Reproductive biology of the scalloped hammerhead shark Sphyrna

aqua, International Journal of Ichthyology
Reproductive biology of the scalloped hammerhead shark Sphyrna lewini
(Chondrichthyes: Sphyrnidae) off south-west Mexico
Marcela Bejarano-Álvarez*, Felipe Galván-Magaña and Rosa Isabel Ochoa-Báez
Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Av. IPN s/n Col.
Playa Palo de Santa Rita, La Paz, B.C.S., Mexico C.P. 23096.
*E-mail: [email protected]
Received: 05 March 2010 – Accepted: 07 August 2010
Abstract
The scalloped hammerhead shark Sphyrna lewini is the
most important species in the artisanal shark fishery in the
Gulf of Tehuantepec, Mexico. Knowledge about the reproductive biology of this species in the area is nonexistent,
despite its being listed worldwide as endangered by the
IUCN. To determine the basic reproductive biology of this
shark would give important data for management or conservation plans for this species in Mexico. Samples were collected of 991 hammerhead sharks (342 females and 649
males), including juveniles (45 to 160 cm TL) and adults
(170 to 288 cm TL), from September 2004 to June 2006.
The sex ratio was 1F: 2M. The scalloped hammerhead was
present year round in the study area with the greatest catch
from May to July, the season when pregnant females were
present. The females reached sexual maturity at 220 cm TL
based on characteristics and measurements of reproductive
organs. A histological analysis showed that testes in males are
a diametric type and have compound spermatozeugmata in
the seminal vesicles, indicating sexual maturity in males at
180 cm TL. We recorded 40 pregnant females, with 14 to
40 embryos per female. The births occurred in July and
August with an embryo size of between 41 and 51 cm TL.
The presence of neonates, juveniles, and pregnant females
with embryos in an advanced development condition suggest that the coastal waters off Oaxaca are an important
nursery area for the scalloped hammerhead shark.
Resumen
El tiburón martillo Sphyrna lewini es la especie de mayor
importancia en la pesquería artesanal en el Golfo de Tehuantepec, México. El conocimiento acerca de la biología reproductiva de esta especie en el área es inexistente a pesar de
estar incluida en la lista de especies amenazadas por la
IUCN. Para determinarla biología reproductiva básica de
esta especie, se presenta información importante que contribuye para futuros planes de manejo ó conservación para
esta especie en México. Se obtuvieron muestras de 991
tiburones martillo (342 hembras y 649 machos), incluyendo
juveniles (45 a 160 cm LT) y adultos (170 a 288 cm LT), de
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Septiembre de 2004 a Junio de 2006. La proporción de
sexos fue de 1H: 2M. El tiburón martillo estuvo presente
durante todo el estudio, registrándose las mayores capturas
en los meses de mayo a julio, época donde se presentaron las
hembras grávidas. Basado en características y medidas del
órgano reproductor, las hembras alcanzan su madurez sexual
a los 220 cm LT. El análisis histológico mostró que los
machos presentan testículos de tipo diamétrico y espermatozeugmata de tipo compuesto en la vesícula seminal, indicando una madurez sexual a los 180 cm LT. Se registraron
40 hembras grávidas con 14 a 40 embriones por hembra.
Los nacimientos ocurrieron en Julio y Agosto con tallas
entre 41 y 51 cm LT. La presencia de neonatos, juveniles y
hembras grávidas con embriones en desarrollo avanzado,
sugiere a las costas de Oaxaca como un área de crianza para
el tiburón martillo.
Zusammenfassung
Der Bogenstirn-Hammerhai Sphyrna lewini ist die
wichtigste Art der handwerklichen Haifischerei im Golf
von Tehuantepec, Mexiko. Es gibt praktisch keine Kenntnisse über die Fortpflanzungsbiologie dieser Art in dem
Gebiet, obwohl sie weltweit vom IUCN zu den gefährdeten Arten gezählt wird. Untersuchungen über die Grundlinien der Fortpflanzungsbiologie dieses Hais könnten
wichtige Fakten für Pläne zum Schutz und zur Bestandsregulierung dieser Art in Mexiko liefern. Von September
2004 bis Juni 2006 wurden Belege von 991 BogenstirnHammerhaien gesammelt (342 Weibchen, 649 Männchen), sowohl von jungen Tieren (45 bis 160 cm Gesamtlänge = TL) als auch von erwachsenen (170 bis 288 cm
TL). Das Geschlechterverhältnis war 1 : 2 Weibchen zu
Männchen. Der Bogenstirn-Hammerhai war in dem Forschungsgebiet das ganze Jahr über anwesend; in der Zeit
der trächtigen Weibchen, von Mai bis Juli, war die
Fangquote am höchsten. Die Weibchen erreichten die
Geschlechtsreife ab einer Größe von 220 cm TL, beurteilt
nach Merkmalen und Messungen der Geschlechtsorgane.
Durch histologische Analysen ließ sich feststellen, dass die
Hoden der Männchen vom diametrischen Typus sind und
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Reproductive biology of the scalloped hammerhead shark Sphyrna lewini (Chondrichthyes: Sphyrnidae) off south-west Mexico
die Samenblasen zusammengesetzte Spermatozeugmen
enthalten; die Geschlechtsreife wird mit 180 cm TL erreicht. Wir registrierten 40 trächtige Weibchen mit 14 bis
40 Embryonen pro Weibchen. Die Geburten ereigneten
sich im Juli und August, bei einer Größe der Embryos von
41 bis 51 cm TL. Die gleichzeitige Anwesenheit von frisch
Geborenen, Jungtieren und trächtigen Weibchen mit
Embryos im fortgeschrittenen Stadium spricht dafür, dass
die Küstengewässer vor Oaxaca als Kinderstube für Bogenstirn-Hammerhaie eine wesentliche Bedeutung haben.
strava che i testicoli dei maschi sono diametrici e hanno
spermatozeugmata composti nelle vescicole seminali, indicando che la maturità sessuale è raggiunta a 180 cm TL.
Abbiamo registrato 40 femmine gravide, con un numero di
embrioni per femmina variabile da 14 a 40. Le nascite si
succedevano in luglio e agosto e le dimensioni dell’embrione
erano comprese tra 41 e 51 cm TL. La presenza di neonati,
giovani e femmine gravide con embrioni in avanzato stadio
di sviluppo suggeriscono che le acque costiere di Oaxaca rappresentano un importante vivaio per lo squalo martello
smerlato.
Résumé
Le requin marteau, Sphyrna lewini, est l’espèce la plus
importante pour la pêche au requin artisanale dans le golfe
de Tehuantepec, Mexique. La biologie reproductive de cette
espèce dans la région est ignorée, alors qu’elle est partout
reprise comme menacée par l’IUCN. Déterminer la biologie
reproductive de base de ce requin fournirait d’importantes
données pour la gestion ou les projets de préservation de
cette espèce au Mexique. Des échantillons de 991 requins
marteaux (342 femelles et 649 mâles), comprenant des juvéniles (45 à 160 cm de LT) et des adultes (170 à 288 cm de
LT), ont été collectés de septembre 2004 à juin 2006. Le sex
ratio était de 1 F : 2M. Le requin marteau était présent toute
l’année dans le secteur étudié avec les meilleures captures de
mai à juillet, la saison où des femelles en gestation étaient
présentes. Les femelles atteignent la maturité sexuelle à la
taille de 220 cm LT, prouvée par les caractéristiques et
les mensurations des organes reproducteurs. Une analyse
histologique a montré que les testicules des mâles sont de
type diamétrique et ont des spermatozeugmata composés
dans les vésicules séminales, signalant la maturité sexuelle
des mâles à 180 cm LT. Nous avons examiné 40 femelles en
gestation avec de 14 à 40 embryons par femelle. Les naissances ont eu lieu en juillet et août avec une taille d’embryons de 41 à 51 cm LT. La présence de nouveau-nés, de
juvéniles et de femelles pleines avec des embryons bien
développés suggère que les eaux côtières au large d’Oaxaca
sont un site important de nurserie pour ce requin marteau.
Sommario
Lo squalo martello smerlato Sphyrna lewini è la specie più
importante nell’industria della pesca dello squalo nel golfo
di Tehuantepec, Messico. Le conoscenze sulla biologia riproduttiva di questa specie nell’area sono pressoché nulle, malgrado sia considerata specie a rischio di estinzione dallo
IUCN. Determinare gli aspetti fondamentali della biologia
riproduttiva di questo squalo è di grande importanza per la
gestione e la conservazione della specie in Messico. Nel periodo compreso tra settembre 2004 e giugno 2006 sono stati
raccolti 991 squali martello smerlati (342 femmine e 649
maschi), inclusi individui giovani (45-160 cm TL) e adulti
(170-288 cm TL). Il rapporto tra i sessi era 1F: 2M. Lo
squalo martello smerlato era presente tutto l’anno nell’area
di studio con un picco massimo tra maggio e luglio, la stagione in cui erano presenti femmine gravide. La femmina
raggiunge la maturità sessuale a 220 cm TL, come è risultato
dall’esame degli organi riproduttivi. L’analisi istologica moaqua vol. 17 no. 1 - 15 January 2011
INTRODUCTION
The scalloped hammerhead shark Sphyrna lewini
(Griffith & Smith, 1834) is a semi-oceanic species
globally distributed in coastal, warm temperate and
tropical seas. In the eastern Pacific Ocean, it is distributed from the coast of southern California to
Ecuador and probably to Peru (Compagno et al.
2005). Sphyrna lewini, like other species, has sexual
segregation. The females move offshore at a smaller
size than males and form schools, including primarily intermediate-size female sharks. Klimley
(1987) suggested that female S. lewini grow faster
than males, because the body size required for
female gestation is larger than that for the male
production of spermatozoa.
The reproductive mode of S. lewini is placental
viviparity (Hamlett 1999). Biological analysis of S.
lewini is based on fishery reports, movements, and
feeding habits (Klimley & Nelson 1984; Klimley et
al. 1993; Campuzano 2002). However, there few
reports on the reproductive biology of this shark
(Chen et al. 1988; Pratt 1988, 1993; Torres 1999;
Hazin et al. 2001). The IUCN has classified
Sphyrna lewini as Endangered worldwide. All lifestages are vulnerable to capture in target fisheries
and in bycatch. In south-west Mexico, this species
is the most abundant and supports the fishery in
the area, making it susceptible to overfishing in the
region. Despite this, the existing information on
the reproductive biology of the species in the region
is scarce and it is still not protected under any conservation measures. A large number of juveniles are
captured by different fishing gear close to coastal
waters, whereas adults are caught in gillnets and
longlines along the shelf and offshore in oceanic
waters. Therefore, the goal of our study is to provide biological information on the reproductive
biology of S. lewini based on specimens caught in
the artisanal fishery in the Gulf of Tehuantepec.
This information on the reproductive biology of
the species, will help to establish management plans
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Marcela Bejarano-Álvarez, Felipe Galván-Magaña and Rosa Isabel Ochoa-Báez
Table I. Number sampled of the scalloped hammerhead
shark Sphyrna lewini taken from 2004-2006 off south-west
Mexico.
YEAR
FEMALES
MALES
2004
17
50
67
2005
233
516
749
2006
92
83
175
342
649
991
TOTAL
TOTAL
for fisheries or conservation of this shark species in
the area. Sphyrna lewini also has been proposed for
entry into Appendix II of CITES (Convention on
International Trade in Endangered Species of Wild
Fauna and Flora), to be protected worldwide. Our
research also provides important information about
the reproductive status of this species covering
embryos, neonates, juveniles and adults of both
sexes using morphometric and histological methods
which allow a detailed description of the male
reproductive organs.
MATERIALS AND METHODS
Samples of Sphyrna lewini were collected weekly
from September 2004 to June 2006 at the
Chipehua fishing camp located on the Oaxacan
coast (16°02’3.422”N, 95°22’6.49’’W). In the
fishing camp, biometric measurements were made
for all specimens (total and clasper lengths in cm)
and the sex was recorded. Different stages of
growth were distinguished using the work of Cas-
tro (1983): embryos, neonates (signs of umbilical
scars), juveniles, adults and pregnant females. The
maturity stage for both males and females was
determined. In males, the length of claspers was
measured and the maturity was determined by the
presence of calcified claspers, which must rotate
180º relative to their normal position, as well as a
freely opening rhipidion and fully developed siphon
sacs (Clark & von Schmidt 1965; Pratt 1979). The
testes were excised from the epigonal organ and the
length and width of the testes were measured. The
condition of the epididymides and the ductus deferens were observed and the genital ducts were
checked for the presence of seminal fluid.
In females, the oviducal gland width and uterus
were measured. Females were considered mature if
they were gravid or had enlarged oviducal glands,
an expanded uterus and an ovary with large yolked
eggs. If the uterus was developed, it was dissected
to determine if embryos or uterine eggs were present. If embryos were present, their total length
and the sex of embryos were recorded.
The reproductive system was removed and preserved in 10% formalin. The reproductive organs
were used for histological analysis, embedded in
paraffin and hematoxiline-eosine stained. In the
laboratory, the organs of the reproductive system
were identified and analyzed. We used microscopy
to recognize the criteria for characterization of the
gonadic development phases. The gestation period
and sexual cycle were estimated and embryos were
counted and measured to determine fecundity.
Fig. 1. Size composition of male and female scalloped hammerhead shark S. lewini off south-west Mexico.
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Reproductive biology of the scalloped hammerhead shark Sphyrna lewini (Chondrichthyes: Sphyrnidae) off south-west Mexico
RESULTS
A total of 991 S. lewini were recorded (342
females and 649 males). Sphyrna lewini were present year round, but the greatest abundance was
from May to July, the months in which pregnant
females were found (Table I).
Size range were from 45 cm to 288 cm total
length (TL) in both males and females and showed
two well-differentiated groups; one of neonates
and juveniles (45 to 160 cm TL) and another of
adults (170 to 288 cm TL) (Fig. 1). As seen in Figure 1, adult males from 170 to 250 cm TL were
more abundant than females, and showed a sex
ratio of 1F:2M with significance differences in the
ratios (X2 <125; P >0.05), whereas juveniles had a
sex ratio of 1F:0.75M (X2 <9.46; P >0.05). The
embryo ratio was 1F:1M (X2 <0.17; P >0.05).
To determine sexual maturity in males, reproductive data were obtained from 649 males from 45 to
288 cm TL. Based on the rigidity of claspers, male
Sphyrna lewini reached their first maturity at a TL
of 180 cm. Males from 63.5 cm to 100 cm TL had
uncalcified claspers (2.2 to 8 cm). The clasper
length of males increased rapidly and was associated with total length, with calcified claspers of 1623 cm in males from 180 to 188 cm TL suggesting
that sexual maturity has been obtained (Fig. 2).
The testes length was 3-25 cm in immature and
11-30.5 cm for mature individuals. From 180 cm
TL, the length of testes in males increased as the
shark grew. The male reproductive system has a
paired and elongated testis, an epididymis and an
epigonal organ, deferens ducts, and seminal vesicle.
Both testes were well-developed and functional,
and were embedded by paired mesochia in the forward end of the abdominal cavity, just under the
vertebral column.
Microscopic examination of the testes indicates
that males have diametric testes (Fig. 3). There was
a mature follicle with sperm in the middle zone
between the germinal and distal zones of the testis
(Pratt 1988). In cross section, different phases of
development of the testis were observed. In the initial phase (spermatogenesis), there were two types of
cells; spermatogonias (spherical, nuclei rich in chromatin) and Sertoli cells (small, nuclei with few chromatin). Both types of cells had a mitotic prophase,
the spermatogonias appeared and each Sertoli cell
appeared in primary and secondary spermatocytes.
In the second meiotic prophase, the spermiogenesis
began and the sperm was differentiated (Fig. 3).
The development of the testes continued with
spermiogenesis. In this phase, the sperm was
formed. The sperm had a spiral shape and then was
liberated (Fig. 4). In this study, sharks >180-cm TL
had each phase of development of the testes
described, confirming that the size of first maturity
for Sphyrna lewini males was at 180 cm TL.
Fig. 2. Relationship between total length and clasper length in Sphyrna lewini off south-west Mexico.
aqua vol. 17 no. 1 - 15 January 2011
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Marcela Bejarano-Álvarez, Felipe Galván-Magaña and Rosa Isabel Ochoa-Báez
For sperm storage, the sharks had two paired
ampulla epididymides located in the posterior dorsal wall of the abdominal cavity just below the kidney. The sperm aggregates were formed and stored
between the septa and the lumen of these ampullae
(Pratt & Tanaka 1994). Sphyrna lewini had a pseudostratified ciliate epithelium with sperm aggregation (Fig. 5).
Sphyrna lewini was fund to have a large compound
mass of spermatozeugmata. The spermatozeugmata
were organized masses of sperm bound with a cohesive matrix. In cross section, the spermatozeugmata
were circular to oval and were composed of several
layers of sperm clumps inside an eosinophilic material. The sperm clumps were oriented with heads to
the inside of the mass (Fig. 6). In this study, 40 males
B
A
C
D
Fig. 3. Phases of testes development in S. lewini: Spermatogenesis. A. Spermatogonias. B. Primary Spermatocytes. C. Secondary Spermatocytes. D. Spermatids. (CS: Sertoli cells). X100, X400, H-E Stain.
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Reproductive biology of the scalloped hammerhead shark Sphyrna lewini (Chondrichthyes: Sphyrnidae) off south-west Mexico
of 180-251 cm TL were reviewed. All had large
quantities of spermatozeugmata. Our result confirms
that the maturity size of males was at 180 cm TL.
To determine maturity in females, we analyzed
342 females, of which 79 were mature at 200-288
cm TL. In contrast to males, the maturity of
females could be determined by the mating scars,
presence of semen in the cloaca, condition of the
uterus, and oocyte diameter. Mature females from
228-259 cm TL had an oocyte diameter from 1-3
Fig. 4. Spermiogenesis (CS: Sertoli cells; ESP: sperm). X100. X400. H-E Stain.
Fig. 5. Deferens ducts of Sphyrna lewini (ESP: sperm; ESC: pseudostratified epithelium). X400. H-E Stain.
aqua vol. 17 no. 1 - 15 January 2011
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Marcela Bejarano-Álvarez, Felipe Galván-Magaña and Rosa Isabel Ochoa-Báez
cm between May and July, although a female at
253 cm TL had the largest oocyte, 6.5 cm diameter, in August 2005. Immature females had undeveloped ovaries with small oocytes (0.5 cm) (Fig.
7). Torres (1999) found similar values, with
females from 212-307 cm TL with oocyte diameters between 0.8-3.8 cm.
The relationship between oocyte diameter, uterus
width, and oviducal gland width to the TL showed
an increase between 200 and 220 cm TL. Based on
Fig. 6. Sperm storage of Sphyrna lewini: compound spermatozeugmata (ESC: pseudostratified ciliate epithelium; CI: inner
layer; NE: eosinophilic nuclei; CE: external layer; CCS: Sertoli cellular cytoplasm; SPZ: spermatozeugmata). X400. H-E
Stain.
Fig. 7. Relation between oocyte diameter (cm) and total length (cm) of Sphyrna lewini.
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Reproductive biology of the scalloped hammerhead shark Sphyrna lewini (Chondrichthyes: Sphyrnidae) off south-west Mexico
the condition of the uterus and ovary, female
Sphyrna lewini mature at 220 cm TL.
The females had only one functional ovary, the
right attached to the anterior end of the epigonal
organ. The left ovary was rudimentary, small and
without ova. Immature females had undeveloped
ovaries and small ova (0.5 cm) were seen at this
stage. As the female reached maturity, several eggs
developed more quickly than others (1-3 cm). The
ovarian eggs passed through the common ostium
Fig. 8. Transversal fold of oviducal gland in mature female Sphyrna lewini. ESC: Pseudostratified epithelium; TCo: Conjunctive tissue. X400. H-E Stain.
Fig. 9. Length interval of S. lewini embryos off south-west Mexico.
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Marcela Bejarano-Álvarez, Felipe Galván-Magaña and Rosa Isabel Ochoa-Báez
into the oviducts, where they were fertilized and
become encased into an embryonic membrane to
pass to the oviducal gland and descend into the
uterus where the embryonic development occurs
(Chen et al. 1988).
Sphyrna lewini, Mazatlan, Sinaloa,. Mexico. Photo by Y.
Torres Rojas.
Sphyrna lewini is a viviparous species. The oviducal
gland function was to fertilize, encapsulate eggs and
store sperm. Sphyrna lewini had different sizes of
oviducal glands. In immature females the diameter
was 5 mm and in mature females it was 3-5 cm. In
our study it was not possible to find sperm stored in
the oviducal glands of the examined females (Fig. 8),
although Pratt (1993) had evidence of long-term
sperm storage in S. lewini for months or even years.
Posterior to the oviducal gland were the reproductive ducts, which were enlarged to form the uterus.
In immature females, the uterus was thin and small,
from 0.3 to 0.5 cm in females of 99-165 cm TL. As
females grow, the uterus increased in length. The
maximum uterine size was 70 cm in a postpartum
female (276 cm TL). In gravid females, the uterus
length reached 52 cm and contained uterine eggs or
embryos.
In our study, all embryos were ready to be born.
We found no embryos in different stages of development. A total of 50 gravid females were counted
with lengths from 239-288 cm TL. The number of
embryos was between 6 and 40, for a total of 1083
embryos. The most common fecundity was 14 to 30
embryos. There was no relation between the maternal size and the number of embryos (R2 = 0.33).
The period of parturition for pregnant females
was in summer, when the embryos reached total
Sphyrna lewini, Revillagigedo. Photo by M. Bejarano Alvarez.
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Reproductive biology of the scalloped hammerhead shark Sphyrna lewini (Chondrichthyes: Sphyrnidae) off south-west Mexico
lengths between 41 and 51 cm. We measured only
569 of the 1083 embryos because they had similar
sizes at birth (Fig. 9). The embryos were recorded
from April to August 2005 with the highest number of embryos during June (345) and July (292)
2005. During May 2006 we found 214 embryos.
Based on the oocyte growth and parturition, we
estimated a gestation period of 10 months, similar
to that Chen et al. (1988) reported from Taiwan.
We found 50 gravid females and 70 neonates of
Sphyrna lewini. The neonate catches were near the
coast, whereas the adults were caught offshore,
except for gravid females and postparturition
females, which were caught with the neonates. The
occurrence of pregnant females in the summer with
embryos at advanced stages of development and of
neonate specimens with lengths between 51-60 cm
TL indicates a well-defined reproductive period for
this species and suggests that there could be a nursery ground for S. lewini off south-west Mexico.
DISCUSSION
Sphyrna lewini is the most abundant species of
shark and remains all year off the south-west Mexican coast (Oaxaca coast), mainly during the summer with gravid females and neonates. Sierra (1995)
reported that S. lewini is the main component in the
fisheries of the Gulf of Tehuantepec, followed by the
silky shark Carcharhinus falciformis, and Campuzano (2002) reported this shark as the mostcaught species off Chiapas. In the Gulf of California,
Galván et al. (1989) mentioned that S. lewini was
one of the most abundant sharks caught off Isla Cerralvo. In contrast to these investigations where juveniles predominated, this study generates a contribution to the reproductive biology of the species in the
area because it represented all stages of maturity of
both sexes and all year round.
In our study, we observed two well-differentiated
groups: one of neonates and juveniles (45-160 cm
TL) and another of adults (170-288 cm TL) where
males were more abundant than females. For juveniles and neonates, the sex ratio was about 1:1.
Klimley (1987) suggests that female S. lewini move
offshore at a smaller size than males for feeding,
and this causes the females to grow more rapidly
and mature at a larger size than males. The mature
females are the first in summer to give birth,
whereas males arrive for mating (Torres 1999).
During 2005 the greater abundance of males was
in spring and summer and the gravid females and
neonates were more abundant in summer. Torres
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(1999) reported sizes in juveniles between 67 and
121 cm TL, which were the most abundant and
supported the fishery off north-west Mexico. In
this study, the females were larger than males. The
largest female seen was 288 cm TL. Similar sizes
were reported by Clarke (1971), Branstetter
(1981), Torres (1999) and Campuzano (2002).
Based on clasper calcification and growth of males,
we identified three sexual stages: immature, juveniles and adults. Sexual maturity in males begins at
about 110 cm TL, a size when claspers are semicalcified. Males off the Oaxacan coast reached sexual
maturity at 178 cm TL. Bass et al. (1975) reported
that males matured between 140 and 165 cm TL,
whereas Castro (1983) reported that S. lewini from
North American waters probably mature at about
180 cm TL and Chen et al. (1988) reported maturity size at 198 cm TL. In the Gulf of California,
Torres (1999) found that maturation in males
begins at 142 cm TL, reaching full maturity at 173
cm TL. Similar results were obtained by Klimley
(1987) who reported sizes at maturity of 177 cm
TL in males, whereas Campuzano (2002) reported
a size of maturity of 175 cm TL off Chiapas.
In different species of sharks, the number and size
of follicles in development depends on the stage of
the reproductive cycle and reproductive mode. In
viviparous species, the phase of follicle development is longer than in that of those oviparous
(Hamlett & Koob 1999). In the analysis of the
testes of S. lewini, we found a pattern in the follicle development of a diametric type, similar to
other carcharhinid sharks (blue shark) (Pratt
1988). We found that Sertoli cells were in the
periphery of the follicle, and the spermatozoa were
with their heads facing the cells. The type of sperm
storage in S. lewini was a compound spermatozeugmata. This had been described for other
species of carcharhinids, such Rhizoprionodon terranovae and Prionace glauca (Pratt & Tanaka 1994).
This sperm storage system resists loss during mating. Sperm storage is an advantage to nomadic
species such as Sphyrna lewini or Prionace glauca,
for which copulation may be infrequent. Sperm
storage insures that the investment in sexual products is used most efficiently (Pratt 1979).
We found that females with 220 cm TL were
mature, with characteristics such as embryos in the
uterus, a developed ovary, mating scars, and in
some females the presence of semen in the cloaca.
Similar sizes of mature females had been reported
by other authors. Chen et al. (1988) found a size of
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Marcela Bejarano-Álvarez, Felipe Galván-Magaña and Rosa Isabel Ochoa-Báez
210 cm TL in mature females in Taiwan waters.
Off Mexico, Torres (1999) and Campuzano (2002)
reported a maturity size of 212 cm and 215 cm TL.
The females grow faster than males to reach maturity because they must have the necessary size to
support the gestation of embryos (Klimley 1987).
We observed a difference in the size of oviducal
glands (structure that allows the storage of sperm)
between juveniles and adult females. In viviparous
species like S. lewini, the oviducal gland produces a
thin membrane to separate the embryos for their
individual development in the uterus.
In our study, we found no sperm in the oviducal
glands, but this condition had been reported by
Pratt (1993) in S. lewini. This species has longterm sperm storage, a characteristic of nomadic
sharks, such as Prionace glauca and Carcharhinus
obscurus, that can store sperm in specialized tubules
for months or years.
Sphyrna lewini is a species with intermediate
fecundity (40 embryos in this study), compared
with other species as the blue shark, Prionace glauca
(100 embryos) or tiger shark Galeocerdo cuvier (82
embryos) (Compagno et al. 2005). In our study we
found a wide range of fecundity, between 6 and 40
embryos. These values are comparable to those
obtained by Torres (1999) (R2 = 0.20), who
explained that this relation was influenced by the
stress caused in females that have been caught in
the shark fishery. The highest fecundity observed
was 40 embryos. Chen et al. (1988), Torres (1999)
and Campuzano (2002) found fecundity of 38, 32
and 43 embryos respectively.
The relationship between the growth pattern of
embryos and ovarian eggs in the uterus suggests
that eggs had been fertilized immediately after parturition (Chen et al. 1988). Based on this information, we estimated a gestation period of 10 months.
The nursery grounds are geographical locations,
where gravid females give birth their young and
where neonates and juveniles spend their first
weeks, months, or years (Castro 1993). The adults
are migratory and they congregate offshore;
whereas neonates and juveniles inhabit coastal
nursery areas during the summer months. The
coastal nursery areas are well-documented in the
western Atlantic from Cape Cod to Cape
Canaveral (Carlson 1999).
Off Mexico there are nursery grounds for different species of sharks, mainly off the Caribbean
coast. The central and southern Gulf of California
also serves as a mating, birthing, and nursery area
21
for several shark species during spring and summer,
including S. lewini (Salomon-Aguilar et al. 2009).
We found 50 gravid females and 70 neonates of S.
lewini. The neonate catches were near the coast,
whereas the adults were caught offshore, except for
gravid females and postparturition females, which
were caught with the neonates.
The neonates were caught off Oaxaca during
summer, which is similar to reports of births of this
shark in other places, indicating that the pupping
season is during summer (June to August) (Castro
1983; Chen et al. 1988).
Bass (1978) described these areas and named
them as primary nursery grounds. Many nursery
grounds are found in productive zones where
sharks find the biotic (abundant prey) and abiotic
conditions that allow neonates to grow (Castro
1993; Salomon-Aguilar et al. 2009). The presence
of pregnant females in the summer with embryos
at advanced stages of development and of neonate
specimens with lengths between 51-60 cm TL suggests a well-defined reproductive period for this
species off south-west Mexico.
Our research provides important information
about the reproductive status of this species covering embryos, neonates, juveniles, and adults of
both genders. This basic information on the reproductive biology of a species, whose status is vulnerable according to the IUCN Red List, will help to
establish management plans for fisheries or conservation of this shark species. It is also important to
know that thanks to the results obtained in this
study, S. lewini has been proposed for listing in
Appendix II of CITES and in standards of protection of the species in Mexico.
ACKNOWLEDGEMENTS
We would like to thank SAGARPA-CONACYT
for the financial support in the project 2003-101
“Characterization of artisanal fisheries of sharks
landed in Salina Cruz, Oaxaca, Mexico” to fishermen of Chipehua, Maribel Carrera for helping in
the sampling, and the Morphophysiology Laboratory at CICIMAR-IPN. The first author thanks
CONACYT and PIFI. Felipe Galvan-Magaña and
Rosa Isabel Ochoa-Baez thank Instituto Politécnico Nacional for fellowships (COFAA and EDI).
Also thanks to Lucía Briseño Haro and Dr. Ellis
Glazier for editing the English-language text and
thanks to Helen Larson and the anonymous referees for their comments and corrections. This paper
is dedicated to my parents Cesar Bejarano and
aqua vol. 17 no. 1 - 15 January 2011
Reproductive biology of the scalloped hammerhead shark Sphyrna lewini (Chondrichthyes: Sphyrnidae) off south-west Mexico
Gilma Alvarez as well as my brothers Cesar,
Ernesto and my sister Angela.
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