Reproductive Aspects of The Atlantic Angel Shark

Journal of Fish Biology (2010) 76, 1682–1695
doi:10.1111/j.1095-8649.2010.02608.x, available online at www.interscience.wiley.com
Reproductive aspects of the Atlantic angel shark

Squatina dumeril
I. E. Baremore
National Marine Fisheries Service, Southeast Fisheries Science Center, 3500 Delwood Beach
Road, Panama City, FL 32408, U.S.A.
(Received 20 April 2009, Accepted 1 February 2010)
Atlantic angel sharks Squatina dumeril were collected by fishery-dependent and independent trawls
from 2002 to 2008 for reproductive analysis. Female S. dumeril have only one functional ovary
(left), with an average litter size of seven pups. The reproductive cycle is at least biennial, though
the seasonality of vitellogenesis could not be determined. Gestation is c. 12 months, and embryo
data support a seasonal trend in reproduction, with parturition occurring in the
spring months (February to June). Mature male S. dumeril have spines on the outer margins
of their pectoral fins, and there is an apparent peak in gonad size in the spring. The total length
at which 50% of the population is mature is 85·8 and 92·9 cm for females and males,
respectively. Journal compilation © 2010 The Fisheries Society of the British Isles
No claim to original US government works
Key words: elasmobranch; lecithotrophic viviparity; maturity; senescence; Squatinidae.
INTRODUCTION
Information on reproductive biology is crucial for quantitative analysis of popula-
tions. Measures of biological productivity of elasmobranchs are derived from repro-
ductive rates and are required for stock assessments, demographic assessments and
ecological risk assessments (Cortés, 1998; Walker, 2005). These types of assessments
use key variables of reproduction such as size at birth, fecundity at size, proportion
of animals in the population that are mature and age and size of first reproduction.
Angel sharks (Squatinidae) are dorso-ventrally flattened, benthic elasmobranchs
that occur circumglobally in temperate and tropical marine waters (Compagno, 1984).
The reproductive method of angel sharks is lecithotrophic viviparity (Hamlett et al.,
2005); oocytes are internally fertilized, developing embryos receive nourishment
from an external yolk sac and pups are born live once the external yolk sac is
absorbed. A small internal yolk sac is present around the time of birth and is pre-
sumably absorbed as external feeding begins.
Though the reproductive method of angel sharks is known, aspects of their repro-
duction vary by species. For example, the angel sharks Squatina californica Ayres
(Natanson & Cailliet, 1986), Squatina guggenheim Marini (Colonello et al., 2006)
Tel.: +1 850 234 6541; fax: +1 850 235 3559; email: Ivy.Baremore@noaa.gov
1682
Journal compilation © 2010 The Fisheries Society of the British Isles
R E P RO D U C T I O N O F S Q UAT I NA D U M E R I L 1683
and Squatina occulta Vooren & da Silva (Sunye & Vooren, 1997) have only one
functional ovary (left), while Squatina tergocellata McCulloch (Bridge et al., 1998),
Squatina oculata Bonaparte, Squatina squatina (L.) (Capapé et al., 1990, 2002)
and Squatina africana Regan (Shelmerdine & Cliff, 2006) have two functional
ovaries. Most reports agree that angel sharks have a 10–12 month gestation period
(Natanson & Cailliet, 1986; Capapé et al., 1990, 2002; Sunye & Vooren, 1997;
Bridge et al., 1998; Colonello et al., 2006; Shelmerdine & Cliff, 2006). Studies have
estimated ovulation cycles to be biannual (Awruch et al., 2008), annual (Natanson &
Cailliet, 1986), biennial (Bridge et al., 1998; Shelmerdine & Cliff, 2006) and trien-
nial (Colonello et al., 2006). Of the published studies on the reproduction of angel
sharks, few have definitively described the ovulation cycle, and most expressed some
degree of uncertainty as to the seasonality of oocyte development (i.e. vitellogenesis)
and fertilization.
Atlantic angel sharks Squatina dumeril LeSueur are found along the coast of the
north-western Atlantic Ocean, ranging from Massachusetts to Jamaica and Venezuela
and throughout the Gulf of Mexico (McEachran & Fechhelm, 1998). Squatina
dumeril are currently only caught as by-catch in trawl fisheries in the Gulf of
Mexico and U.S. South Atlantic Ocean but are listed as prohibited (no commer-
cial landings allowed) because of a lack of available life-history information and the
precautionary approach to fisheries management (NMFS, 1993). The aim of this arti-
cle is to describe the reproductive cycle, fecundity and to give general reproductive
information for S. dumeril in the northern Gulf of Mexico.
MATERIALS AND METHODS

Squatina dumeril were collected from a commercial trawl vessel in the north-eastern Gulf
of Mexico (n = 944), and from fishery-independent trawl surveys conducted throughout the
northern Gulf of Mexico (n = 147) from November 2002 to November 2008. Most S. dumeril
collected for this study were caught between 90 and 300 m in depth, and sampling locations of
the two sources overlapped in time and area (Fig. 1). Samples from fishery-dependent trawls
were collected at the processing plant as the catch was sorted, while fishery-independent
samples were collected as the trawl came aboard the vessel. Fish were either placed on ice or
frozen whole and transported to the Panama City, Florida, National Oceanic and Atmospheric
Administration (NOAA) Fisheries Laboratory for processing. They were measured for fork
(LF ) and total (LT ) lengths (±0·5 cm) and weighed (±0·02 kg).
Missing LT measurements (n = 12) were converted from LF using the equation LT =
1·0514 LF − 0·1183 (n = 1069, r 2 = 0·99, P < 0·001), and mass (M) values (n = 12) were
calculated with the equation M = [6·696 × 10−6 ]LT 3·033 (n = 988, r 2 = 0·99, P < 0·001).
The length and mass data were obtained from ongoing life-history research for this species
using the same sampling sources, and regressions were chosen based on best fit: lowest mean-
square error, highest r 2 , examination of residuals. There was no significant difference in the
regressions between males and females (ANCOVA, P > 0·05), and gravid females were not
included in the length and mass regressions.
Maturity was assessed by internal and external examination based on standardized methods
for elasmobranch reproduction (Walker, 2005). Mature females possessed well-developed
nidamental glands, yolked oocytes in the ovary >5 mm in diameter and had uterine widths
>10 mm, while males that possessed calcified claspers and spines on the outer margins of
the pectoral fins were considered mature. Females were only considered mature (able to
reproduce) if all three of the previous conditions were met. Females were considered in
maternal condition only if gravid or with a uterine width >20 mm and oocyte diameter
>15 mm, indicating that vitellogenesis was advanced and the female would presumably be
Journal compilation © 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 76, 1682–1695
1684 I. E. BAREMORE
United States
30° 0'
25° 0'
Mexico 20° 0'
100° 0' 95° 0' 90° 0' 85° 0' 80° 0'
Fig. 1. Sampling area in the northern Gulf of Mexico. The shaded area represents the approximate area
sampled by fishery-independent surveys, while the area in the oval represents approximate locations for
fishery-dependent samples in the U.S. Gulf of Mexico.
gravid within the year. Juvenile females’ nidamental glands could not be distinguished in the
oviducts, and their ovaries possessed only small (<5 mm), un-yolked oocytes, while juvenile
males lacked calcified claspers and spines on the margins of the pectoral fins.
Upon dissection, several measurements were taken for reproductive analysis from all
mature and sub-adult animals and from a sub-set (n = 62 females and 112 males) of juve-
niles. For females, the length (±1 mm), width and mass of the left ovary (±0·1 g), and the
diameter of the largest oocyte (DO ) of the left ovary was recorded, along with the nidamental
gland width, and the width of the uterus (WU , ±1 mm). When present, pups were counted per
uterus, then sexed, measured for stretched total length (LTS , ±0·1 cm) and weighed without
their external yolk sacs. For males, clasper length from the outer margin of the anal fin was
recorded (±1 mm), as was the length, width (WT ) and mass (±0·1 g) of the left testis.
Sex-specific maturity ogives were constructed to determine the LT at which 50% of the
animals within the population were mature (LT50 ). The relationship is described with a logis-
tic equation by the maximum likelihood method: Y = 1[e(a+bLT ) ]−1 , where Y are binomial
maturity data (0, juvenile; 1, mature). An additional ogive of females in maternal condition
was also produced (Walker, 2005), and a likelihood ratio test was used to test for differences
in size at maturity between the sexes and between female ogives.
A gonado-somatic index (IG ) was calculated for females and males from: IG = 100
MG M −1 , where MG is the gonad mass, and plotted by month to visually assess seasonal
trends in reproduction. Additionally, scatter plots of the uterine width index (IUW ), calculated
from: IUW = 100 WU LT −1 , and DO and WT by month were constructed. ANOVA tests of IG
among months were used to determine whether differences were significant over the course
of the year using the PROC GLM procedure (SAS Inst. Inc.; www.sas.com). Levene’s test
(Levene, 1960) was used to assess homogeneity of the variance. The number of pups per
female was also plotted with maternal LT to examine changes in fecundity with size.
RESULTS
M AT U R I T Y E S T I M AT E S A N D S I Z E R E L AT I O N S H I P S
In total, 1091 S. dumeril were examined for maturity state (Fig. 2), while further
reproductive analysis was performed on 62 juvenile and 62 mature females, and 112
juvenile and 72 mature males. Males and females were collected in nearly equal
numbers within every size class, though more males were collected than females
at the largest sizes from the fishery-dependent source. Fishery-independent samples
showed a slight bimodality in LT frequency, but the distribution was similar for
males and females (Fig. 2).
Females matured at a smaller size than males, with LT50 of 86·9 ± 6·2 and 92·9
± 7·7 cm (mean ± s.e.) for females (n = 535) and males (n = 556), respectively
[Fig. 3(a)]. A likelihood ratio test showed a significant difference in the size of
maturity between the sexes (P < 0·001). The LT50 of females in maternal condition
was 94·6 ± 4·7 (mm) [Fig. 3(b)], which was significantly larger than LT50 for all
females (P < 0·001).
F E M A L E R E P RO D U C T I V E C H A R AC T E R I S T I C S
Mature females showed wide ranges in ovary mass and oocyte diameter through-
out the year. Only the left ovary of S. dumeril females is functional, and the
ovary undergoes a dramatic increase in size during vitellogenesis (IG = 0·001–0·09,
120
100
80
Frequency
60
40
20
0
20 40 60 80 100 120
LT (cm)
Fig. 2. Total length (LT ) frequency of Squatina dumeril sampled for maturity assessment for females
( , fishery-dependent; , fishery-independent) and males ( , fishery-dependent; , fishery-independent).
1686 I. E. BAREMORE
1·0
(a)
0·8
0·6
0·4
0·2
Proportion mature
0·0
0 20 40 60 80 100 120
1·0
(b)
0·8
0·6
0·4
0·2
0·0
20 40 60 80 100 120
LT (cm)
Fig. 3. (a) Maturity ogive for female ( ) and male ( ) Squatina dumeril [total lengths at 50% maturity (LT50 )
were 85·8 and 92·9 cm for females and males, respectively] and (b) maternity ogive female S. dumeril
(LT 50% maternal condition was 94·6 cm).
DO = 5·5–95 mm) [Fig. 4(a), (b)], filling nearly the entire body cavity just before
ovulation. Because gravid females did not exhibit signs of oocyte development dur-
ing gestation, the reproductive cycle is at least biennial [Fig. 4(a)]. One gravid female
caught in July had a high IG (0·04) and oocyte diameter (95 mm) values [Fig. 4(a),
(b)]; however, this female appeared to be in mid-ovulation, as both uteri contained
0·12 (a) 100 (b)
0·10
80
0·08
60
0·06
IG
DO (mm)
0·04 40
0·02

20
0·00
0
0 1 2 3 4 5 6 7 8 9 10 11 12 0 1 2 3 4 5 6 7 8 9 10 11 12
30 0·10 (d)
(c)
25 0·08
20 0·06
IUW
15 0·04
R E P RO D U C T I O N O F S Q UAT I NA D U M E R I L
Nidamental width (mm)

10 0·02
5 0·00
0 1 2 3 4 5 6 7 8 9 10 11 12 0 1 2 3 4 5 6 7 8 9 10 11 12
Month
Fig. 4. (a) Gonado-somatic index (IG ) of gravid ( , n = 15) and mature, non-gravid ( , n = 47), (b) diameter of the largest oocyte (DO ) of gravid ( , n = 15) and mature,
non-gravid ( , n = 46), (c) nidamental width of gravid ( , n = 15) and mature, non-gravid ( , n = 46) and (d) uterine width index (IUW ) of gravid ( , n = 15) and
1687
mature, non-gravid ( , n = 47) Squatina dumeril by month (January to December, 1–12).

1688 I. E. BAREMORE
fertilized yolk sacs with germinal discs, along with two pre-ovulatory oocytes in the
ovary. Ovulation occurred at a DO of 60–95 mm.
The nidamental glands of juvenile S. dumeril were difficult to distinguish from
the thread-like uteri. Nidamental gland widths of mature females ranged from 10·2
to 28·5 mm (non-gravid) and 13·5 to 22·0 mm (gravid) [Fig. 4(c)]. WU and DO were
the best indicators of maturity in females, with mature females having WU > 10 mm
and DO > 5 mm. Non-gravid IUW values ranged from 0·004 to 0·070 [Fig. 4(d)],
though the highest value was from a female with distended uteri, indicating that she
had either aborted or recently pupped. IUW and nidamental gland widths did not
show a trend across months for gravid or non-gravid females [Fig. 4(c), (d)].
Gestation is c. 12 months, with parturition occurring from February to June
[Fig. 5(a)]. Pups with only internal yolk sacs and very reduced external yolk sacs
were observed between 25 and 30 cm LT , and the smallest free-swimming (no exter-
nal yolk sac) pup was 27 cm LT , therefore the approximate size at birth is within
this range. The only near-term pups (>20 cm LT ) collected were aborted embryos,
as determined by the presence of external yolk sacs. Litter size ranged from four
to 10 pups, with mean ± s.d. of 7·4 ± 2·0 pups per female, and litter size did not
appear to increase with female size [Fig. 5(b)]. Only 15 gravid females, however,
were collected in the course of this study; hence, no regression analyses were run to
test this hypothesis. Approximately 24% of mature females collected were gravid.
Seasonal trends in oocyte development were unclear. No significant differences
were detected in the IG (ANOVA, n = 45, P > 0 · 05) by month. Embryo data,
however, show a clear seasonal trend in embryo growth and suggest that pups are
born from February to June [Fig. 5(a)]. Pups with small internal yolk sacs only were
observed in April, May and June.
M A L E R E P RO D U C T I V E C H A R AC T E R I S T I C S
Mature males exhibited folding of one or both testes and had highly coiled and
compacted spermatozoan packets in the epididymedes. Spines were present on the
outer margins of the pectoral fins of mature males only, and their presence was
as reliable an indicator of maturity as calcification of the claspers. The testes of
mature males were often quite different in length and mass in the same animal, and
often one testis was highly folded while the other was straight and smooth. Highly
coiled and compacted spermatozoan packets were prominent in the epididymedes of
mature males year round. Differences were detected in monthly IG values (ANOVA,
n = 72, P < 0·001), with a peak in the spring [Fig. 6(a)], but WT did not show a
trend [Fig. 6(b)].
DISCUSSION
Females matured at a significantly smaller size than males, which has not been
reported for angel sharks and is rare among elasmobranchs (Cortés, 2004). In general,
female sharks grow more slowly and reach maturity at a larger size (and older age)
than males (Cortés, 2000). This bimaturism can be attributed to the necessity of
partitioning of resources to reproduction rather than somatic growth, and the need
for a larger body size to carry pups. It is unclear why S. dumeril females mature at
35 (a)
30
25
20
Embryo L TS (cm)
15
10
0 1 2 3 4 5 6 7 8 9 10 11 12
Month
12
(b)
10
8
Number of pups
0
90 92 94 96 98 100 102 104 106 108
Maternal L T (cm)
Fig. 5. (a) Squatina dumeril embryo total stretched length (LTS ) by month (n = 15 litters, 23 individuals
aborted). Months on the x-axis are January to December (1–12). (b) Number of embryos by maternal
total length (LT ) (n = 15).
1690 I. E. BAREMORE
0·040
(a)
0·035
0·030
0·025
IG (%)
0·020
0·015
0·010
0·005
0 1 2 3 4 5 6 7 8 9 10 11 12
35
(b)
30
25
WT (mm)
20
15
10
5
0 1 2 3 4 5 6 7 8 9 10 11 12
Month
Fig. 6. (a) Gonado-somatic index (IG ) of male Squatina dumeril by month (n = 72). (b) Testis width (WT ) of
males by month (n = 72). Months on the x-axis are January to December (1–12).
a smaller size than males; however, because fecundity does not appear to increase
with increasing maternal size, the need for increased size may be less important in
this species. It is also possible that more than one population was sampled, thereby
confusing the results. The vast majority of samples in this study, however, were
from a fishery-dependent trawl, which surveyed a very limited area (Fig. 1) at depths
between 90 and 200 m. While it is possible that some of the largest size classes were
under sampled by this survey, the animals around the predicted size at maturity were
well represented and therefore these estimates are probably robust.
Size at maternal condition was significantly larger than size at first maturity,
which was expected, because of the relatively small proportion of mature females
that were in maternal condition (Walker, 2005). Maternity ogives are useful for
estimation of the size and proportion of females that are in reproductive condition at
any given time, and are especially important for population assessments of species
with complex or asynchronous reproductive cycles (Braccini, 2006) because of the
potential to overestimate recruitment.
Females exhibited wide ranges of IG , IUW and DO within months. This was also
observed in S. guggenheim in South America (Colonello et al., 2006) and S. africana
in South Africa (Shelmerdine & Cliff, 2006); however, the authors interpreted these
findings differently. Colonello et al. (2006) used multivariate analysis to provide
evidence of a 3 year cycle (2 years of vitellogenesis, 1 year of gestation), while
Shelmerdine & Cliff (2006) described the reproductive cycle as ‘weakly seasonal’
and biennial, with an approximate gestation period of 1 year. Awruch et al. (2008)
estimated a biannual cycle with 1 year of gestation for S. guggenheim in Patagonian
waters, with near-term gravid females found in January, May and September. In this
case, the authors surmised that non-gravid females found in differing reproductive
conditions throughout the year were due to 6 month differences in the ovulatory
cycle. Bridge et al. (1998) estimated that the ovulation cycle was biennial, but noted
that oocyte diameter was bimodal, with peaks in autumn and spring, and suggested
that parturition may be pluriannual for S. tergocellata. Capapé et al. (1990) found
postovulatory S. squatina females in spring and autumn months and were unable
to definitively describe the reproductive season for that species and for S. oculata
(Table I). In fact Capapé et al. (2002) stated that they, in the ‘same period of the year
have encountered non-gravid females with oocytes different in diameter’. Capapé
et al. (1990, 2002) used the term ‘semi-delayed vitellogenesis’ to describe the cycles
of females, reporting that females began to show evidence of vitellogenesis mid-
gestation. The authors concluded that this phenomenon made it difficult to determine
the duration of vitellogenesis. Likewise, Natanson & Cailliet (1986) had some dif-
ficulty determining time of parturition, and noted that gravid females were found
during all months (Table I).
The reproductive periodicity of females was difficult to analyse because of lack of
identifiable trends in IG and DO . Female S. dumeril very close to or mid-ovulation
were observed from April to November, which may have made the cycle difficult
to discern. A lack of data in the summer months may have inhibited the ability to
identify trends in IG and oocyte development. Alternately, given the clear trend seen
in the embryo data and the peak in male IG , the broad spread of female reproductive
indicators could be indicative of a 3 year cycle, with 2 years of vitellogenesis and
1 year of gestation. Unlike Colonello et al. (2006), however, two distinct stages of
oocyte development were not clearly evident, and attempts to classify females into
1692
Table I. Summary of published reproductive variables for Squatina species
Functional Fecundity Pupping Gestation Reproductive

Study Species Region ovary (mean) season period cycle
Natanson & Cailliet (1986) S. californica Eastern Pacific Left 5·5 July 10 months 1 year
Ocean, U.S.A.
Capapé et al. (1990) S. squatina Mediterranean Both 10
Sea, Tunisia
Capapé et al. (1990) S. oculata Mediterranean Both 8 February to
Sea, Tunisia April
Capapé et al. (2002) S. oculata Eastern Atlantic Both 6·2 May to June 12 months
Ocean, Senegal
Colonello et al. (2006) S. guggenheim Western Atlantic Left 4·1 November to 10 to 12 months 3 years
Ocean, South December
America
Shelmerdine & Cilff (2006) S. africana South-western Both 6 January 12 months 2 years
I. E. BAREMORE
Indian Ocean,
South Africa
Awruch et al. (2008) S. guggenheim South-western Left 7 12 months 6 months
Atlantic Ocean,
South America
Present study S. dumeril Gulf of Mexico, Left 7 February to 12 months 2 to 3 years
U.S.A. July

stages by oocyte diameter were unsuccessful. Given the large amount of energy that
is probably needed to produce up to 10 oocytes >60 mm in diameter, 2 years of
vitellogenesis may be necessary, or they may have 1 year of a resting phase and
1 year of vitellogenesis. Mature, non-gravid females with oocytes <20 mm were
observed in most months, which could be indicative of females in a resting phase.
About 24% of mature females collected were gravid, which could indicate a
3–4 year reproductive cycle; however, it is also probable that these numbers are
representative of poor sampling due to spatial segregation by gravid females. Most
autumn samples were fishery-independent, while spring–winter samples were from
both sources. Finally, these confounding findings could be due to the relatively broad
area sampled, as these data could represent more than one population or cohort of
S. dumeril in the Gulf of Mexico. Future reproductive studies of species in this genus
should focus on histology and year-round sampling to correctly stage the oocytes
and reproductive condition.
Fertilization appears to occur between June and October and parturition from
April to June; however, these results may actually portray poor sampling of gravid
females, as embryos from only 15 gravid females were collected in the course of
this study. While no near-term pregnant females were collected, several pups with
external yolk sacs were found in trawls along with mature females showing signs
of uterine and cloacal trauma. These pups were probably aborted due to the stress
of capture, which is common in many elasmobranchs (Braccini, 2006), and may be
especially common in this genus because of the phenomenon of cloacal gestation
(Sunye & Vooren, 1997). Because near-term pups were not observed in utero, those
found in the trawl catch with external yolk sacs were considered to be embryos.
Length data from embryos provide strong evidence of a 12 month gestation period,
consistent with a seasonal reproductive cycle.
The peak of male IG coincides with the smallest embryo measurements, indicat-
ing that mating may occur in the spring months. Although there were significant
differences in the IG of males among months, the disparity in size and folding
pattern between testes may have accounted for these differences, as only the left
testis was measured for this study due to sampling methodology. Folding of both
testes was always evident in the largest males, and there was no evidence of a pat-
tern as to degree of folding. No seasonal differences in IG were found for male
S. guggenheim (Awruch et al., 2008). While widely reported in the elasmobranch
reproduction literature, IG in males is not necessarily indicative of mating season
(Parsons & Grier, 1992). Some male elasmobranchs that mate year round, as well
as some species that mate seasonally, do not show trends in testes size with month
(Parsons & Grier, 1992). There are also cases in which male IG and female fertil-
ization are asynchronous (Teshima, 1981), probably due to sperm storage in females
(Carrier et al., 2004).
Spines have been previously reported on the pectoral fins of mature male angel
sharks [S. guggenheim (Colonello et al., 2006) and S. africana (Shelmerdine & Cliff,
2006)], though their function is unknown. In this study, the presence of spines was
always indicative of maturity, suggesting that they are a secondary sexual character-
istic. It is possible that they are used during copulation, as for example skates are
known to use alar thorns to maintain position while mating (Luer & Gilbert, 1985).
The largest S. dumeril collected from this study (116 cm LT ) was a reproduc-
tively inactive female, possessing very small ovaries with no visible oocytes and
1694 I. E. BAREMORE
uteri <5 mm in width. This could suggest reproductive senescence or infertility in

this individual. Senescence in fishes is generally found in long-lived species with low
mortality rates and occurs in part due to indeterminate growth and the capacity for
increased fecundity with age (Reznick et al., 2002). Ebert (2005) found that some of
the largest, and presumably oldest, female skates (Bathyraja) examined in the Bering
Sea had atrophied ovaries, and concluded that those individuals had most proba-
bly undergone senescence or diapause. Peres & Vooren (1991) also reported that a
41 year-old school shark Galeorhinus galeus (L.) had reduced ovary and nidamental
glands, which could be an indication of senescence in that species.
A paucity of published life-history studies exist for squatinids, probably stem-
ming from sampling difficulties and angel sharks do not appear to adhere to typical
elasmobranch life-history theory (i.e. seasonal growth and reproduction) (Natan-
son & Cailliet, 1990; Baremore et al., 2009). The challenges that these species
have presented highlight the need for a new way of thinking about life history and
management of atypical fish populations. While this study has lent insight into the
reproduction of S. dumeril, the reproductive cycle could not be fully determined for
this species. Age and growth for S. dumeril has yet to be determined, and their com-
plete fecundity and reproductive cycles are unclear; therefore, management strategies
for this genus should remain precautionary.
I would like to thank J. Carlson for allowing me to take this species and run with it, and
for giving me my start in fishery biology. Thanks also to the personnel at Raffield Fisheries,
especially Marie, who provided most of the samples for this project and have been extremely
helpful to me over the years. D. Bethea and L. Hollensead collected many samples in my
absence. C. Slager (Aquarium of the Bay, Embarcadero at Beach Street, San Francisco, CA)
provided useful information on captive angel sharks. Finally, a big thanks to K. Johnson on
the U.S. National Oceanic & Atmospheric Administration (NOAA) R.V. Oregon II and A.
Hamilton on the R.V. Gordon Gunter for keeping up with my crazy sample requests. Angel
sharks sampled from the fishery-dependent source were collected with a NOAA Fisheries
Service Exempted Fishing Permit (HMS-EFP-0301, EFP-04-01, EFP-05-01).
References
Awruch, C. A., Lo Nostro, F. L., Somoza, G. M. & Di Giacomo, E. (2008). Reproductive
biology of the angular angel shark Squatina guggenheim (Chondrichthyes: Squatinidae)
off Patagonia (Argentina, southwestern Atlantic). Ciencias Marinas 34, 17–28.
Baremore, I. E., Andrews, K. I. & Hale, L. F. (2009). Difficulties associated with model-
ing growth in the Atlantic angel shark (Squatina dumeril ). Fisheries Research 99,
203–209.
Braccini, J. M. (2006). Determining reproductive parameters for population assessments of
chondrichthyan species with an asynchronous ovulation and parturition: piked spurdog
(Squalus megalops) as a case study. Marine and Freshwater Research 57, 105–119.
Bridge, N. F., Mackay, D. & Newton, G. (1998). Biology of the ornate angel shark (Squatina
tergocellata) from the Great Australia Bight. Marine and Freshwater Research 49,
679–686.
Capapé, C., Quignard, J. P. & Mellinger, J. (1990). Reproduction and development of two
angel sharks, Squatina squatina and S. oculata (Pisces: Squatinidae), off Tunisian
coasts: semi-delayed vitellogenesis, lack of egg capsules, and lecithotrophy. Journal
of Fish Biology 37, 347–356.
Capapé, C., Seck, A. A., Gueye-Ndiaye, A., Diatta, Y. & Diop, M. (2002). Reproductive biol-
ogy of the smoothback angel shark, Squatina oculata (Elasmobranchii: Squatinidae),
from the coast of Senegal (eastern tropical Atlantic). Journal of the Marine Biological
Association of the United Kingdom 82, 635–640.
Carrier, J. C., Pratt, H. L. & Castro, J. A. (2004). Reproductive biology of elasmobranchs. In

Biology of Sharks and Their Relatives (Carrier, J. C., Musick, J. A. & Heithaus, M. R.,
eds), pp. 269–286. Boca Raton, FL: CRC Press.
Colonello, J. H., Lucifora, L. O. & Massa, A. M. (2006). Reproduction of the angular angel
shark (Squatina guggenheim): geographic differences, reproductive cycle, and sexual
dimorphism. ICES Journal of Marine Science 64, 131–140.
Compagno, L. J. V. (1984). Sharks of the World. An annotated and illustrated catalogue of
shark species known to date. FAO Fisheries Synopsis 4 (Part 1).
Cortés, E. (1998). Demographic analysis as an aid in shark stock assessment and management.
Fisheries Research 39, 199–208.
Cortés, E. (2000). Life history patterns and correlations in sharks. Reviews in Fisheries Science
8, 299–344.
Cortés, E. (2004). Life history patterns, demography, and population dynamics. In Biology
of Sharks and Their Relatives (Carrier, J. C., Musick, J. A. & Heithaus, M. R., eds),
pp. 449–470. Boca Raton, FL: CRC Press.
Ebert, D. A. (2005). Reproductive biology of skates, Bathyraja (Ishiyama), along the eastern
Bering Sea continental slope. Journal of Fish Biology 66, 618–649.
Hamlett, W. C., Kormanik, G. A., Storrie, M., Stevens, B. & Walker, T. I. (2005). Chon-
drichthyan parity, lecithotrophy and matrotrophy. In Reproductive Biology and Phy-
logeny of Chondrichthyes: Sharks, Batoids, and Chimaeras (Hamlett, W. C., ed.),
pp. 395–434. Enfield, NH: Science Publishers, Inc.
Levene, H. (1960). Contributions to probability and statistics. In Robust Tests for Equal-
ity of Variance (Levene, H. & Olkin, I., eds), pp. 278–292. Palo Alto, CA: Stanford
University Press.
Luer, C. A. & Gilbert, P. W. (1985). Mating behavior, egg deposition, incubation period, and
hatching in the clearnose skate, Raja eglanteria. Environmental Biology of Fishes 13,
161–171.
McEachran, J. D. & Fechhelm, J. D. (1998). Fishes of the Gulf of Mexico. Austin, TX:
University of Texas Press.
Natanson, L. J. & Cailliet, G. M. (1986). Reproduction and development of the Pacific angel
shark, Squatina californica, off Santa Barbara, California. Copeia 1986, 987–994.
Natanson, L. J. & Cailliet, G. M. (1990). Vertebral growth zone deposition in Pacific angel
sharks. Copeia 1990, 1133–1145.
NMFS (1993). Fisheries Management Plan for Sharks of the Atlantic Ocean. Silver Springs,
MD: U.S. Department of Commerce, National Oceanic and Atmospheric Administra-
tion.
Parsons, G. R. & Grier, H. J. (1992). Seasonal changes in shark testicular structure and sper-
matogenesis. Journal of Experimental Zoology 261, 173–184.
Peres, M. B. & Vooren, C. M. (1991). Sexual development, reproductive cycle, and fecun-
dity of the school shark Galeorhinus galeus off southern Brazil. Fishery Bulletin 89,
655–667.
Reznick, D., Ghalambor, C. K. & Nunney, L. (2002). The evolution of senescence in fish.
Mechanisms of Ageing and Development 123, 773–789.
Shelmerdine, R. L. & Cliff, G. (2006). Sharks caught in the protective gill nets off Kwa-Zulu-
Natal, South Africa. 12. The African angel shark Squatina africana (Regan). African
Journal of Marine Science 28, 581–588.
Sunye, P. S. & Vooren, C. M. (1997). On cloacal gestation in angel sharks from southern
Brazil. Journal of Fish Biology 50, 86–94.
Teshima, K. (1981). Studies on the reproduction of Japanese smooth dogfishes Mustelus man-
azo and M. griseus. Journal of Shimonoseki University of Fisheries 29, 113–199.
Walker, T. I. (2005). Reproduction in fisheries science. In Reproductive Biology and Phy-
logeny of Chondrichthyes: Sharks, Batoids, and Chimaeras (Hamlett, W. C., ed.),
pp. 81–127. Enfield, NH: Science Publishers, Inc.

Reproductive Aspects of The Atlantic Angel Shark

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Reproductive Aspects of The Atlantic Angel Shark

Uploaded by

Copyright:

Available Formats

Journal of Fish Biology (2010) 76, 1682–1695

doi:10.1111/j.1095-8649.2010.02608.x, available online at www.interscience.wiley.com

Reproductive aspects of the Atlantic angel shark

(Received 20 April 2009, Accepted 1 February 2010)

Key words: elasmobranch; lecithotrophic viviparity; maturity; senescence; Squatinidae.

MATERIALS AND METHODS

Mexico 20° 0'

No claim to original US government works

Nidamental width (mm)

mature, non-gravid ( , n = 47) Squatina dumeril by month (January to December, 1–12).

Table I. Summary of published reproductive variables for Squatina species

Functional Fecundity Pupping Gestation Reproductive

No claim to original US government works

uteri <5 mm in width. This could suggest reproductive senescence or infertility in

Carrier, J. C., Pratt, H. L. & Castro, J. A. (2004). Reproductive biology of elasmobranchs. In

You might also like