Introduction
The scalloped hammerhead (Sphyrna lewini) is a coastal-oceanic species distributed throughout tropical and warm temperate oceans around the world (Compagno, Reference Compagno1984). It occupies a wide range of habitats; the young typically inhabit shallow bays and estuaries, while adults live in continental shelves and adjacent waters, occurring at depths to 1043 m (Moore & Gates, Reference Moore and Gates2015). In the eastern tropical Pacific, S. lewini migrate during the summer to the Gulf of California to reproduce (Klimley, Reference Klimley1987). This shark is a placental viviparous species with a gestation period of 11 months (Torres-Huerta et al., Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008). They give birth to 14–41 pups (Bass et al., Reference Bass, D'Aubrey and Kistnasamy1975; Branstetter, Reference Branstetter1987; Hazin et al., Reference Hazin, Fischer and Broadhurst2001a; White et al., Reference White, Bartron and Potter2008; Bejarano-Álvarez et al., Reference Bejarano-Álvarez, Galván-Magaña and Ochoa-Baéz2011; Chodrijah & Setyadji, Reference Chodrijah and Setyadji2015; Gallagher & Klimley, Reference Gallagher and Klimley2018) in which the size at birth has been reported to be between 40–53 cm total length (TL) (Clarke, Reference Clark1971; Bass et al., Reference Bass, D'Aubrey and Kistnasamy1975; Branstetter, Reference Branstetter1987; Chen et al., Reference Chen, Leu, Joung and Lo1990; Torres-Huerta et al., Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008; Bejarano-Álvarez et al., Reference Bejarano-Álvarez, Galván-Magaña and Ochoa-Baéz2011). In the Pacific Ocean, male S. lewini reach sexual maturity between 170 and 177 cm TL (Klimley, Reference Klimley1987; Torres-Huerta et al., Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008), while females reach maturity between 207 and 212 cm TL (Compagno, Reference Compagno1984; Torres-Huerta et al., Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008).
Given the large size at maturity and low fecundity, this species may be vulnerable to overexploitation (Chapman et al., Reference Chapman, Pikitch, Babcock and Shivji2005; Simpfendorfer & Heupel, Reference Simpfendorfer, Heupel, Carrier, Musick and Heithaus2012). Internationally, a large number of S. lewini are subject to direct fishing and bycatch by a variety of fishing gears (e.g. gillnets, long-lines, trammel nets, trawls, static demersal) in both inshore and offshore areas (Maguire et al., Reference Maguire, Sissenwine, Csirke, Grainger and Garcia2006; Martínez-Ortíz et al., Reference Martínez-Ortíz, Aires-da-Silva, Lennert-Cody and Maunder2015; Rigby et al., Reference Rigby, Barreto, Carlson, Fernando, Fordham, Herman, Jabado, Liu, Marshall, Pacoureau, Romanov, Sherley and Winker2019a). For instance, in the north-west and central-west Atlantic Ocean (USA), it was estimated that Sphyrnidae (S. lewini, S. mokarran and S. zygaena) abundance decreased 89% during 1986–2005 (Rigby et al., Reference Rigby, Barreto, Carlson, Fernando, Fordham, Herman, Jabado, Liu, Marshall, Pacoureau, Romanov, Sherley and Winker2019a), whereas in the north-eastern Pacific Ocean, countries such as Costa Rica and Mexico demonstrated a 60% decrease in the relative abundance of S. lewini (e.g. Arauz et al., Reference Arauz, Choen, Ballestero, Bolaños and Pérez2004; Soriano-Velásquez et al., Reference Soriana-Velásquez, Acal-Sánchez, Castillo-Géniz, Vázquez-Gómez, Ramírez-Santiago, Arreguín-Sánchez, Beléndez-Moreno, Méndez Gómez-Humarán, Solana-Sansores and Rangel-Dávalos2006). Conversely, in Ecuador's central-eastern Pacific Ocean, the landings of S. lewini decreased by 50% from 2003–2006 (Martínez et al., Reference Martínez-Ortíz, Galván-Magaña, Carrera-Fernández, Mendoza-Intriago, Estupiñán-Montaño, Cedeño-Figueroa, Martínez-Ortíz and Galván-Magaña2007) and 45.4% between 2008–2010 (Ministerial Agreement No. 116 in 2013). In accordance, S. lewini is categorized as Critically Endangered by the IUCN Red List (Rigby et al., Reference Rigby, Dulvy, Barreto, Carlson, Fernando, Fordham, Francis, Herman, Jabado, Liu, Marshall, Pacoureau, Romanov, Sherley and Winker2019b), and it is included in CITES Appendix II in order to verify that such trade is not prejudicial to the survival of this species in the wild (CITES, 2013).
In Ecuador, S. lewini is one of the main species caught by artisanal and industrial fisheries. However, few efforts have been carried out to gather information on the reproductive biology of the species, despite the importance of generating information for stock assessments and developing management for conservation plans in the region. Currently, there are no studies regarding the reproduction of S. lewini in Ecuadorian waters, which would permit the generation of adequate management measures (i.e. minimum size for capture, closed fishing seasons, identification of nursery areas, etc.). However, the Ministry of Agriculture, Livestock, Aquaculture, and Fishing (MAGAP) has promulgated precautionary regulations for the management of hammerhead shark stocks. The MAGAP has restricted the captures of S. lewini to a maximum of five individuals per each small artisanal boat (‘fibres’ from 7–9 m of length), in which the caught individuals must not be smaller that 150 cm TL. Additionally, there should be no gravid females on board; if they are captured, they should be returned to the sea immediately. Furthermore, the capture of hammerhead sharks (S. lewini and S. zygaena) is prohibited for industrial fishing vessels (Ministerial Agreement No. 116 in 2013). In Ecuador, few efforts have been developed for the regulation of S. lewini fisheries; therefore, there is a need to increase the knowledge of Ecuador's shark species to appropriately manage their populations. This study aims to provide baseline data on the reproductive biology of S. lewini to inform fisheries management plans in the central-eastern Pacific Ocean.
Materials and methods
This study was based on 1664 Sphyrna lewini specimens (595 males and 1069 females) collected from various commercial fisheries (e.g. pelagic longline, surface gillnets, purse seines, ‘mother-ship’ [barco nodiriza in Spanish]) operating in the central-eastern Pacific Ocean (between 4°N and 4°S and from the coast to 93°W; Figure 1) and landed in Manta, Ecuador during 2003–2009.
Fig. 1. Study area showing the port of Manta, Ecuador, where specimens of Sphyrna lewini were collected from commercial landings (2003–2009, except 2007), with the fishing grounds (crossed area) and bathymetry indicated.
Once landed at the port, the TL for each specimen was recorded, and the gonads of a subsample (57 males and 92 females) were examined in detail for the evaluation of their reproductive state. Reproductive organs were removed and stored in a solution of 10% formalin prior to transportation to the laboratory. Data collected from males included length and width of the testes, and the outer length and calcification state of the claspers (Pratt, Reference Pratt1979; Hazin et al., Reference Hazin, Fischer and Broadhurst2001a, Reference Hazin, Lucena, Souza, Boeckman, Broadhurst and Menni2001b). In the case of females, the oviducal gland width, the maximum ovarian follicle diameter (MOFD), uterine width and, if present, the number of embryos and length and sex of the pups were recorded (Pratt, Reference Pratt1979; Hazin et al., Reference Hazin, Fischer and Broadhurst2001a, Reference Hazin, Lucena, Souza, Boeckman, Broadhurst and Menni2001b).
Inferences on stages of maturation were made according to definitions provided in previous studies (Pratt, Reference Pratt1979; Hazin et al., Reference Hazin, Fischer and Broadhurst2001a, Reference Hazin, Lucena, Souza, Boeckman, Broadhurst and Menni2001b; ICES, 2013). Male maturation was evaluated based on the development of the testes and the calcification of the claspers; thus, males were classified in three stages. Individuals with relatively short, flexible and non-calcified claspers that did not extend beyond the posterior edge of the pelvic fins and had small and undeveloped testes were considered immature. Males with claspers that were flexible, partially calcified and as long as or longer than the pelvic fins, as well as with developing and commenced segmented testes, were classified as developing males. Mature males were characterized by elongated and calcified claspers (ICES, 2013). Females were separated into four stages based on the development of the oviducal gland, uteri, MOFD and ovary. Specimens were considered immature if they had undeveloped sexual organs, filiform uteri and no vitellogenic activity in their ovaries (Pratt, Reference Pratt1979; Hazin et al., Reference Hazin, Fischer and Broadhurst2001a, Reference Hazin, Lucena, Souza, Boeckman, Broadhurst and Menni2001b; ICES, 2013). Developing females had distinguishable and developing oviducal glands, follicles of different stages of development, some small and median sized follicles with yolk, and enlarging uteri (ICES, 2013). Mature females had large follicles ready to be ovulated, as well as fully developed oviducal glands and uteri (ICES, 2013). Finally, females with fully formed embryos and reduced or absent yolk sacs were classified as in late pregnancy (ICES, 2013).
A Chi-squared goodness-of-fit test was used to examine the hypothesis of an equal sex ratio (1:1) among the total number of S. lewini landed specimens between 2003–2009. The relationship between TL and the different reproductive structures (e.g. clasper length, testes length and width, oviducal gland width and uterine width) were plotted to indicate the onset of sexual maturity (Natanson & Caillet, Reference Natanson and Cailliet1986). Size at maturity (TL50), which was defined as the length at which 50% of the population is mature, was estimated for males and females by fitting a logistic regression model to the binomial maturity data based on their condition (0 = immature and developing, 1 = mature) (Mollet et al., Reference Mollet, Cliff, Pratt and Stevens2000). The length at which 50% of the individuals had reached sexual maturity was modelled using the maximum likelihood as follows: TL50 = 1/1 + ea+b (TL), where TL50 is the proportion of mature individuals, a and b are model parameters, and TL is the total length of each specimen. The goodness of fit of the model logistic was examined using the Hosmer–Lemeshow test.
Fecundity was estimated by counting the total number of embryos and plotted as mean embryo size against time (months) to estimate the length and timing of the gestation period. To construct the gestation period graph, the quartiles were used with 95% confidence intervals. Size at birth ranged from the measurement of the largest embryo to that of the smallest neonate. All analyses were conducted with the significance level set at α = 0.05.
Results
In total, 35.8% (N = 595) of the 1664 specimens were males, and 64.2% (N = 1069) were females. Males ranged from 65–310 cm TL, with a modal TL class between 130–209 cm (Mean ± SD = 181.6 ± 38.8 cm TL), whereas females ranged from 50–300 cm TL, with a modal TL class between 130–209 cm TL (188.3 ± 46.5 cm TL) (Figure 2). More females were landed, with an overall sex ratio of 1M:1.8F (χ2 = 135.02; P < 2.2 × 10–16); this trend was observed in all years except 2003, when the sex ratio was not significantly different from 1:1 (Table 1).
Fig. 2. Length frequency distribution of males and females of Sphyrna lewini landed in the port of Manta, Ecuador, between 2003–2009 (except 2007).
Table 1. Number of individuals of scalloped hammerhead (Sphyrna lewini) in the central-eastern Pacific Ocean landed in the artisanal port of Manta (Ecuador), between 2003–2009 (except 2007), expressed in the number of individuals (N), total length (TL, in Interval and mean ± SD) and sex ratio.
In the males that measured between 65–195 cm TL, non-calcified claspers were present (varying in length from 2–17 cm) and clasper length increased rapidly with TL. Males between 151–316 cm TL had calcified claspers that measured 15–24 cm; thus, 285 individuals were mature, 32 were developing and 278 were mature specimens (Figure 3). Of the total male specimens landed (N = 595), only 57 of them were examined in detail: 25 were immature, 8 were developing and 24 were mature specimens (Table 2). The TL50 at maturity of the males was estimated to be 178.1 cm (95% CI: 175.5–180.6, TL50 = 1/1 + e –19.211 + (0.108 × TL); Hosmer–Lemeshow test, χ2 = 3.47, P = 0 0.90) (Figure 4A). According to the estimated TL50, the percentage of immature and mature males caught between 2003–2009 (except 2007) was 54.3 and 45.7%, respectively.
Fig. 3. Relationship between clasper length and total length according to the degree of calcification of the clasper in males of Sphyrna lewini landed in the port of Manta, Ecuador, between 2003–2009 (except 2007).
Fig. 4. Maturity ogives for males (A; N = 595 specimens) and females (B; N = 92 specimens) of Sphyrna lewini landed in Manta, Ecuador, between 2003–2009 (except 2007), representing the length at which 50% of the population had reached sexual maturity.
Table 2. Characteristics of maturation stages, size range (total length) and number of males of Sphyrna lewini
All lengths are in cm.
Of the total number of female specimens recorded (N = 1069), only 92 were examined in detail: 49 were immature, 27 were developing, 4 were mature and 12 were in late pregnancy (Table 3). From this sample, the TL50 for females was estimated at 219.4 cm TL (95% CI: 208.89–229.9, TL50 = 1/1 + e –15.516 + (0.071 × TL); Hosmer–Lemeshow test, χ2 = 1.06, P = 0 0.98) (Figure 4B). On this basis, few mature females (17.3%) were recorded between 2003 and 2009, as compared with immature females (82.7%).
Table 3. Characteristics of maturation stages, size range (total length) and number of females of Sphyrna lewini
MOFD, Maximum ovarian follicle diameter. All lengths are in cm.
A total of 12 gravid females were analysed in detail; a total of 127 embryos were counted, with an estimated fecundity of 16–22 embryos. Smaller embryos were observed during October and measured between 11.1–14.2 cm TL (13.1 ± 0.74 cm TL). Larger embryos were recorded in June and measured 43.6–54.6 cm TL (50.2 ± 3.31 cm TL) (Figure 5). Size at birth was estimated as the interval between the largest embryo and the smallest neonate, which ranged from 47 (smallest neonate) to 55 (largest embryo) cm TL.
Fig. 5. Length of Sphyrna lewini embryos according to the month, with the number of gravid females examined (NL = 12) and the total number of pups (NP = 127) as observed from the landings at Manta, Ecuador, between 2003–2009 (except 2007). The length of the smallest free-living specimen observed (50 cm) is shown as a dashed line.
Discussion
This is the first study to estimate the length-at-maturity (males = 178.1 cm TL, females = 219.4 cm TL) and the size at birth (47–55 cm TL) of Sphyrna lewini in Ecuadorian waters. Although the results were based on limited data, fecundity was observed as 16–22 pups, and the gestation period was likely to be <12 months, although the reproductive cycle may be longer.
Over the study period, there were proportionally more females caught, with the mean annual sex composition over the years 2003–2009 comprising 62.2% females and 37.8% males, and the sex ratio significantly favouring females in five of the six years. These results contrast with previous studies in the Gulf of California (Mexico), where males dominated in the catches (Torres-Huerta et al., Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008). This may be due to: (1) the location of the sampling areas; (2) the individuals that are most likely caught by different fishing gear and methods (e.g. long-lines, gillnet, purse seines); (3) the use of different habitats, possibly in deeper waters beyond the continental shelf (Stevens & Lyle, Reference Stevens and Lyle1989); and (4) tendencies for sexual segregation in different areas (Wearmouth & Sims, Reference Wearmouth and Sims2008; Harry et al., Reference Harry, Macbeth, Gutteridge and Simpfendorfer2011); whereby females may spend more time in oceanic areas, whilst males exhibit a preference for coastal environments (Estupiñán-Montaño et al., in press). The potential for a high fishing pressure on females of the stock could affect recruitment, which could indicate that further management measures may be required.
The length range recorded in this study is consistent with those reported by Torres-Huerta et al. (Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008) in the Gulf of California, Mexico (males = 42–290 cm TL; females = 41–363 cm TL) which included neonates, juveniles and adults. However, the most frequent measurements for males and females in this study ranged between 140–186 cm TL and 118–208 cm TL, respectively (N ≥ 100; Figure 2). The results of the length–frequency distribution produced by the study according to the LT50, showed that more juveniles of both sexes were captured. This information suggests that fishing activity in the Pacific Ocean is mainly carried out near the coast and around seamounts (Estupiñán-Montaño et al., in press). In such habitats, there may be access to nursery areas and other aggregation zones, which increases the likelihood of capturing immature organisms. Therefore, if significant numbers of immature and gravid specimens continue to be caught in the future, the rate of recruitment will likely decrease, and recovery could take several years (Chodrijah & Setyadji, Reference Chodrijah and Setyadji2015). These results show the need to revise and adjust existing regulations, given that the Ministerial Agreement No. 116 of 2013 prohibits the capture of individuals smaller than 150 cm TL and gravid specimens. The present results could be adopted to establish a minimum size for capture (LT50; males: 178.1 cm; females: 219.4 cm), and to implement other potential protective measures (e.g. quotas and/or size limits) with regard to the management of relevant fisheries and the capture of hammerhead shark species (Sphyrna spp.).
This study estimated that male and female of S. lewini reach sexual maturity at larger sizes in Ecuadorian waters in comparison to other sites of the north-eastern Pacific Ocean (i.e. Gulf of California, Mexico), where smaller sizes for sexual maturity have been recorded (170 cm TL and 207 cm TL for males and females, respectively; Torres-Huerta et al., Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008). This discrepancy may be due to: (1) S. lewini from the Gulf of California have been heavily exploited and may have responded by reducing the median size at maturity; (2) methodological differences being used to assess sexual maturity (e.g. statistical analysis, direct observation, or microscopic analysis of gonads); (3) the effects of other fisheries and activities; and (4) latitudinal and/or stock-related differences in life-history parameters which may related to different environmental factors, conditions and food sources (e.g. Conover, Reference Conover1990; Lombardi-Carlson et al., Reference Lombardi-Carlson, Cortés, Parsons and Manire2003).
In the present study, the smallest embryos (11.1–14.1 cm TL) were recorded in early (12th) October. This is similar to that observed in the Gulf of California, Mexico, where embryos with an average size of 10.4 cm TL were reported in September (Torres-Huerta et al., Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008), suggesting that ovulation for this species occurs in August/September. The largest embryos observed in the present study (>43 cm TL) were observed in June. This also coincides with the observations reported by Torres-Huerta et al. (Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008) in the Gulf of California, Mexico, where embryos of 41–59 cm TL were detected in July, suggesting a gestation period of about 11 months in which the birth occurred during the latter month. The high similarity in terms of the period of the gestation and birth may be explained by the genetic relationship among small populations of S. lewini along the eastern Pacific Ocean (Nance et al., Reference Nance, Klimley, Galván-Magaña, Martínez-Ortíz and Marko2011), as well as the presence of neonates in the Pacific coast of Costa Rica during July–August (Zanella & López-Garro, Reference Zanella and López-Garro2015) and in Panama during March–June (Robles et al., Reference Robles, Montes and Vega2015). In spite of the similarities between our results and those from other studies, our results should be interpreted with caution due to the low number of gravid females analysed (N = 12); hence, more studies are needed to support these findings.
Furthermore, this study suggests that the size at birth of S. lewini in Ecuadorian waters is estimated between 47–55 cm TL, considering the largest embryos and the smallest neonates observed. Although few neonates were registered in this study, our approach to the size at birth for this species is consistent with the approach taken by Torres-Huerta et al. (Reference Torres-Huerta, Villavicencio-Garayzar and Corro-Espinoza2008) whose estimation was between 41–53 cm TL.
In conclusion, based on the similarities with other studies in the eastern Pacific Ocean which have focused on the reproductive biology of S. lewini, this work suggests that for the central-eastern Pacific Ocean: (1) the fishing activity is in nearshore areas and oceanic islands (i.e. seamounts), from where mostly immature individuals are landed; (2) the size at maturity in this area is larger than in other localities; and (3) the gestation period starts in September and ends between June–July (10–11 months), with sizes at birth between 47–55 cm TL. Additionally, this work highlights the need to increase the basic knowledge of S. lewini in Ecuadorian waters and the central-eastern Pacific Ocean, which along with other research (e.g. demography and genetics) can support the development and implementation of appropriate management and conservation measures for the species.
Acknowledgements
The authors would like to thank the fishermen and processors of Manta, Ecuador, for facilitating data and sample collection, and the Facultad de Ciencias del Mar of the Universidad Laica ‘Eloy Alfaro’ de Manabí. C. Estupiñán-Montaño thanks L. Castillo-Géniz and J.C. Pérez-Jiménez for their support during the course of this study. F. Galván-Magaña thanks the Instituto Politécnico Nacional for the fellowships provided (COFAA, EDI). Thanks to K. Sullivan, B. Finley and D. Edgar for translating the text to English. We thank the anonymous reviewers for improving the manuscript.
Financial support
This study was supported by the Fundación Alium Pacific through a grant to Colombo Estupiñán-Montaño.
