1829
Reproductive biology of the Brazilian sharpnose shark
(Rhizoprionodon lalandii) from southeastern Brazil
Fabio S. Motta, Rafael C. Namora, Otto B. F. Gadig, and F. M. S. Braga
Motta, F. S., Namora, R. C., Gadig, O. B. F., and Braga, F. M. S. 2007. Reproductive biology of the Brazilian sharpnose shark (Rhizoprionodon
lalandii) from southeastern Brazil. – ICES Journal of Marine Science, 64: 1829 – 1835.
The reproductive biology of the Brazilian sharpnose shark, Rhizoprionodon lalandii, off southeastern Brazil was investigated using data
from gillnet landings. The size-at-maturity for males and females was estimated to be 59 and 62 cm total length (LT), respectively.
Ovarian fecundity ranged from 3 to 7 follicles (mean ¼ 4.54), and uterine fecundity from 1 to 5 embryos (mean ¼ 3.3). There was
a slight positive relationship between female LT and the number of ovarian follicles, but uterine fecundity was not related to
female LT. Embryonic growth is fast following fertilization during summer and autumn. Gestation requires 11– 12 months, and
peak parturition is between August and September. A comparison of size-at-maturity between animals from northeastern and southeastern Brazil suggests the existence of at least two stocks of R. lalandii along the Brazilian coast.
Keywords: Elasmobranchii, fecundity, reproduction, shark, size-at-maturity.
Received 22 January 2007; accepted 7 October 2007; advance access publication 13 November 2007.
F. S. Motta and O. B. F. Gadig: Universidade Estadual Paulista, Campus do Litoral Paulista, Praça Infante Dom Henrique s/n, Parque Bitarú, CEP
11330-900 São Vicente SP, Brazil. R. C. Namora and F. M. S. Braga: Departamento de Zoologia, Instituto de Biociências, Universidade Estadual
Paulista, Av. 24-A, 1515, Bela Vista, CEP 13506-900, Rio Claro SP, Brazil. Correspondence to F. S. Motta: tel: þ55 13 35699400; fax: þ55 13
35699446; e-mail: [email protected]
Introduction
The genus Rhizoprionodon is represented worldwide by at least
seven species of small coastal placental sharks (maximum length
140 cm), identified among carcharhinids by their long upper
labial furrow, and the second dorsal fin origin posterior to the
origin of the anal and preanal ridges (Parsons, 1983; Compagno,
1984). Because of their abundance and habits, these sharks are
caught in several parts of the world, with estimates varying from
46% to 81.7% (by numbers) of the total catch of sharks in
coastal fisheries (Sadowsky, 1967; Cody and Avent, 1980; Lessa,
1986; Grace and Henwood, 1997; Trent et al., 1997;
Castillo-Géniz et al., 1998; Thorpe et al., 2004; Motta et al.,
2005). In the western Atlantic, three species have been recorded:
R. terraenovae, known from the western North Atlantic, but probably also in the tropical western South Atlantic; R. porosus, from the
central US to Uruguay and Brazil; and R. lalandii, from western
Panama to Uruguay and Brazil (Figueiredo, 1977; Compagno,
1984).
The Brazilian sharpnose shark (R. lalandii) is the most
common shark species of the continental shelf of southern
Brazil, representing 60% of the total shark landings from
small-scale fisheries there (Gadig et al., 2002; Motta et al., 2005).
It attains a maximum size of 80 cm with a life cycle restricted to
the continental shelf, from very shallow water to 70 m deep,
usually over muddy and sandy seabed (Compagno, 1984). Off
southern Brazil, the species has suffered from the effects of
marine pollution (Sazima et al., 2002) and is listed by IUCN as
data-deficient because of the paucity of biological information
over its entire distribution (Rosa et al., 2004).
# 2007
Despite the abundance and distribution of Rhizoprionodon
along the continental shelf of Brazil, biological data on these
sharks are limited. Ferreira (1988) reported that off southern
Brazil (n ¼ 314), the species attains sexual maturity at 60 –65 cm
LT, and that the mean uterine fecundity is 3 embryos. Lessa
(1988) examined 294 sharks in Maranhão (northern Brazil) and
concluded that R. lalandii reaches sexual maturity between 52
and 56 cm LT and that the fecundity varies from 2 to 5 embryos.
More recently, Motta et al. (2005) investigated the size and sex
compositions, occurrence, and distribution patterns of R. lalandii
along the coast of São Paulo State, providing insights into the life
cycle and reproductive patterns, as well as nursery habitats. The
aim of this study is to provide complementary information on
the reproductive biology of R. lalandii based on fishery-dependent
data. We estimated size-at-maturity, fecundity, and gestation
period, and include data on embryo development and growth.
Material and methods
Our work is based on a study of the fishery biology of coastal
sharks from southeastern Brazil (Projeto Cação; Gadig et al.,
2002), which has been ongoing since 1996. The data used in this
analysis come from specimens landed at Fishermen’s Beach,
Itanhaém city, south São Paulo (24811’S 46848’W), and in adjacent
areas (Figure 1), between July 1996 and June 2002. The fishing fleet
consists of 12 small motorized boats (4–10 m long), which fish
with monofilament gillnets 1500 m long and stretched mesh
sizes of 7, 12, and 14 cm on average. The nets are set at distances
of 2 –12 nautical miles from shore, in waters between 5 and 30 m
deep, and checked once a day, usually in the morning.
International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved.
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1830
F. S. Motta et al.
Figure 1. Map of fishing area and landing beach of the artisanal fishery fleet in Itanhaém, southeastern Brazil.
All sharks were measured (total length, LT, in cm), weighed
(total weight, WT, in g), and their sex was determined. From
males, the clasper length was measured from the tip to the inner
pelvic junction, and the stage of calcification was classified as
flexible or rigid.
Maturity stages were assessed according to Castro (1993) and
Simpfendorfer and Milward (1993) as follows: neonates, recognized by the presence of an open umbilical scar between their pectoral fins; juveniles, umbilical scar healed or absent, the males with
flexible claspers and females with ovaries not clearly differentiated
and filiform uteri; adults, males with elongated and calcified
claspers and females carrying vitellogenic oocytes in the ovary
and/or eggs or embryos in the uterine cavity.
After evisceration, the reproductive organs of some sharks were
removed and fixed in a solution of 10% formaldehyde in fresh
water. In the laboratory, the length and width of epididymides
and testes from males were measured, and the latter were
weighed. For females, the following data were collected: width of
the oviducal gland, number of ovarian follicles, and diameter of
the largest ones. For pregnant females, the numbers of eggs or
embryos were counted. Embryos were measured, weighed, and
the sex was determined.
Size-at-maturity was estimated from the allometric growth patterns (against LT) of clasper, testis, and epididymides in males, and
from the oviducal glands and follicles in females. The length at
which 50% of the sharks from both sexes were sexually mature
(LT50) was estimated from a logistic curve fitted to the data by
maximum-likelihood procedures, based on maturity proportion
by 1-cm length class (Roa et al., 1999).
Results
General compositions of size, weight, sex,
and state of maturity
In all, 7330 R. lalandii were examined in the field (3912 males,
3418 females). The total length of males ranged from 30 to
Reproductive biology of Rhizoprionodon lalandii from SE Brazil
1831
Figure 2. Length frequency distribution of Rhizoprionodon lalandii sampled from Itanhaém’s artisanal fisheries in southeastern Brazil between
July 1996 and June 2002 (pooled data; males n ¼ 3912; females n ¼ 3418).
77.5 cm, and of females from 30 to 80 cm (Figure 2). Total weight
of males was 75 –1925 g, and of females 75 –2950 g. We found
2031 (27.7%) neonates, 3049 (41.6%) juveniles, and 2250
(30.7%) adults. Between November and March, juveniles were
most frequent. From April to July, adults were most common,
but in June, neonates started to appear, then dominated in
August and September (the birth season; Figure 3).
Maturation
The relationship between clasper length and total length of males
was characterized by a sigmoid pattern (Figure 4a) corresponding
to three phases of clasper growth. The first comprised sharks up to
46 cm LT, with flexible claspers measuring 0.5 –1.5 cm, with slow
growth relative to LT. The second phase included animals from
46 to 58 cm LT, whose claspers ranged from 0.7 to 5 cm,
showing fast positive allometric growth and becoming calcified.
In the third phase, the claspers showed negative allometric
growth and varied from 3.6 to 6.1 cm in mature sharks .58 cm
LT. Additionally, all males with claspers ,3.5 cm were unable to
copulate, because the organs were flexible, i.e. lacking skeletal
support. Maturity was attained by 79.6% of sharks with rigid claspers .4 cm. The growth in length of testes was gradual, ranging
from 1.41 to 6.3 cm (mean ¼ 4.29 + 1.21 s.d.) in juveniles, and
from 5.8 to 12.19 cm (mean ¼ 8.97 + 1.32 s.d.) in mature
sharks .59 cm LT (Figure 4b). The width and the weight of the
testes increased as males exceeded 58 cm LT (Figure 4c and d),
but there was great variation in both parameters in mature
sharks, probably because of the presence in the sample of sharks
at different phases of their reproductive cycle. Width of the epididymides ranged from 0.48 to 1.2 cm (mean ¼ 0.83 + 0.14 s.d.) in
mature sharks .59 cm LT (Figure 4e). On the basis of previous
analysis and on the fact that the smallest mature male measured
was 56 cm LT and the largest immature was 63 cm LT, the size at
first maturity was recorded as being near 59 cm LT. This estimate
was corroborated by the value calculated for LT 50, which was
58.65 cm (Figure 5).
Figure 3. Monthly frequency of occurrence of R. lalandii sampled from Itanhaém’s artisanal fisheries in southeastern Brazil between July 1996
and June 2002 (pooled data). The number of individuals sampled per month is shown above the vertical bars.
1832
F. S. Motta et al.
Figure 4. Relationship between total length and (a) clasper length (n ¼ 1770), (b) length of testis (n ¼ 132), (c) width of testis (n ¼ 145),
(d) weight of testis (n ¼ 116), and (e) width of epididymides (n ¼ 113) in male R. lalandii from Itanhaém, southeastern Brazil.
The width of the female oviducal gland ranged from 0.24 to
0.85 cm (mean ¼ 0.41 + 0.22 s.d.) in juveniles. Adult females
could be divided into three groups: pregnant females at the
onset of gestation (caught between October and February),
whose glands ranged from 0.32 to 1.34 cm (mean ¼ 0.89 +
0.25 s.d.); females at first ovulation, between 61 and 68.5 cm
LT (caught between March and June), whose glands ranged
from 0.9 to 1.83 cm (mean ¼ 1.37 + 0.26 s.d.); and post
partum females and females carrying term embryos between
67 and 78.5 cm LT (caught between June and August), whose
glands ranged from 0.95 to 1.81 cm (mean ¼ 1.45 + 0.21 s.d.)
(Figure 6a). A similar dispersion of data was observed relative
to the diameter of the ovarian follicles (Figure 6b). Pregnant
females at the start of gestation had follicles ranging from 0.12
to 0.7 cm (mean ¼ 0.41 + 0.20 s.d.). The follicles of ovulating
females ranged from 1.04 to 2.08 cm (mean ¼ 1.65 +
0.23 s.d.). The smallest female with vitellogenic activity was
58 cm LT, the smallest pregnant female was 65 cm LT, and the
largest immature was 63.5 cm LT. Therefore, we conclude that
females mature between 60 and 63 cm LT, with LT 50 at
62.05 cm (Figure 7).
Fecundity
Figure 5. Proportion of mature male R. lalandii per 1 cm total
length intervals. Dashed lines mark the total length at which 50% of
the sharks are mature.
The ovarian fecundity of R. lalandii varied from 3 to 7 follicles
(mean ¼ 4.54 + 0.9 s.d.), and the uterine fecundity (litter size)
from 1 to 5 embryos or eggs (mean ¼ 3.3 + 0.91 s.d.). There
was a positive linear relationship between total length and the
number of ovarian follicles (Figure 8a), but the relationship
between uterine fecundity and total length was not significantly
correlated (Figure 8b).
1833
Reproductive biology of Rhizoprionodon lalandii from SE Brazil
Figure 8. Relationship between total length and (a) ovarian
fecundity (FO ¼ 0.0965 LT 22.2776; r 2 ¼ 0.256; n ¼ 97), (b) uterine
fecundity (FU ¼ 0.0255 LT þ1.4891; r 2 ¼ 0.0092; n ¼ 76) in female
R. lalandii from Itanhaém, southeastern Brazil.
Figure 6. Relationship between total length and (a) width of
oviducal gland (n ¼ 96), (b) diameter of the largest follicle (n ¼ 78)
in female R. lalandii from Itanhaém, southeastern Brazil.
Embryos
In all, 137 embryos from 47 females were examined. Their total
length and weight ranged from 3.5 to 35 cm and from 4.5 to
175 g, respectively. The length –weight relationship was described
by the equation WT ¼ 0.0025 L T3.14 (r 2 ¼ 0.965; n ¼ 105). Of the
total examined, the sex of 115 was determined, 57 (49.6%) being
males and 58 (50.4%) females, a sex ratio (1: 1.02) not significantly
different from 1:1 (p ¼ 0.936).
Eggs were present in the uteri between October and January. In
January, embryos measuring an average of 4.0 cm LT (+0.49 s.d.)
were also registered. With eggs in the uteri between October and
January and looking at the plot of embryo mean total length
against month (Figure 9a), we conclude that embryonic development takes 11 –12 months in R. lalandii. Increase in the length
of embryos approximates a sigmoid curve, indicating that after
fertilization there is a period of rapid growth between summer
and autumn (January –June), when embryos grow from 3.5 to
29.7 cm LT. Embryonic development ended in July and
September (winter), when the embryos had attained an average
of 30.6 (+2.6 s.d.) and 32.1 cm (+1.5 s.d.) LT, respectively, and
parturition took place. The increase in weight (Figure 9b) differed
from the increase in total length. Embryo weight increased slowly
during the first few months (until May), embryos increasing from
4.5 to 23.0 g. During the final three months of gestation, growth in
weight was the greatest, embryos reaching 120–160 g.
Discussion
Figure 7. Proportion of mature female R. lalandii per 1 cm total
length interval. Dashed lines mark the total length at which 50% of
the sharks are mature.
The largest female (80 cm LT) examined in our study is the
maximum size recorded for the species. The peak occurrence of
neonates indicates a birth season between August and September
(winter), consistent with the results of previous studies (Ferreira,
1988; Motta et al., 2005).
The relationship between clasper length and LT can be used to
determine sexual maturation in male sharks. Stable allometric or
isometric relationships are shown during the growth of these
organs, with reference to that of the body, at least during the
1834
Figure 9. Monthly variation of (a) mean total length and (b) mean
weight of R. lalandii embryos from Itanhaém, southeastern Brazil.
Boxes indicate mean + s.d., whiskers show the range of the data, and
numbers in parentheses are embryos examined.
juvenile and adult stages (Capapé et al., 1990). For R. terraenovae,
Parsons (1983) noted that the clasper lengthens at a faster rate
than total length at the onset of maturation (positive allometric
growth), but that then there is a period of negative allometric
growth (slow growth) when claspers attain their functional length.
A similar pattern was verified for R. lalandii in the present
study, although here, possibly because of the large sample size,
three phases in clasper growth were identified. Off northern
Brazil, Lessa (1988) observed two phases in clasper growth of
R. lalandii, a juvenile phase for sharks between 40 and 48 cm LT,
with flexible claspers measuring an average 3.7 cm, and an adult
phase for sharks between 49 and 71 cm LT, with rigid claspers
ranging from 4 to 6.6 cm.
The sizes at first maturity of R. lalandii estimated here (59 cm
LT for males, 62 cm LT for females) were similar to those reported
by Ferreira (1988) off Rio de Janeiro (60 cm LT for males, 65 cm LT
for females). In contrast, the lengths-at-maturity found by Lessa
F. S. Motta et al.
(1988) at Maranhão, 52 cm LT for males, 56 cm LT for females,
were quite different from our findings and previous estimates
for southeastern Brazil. These differences could have resulted
from distinctive oceanographic conditions among the areas,
which could cause differences in biological parameters between
populations, such as maximum size, growth rate, size-at-maturity,
and fecundity (Parsons, 1993; Lombardi-Carlson et al., 2003).
Menni and Lessa (1998) argued that differences observed
between samples from Maranhão (north) and Rio de Janeiro
(southeast) could be attributed to differences in water temperature
(15–188C off Rio de Janeiro, 27 –308C off Maranhão). The pattern
found in R. lalandii could also be attributable to the effect of latitudinal variation on its life history. This effect has been shown for
other sharks, and one of the more commonly observed trends is an
increase on body size and size-at-maturity with increasing latitude
(Lombardi-Carlson et al., 2003; Colonello et al., 2006). Latitudinal
differences are thought to be an adaptive response by an individual
to different environmental factors (Lombardi-Carlson et al., 2003)
such as, for instance, the advantages that a larger body size in
higher latitudes might allow more energy storage for the season
with low resource availability (Colonello et al., 2006). The difference in reproductive parameters among areas suggests that at
least two different stocks of R. lalandii (north vs. southeast) may
exist along the Brazilian coast.
The observation of females simultaneously carrying term
embryos and vitellogenic follicles indicates an annual reproductive
cycle with concurrent ovarian and gestation cycles. This aspect has
been observed for other Rhizoprionodon species (Parsons, 1983;
Stevens and Mcloughlin, 1991; Simpfendorfer, 1992; Castro and
Wourms, 1993). Mating of R. lalandii in Brazilian waters takes
place between April and June for first-maturing females, and
between July and September for post partum females (Motta
et al., 2005). All females caught between July and September are
pregnant or with characteristic signs of recent parturition, which
may indicate that there is no resting phase between pregnancies.
Our fecundity estimates for R. lalandii were similar to those in
the literature. We observed ovarian and uterine fecundity ranging
from 3 to 7 follicles (mean ¼ 4.54) and from 1 to 5 embryos
(mean ¼ 3.3), respectively. Off Rio de Janeiro, Ferreira (1988)
reported mean values of 4.7 for the ovary and 2.9 for the uteri.
Estimates from northern Brazil ranged from 2 to 6 follicles and
from 2 to 5 embryos (Lessa, 1988).
A significant relationship between litter size and total length of
females has been recorded for other Rhizoprionodon species
(Parsons, 1983; Stevens and Mcloughlin, 1991; Simpfendorfer,
1992; Castillo-Géniz et al., 1998; Mattos et al., 2001). For R. lalandii,
Ferreira (1988) stated that the fecundity varies with female size, but
no correlation analyses were presented. Here, only ovarian fecundity was related significantly with female size. Uterine fecundity
data can be biased because of the abortion of term embryos (sometimes reported by local fishers) caused by stress during capture.
Also, Lessa (1988) failed to find a significant relationship
between fecundity and LT in northern Brazil. According to
Stevens and Mcloughlin (1991), the relationship between litter
size and female size should not be considered as a rule for
carcharhinids.
The gestation period estimated here for R. lalandii was 11 –12
months. Ferreira (1988) suggested a gestation period of 12
months for Rio de Janeiro, but off northern Brazil, the gestation
period for R. lalandii could not be determined (Lessa, 1988).
The embryonic growth patterns we observed (a period of rapid
Reproductive biology of Rhizoprionodon lalandii from SE Brazil
growth after conception, and a difference between the increases in
length and in weight) were similar to those reported for R. terraenovae (Parsons, 1983). However, a more detailed study on
embryonic development of R. lalandii will be required for the
main morphological and physiological changes that occur
during gestation to be described adequately.
Acknowledgements
We thank the fishers of Itanhaém for their collaboration with
PROJETO CAÇÃO, for their friendship, and for their permission
to examine all sharks landed, P. Pepin, R. L. Moura, J. P. Barreiros,
and an anonymous reviewer for comments that greatly improved
the manuscript, and São Paulo’s Research Support Foundation
(FAPESP—Proc. n8 99/04 085-1) for essential financial support.
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