oocytes present in
the species ranged from 7 to 8, with a mean diameter of
15e18 mm.
The egg cases of A. microps (Figure 3c) are small,
47e52 mm long (four fish) from anterior to posterior (excluding horns), broad, and fairly thick, with the posterior
width about 32e37% of case length and greatest case
height about 17e23% of case length and 53e67% of posterior case width. They have thin walls and are flat when
eggs are absent from the lumen; the waist of the case is
prominent in filled examples, but less obvious when the
cases are flat. Fine, straight, smooth longitudinal striations
or ridges are present on the dorsal and ventral surfaces of
the case, about 73 ridges being counted on the dorsal surface of one case. The lateral flanges of cases are narrow
(about 1 mm wide), flat, and without a T-shaped lateral surface, extending the length of the egg case. The anterior border of the case is nearly straight, broad, and transverse, with
very short 1 mm anterior horns that are straight, directed
anteriorly, with anterior tendrils absent. The posterior border is narrow and concave, and the posterior horns are very
short, stout, and curved medially towards each other. The
posterior tendrils are very short, curled, slender, filamentous, and less than the width of the posterior egg case.
The anterior and posterior respiratory fissures are dorsally
situated on the left side of the case and ventral on the right
side. The egg cases removed from preserved catsharks are
dark uniform green in colour.
Apristurus saldanha
Figure 3. Relationships for Apristurus microps between (a) clasper
length (% LT) and LT, and (b) oviducal gland width (% LT) and LT.
(c) Egg case. Iziko e South African Museum, SAM uncatalogued.
Ventral views with anterior end to left and showing fine smooth
striations and small posterior horns and tendrils. Egg cases removed from the oviducts of (A) a 520 mm female, ‘‘full’’ case
with anterior end somewhat damaged and showing prominent
waist, and (B) a 490 mm female, empty flattened case with anterior
end intact and showing small anterior horns. Scale bar ¼ 10 mm.
Photo LJVC.
A total of 95 specimens (45 males and 40 females) was collected. This was the largest of the three Apristurus species
commonly collected during the study. The overall F:M sex
ratio was 1:1.13, not significantly different from the expected 1:1 ratio ( p > 0.05). A significant difference was
found in the F:M ratio for adults, 1:2.25 (c2 ¼ 5.03,
d.f. ¼ 1, p < 0.05), and juveniles, 1:0.44 (c2 ¼ 4.69,
d.f. ¼ 1, p < 0.05), but not for adolescents ( p > 0.05).
Comparison of LTeW regressions between males and females showed a significant difference ( p < 0.05; Table 1).
D. A. Ebert et al.
(a)
10.0
Adult
Adolescent
Juvenile
9.0
8.0
Clasper length (%)
Males ranged from 33.5 to 88.5 cm LT, with 27 of 45
(60.0%) determined to be mature. Clasper length increased between 50.0 and 60.0 cm LT, and all males
>74.0 cm LT were considered mature (Figure 4a). The
smallest mature male measured 74.0 cm LT, and LT50
was estimated to be 69.2 cm LT (Table 1). The largest immature individual was 64.5 cm LT. First maturity was at
83.6% of LTmax (Table 1). Females ranged from 38.2 to
77.3 cm LT, with 12 of 40 (30.0%) mature. Shell gland
width increased between 65.0 and 70.0 cm LT, the smallest mature female measuring 70.0 cm LT and the largest
immature one measuring 69.0 cm LT (Figure 4b). First
maturity occurred at 90.6% of LTmax, and LT50 was estimated to be 69.5 cm LT (Table 1). Only the right ovary
of A. saldanha is functional. The total number of mature
oocytes ranged from 16 to 20, with a mean diameter ranging from 17 to 22 mm.
The egg cases of this species are unknown, and none
were found in utero during this study. However, five egg
cases from an unidentified scyliorhinid were brought up
at a bottom trawl station in an area and depth (near
Cape Point at 485 m) close to where A. saldanha was
caught at other trawl stations, so they may belong to
that species. These egg cases (Figure 4c) are strikingly different from those of Apristurus microps and Scyliorhinus
capensis, and are moderately large, 62e67 mm long
from anterior to posterior borders (excluding horns), broad
and fairly thick, with posterior width about 38e48% of
case length and greatest case height about 22e27% of
case length and 58e64% of posterior case width. The
egg cases are thick walled and do not flatten when eggs
are absent from the lumen. The waist is prominent in all
cases examined. The case is stout, straight, high, undulated, and rough longitudinal striations or ridges are conspicuous on the dorsal and ventral surfaces of the case,
giving it a rough overall texture, with about 25 ridges
counted on the dorsal surface of one case. The lateral
flanges of the egg cases are broad (about 4 mm wide),
ridged, rough, and without a T-shaped lateral surface extending the length of the egg case. The anterior border
of the case is broadly concave and the nearly transverse,
anterior horns are short, about 4 mm long, straight, thick,
and directed anteriorly; the anterior tendrils are absent,
but moderately long and narrow fibrous sheets of material
are present on the ventral surface of each anterior horn.
The posterior border of a case is narrow and concave,
with long, very stout, posterior horns that are curved
medially towards each other and anteroventrally below
the case. The posterior tendrils are long, curled, thick to
slender, filamentous, apparently longer than the egg case
length, and very adherent to each other and to the tendrils
of other cases. The anterior and posterior respiratory fissures are dorsally situated on the left side of the egg
case and ventrally on the right side. The deposited egg
cases, with hydroids sparsely attached, are dark green,
almost black in colour.
7.0
6.0
5.0
4.0
3.0
2.0
1.0
0.0
20
30
40
50
60
70
80
90
100
LT (cm)
(b)
Oviducal gland width (%)
1058
5.0
Adult
Adolescent
Juvenile
4.0
3.0
2.0
1.0
0.0
30
40
50
60
70
80
LT (cm)
(c)
Figure 4. Relationships for Apristurus saldanha between (a) clasper
length (%LT) and LT, and (b) oviducal gland width (%LT) and LT.
(c) Egg case. Iziko e South African Museum, SAM uncatalogued,
trawled at 485 m. Ventral view with anterior end to left and showing
strong rough ridges and strong posterior tendrils. Scale bar ¼ 10 mm.
Photo LJVC.
Reproductive biology of catsharks off southern Africa
Galeus polli
A total of 195 specimens (94 males and 101 females) was
caught during the surveys, and were fairly abundant off
southern Namibia. The overall F:M sex ratio was 1:0.93,
and it did not differ significantly from the expected unity
( p > 0.05). Comparison of the sex ratios of adults and adolescents, however, did show a significant difference, with
an F:M ratio of 1:0.65 (c2 ¼ 6.21, d.f. ¼ 1, p < 0.05) and
1:4.20 (c2 ¼ 8.65, d.f. ¼ 1, p < 0.05), respectively. The
sex ratio of juveniles showed no significant difference
( p > 0.05). Comparison of LTeW regressions between
males and females also revealed no significant difference
( p > 0.05; Table 1).
Males ranged from 19.3 to 36.2 cm LT, and 57 of 94
(60.6%) were determined to be mature, with LT50 estimated
at 30.3 cm LT (Table 1). The smallest mature male measured 30.2 cm LT, and the largest immature one measured
30.1 cm LT. Clasper length increased between 26.0 and
30.0 cm LT (Figure 6a). First maturity was at 83.7% of
LTmax (Table 1). Females ranged from 15.5 to 43.0 cm
LT, with 88 (87.1%) mature, the smallest measuring
29.5 cm LT; the largest immature female was 29.4 cm LT.
Shell gland width increased between 25.0 and 30.0 cm LT
(Figure 6b). First maturity was at 68.8% of LTmax, and
LT50 was estimated to be 29.6 cm LT (Table 1).
Galeus polli, unlike the other catsharks in this study,
gives birth to live young rather than by oviposition. The
number of mature ovarian oocytes ranged from 3 to 7,
with a mean diameter of the largest mature oocytes ranging
from 7 to 15 mm. Half (50%) of the adult females examined
10.0
Adult
Adolescent
Juvenile
9.0
Clasper length (%)
In all, 52 specimens (20 males and 32 females) were collected during the study. The overall F:M sex ratio of
1:0.63 did not differ significantly from unity ( p > 0.05).
Similarly, the sex ratios of adults, adolescents, and juveniles did not differ significantly ( p > 0.05). The LTeW
regressions of males and females were not significantly
different ( p > 0.05; Table 1).
Males ranged from 34.5 to 68.5 cm LT, with nine
(45.0%) of them mature, the smallest of which measured
48.8 cm LT; the largest immature Apristurus sp. measured
47.0 cm LT. Clasper length increased between 42.0 and
50.0 LT (Figure 5a), and first maturity was at 71.2% of
LTmax; LT50 was estimated to be 47.9 cm LT (Table 1).
Females ranged from 29.8 to 62.5 cm LT, with 17 (53.1%)
mature. Shell gland width increased between 45.0 and
50.0 cm LT (Figure 5b). The smallest mature female measured
48.5 cm LT, LT50 was estimated to be 47.5 cm LT, and the
largest immature measured 47.5 cm LT. First maturity was
at 77.6% of LTmax (Table 1). The same as the other species
of Apristurus, only the right ovary is functional. The total
number of mature oocytes from five females ranged from 3
to 5, with a mean diameter ranging from 9 to 14 mm. Egg
cases were not found in any females during the study.
(a)
8.0
7.0
6.0
5.0
4.0
3.0
2.0
30
40
50
60
70
80
LT (cm)
(b)
Oviducal gland width (%)
Apristurus sp.
1059
5.0
Adult
Adolescent
Juvenile
4.0
3.0
2.0
1.0
0.0
20
25
30
35
40
45
50
55
60
65
LT (cm)
Figure 5. Relationships for Apristurus sp. between (a) clasper
length (%LT) and LT, and (b) oviducal gland width (%LT) and LT.
carried either fully developed embryos or uterine eggs. In
all, 32 of 88 adults (36.4%) carried embryos, with the number per right uterus ranging from 2 to 6 (mean s.d.
4.4 0.9), and the left uterus from 3 to 7 (4.5 1.1). There
was no significant difference between the number of embryos in the left and the right uterus (t ¼ 0.89; d.f. ¼ 31;
p > 0.38). Litter size ranged from 5 embryos in a 33.3 cm
catshark to 13 in a 37.0 cm individual (Figure 6c). The litter
size to LT relationship showed a weak linear correlation
(r2 ¼ 0.35) of increasing litter size with increasing maternal
size (Figure 6c). The largest embryos were 11.7 cm, and the
smallest free-swimming catshark caught was 15.5 cm LT.
Embryo LT increased with closeness to the cloacal opening,
those close to that opening being slightly larger, by up to
1.0 cm, than those closer to the oviducal gland. A random
subsample of 60 embryos (32 males and 28 females) from
eight litters had a sex ratio (M:F) of 1:0.9, not significantly
different from unity ( p > 0.05). Additionally, 12 females
carried only uterine eggs, the number in the right uterus
ranging from 3 to 6 (4.1 1.2) and in the left also ranging
from 3 to 6 (4.3 1.2), but with no significant difference
in the observed number between the left and right uterus
(t ¼ 0.80; d.f. ¼ 11; p > 0.44). The remaining 44 mature females had spent or empty uteri. Surveys in Namibian waters
1060
(a)
D. A. Ebert et al.
12.0
Adult
Adolescent
Juvenile
Clasper length (%)
10.0
8.0
6.0
4.0
2.0
0.0
10
15
20
25
30
35
40
LT (cm)
Oviducal gland width (%)
(b)
2.5
Adult
Adolescent
Juvenile
2.0
1.5
1.0
0.5
0.0
0
10
20
30
40
50
LT (cm)
(c)
13
Embryo number
12
11
10
9
8
7
6
5
4
28
30
32
34
36
38
40
42
44
LT (cm)
Figure 6. Relationships for Galeus polli between (a) clasper length
(%LT) and LT, (b) oviducal gland width (%LT) and LT, and (c) total
number of embryos and LT for gravid specimens.
were conducted only during summer, so no comparative
seasonal data were available to determine the breeding cycle
of the species.
Scyliorhinus capensis
A total of 192 specimens was caught, 95 males and 97
females. The F:M sex ratios overall and for all maturity
groups compared did not show any significant difference
( p > 0.05). LTeW regressions of males and females were
significantly different ( p < 0.05; Table 1).
Males ranged from 22.3 to 102.0 cm LT, and 14 of 95
(14.7%) were mature. Clasper length increased between
75.0 and 80.0 cm LT, with the smallest mature and the largest immature males measuring 84.0 and 82.5 LT, respectively (Figure 7a). First maturity was at 82.4% of LTmax,
and LT50 was estimated to be 82.9 cm LT (Table 1). Females
ranged from 16.6 to 88.0 cm LT, with 14 of 97 (14.7%) determined to be mature. Shell gland width increased between
65.0 and 75.0 cm LT, and the smallest mature catshark measured 75.0 cm LT, with LT50 estimated at 75.6 cm LT
(Figure 7b). The largest immature specimen measured
80.0 cm LT. First maturity was at 85.2% of LTmax (Table 1).
Adult females carried between 9 and 12 mature oocytes, with
a mean diameter of 17e21 mm. Three females (21.4%)
had single egg cases in each uterus, all caught during winter.
The egg cases of Scyliorhinus capensis (Figure 7c) are
large, 80e84 mm long from anterior to posterior borders
(excluding horns), broad and flat, with posterior width
about 42e43% of case length and greatest case height
about 16e20% of case length and 37e47% of posterior
case width. The cases have thick, smooth walls, with longitudinal striations and ridges that are weak and poorly defined or absent. The lateral flanges are broad (about 2 mm
wide), with a low T-shaped lateral surface extending the
length of the egg case. The anterior border is nearly
straight, broad, and transverse, with long anterior horns,
nearly the same width as the anterior border, but curved
and directed medially, each having a strong, greatly elongated (longer than case length), loosely to tightly curled
tendril that extends medially then posteroventrally below
the case. The posterior border of the egg case is broad
and concave, with long, stout, posterior horns spiralling medially, laterally, and posteroventrally, giving rise to the
long, stout to slender, strongly curled posterior tendrils
that extend ventrally and anteriorly under the egg case.
The highly adherent tendrils, both anterior and posterior,
tend to catch on to one another, on to the tendrils of other
egg cases, and/or on to the substratum. The anterior and
posterior fissures are dorsally situated on the left side of
the egg case and ventrally on the right side. The egg cases
removed from preserved specimens are uniformly a pale to
dark green.
Discussion
Oviparity is the reproductive mode for most members of the
family Scyliorhinidae, with the genus Galeus being an exception. Members of that genus may exhibit either oviparity
or aplacental viviparity. Moreover, the egg-laying members
of the genus may exhibit either single or multiple oviparity;
a condition considered primitive among elasmobranchs
(Nakaya, 1975; Dulvy and Reynolds, 1997; Iglesias et al.,
Reproductive biology of catsharks off southern Africa
(a)
12.0
Adult
Adolescent
Juvenile
Clasper length (%)
10.0
8.0
6.0
4.0
2.0
0.0
0
20
40
60
80
100
120
LT (cm)
Oviducal gland width (%)
(b)
5.0
Adult
Adolescent
Juvenile
4.0
3.0
2.0
1.0
0.0
0
20
40
60
80
100
LT (cm)
(c)
Figure 7. Relationships for Scyliorhinus capensis between (a)
clasper length (%LT) and LT, (b) oviducal gland width (%LT) and
LT. (c) Egg case. Iziko e South African Museum, SAM uncatalogued, removed from oviduct, size of mother not recorded. Ventral
view with anterior end to left and showing strong anterior and posterior horns and long curled tendrils. Scale bar ¼ 10 mm. Photo LJVC.
2002; Carrier et al., 2004). All oviparous species in this
study appear to exhibit single oviparity, with only a single
egg case deposited in each uterus at a time. This reproductive mode is consistent for all known species of the genera
Apristurus and Scyliorhinus (Compagno, 1988).
Members of the genus Galeus are reproductively more
advanced than other catshark genera such as Apristurus
1061
and Scyliorhinus, the reproductive mode of these last two
genera being considered to be primitive (Springer, 1979;
Iglesias et al., 2002). It has been suggested that the viviparous G. polli is, in a sense, exhibiting an extreme example
of multiple oviparity (Springer, 1979). Of the 17 species
within the genus Galeus, only G. polli definitely exhibits
aplacental viviparity, 11 species exhibit single oviparity,
two show multiple oviparity, and the reproductive mode
for three is unknown (Springer, 1979; Compagno, 1984;
Compagno and Stevens, 1993; Chen et al., 1996; Horie
and Tanaka, 2000; Konstantinou et al., 2000; Iglesias
et al., 2002). Galeus arae was initially thought to exhibit
aplacental viviparity (Bullis, 1967), but recent evidence
has revealed the species to be oviparous (Konstantinou
et al., 2000). An erroneous report by Myagkov and Kondyurin (1978) claimed that A. saldanha exhibited aplacental
viviparity. However, the embryos depicted in Figure 1 of
Myagkov and Kondyurin (1978) are actually G. polli.
Also, based on the present study, the adult female sizes
of the Myagkov and Kondyurin (1978) study were too
small, at 39.5 and 37.3 cm LT, to be A. saldanha.
Males of all species studied here attained first maturity at
a greater LT than females. Further, males matured at a slightly
larger LT50 than females in A. microps and S. capensis, with
LT50 broadly similar in the other species. Studies on catsharks elsewhere have indicated that males of many species
mature at about the same size or often slightly larger than females (Compagno, 1984; Cross, 1988; Richardson et al.,
2000). This is contrary to the condition found in most viviparous sharks, females tending to mature larger than males.
Cortes (2000), in a survey of shark life history patterns,
found that of 162 species studied, males matured larger in
just 23 (14.2%) cases. However, males of 9 of the 17 species
of catshark included in the survey matured at a size equal to
or greater than that of the female (Cortes, 2000).
Besides maturing at a size similar to or larger than
females, males of the four oviparous species grew to a larger
LTmax than females. Female G. polli, the lone viviparous
species, grew larger than males. This appears to be a common
characteristic among oviparous catsharks, males tending
to grow to about the same size or larger than females
(Compagno, 1984; Castro et al., 1988; Cross, 1988; Taniuchi, 1988; Richardson et al., 2000).
Elasmobranchs separate by size, maturity status, and sex
(Bullis, 1967; Springer, 1967; Ebert, 2003), but the relatively even sex ratios found for most species indicated that
both sexes of each maturity category were relatively evenly
distributed within the study area. The overall sex ratio of
four of the five species studied here approximated 1:1,
only A. microps significantly biased towards males. The
sex ratios of Apristurus sp. and S. capensis were not significantly different for any maturity category. Adult male
A. microps and A. saldanha and adolescent G. polli were
found in greater proportions than females, whereas adult
female G. polli and juvenile A. saldanha were found in
a higher proportion than males. These differences in the
1062
D. A. Ebert et al.
sex ratios for some species may be associated with depth
distribution, geography, habitat, season, or temperature
(Compagno et al., 1991). However, given the relatively
few specimens captured, and the time frame over which
they were caught, the differences in the sex ratios may be
simply a sampling artefact. Further sampling may reveal
more about the distribution of these catsharks off
southern Africa.
Intraspecific lengtheweight relationships of males and
females were similar, but it is not known whether males
and females grow at the same rate because the age of these
sharks has not yet been determined. Studies on catsharks
elsewhere have shown that males and females of the
same species exhibit similar growth characteristics to those
found here (Castro et al., 1988; Cross, 1988). However, attempts to age scyliorhinids, particularly those of the genera
studied here, have to date met with limited success (Castro
et al., 1988; Cross, 1988; Correia and Figueiredo, 1997;
Cortes, 2000).
All species studied, except male Apristurus sp. and female
G. polli, matured at a length >75% LTmax. Once mature, the
oviparous females appear to grow little. Holden (1974) observed that most elasmobranchs matured at between 60%
and 90% of their maximum length. Cortes (2000), in a separate study, and supporting Holden’s (1974) generalization,
found that the average ratio of length at maturity for both
males and females was 75% of the shark’s maximum length.
Although the reproductive modes were not separated into
oviparous and viviparous species, it appears that viviparous
species may mature on average at a slightly smaller LT relative to LTmax, whereas oviparous species may mature on
average at a higher LT relative to LTmax.
Estimates of LT50 were lower than the smallest mature
male and female A. saldanha and Apristurus sp. and mature
male S. capensis observed. However, the size differences
were relatively small, most likely related to sample size
or sampling bias. Given bigger samples, these theoretical
estimates of maturity would likely be more reflective of
LT50 within the population, and smaller mature individuals
would be found, so decreasing the size at first maturity.
Although no determination of the time egg cases are held
in utero could be made from our data, studies elsewhere reveal that in single egg case oviparity, the time an egg case
is held until it is deposited may be just a few days (Hamlett
and Koob, 1999). In species that exhibit multiple oviparity,
the egg capsules are retained in utero for up to several
months, while the embryos begin to develop prior to oviposition (Iglesias et al., 2002). In single oviparity, embryonic
development occurs only after deposition (Hamlett and
Koob, 1999).
Elasmobranch egg cases can be a useful tool for identifying individual species (Ishiyama and Ishihara, 1977; Gomes
and de Carvalho, 1995). Of the four oviparous species discussed here, the egg cases of three have not been described
or illustrated before. Although catshark egg cases have
rarely been observed in situ, variations in egg case structure
between species may indicate a difference in the habitat
where they are deposited. For example, the egg case of
A. microps has minute tendrils, whereas those of other
Apristurus species, e.g. A. brunneus and A. laurussonii
(Cox, 1963; Iglesias et al., 2002), may have very long tendrils. This would suggest a possible difference in preferred
habitat. An egg case with long tendrils suggests that the tendrils are wrapped around structures such as gorgonian
corals, whereas those with minute tendrils may deposit
the egg cases in cracks and crevices on rocky reefs (Castro
et al., 1988). The egg case of S. capensis, with its long,
highly adherent tendrils, strongly suggests that it may use
these tendrils as a means to anchor the egg case to a firm
substratum such as a gorgonian or other hard structure.
This has been observed for the chain dogshark (S. retifer;
Castro et al., 1988). The lesser-spotted dogfish (S. canicula)
primarily attaches its egg cases to macroalgae and sessile
erect invertebrates such as sponges, hydroids, and bryozoans (Ellis and Shackley, 1997).
The number of G. polli embryos, as shown in the present
study, appears to increase in relation to size of the female.
Although G. polli is the only confirmed viviparous member
of the genus, two other Galeus species are known to exhibit
multiple oviparity: G. melanstomus, with up to 13 egg capsules in the oviducts at one time, and G. atlanticus, which
may have up to 9 (Nakaya, 1975; Munoz-Chapuli and Perez
Ortega, 1985; Iglesias et al., 2002). However, it is not
known whether the number of egg cases increases with
size of the female in either of these cases of multiple oviparity. An increase in embryo number with female size
has been observed in other viviparous elasmobranchs, notably members of the family Triakidae, including the soupfin
shark or tope (Galeorhinus galeus), the brown smoothhound (Mustelus henlei), the smoothhound (M. mustelus),
the whitespotted houndshark (M. palumbes), the spotted
gully shark (Triakis megalopterus), and the leopard shark
(T. semifasciata; Ripley, 1946; Ackerman, 1971; Smale
and Compagno, 1997; Smale and Goosen, 1999; Ebert,
2003; Ebert and Ebert, 2005). These are all sharks of
medium size, ranging between 1.2 and 2.0 m LTmax
(Compagno et al., 1989; Ebert, 2003). To our knowledge,
increase in litter size associated with female size for
G. polli has not been observed in such a small shark species. The embryos of G. polli averaged about 30% of the
length of the female, whereas the triakid embryos referred
to above all averaged <30% of the length of the female
(Ripley, 1946; Ackerman, 1971; Smale and Compagno,
1997; Smale and Goosen, 1999; Ebert and Ebert, 2005).
Further, the average birth size for the 12 catshark species
discussed by Cortes (2000) was approximately 5% of the
average length of the female. Cortes (2000) commented
that, on average, elasmobranch offspring were 25% of the
length of the female at birth.
Neonates for the four oviparous species were noticeably
absent from the study. It may be that at birth, neonates
migrate into areas not sampled effectively by the trawl
Reproductive biology of catsharks off southern Africa
used, e.g. rough grounds or into midwater, and remain there
for an unspecified period of time. The scyliorhinids Apristurus brunneus and Parmaturus xaniurus apparently migrate up into the water column after birth and remain
there until approximately 38 and 23 cm LT, respectively,
whereupon they return to their more demersal lifestyle
(Lee, 1969; Jones and Geen, 1977; Springer, 1979; Cross,
1988; Ebert, 2003). Based on the diet of the three Apristurus species studied here, at least that of the adults, all feed
in epipelagic waters (Ebert et al., 1996). Neonates of G.
polli, contrary to these other species, appear to have a demersal lifestyle throughout their life, because neonates
were captured during bottom trawling. However, given
the extremely small size at birth and generally small size
even at LTmax, they appear to be less vulnerable to trawl
fisheries than most other, larger, elasmobranchs in the
region.
Seasonality in breeding cycle was difficult to determine
given the small sample of adult females collected during
the survey and the increased sampling effort during summer. Galeus polli, for example, was collected only during
summer, because this species’ southerly distribution extended only to the northern extreme of the survey area.
Sampling surveys conducted during winter did not extend
far enough north and into its range. Likewise, most of the
deep trawl sampling took place during summer, biasing
the seasonal data for the deeper-occurring Apristurus species. However, the occurrence of egg cases in both summer
and winter surveys for A. microps suggests that they may
not have a defined breeding season. The only S. capensis
egg cases found were taken during winter, although the
sample size was too small to draw firm conclusions. Studies
on other catsharks, including A. brunneus, Galeus sauteri,
H. regani, P. xaniurus, and S. canicula, indicate that they
all reproduce throughout the year, but with seasonal peaks
in egg production (Cross, 1988; Chen et al., 1996; Ellis and
Shackley, 1997; Richardson et al., 2000). Clearly, future
studies need to be carried out seasonally and to focus on
changes in mature oocyte number, largest diameter, gonad
weight, fecundity, and seasonal peaks in egg deposition.
Prior to this study, reproductive information for these
catshark species was largely unknown, or based on anecdotal accounts. This study, although limited, has provided
the first information on the reproductive biology of these
five southern African catsharks. Four of the five species
are endemic and possibly have a limited distributional
range. Therefore, intensive fishing pressure on their preferred habitat may have a far-reaching impact on their population structure.
Acknowledgements
We thank A. I. L. Payne (now with Cefas), C. J. Augustyn,
M. R. Lipiński, A. Badenhorst, R. W. Leslie, B. Rose (now
with Irvin and Johnson), P. F. Sims, and A. A. Robertson
1063
of MCM (formerly Sea Fisheries Research Institute), Cape
Town, the late Capt. D. Krige and the officers and crew of
the FRS ‘‘Africana’’, B. Ranchod, E. Matama, and S. Matama of the South African Institute for Aquatic Biodiversity
(SAIAB, formerly the J. L. B. Smith Institute of Ichthyology,
JLBSII), P. White, M. Boon, and A. Macras of the Shark
Research Center at SAIAB and the South African Museum
(I-SAM, now Iziko e South African Museum), T. Hecht of
the Department of Ichthyology and Fisheries Sciences, Rhodes University, M. A. Compagno-Roeleveld (I-SAM), and
G. Cailliet and C. Rinewalt, Pacific Shark Research Center
(PSRC) and Moss Landing Marine Laboratories (MLML).
DAE thanks NOAA/NMFS for their support of the National
Shark Research Consortium and PSRC, and the International
Union for the Conservation of Nature Shark Specialist Group
(IUCN-SSG) for support during the final phase of this project. During the fieldwork for this study, DAE and PDC
were supported by South Africa’s Foundation for Research
Development, now the National Research Foundation
(NRF). LJVC’s research funding was provided by South
Africa’s Council for Scientific and Industrial Research,
NRF, JLBSII, I-SAM, and the IUCN-SSG.
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