sharks of the open ocean || the reproductive biology of pelagic elasmobranchs

Chapter 3

The Reproductive Biology of Pelagic Elasmobranchs

Franklin F. Snelson Jr., George H. Burgess and Brenda L. Roman

Abstract

We review the reproductive biology of 13 species of pelagic elasmobranchs – family Alopiidae: Alopias pelagicus (pelagic thresher), A. superciliosus (bigeye thresher), and A. vulpinus (common thresher); family Lamnidae: Isurus oxyrinchus (shortfi n mako), I. paucus (longfi n mako), Lamna ditropis (salmon shark), L. nasus (porbeagle), and Carcharodon carcharias (white shark); family Carcharhinidae: Carcharhinus falciformis (silky shark), C. longimanus (oceanic whitetip shark), C. signatus (night shark), and Prionace glauca (blue shark); and family Dasyatidae: Pteroplatytrygon violacea (pelagic stingray). All of these species are viviparous, but they exhibit diverse modes of repro-duction. The lamniform sharks of the families Alopiidae and Lamnidae exhibit aplacental viviparity with embryonic oophagy. The requiem sharks, family Carcharhinidae, exhibit placental viviparity. Reproduction in the stingray involves aplacental viviparity with tro-phonemata. For each species, we summarize information on litter size, birth size, gesta-tion period, reproductive periodicity, age and size at maturity, and development. When known, patterns of geographic variation in these parameters are also discussed.

Key words: embryo, fecundity, gestation, maturity, reproduction, litter size, birth size, shark, stingray, Alopiidae, Lamnidae, Carcharhinidae, Dasyatidae.

Introduction

Elasmobranchs are threatened globally in large part because life-history traits that have served so admirably over evolutionary time have become serious liabilities in a world where intense fi shing pressure and habitat alteration have become commonplace. The reproductive characteristics of elasmobranchs, such as their growth and longevity attributes, make this group of fi shes vulnerable to intensifying anthropogenic threats and impacts.

Reproduction in elasmobranch fi shes is variable in scope and style and is novel in many ways (see Hamlett, 1999; Hamlett and Koob, 1999; Carrier et al., 2004, for recent overviews). In this chapter we review the modes of reproduction and related life-history parameters of 13 species of pelagic sharks and rays. The types of reproduction exhibited

Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock

© 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

Reproductive Biology of Pelagic Elasmobranchs 25

represent a cross section of the breadth of innovation encountered within the viviparous elasmobranchs. As is the case for other aspects of elasmobranch biology, knowledge of reproduction is advanced for some species and rudimentary for others.

Methods and defi nitions

The life-history traits discussed in this review are litter size, birth size, gestation period, reproductively related migrations and seasonality, maturity size and age, and embryonic development. We defi ne these terms and briefl y describe the usual means by which these characteristics are determined. The possibilities for error arising from these methods are discussed at the end of this chapter.

Litter size refers to the number of young produced from a single gestation and is typi-cally based on the number of developing young found in the uteri of pregnant females. Size at birth is generally estimated by noting the sizes of the largest intrauterine fetuses and the smallest free-swimming neonates. However, age and growth data are sometimes used to back-calculate size at birth. The length of gestation is usually estimated from data on embryo and neonate sizes throughout the year. Also, evidence of mating and parturi-tion time, such as bite marks on females and the occurrence of small free-swimmers, is sometimes used to approximate gestation time.

The detection of sexual maturity in elasmobranchs is based on varied criteria that differ between the sexes. In males, the detection of sexual maturity is often based on gross exami-nation of the claspers, the modifi cations of the pelvic fi ns that serve to transfer sperm to the female. Traits such as the calcifi cation and/or relative length of the claspers and the ability to rotate the claspers medially have been used. In females, the enlargement and differentia-tion of the reproductive tract, the presence of yolked oocytes in the ovary, and the presence of embryos in the uterus are all characteristics commonly used to determine maturity. The corresponding age at maturity for both males and females is determined from aging of the vertebrae and other hard structures such as spines, which form annual growth rings in many elasmobranch species. These age data are used to create an age and growth curve, from which a maturity age is extrapolated using estimates of maturity size. Unless otherwise noted, all sizes reported in this chapter are total length (TL).

Information about embryonic development is obtained from observation of the size, stage, and morphology of eggs and embryos in the maternal reproductive tract. The following section discusses the three modes of reproduction exhibited by pelagic elasmobranchs.

Modes of reproduction

We follow the terminology of Hamlett and Koob (1999) in our discussion of reproduc-tive modes. All species treated here are viviparous in that they give birth to living young, although we include a brief description of oviparity for comparison. The method by which the young are nourished during gestation differs among species, and we use this as a system for grouping species into similar reproductive modes.

26 Sharks of the Open Ocean

Oviparity

In oviparous species of elasmobranchs, fertilized eggs are encapsulated in an egg case and deposited in the external environment. All the nutrients that the embryo requires through the course of development are contained within this egg capsule. None of the pelagic spe-cies exhibit oviparity.

Aplacental viviparity with oophagy

The lamniform sharks (family Alopiidae, genus Alopias; and family Lamnidae, genera Lamna, Isurus, and Carcharodon) all exhibit aplacental viviparity with embryonic oophagy. Only the right ovary is functional (Pratt, 1988; Gilmore, 1993). After the ova are fertilized, they are packaged singly in egg capsules, called blastodisc capsules, in the nidamental gland. These capsules then move into the uterus, where development takes place. In the fi rst phase of gestation, the embryos are nourished by yolk from the yolk sac inside the capsule (the encapsulated or prehatching phase). Once the yolk is depleted, the still relatively small embryos hatch from the capsule, beginning the posthatching phase of development. During this phase the embryos feed on the unfertilized yolked ova (oophagy) that the mother has continued to produce during gestation. The consumption of these nutritive capsules causes the embryonic stomachs to become distended, so that they are often referred to as “yolk stomachs.” Embryos in the posthatching phase may also be nourished by uterine fl uids. Toward the end of gestation, the female stops producing nutritive capsules and the late-stage embryos rely on the digestion of yolk in the yolk stomach for energy until birth. As the name implies, there is no placental connection between fetal and maternal systems in these species. White shark reproduction is very poorly understood, but the limited observations available suggest that this species is similar to other lamnid species.

Placental viviparity

The requiem sharks (family Carcharhinidae, genera Carcharhinus and Prionace) are all placental viviparous species. Ova ovulated from the single functional ovary pass through a common ostium into the paired oviducts. In the shell (nidamental) glands they are fertilized and wrapped in a thin capsule. These fertilized capsules move into the paired uteri, where development takes place. During early development, the embryos draw nourishment from the yolk stored in the egg. When the yolk supply is exhausted, the empty yolk sac forms a placenta-like connection with the maternal uterine wall, which becomes highly vascular-ized. This “pseudoplacenta” or yolk sac placenta is unlike a mammalian placenta in deri-vation, but it functions like a true placenta, providing nutrient and probably gas exchange between the maternal and fetal systems (see Hamlett and Koob, 1999, for a review). The embryos rely on placental nutrition to fuel the latter part of their intrauterine devel-opment. The placental connection is broken just before birth and the embryos resorb the remainder of the yolk sac. Newborn young retain only a faint “umbilical” scar.

Aplacental viviparity with trophonemata

The details of reproduction in the pelagic stingray, Pteroplatytrygon violacea (also appear-ing in the literature under the old name Dasyatis violacea), are not well known. What is


known, however, is in general agreement with the patterns of reproduction and develop-ment that have been reported for other species of stingrays (Struhsaker, 1969; Snelson et al., 1988, 1989; Capapé, 1993; Capapé and Zaouali, 1995; Hamlett et al., 1996; Henningsen, 2000). Ova produced in the left ovary pass into the left oviduct and then move through the shell gland, where they are fertilized and collectively wrapped together in a thin egg cap-sule or membrane. The capsule moves into the left uterus, where development takes place. At some point in early gestation the egg capsule ruptures and disappears, either being voided or resorbed. Early development of the embryos is nourished by yolk stored in the egg. The yolk is fully utilized by the midpoint of gestation and the yolk sac is resorbed. During the lat-ter half of gestation, the wall of the female’s uterus becomes modifi ed with dense fi ngerlike projections called trophonemata that extend into the lumen of the uterus. Specialized secre-tory cells on the elongated trophonemata produce a rich nutritious fl uid called histotroph or “uterine milk.” The embryos are bathed in this fl uid, which they either ingest or passively absorb as the primary source of their nutrition during the latter half of development.

Reproductive trends in pelagic elasmobranchs

Despite the methodological limitations of the reproductive study of elasmobranchs and the specifi c limitations on the study of pelagic species, some general trends in the reproduc-tion of these species can be identifi ed. First, none of the pelagic species exhibit the ovipa-rous mode of reproduction. Obviously, this mode would be unsuitable in an open ocean habitat, as large, yolky eggs would be swept away or would sink to the ocean fl oor. Second, although there are obvious taxonomic differences among the species studied here, the sharks, at least, exhibit many commonalities in reproduction. In general, elasmobranchs are characterized by low reproductive rates, with typically low fecundity and long gesta-tion periods relative to other fi sh species (Cortés, 2000, 2004). However, pelagic elasmo-branchs differ from coastal elasmobranchs in having slightly larger litters of smaller young. The carcharhinids and the lamniforms each exhibit their largest litter sizes among pelagic species (Prionace glauca and Isurus oxyrinchus, respectively), as well as typically lower birth sizes relative to maximum adult size. Also, though almost all the pelagic species stud-ied here have relatively rapid growth over their lifetime (Brody or von Bertalanffy growth coeffi cient k � 0.10), their growth during their fi rst free-swimming year is typically slower than that of coastal species (Branstetter, 1990).

The similarities among the pelagic lamniforms and carcharhinids with respect to these traits lend credence to the idea that habitat is a strong selective force on reproduction, and is a better indicator of reproductive characteristics than taxonomic relationship. Thus, the reproductive trends outlined herein may be better understood if we consider the different challenges presented by coastal and pelagic environments. In a coastal habitat, we would expect higher abundance of both food and predators of varying sizes, as compared to in a pelagic habitat, where food availability would be much more scarce and patchy and preda-tor density much lower. In other words, there may be more selective pressure to produce larger, faster-growing young in coastal habitats, where the food resources exist to sustain them and predator avoidance is more important. In the pelagic environment, having larger litters with smaller young may be more appropriate because of limited resources and the necessity of dispersal.


Because information on the reproduction of the pelagic stingray and its coastal rela-tives is limited, it is diffi cult to make such comparisons in this case, but some general dif-ferences are clear. For comparative purposes, we group Pteroplatytrygon violacea with its close relatives, the members of the genus Dasyatis, in which the pelagic stingray was once taxonomically grouped. When considered together with Dasyatis species, P. violacea has similar birth size as a percentage of maximum size. However, it has a shorter gestation time (2 months) than that reported for any Dasyatis species. Also, P. violacea has a larger mean litter size (6) and maximum litter size (9–13) than the Dasyatis species. Thus, it is probable that P. violacea has experienced similar selective pressure as the other pelagic elasmobranchs reviewed here, and that this pressure has infl uenced its reproduction in similar ways, leading it to produce larger litters in a shorter amount of time. In addition, the organically rich uterine fl uid observed by Ranzi (1934) may be a related adaptation to faster growth of the embryos.

Reproduction in lamniform sharks

Perhaps the most obvious difference in reproduction between the lamniform species and the other pelagic species is that the lamnids exhibit oophagy, or ingestion by embryos of ovulated unfertilized ova. Although the aplacental oophagous strategy is not as prevalent in elasmobranchs as placental viviparity, it is interesting that species representing both reproductive strategies have successfully colonized the pelagic habitat, and their repro-ductive parameters are in many ways comparable.

Litter size

Compared to many of the other species in this review, the alopiids have relatively small litters (Table 3.1). Both the pelagic thresher (Alopias pelagicus) and the bigeye thresher (A. superciliosus) typically have two young per litter, although litters of one, three, and four have been reported for the latter species (Nakamura, 1935; Bass et al., 1975; Guitart Manday, 1975; Moreno and Morón, 1992; Taniuchi, 1997; Liu et al., 1999; Compagno, 2001). In the common thresher (A. vulpinus), litters of two to four appear to be common, but as many as seven in a litter have been reported (Strasburg, 1958; Moreno et al., 1989; Compagno, 2001). The reports of only one fetus in a litter probably are due to premature abortion (Moreno et al., 1989). No correlation between the size of the litter and the size of the mother has been reported for any Alopias species.

Litter sizes for the shortfi n mako (Isurus oxyrinchus) are higher, ranging from 4 to 25, with most reports in the range of 8–18 (Branstetter, 1981; Stevens, 1983, 2008; Taniuchi, 1997; Mollet et al., 2000). Using data from several studies, Mollet et al. (2000) calculated the mean litter size for this species as 12.5. Maximum litter size may be as large as 25–30, based on one observation of a lamnid litter from the Mediterranean Sea. However, the identifi cation of the species involved is debatable (Sanzo, 1912; Tortonese, 1950; Mollet et al., 2002b). Larger females appear to have larger litters (Mollet et al., 2000). From the few data available for the longfi n mako (I. paucus), litters of two, with a single embryo in each uterus, appear to be common (Guitart Manday, 1975; Gilmore, 1983). However,

R

eproductive Biology of Pelagic E

lasmobranchs

29

Table 3.1 Summary of litter size and birth size, as estimated by largest embryos and smallest free-swimming neonates, in 13 species of pelagic elasmobranchs.*

Species Litter size Birth size (cm)

Largest embryos Smallest free-swimmers

AlopiidaeAlopias pelagicus 245,86,101,137 15886 13745; 19085

Alopias superciliosus 2–48,20,21,39,65,70,96,101,141; mean�296,141 639; 6820; 73101; 9496; 10067; 10659; 13739 1309; 155–1618,65,96,136

Alopias vulpinus 266,137; 2–645; 3–797 11466,137; 155–1599,45,97 1179,45; 12097; 14525

LamnidaeIsurus oxyrinchus 4–1641,49,62,93,131,141; 1814; 25–30(?)95 6062; 64131; 7193; 7749 �6333; 65–718,55,103,113

Isurus paucus 2–459,60,70,99; 2–832,45 8799; 9270; 9759 12355

Lamna ditropis 2–545; 4–5100,140 7045 �5010; 70103; 8763; 96100

Lamna nasus 1–69,53,57,81,122,142; mean�453,57,81 64–669,81,105; 7757; 7953 6853; 749; 76105

Carcharodon carcharias 2–1452; 2–1719; 4–1418; 5–10146; 99; 16–18(?)42 14552; 151146 12234,83;12926; 13952

CarcharhinidaeCarcharhinus falciformis 2–166,12,15,21,58,107,135,137,141; mean�5–7137,141 67107; 706; 7712; 8021 64137; 6512; 70107; 789,21

Carcharhinus longimanus 1–155,7,9,13,62,67,118,121,132,137,141; mean�6–85,7,13,118,132,137,141 617; 64132; 75121 66121; 7184

Carcharhinus signatus 4–189,21,76,107,117; mean�1176 5656; 5921; 63117; 65107 6021; 6217; 66107; 67117

Prionace glauca 1–62102; 4–757,9,21,37,108,132,137; up to 82110;10–13568; 45–519,110,132,137 35103; 4521

mean�26–3737,102,132,135,139,141

DasyatidaePteroplatytrygon violacea 2–994; 4–789; 5–687,114; 9–13148; mean�6106 1989; 2494 �2590

*Size is total length (cm) for sharks and disk width (cm) for the ray. Superscript numbers refer to reference numbers.


litters of three (Muñoz-Chápuli, 1984) and four (H. L. Pratt Jr. and J. G. Casey, personal communication, 1988, as cited in Gilmore, 1993) have been reported. Compagno (2001) reported litter sizes ranging from two to eight, probably based on an unconfi rmed litter of eight reported by Casey (1986).

Both species of Lamna usually have four young per litter, with two embryos per uterus. For the porbeagle (L. nasus), reports range from one to six per litter (Gauld, 1989; Francis and Stevens, 2000; Jensen et al., 2002); the salmon shark (L. ditropis) has litters of two to fi ve embryos (Tanaka, 1980; Nagasawa, 1998; Compagno, 2001).

Litter size for the white shark (Carcharodon carcharias), like all aspects of its reproduc-tion, is known from only a few documented records. Documented fecundity ranges from 2 to 14, with an average of about 9 (Bigelow and Schroeder, 1948; Uchida et al., 1987, 1996; Bruce, 1992; Francis, 1996; Malcolm et al., 2001; Mollet, 2004). Some of the smaller brood sizes likely resulted from embryos being aborted prior to examination (Bruce, 2008). A lit-ter that possibly consisted of 16–18 embryos was reported by Cliff et al. (2000), but the exact count is in question.

Birth size

Size at birth in Alopias species ranges from 100 to 190 cm TL (Table 3.1). These are rel-atively large birth sizes for sharks, and the largest among the pelagic species reviewed here. However, the total length measurement in these species is greatly infl uenced by the long upper lobe of the caudal fi n.

Most estimates of birth size of A. superciliosus range from 100 to 140 cm (Bass et al., 1975; Gilmore, 1983; Moreno and Morón, 1992; Chen et al., 1997; Compagno, 2001). Although some authors have suggested much smaller birth sizes, from 60 to 75 cm (Nakamura, 1935; Bigelow and Schroeder, 1948; Cadenat, 1956), these lower estimates may be based on premature embryos (Bass et al., 1975) or small sample sizes. Nonetheless, there may be regional differences in birth size for this species, pups being born at larger sizes (135–140 cm) in the Northwest Pacifi c than in other regions (Chen et al., 1997). The larg-est embryo recorded for this species was 137 cm (Chen et al., 1997). The smallest captured free-swimming neonate was 130 cm (Bigelow and Schroeder, 1948).

The only estimate of birth size for A. pelagicus based on a large sample is 158–190 cm for sharks taken in Taiwanese waters (Liu et al., 1999). However, Compagno (2001) reported a 137-cm free-swimming individual from the western Indian Ocean, suggesting that there may also be regional differences in birth size for this species.

Estimates of size at birth in A. vulpinus range from 110 to 160 cm and are compara-ble throughout its range (Gubanov, 1972; Moreno et al., 1989; Compagno, 2001). Free-swimming young as small as 117–120 cm and term fetuses as large as 159 cm have been reported (Bigelow and Schroeder, 1948; Moreno et al., 1989). Cailliet et al. (1983) estimated size at birth at 158 cm from the von Bertalanffy growth equation. It has been suggested that larger females give birth to larger neonates (Bigelow and Schroeder, 1948; Gubanov, 1978), but Moreno et al. (1989) found no correlation between the maximum embryo size and maternal size.

Isurus oxyrinchus has a rather large size at birth, with most estimates ranging from 60 to 70 cm (Bass et al., 1975; Stevens, 1983; Mollet et al., 2000; Compagno, 2001).


However, embryos may occasionally reach larger sizes. Mollet et al. (2000) reported embryos as large as 71 cm, and Duffy and Francis (2001) observed a litter of eight with sizes ranging up to 77 cm. Free-swimming neonates of this species have been reported as small as 63 cm (Casey and Kohler, 1992).

The young of I. paucus are probably born at sizes greater than 90 cm. The largest embryos recorded are 92 cm (Guitart Manday, 1975) and 97 cm (Gilmore, 1983), and the smallest free-swimming individuals reported are 123 and 125 cm (Garrick, 1967). Compagno (2001) suggested birth sizes in the range of 97–120 cm.

Estimates of birth size for Lamna nasus are in the range of 68–80 cm, and this appears to hold for both Northern and Southern Hemispheres (Aasen, 1963; Bass et al., 1975; Francis and Stevens, 2000; Jensen et al., 2002). The largest reported embryos were 73–79 cm, and the smallest reported free-swimming neonate was 68 cm (Francis and Stevens, 2000). Reports of large embryos and small free-swimming young of L. ditropis are scanty. Birth size for this species is probably 84–96 cm (Nagasawa, 1998; Goldman, 2002). However, Blagoderov (1994) reported a free-swimming individual less than 50 cm long.

Birth size for Carcharodon carcharias is estimated in the range of 120–150 cm (Francis, 1996). The largest embryos reported are 145 cm (New Zealand; Francis, 1996) and 151 cm (Japan; Uchida et al., 1996). The length of the smallest known free-swimming neonate is 122 cm based on three specimens, one taken in the western North Atlantic off New York and the other two taken in the eastern North Pacifi c off California (Casey and Pratt, 1985; Klimley, 1985). It is interesting that two of these neonates weighed 12 and 16 kg, respectively (Casey and Pratt, 1985), whereas large embryos weighed as much as 26–32 kg (Francis, 1996; Uchida et al., 1996). Perhaps newborn white sharks lose weight initially as they are learning to feed (Francis, 1996). Questionable or erro neous reports of birth size are discussed by Francis (1996).

Gestation period

The apparent lack of seasonality in the reproductive cycles of the alopiids makes it dif-fi cult to determine the length of their gestation, and so far no direct evidence has been obtained. The best estimate to date of the gestation period for all three Alopias species appears to be Holden’s (1974) calculation of 12 months using the von Bertalanffy growth equation (Table 3.2).

Because they captured two pregnant Isurus oxyrinchus females with embryos of sig-nifi cantly different sizes in January off Puerto Rico, Mollet et al. (2000) concluded that gestation in this species must be longer than 1 year. Using a variety of assumptions, they predicted a gestation period of 15–18 months, and possibly as long as 24 months. However, Duffy and Francis (2001) reported a litter from New Zealand waters that was almost 6 months out of phase with the Mollet et al. (2000) seasonal data for embryo size. From the Mollet et al. embryonic growth model, gestation for the largest embryo in this litter would be 21 months. They suggested that the entire reproductive cycle is 3 years, which includes a resting period of about 18 months. The length of gestation is unknown in I. paucus owing to a general lack of knowledge of the biology of the species.

The gestation period of Lamna nasus is diffi cult to estimate because of confl icting reports of reproductive seasonality. A period of 8–9 months has been suggested based on


embryo lengths during given months and estimated embryo growth rates (Aasen, 1963; Francis and Stevens, 2000; Jensen et al., 2002). Some authors have suggested gestation periods of more than a year for this species, citing evidence of two distinct size groups of embryos at some times of year (Shann, 1923; Gauld, 1989). Shann (1923) suggested a gestation period between 18 and 24 months. Using limited information about the tim-ing of mating and parturition, Compagno (2001) and Goldman and Musick (2008) sug-gested that L. ditropis has a gestation period of about 9 months. It is not known whether females of either Lamna species have any signifi cant resting period during the reproductive cycle; however, Gauld (1989) reported large numbers of mature but nongravid females of L. nasus in catches off Scotland.

The gestation period of the white shark is not known with certainty (Francis, 1996). From a variety of observations, the gestation period is assumed to be longer than 12 months and may be closer to 18 months from fertilization to parturition (Mollet et al., 2000; Bruce, 2008).

Reproductive periodicity

Like gestation period, the reproductive cycle in alopiids has also not been specifi cally defi ned. Adult females of Alopias species carry embryos throughout the year, and embryos are found in varying stages of development at practically any given time (Gubanov, 1972, 1978; Gruber and Compagno, 1981; Chen et al., 1997; Liu et al., 1999). Thus, reproduc-tive seasonality appears to be insignifi cant, if not nonexistent, for these species, and there appears to be no resting period between pregnancies.

There is, however, some evidence for protracted, but perhaps seasonal, periods of parturition in A. superciliosus and A. vulpinus. Gilmore (1993) suggested parturi-tion periods for A. superciliosus in the summer, fall, and winter in the Florida Straits.

Table 3.2 Summary of gestation period and resting period in 13 species of pelagic elasmobranchs.*

Species Gestation period (months) Resting period (months)

AlopiidaeAlopias pelagicus 1280 No86

Alopias superciliosus 1280 –Alopias vulpinus 1280 –

LamnidaeIsurus oxyrinchus �12113; 15–1841,93; 2149 1893

Isurus paucus – –Lamna ditropis 945,64 –Lamna nasus 82; 8–953,81; �1257; 18–24122 3–42,53,81

Carcharodon carcharias �1293; 1893 No52; 1892

CarcharhinidaeCarcharhinus falciformis 11–12107; 1212,15 Yes107; 1215

Carcharhinus longimanus 9–12121; 125,7 125

Carcharhinus signatus 12–13107 12107

Prionace glauca 9139; 9–1277,110; 1899 No77,110

DasyatidaePteroplatytrygon violacea 2114–116; 2–387 –

*Superscript numbers refer to reference numbers. A dash indicates no data available.


Moreno and Morón (1992) concluded that birth occurs over a protracted period from autumn to winter in the Strait of Gibraltar. Another primary or secondary nursery for this species may exist in nearshore Cuban waters, since many small juveniles and females with full-term litters have been observed there (Guitart Manday, 1975). Cailliet and Bedford (1983) suggested that pupping in A. vulpinus in northeastern Pacifi c populations occurs annually from March to June. There appears to be a nursery ground in this region in the shallow, warm-temperate coastal waters off southern California (Compagno, 2001).

Reproductive seasonality in Isurus oxyrinchus seems to be more or less synchronous in populations from both hemispheres, with parturition from late winter to spring (Pratt and Casey, 1983; Stevens, 1983, 1984a; Cliff et al., 1990; Mollet et al., 2000). Duffy and Francis (2001), however, suggested that birth in New Zealand and Australian waters may occur over a protracted period from winter to summer or possibly even year-round, with a peak in the winter to spring period. Recently fertilized females caught off South Africa in March and June suggest that mating occurs there in autumn, just before ovulation (Cliff et al., 1990; Mollet et al., 2000).

The reproductive seasonality of I. paucus is a matter of conjecture. Gilmore (1993) suggested a possible mating area in the northern Gulf of Mexico in April, based on the capture of three ripe males and one large female. Since three of the four pregnant longfi n makos reported in the literature were captured in the Gulf of Mexico or near the Florida Straits, it is also possible that this is a parturition or midgestation area for the species (Guitart Manday, 1975; Gilmore, 1983, 1993).

Reproduction in Lamna species is likely seasonal, but regional differences may occur. Segregation by both size and sex also appears to play a signifi cant role in the reproduc-tive cycles of both species (Aasen, 1963; Tanaka, 1980; Gauld, 1989; Ellis and Shackley, 1993; Blagoderov, 1994; Nagasawa, 1998; Goldman, 2002). For L. nasus, Bigelow and Schroeder (1948) suggested that parturition in the Northwest Atlantic occurs in summer, but Aasen (1963) and Jensen et al. (2002) both supported a spring parturition period (May to June) in this region. Assuming an 8-month gestation period, mating would then be in autumn (September to October), which would concur with Jensen et al. (2002). On the other hand, in populations studied off Scotland, parturition appears to be in the summer, and mating in the winter (Gauld, 1989). For populations in New Zealand and Australian waters, parturition peaks in winter (June to July), but may extend over a protracted period from April to September (Francis and Stevens, 2000). Thus, reproductive seasonality in the two hemispheres may be out of phase by a few months. The considerable variation in embryo length (up to 14.6 cm) that is often observed within litters of this species (Shann, 1923; Gauld, 1989; Francis and Stevens, 2000; Jensen et al., 2002) suggests that the mat-ing period may be protracted.

Both the northwestern and the northeastern Pacifi c populations of L. ditropis appear to give birth in the spring (Tanaka, 1980; Blagoderov, 1994; Goldman, 2002). In the north-west population at least, birthing is followed by a northerly migration, so that in the sum-mer, the assumed mating season (Blagoderov, 1994), adults are found near the coasts of Kamchatka and Sakhalin. However, Tanaka (1980) suggested that copulation occurs in autumn, not summer.

Reproductive periodicity and seasonality of Carcharodon carcharias are unknown. Mollet and Cailliet (2002) have suggested that there is an 18-month resting period after


parturition. This, combined with an 18-month gestation period (Mollet et al., 2000; Bruce, 2008), would result in a 3-year reproductive cycle. However, Francis (1996) suggested that there might be no resting period between litters. Evidence in either case is largely circumstantial and indirect, and the time of mating and early embryonic development are unknown. Pupping probably occurs primarily in spring and summer in mostly temperate waters (Fergusson, 1996; Francis, 1996; Uchida et al., 1996). However, off California, pupping may occur into the autumn (Klimley, 1985).

Age and size at maturity

On the basis of clasper morphology (Chen et al., 1997) and structure of the ductus def-erens (Moreno and Morón, 1992), estimates of size at fi rst maturity for males of Alopias superciliosus range from 270 to 288 cm (Table 3.3). This size range would correspond to an age at maturation of about 9–10 years (Liu et al., 1998). Size at fi rst maturity in females of this species ranges from 300 to 355 cm, with most estimates between 332 and 341 cm (Stillwell and Casey, 1976; Gruber and Compagno, 1981; Moreno and Morón, 1992; Chen et al., 1997). Using these sizes, Liu et al. (1998) estimated that females mature at 12.3–13.4 years. In contrast, Gruber and Compagno (1981) reported much lower estimates of age at maturity using a modifi cation of the von Bertalanffy growth equation. Although they assumed that maturity occurs at sizes similar to those noted above, they concluded that females mature at 4.5 years and males at 3.5 years of age. Liu et al. (1998) suggested that Gruber and Compagno’s (1981) method was inaccurate.

Males of A. pelagicus mature at about 267–276 cm, corresponding to an age of 7.0–8.0 years. Females mature at 282–292 cm, corresponding to an age of 8.0–9.2 years (Liu et al., 1999); however, Compagno (2001) reported a mature female of 264 cm. It is possible that regional differences exist.

In A. vulpinus, males reach maturity around 314 cm in the Mediterranean and the Northeast Atlantic (Moreno et al., 1989), and around 333 cm off southern California (Cailliet et al., 1983). Bass et al. (1975) suggested that females mature at about 376 cm. It is possible that regional differences exist in female maturity, since Gubanov (1972) reported pregnant females as small as 260 cm in the northwest Indian Ocean and Gohar and Mazhar (1964) reported a 300-cm pregnant female from the Red Sea. A male matu-rity size of 314 cm would correspond to about 4–5 years of age, and a female maturity size of 376 cm would correspond to about 6–7 years of age (Cailliet et al., 1983). Recent age and growth studies on A. vulpinus suggest that males mature at 293–311 cm and 4.8 years of age, and females at 303 cm and 5.3 years (Smith et al., 2008b).

Estimates of maturity in Isurus oxyrinchus indicate that males reach sexual maturity at a smaller size (180–215 cm) than females (263–293 cm) (Bigelow and Schroeder, 1948; Bass et al., 1975; Gubanov, 1978; Stevens, 1983; Cliff et al., 1990; Mollet et al., 2000). However, from an unsubstantiated observation of a 188-cm female in “post-pregnancy,” Gubanov (1978) asserted that females become sexually mature as small as 180 cm. Age-at-size estimates in this species are unsettled. According to Pratt and Casey (1983), who assumed two pairs of vertebral growth rings per year, females mature at around 7 years and males around 3 years. However, Cailliet et al. (1983), assuming only one pair of ver-tebral rings per year, suggested that males mature at 7 years of age and, by extrapolation,

R

eproductive Biology of Pelagic E

lasmobranchs

35

Table 3.3 Summary of size and age at maturity in 13 species of pelagic elasmobranchs.*

Species Size at maturity (cm) Age at maturity (years)

Male Female Male Female

AlopiidaeAlopias pelagicus 267–27645,86 26445; 282–29286 7–886 8–9.286

Alopias superciliosus 270–28839,96; 290–300136 30067; 332–34139,59,96; 35065,136; 3669 3.565; 9–1085 5–665; 12.3–13.485

Alopias vulpinus 293–311126; 31497; 3198; 4279 26066; 30062; 303126; 315137; 3768; 4279 4–525,126 5.3126; 6–725

LamnidaeIsurus oxyrinchus 18067; 1839; 194–2068,41,131 18067; 26393; 26641; 280131 3113; 725 7113; 13–1425

Isurus paucus 24545 24545,69 – –Lamna ditropis 15863; 177100; 186140 20563; 211–223100,140 3–563,140 6–963; 8–10140

Lamna nasus 150–2001; 16550; 186–20781 1529; 185–20253; 200–2501; 22457; 236–24981 3–61; 8105 6–91; 13105

Carcharodon carcharias 304–3398; 379112; 4429; 45734 4458; 4509; 450–50052; 45734 8–10149; 9–1026; 9–1026; 12–13149; 10–1388 18–2388

CarcharhinidaeCarcharhinus falciformis 18011; 200132; 210–22512,15,21,135; 18011; 200132; 210–220133,135,137; �22515; 6–715; 1012 7–915; �1212

239133; 251107 232–2456,12; 25021; 273107

Carcharhinus longimanus 168–196121; 180–1909,84; 1987 175–189121; 180–1907,9,84; 2005,67,132; 21421 4–5121; 6–884 4–5121; 6–884

Carcharhinus signatus 15421; 1573; 185–19076 1653; 17821; 200–20576; 225107 8119 10119

Prionace glauca 130–160102; 190–19875,78; 218–22077,110; 140–160102; 180–20068,75,130,139; 195–24021; 204–208108,137; 4–5102; 6–725 5–6102; 6–725

222–250132 213–2449; 220–2227,37,110; 232135; 241132

DasyatidaePteroplatytrygon violacea 35–4094; 37144; 40–50148 40–5094,148 2–394 2–394

*Size is total length (cm) for sharks and disk width (cm) for the ray. Superscript numbers refer to reference numbers. A dash indicates no data available.


females mature at 13–14 years. Preliminary data from Campana et al. (2002) and from ongoing age and growth studies on the shortfi n mako suggest that Cailliet et al.’s assump-tion is correct (L. Natanson, personal communication). The smallest reported adults of I. paucus are 245 cm for both sexes (Guitart Manday, 1966; Compagno, 2001). There are no other data relevant to the size or age at maturity in this species.

For Lamna nasus, the onset of sexual maturity appears to occur at a similar size in both sexes, but estimates of size at maturity are highly variable. Based on varied criteria in different populations, estimates of male maturity size are 150–200 cm (Aasen, 1961), 165 cm (Ellis and Shackley, 1993), and 186–207 cm (Jensen et al., 2002). This size range corresponds to an age at maturation of about 8 years (Natanson et al., 2002). Estimates of maturity size for females are more variable. For the North Atlantic population, esti-mates are 200–250 cm (Aasen, 1961) and 236–259 cm (Jensen et al., 2002). In Australian and New Zealand waters, female maturity probably occurs at 185–202 cm, suggest-ing regional differences (Francis and Stevens, 2000; Francis et al., 2008). Bigelow and Schroeder (1948) reported pregnant females of L. nasus as small as 5 ft (152 cm), but no specifi c observations were reported so the signifi cance of this outlier cannot be assessed. Assuming a maturity size of 236 cm, females mature at around 13 years of age (Natanson et al., 2002).

Because reproduction in L. ditropis is poorly known, there are few estimates of matu-rity. Studies in the northwestern Pacifi c suggest that males mature at 177–186 cm and 5 years of age, and females at 200–223 cm and 8–10 years of age (Tanaka, 1980; Nagasawa, 1998). In the northeastern Pacifi c, males mature at 158 cm and 3–5 years, and females at 205 cm and 6–9 years, indicating faster growth in these populations (Goldman, 2002).

Estimates of size and age at maturity for the white shark vary widely and differ between males and females (Bruce, 2008). Males probably fi rst reach sexual maturity some-where between 300 and 400 cm, with most estimates falling in the range of 340–380 cm (Bass et al., 1975; Pratt, 1996; Malcolm et al., 2001). On the basis of a limited number of studies on age and growth, males in this size range would be 7–10 years old (Cailliet et al., 1985; Wintner and Cliff, 1999; Malcolm et al., 2001). Females probably mature somewhere between 450 and 500 cm (Francis, 1996) and 12–18 years of age (Cailliet et al., 1985; Wintner and Cliff, 1999; Malcolm et al., 2001). Several reports of mature females smaller than 430 cm are probably erroneous, and Paterson’s (1986) report of a pregnant 320-cm female is highly unlikely (Francis, 1996).

Development

As described in the Introduction, all the lamniform species demonstrate aplacental vivi-parity and embryonic oophagy. Because embryonic development has been well studied in Lamna nasus, we use it here to illustrate the general pattern of development in the other lamniform sharks.

Encapsulated embryos up to about 4 cm long are nourished by yolk from the yolk sac (Jensen et al., 2002). By the time of hatching, at about 3.2 cm, the yolk sac has been almost completely absorbed. At this point, the embryos have not begun feeding on nutritive egg capsules because they do not yet have teeth capable of tearing them open. Prehatching embryos also have external gills (Francis and Stevens, 2000; Jensen et al.,


2002), which may be the means by which lamnoid embryos absorb yolk from the yolk sac (Mollet et al., 2000).

At about 12–15 cm, the embryonic teeth begin to develop, including two relatively large fangs on the lower jaw but only one functional tooth on each side of the upper jaw. Once these teeth develop, the embryos begin to practice oophagy and the external gills are resorbed (Francis and Stevens, 2000). Oophagy peaks in embryos between 26 and 40 cm (Francis and Stevens, 2000; Jensen et al., 2002). As large numbers of egg capsules are consumed, the yolk stomach weight may reach up to 81% of the embryo’s total weight (Templeman, 1966).

Toward the end of gestation (at 41–46 cm), the embryonic teeth are shed and embryos probably rely on yolk stored in the stomach. It is likely that females cease ovulation at this time (Francis and Stevens, 2000). In the embryos, the adult teeth probably do not become erect and functional until some time immediately before or after parturition.

There is no evidence of adelphophagy (cannibalism of sibling embryos within the uterus) in any of the lamniform species reviewed here, and the lack of erect functional teeth makes embryophagy unlikely. Francis and Stevens (2000) noted one porbeagle embryo that had nonlethal lacerations on its body, probably incurred from a sibling searching for egg capsules in utero. Accordingly, they suggested that this may be the mechanism by which adelphophagy evolved in the sand tiger shark, Carcharias taurus, a related coastal species (Gilmore et al., 1983). Also, if the aggregate blastodiscs observed by Jensen et al. (2002) indeed contain embryos that do not fully develop, it is possible that these encapsulated embryos may be consumed by the more advanced posthatch embryos during the oopha-gous phase of development. If so, this would be a novel form of intrauterine cannibalism.

Early development in Carcharodon carcharias has not been described. With the re-identifi cation of a 36-cm embryo reported to be a white shark as a shortfi n mako (Mollet et al., 2002b), the smallest documented embryonic white shark is approximately 100 cm (estimated from photographs) (Uchida et al., 1987, 1996). Although the general devel-opmental pattern described here for L. nasus may apply to C. carcharias as well, the only thing that is known with certainty is that the latter exhibits aplacental viviparity with oophagy (Uchida et al., 1987, 1996; Fergusson, 1996; Francis, 1996; Bruce, 2008). Although three term embryos had teeth and dermal denticles in their stomachs, embry-ophagy seems unlikely (Francis, 1996; Uchida et al., 1996).

Reproduction in requiem sharks

Reproduction in carcharhinid species differs from that in the other reviewed species by the presence of a placental connection between the maternal and fetal systems dur-ing some phase of gestation. In fact, of about 43 species of carcharhinid sharks, only the tiger shark, Galeocerdo cuvier, is aplacental (Compagno, 1988). However, even with a different reproductive mode, the placental species discussed in this section exhibit some marked similarities in reproductive traits with the aplacental pelagic species.

Litter size

Litter sizes in pelagic requiem sharks fall into two groups. The three species of Carcha-rhinus have relatively small litters, ranging from 1 to 18 young per brood (Table 3.1).


Prionace glauca, in contrast, has much larger litters, ranging in size from 4 to 135. Reports of abnormally small litters, such as 1 or 2 in Carcharhinus species and 4 in the blue shark, may be due to counting young that remained after part of the litter had been aborted, as often happens when pregnant elasmobranchs are boated or handled (Bonfi l et al., 1993). The little information available suggests that litter size is positively correlated with female size in these species – larger females tend to have larger broods.

The oceanic whitetip shark, C. longimanus, has a reported range of litter sizes from 1 to 15. Most reports are in the range of 4–9, with means of about 6–8 (Backus et al., 1956; Strasburg, 1958; Stevens, 1984a; Bonfi l et al., 2008). Gohar and Mazhar (1964) reported a range of 10–15 from the Red Sea, and brood sizes may be slightly larger in some parts of the Pacifi c Ocean (Saika and Yoshimura, 1985; Seki et al., 1998). The silky shark, C. fal-ciformis, has a litter range of 2–16 (Bonfi l et al., 1993; Bonfi l, 2008), and its mean brood size is about 5–7 (Strasburg, 1958; Taniuchi, 1997). Brood size reports for the night shark, C. signatus, range from 4 to 18 (Bigelow and Schroeder, 1948; Osorno, 1992). Where ade-quate data are available, the mean litter size in this species is about 11 (Hazin et al., 2000a).

The blue shark, Prionace glauca, has by far the largest litters and the greatest range of reported litter sizes (4–135) of the four requiem species considered here. If both the smallest and largest reported litters are discounted as artifactual or unusual, then litters in the range of 25 to 50 are normal. In studies based on large numbers of pregnant females, mean brood size has ranged from 26 to 56 (Gubanov and Grigor’yev, 1975; Stevens, 1984a; Stevens and McLoughlin, 1991; Nakano, 1994; Castro and Mejuto, 1995).

Birth size

Estimates of birth size in pelagic carcharhinids range from about 35 to 85 cm TL and fall into two groups. Blue sharks, which produce larger broods, are smaller at birth than the three species of Carcharhinus, which produce fewer young that are larger at birth (Table 3.1). In the blue shark, young are born between 35 and 50 cm (Pratt, 1979; Cailliet and Bedford, 1983; Compagno, 1984; Stevens, 1984a; Castro and Mejuto, 1995). The smallest reported sizes for free-living neonates range from 34 to 53 cm (summarized by Cailliet and Bedford, 1983; Nakano and Nagasawa, 1996). The size at birth estimated from growth equations is 43–44 cm.

In the three Carcharhinus species considered here, birth sizes range from 55 to 85 cm. Reports for C. longimanus range from 55 to 77 cm, with most estimates falling in the range of 60–70 cm (Bigelow and Schroeder, 1948; Bass et al., 1973; Compagno, 1984; Seki et al., 1998; Lessa et al., 1999; Bonfi l et al., 2008). Seki et al. (1998) examined embryos as large as 75 cm, and free-swimmers as small as 66 cm. For C. signatus, birth size ranges from 60 to 65 cm (Raschi et al., 1982; Compagno, 1984; Garrick, 1985; Osorno, 1992). Raschi et al. (1982) reported embryos as large as 63 cm and free-swimmers as small as 67 cm. Branstetter and McEachran (1986) examined three free-swimming juveniles that were 62–80 cm with umbilical scars still visible. The average size of late-term embryos examined by Osorno (1992) was 61 cm. Carcharhinus falciformis may produce the largest young of the pelagic requiem species, with birth sizes from 64 to 78 cm (Bass et al., 1973; Yoshimura and Kawasaki, 1985; Bonfi l et al., 1993). Osorno (1992) reported free-living neonates from 70 to 87 cm; however, Yoshimura and Kawasaki (1985) reported neonates


as small as 64 cm. Bonfi l (2008) suggested that there are regional differences in silky shark size at birth.

Gestation period

All estimates of gestation period for these species are 9–13 months, or roughly 1 year (Table 3.2). These estimates are fairly robust for the blue shark (Suda, 1953; Pratt, 1979; Hazin et al., 2000b) and silky shark (Branstetter, 1987; Osorno, 1992; Bonfi l et al., 1993), but less fi rm for the oceanic whitetip (Backus et al., 1956; Seki et al., 1998). The sole estimate for gestation period in the night shark is 12–13 months (Osorno, 1992). The only estimate that is not consistent with the majority is 18 months for the blue shark (Muñoz-Chápuli, 1984).


It is widely held that in many large viviparous sharks, females do not reproduce every year (Backus et al., 1956; Springer, 1960; Clark and von Schmidt, 1965; Branstetter, 1981). Thus, a female may carry young for about 12 months of gestation, then have a “resting” year before ovulating a new batch of eggs and beginning the gestation of a new litter (Table 3.2). This would result in a 2-year cycle for an individual female. Data to support a biannual cycle are diffi cult to collect, especially when females in different reproductive stages may occur in different geographic zones or undergo extensive migrations.

There is some evidence to support a 2-year reproductive cycle in C. falciformis (Branstetter, 1987; Osorno, 1992; Bonfi l, 2008), C. longimanus (Backus et al., 1956; Seki et al., 1998), and C. signatus (Osorno, 1992). Pratt’s (1979) data suggest that the blue shark has annual reproduction, without an intervening resting year, and there seems to be no strong contradictory evidence (Hazin et al., 1994; Nakano and Stevens, 2008).


For the silky shark, most estimates of size at maturity in females range from 200 to 260 cm, and for males from 210 to 250 cm (Strasburg, 1958; Bane, 1966; Stevens, 1984a, b; Branstetter, 1987; Stevens and McLoughlin, 1991; Bonfi l et al., 1993; Bonfi l, 2008) (Table 3.3). There is evidence of marked geographic variation in size at maturation. For example, in the eastern Pacifi c, silky sharks of both sexes may mature at sizes as small as 180 cm (Bonfi l, 2008). Two estimates for age at maturity in this species, both based on studies in the Gulf of Mexico, reached different conclusions. Branstetter (1987) estimated age at maturity as 6–7 years for males and 7–9 years for females. In contrast, Bonfi l et al. (1993) estimated maturation at 10 years for males and 12� years for females.

For the oceanic whitetip shark, most estimates for male size at maturity are 175–190 cm. The literature suggests that females become sexually mature at a slightly larger size, somewhere between 170 and 220 cm (Backus et al., 1956; Bass et al., 1973; Cadenat and Blache, 1981; Seki et al., 1998). Seki et al. (1998) estimated that both males and females in the central Pacifi c mature at 4 or 5 years. In the southwestern equatorial Atlantic, esti-mated age at maturation in both sexes is 6–7 years (Lessa et al., 1999).


There is very little published information on the size at maturation in the night shark. Branstetter and McEachran (1986) noted that a male of 161 cm and two females, 171 and 226 cm TL, were not mature. Amorim et al. (1998) stated that males and females mature at 157 and 165 cm, respectively, but it is not clear how they evaluated sexual maturity. The most extensive data indicate maturation for males at 185–190 cm and for females at about 200 cm (Hazin et al., 2000a). However, Cadenat and Blache (1981) examined preg-nant females that were 178–179 cm. From samples taken off northeastern Brazil, the age at sexual maturation in the night shark is estimated to be 8 years for males and 10 years for females (Santana and Lessa, 2004).

Most males of the blue shark become sexually mature at about 220 cm, and females become sexually mature at between 200 and 220 cm (Pratt, 1979; Hazin et al., 1994, 2000a; Castro and Mejuto, 1995; Henderson et al., 2001), although Stevens (1974) reported a mature female of 180 cm. Cailliet et al. (1983) estimated age at maturation for both sexes to be 6–7 years. The only noteworthy departure from this estimate is based on a von Bertalanffy growth equation analysis that estimated male maturation at 4–5 years (Nakano, 1994).

Development

There have been no detailed studies of development in any of the four carcharhinid species. However, the general pattern of development can be summarized from limited data on these species and from the more detailed analysis of other large carcharhinid sharks (Springer, 1960; Castro, 1993, 1996). Females have a single functional ovary on the right side, with a common ostium opening into paired left and right reproductive tracts. Ovulated ova are fer-tilized by stored sperm as they pass through the shell (nidamental) gland. A thin, diaphanous egg capsule is deposited around the egg, and it passes into the uterus, where development occurs. During the early part of gestation, the young rely on yolk provisioned in the egg for nutrition. In some cases, the young may also derive nourishment from histotroph (uterine milk) secreted by the female’s uterus and absorbed by the embryo through elongated exter-nal gill fi laments (Hamlett et al., 1985). Later in gestation, when the yolk is depleted, the embryonic yolk sac develops into a yolk sac placenta that lies in contact with a highly vas-cularized attachment site on the wall of the female’s uterus. Since the external gill fi laments of the embryo are resorbed during midgestation, it is believed that the embryo relies entirely on nutrient exchange via the placenta to sustain later stages of development.

It is generally assumed that all of the pups in a litter are born in relatively quick succes-sion, with the birth of the entire litter spanning a few days at most. Individual pups would vary slightly in size at birth depending on the length of gestation and intrauterine growth rate. The hypothesis that blue shark litters are born in “fi ve or six stages” (Gubanov and Grigor’yev, 1975) seems unlikely.

The placentation of the silky shark and the blue shark has been described (Gilbert and Schlernitzauer, 1966; Otake and Mizue, 1985). In the silky shark, the placenta is classifi ed as a discoidal type and lacks appendiculae along the yolk sac stalk (also termed the umbili-cal cord). Both C. longimanus and P. glauca appear to have placentation similar to that of the silky shark (Otake and Mizue, 1985; Compagno, 1988). According to Hamlett and Koob (1999), in most carcharhinid sharks the egg envelope persists throughout gestation


and becomes an integral part of the placenta. However, in the blue shark the egg capsule disappears at some point before the placenta is fully developed (Otake and Mizue, 1985).

Reproduction in the pelagic stingray

The pelagic stingray, Pteroplatytrygon violacea, is the only batoid species that can be considered truly pelagic. Its reproductive strategy is distinct from those of the other species reviewed in this chapter, at least at the physiological level. However, comparison of the stingray’s reproductive parameters reveals similarities that may be attributable to habitat infl uences.

Litter size

Only the left ovary and uterus of this species are functional, which is characteristic of most if not all species of the family Dasyatidae. Normal litter size has been reported to range from four to nine (Mollet, 2002a; Mollet et al., 2002a; Neer, 2008) (Table 3.1). Some authors have reported smaller litters (Wilson and Beckett, 1970; Mollet, 2002a), but these cases may represent abnormal events, associated with either premature abor-tion by stressed females or anomalies of reproduction in captivity. In contrast, Wilson and Beckett (1970) reported one intrauterine egg capsule that contained 13 nonembryonated “egg segments,” though it is unlikely that all of these eggs would have produced term embryos. Capapé (1985) noted that the number of encapsulated eggs is often greater than the number of term embryos in live-bearing rays.

Birth size

A broad range of birth sizes, measured as the width of the body or disk from one “wing tip” to the other, have been reported for P. violacea (Table 3.1). Some of this variation may be due to artifacts mentioned in the Introduction. Mean disk widths (DW) of young at birth range from 14 to 24 cm (Mollet, 2002a; Mollet et al., 2002a). Mollet (2002b) reported that neonates smaller than 25 cm DW are taken between September and April in the eastern Pacifi c off Central America. From this observation, the size at birth is prob-ably in the upper part of the range noted above. Similarly, birth weights show a broad range of variation, both within and between broods (Mollet, 2002a; Mollet et al., 2002a). It is likely that “normal” birth weight is on the order of 200–250 g. Thus, disk width at birth in P. violacea is similar to that in the southern stingray (Dasyatis americana), but birth weight is about 50% less (Henningsen, 2000).

Gestation period

All references to the length of gestation in the pelagic stingray refer back to early lit-erature based on studies in the Mediterranean area (Lo Bianco, 1909; Ranzi, 1932; Ranzi and Zezza, 1936). These studies, although not defi nitive, suggest a gestation period of 2–3 months (Table 3.2). A 2-month gestation cycle would be the shortest recorded for any


elasmobranch species. A 3-month gestation would be similar to that of Dasyatis sabina (Snelson et al., 1988; Johnson and Snelson, 1996). Other stingrays may have longer gestation periods (Capapé, 1993; Henningsen, 2000). Some rays with unusually long gestation have been shown to have a period of embryonic diapause, resulting in delayed development (Snelson et al., 1989; Villavicencio-Garayzar, 1993; Morris, 1999). There is no information suggesting that P. violacea exhibits developmental diapause.


The reproductive period for the pelagic stingray is poorly understood and may vary geo-graphically. The results from a large data set accumulated for the eastern Pacifi c population indicate that the rays reproduce in the winter in warm water off the coast of Central America, after which they migrate northward to the southern California coast (Mollet, 2002b). Observations from the western and central Pacifi c are less clear, but suggest parturition in warmer waters near the equator from November to May. In contrast, Wilson and Beckett (1970) suggested that parturition occurred in August or September in relatively cool waters in the Grand Banks area in the western North Atlantic. Data for the Mediterranean Sea sug-gest that the rays reproduce in relatively cool waters in the Bay of Naples in July and August. During this time, females were found carrying embryos in various stages of development, suggesting a general lack of synchrony in mating events (Lo Bianco, 1909; Ranzi, 1932). There is no evidence that an individual female reproduces more than once a year, and annual reproduction is a reasonable assumption based on what is known about related species. It is possible that females might produce two clutches of ova per year in captivity (Mollet et al., 2002a). On the basis of what is known about other rays, we suspect that most females repro-duce every year, without a “year off ” resting period (Snelson et al., 1988, 1989; Capapé and Zaouali, 1995; Henningsen, 2000).


Males reach sexual maturity between 37 and 50 cm DW at an estimated age of 2 years (Table 3.3). Females reach sexual maturity at a similar size, 40–50 cm DW, at about 3 years (Wilson and Beckett, 1970; Tortonese, 1976; Mollet et al., 2002a). The largest male recorded was a captive specimen that reached 68 cm DW and 12 kg at an estimated age of 6–7 years. The largest female on record, also a captive specimen, was 96 cm DW and 46 kg, with an estimated age of 7–8 years (Mollet et al., 2002a). The largest female captured in nature was 80 cm DW (Wilson and Beckett, 1970). Growth models predict a maximum age of 10 years (Mollet and Cailliet, 2002; Mollet et al., 2002a). The maximum age determined from vertebral banding was also 10 years (Neer, 2008).

Development

The little that is known about development in this species is consistent with the gen-eral pattern of aplacental viviparity with trophonemata characteristic of other stingrays. Intrauterine egg capsules containing several ova weighing 1–2 g each have been noted in both captive and fi eld observations of the pelagic stingray (Lo Bianco, 1909; Ranzi,


1932, 1934; Wilson and Beckett, 1970; Mollet, 2002a; Mollet et al., 2002a; Neer, 2008). As with other species of stingrays, the diaphanous egg capsule disappears early in ges-tation, after which the young are free in the uterus. This occurs at about 11 mm DW in P. violacea (Lo Bianco, 1909). At this size, the embryos have long external gill fi laments and a large external yolk sac, and the pectoral fi ns are not fused with the head (Lo Bianco, 1909; Cavaliere, 1955). Four aborted near-term embryos ranged from 117 to 157 mm DW and from 91 to 120 g. They were fully pigmented and had well-formed tail barbs (H. F. Mollet, personal communication; Mollet, 2002a; Mollet et al., 2002a).

One anomaly reported for this species that is not characteristic of other stingrays is the wide range of sizes and developmental stages among the young in a single brood (Mollet et al., 2002a). Since most of these observations are based on captive individuals, they may be anomalies associated with stress, nutritional defi ciencies, or other artifacts of captivity.

Discussion

With the exception of the pelagic stingray, which has been the subject of limited captive study, data on the reproduction of pelagic species are based on examination of wild-caught specimens. Since these animals are large and diffi cult to handle, studies are often based on relatively few specimens. These limited data are usually collected in different parts of the world’s oceans at different seasons, and interpretation is often based on extrapolation and untested assumptions. Given these limitations, the published literature on reproduction in these species often refl ects a broad range of variation and may even lead to different con-clusions, some of which may reveal real differences within or between populations, others of which may be artifactual.

Some variation in litter size may be related to differences between individual females or to differences between geographically or genetically distinct populations of the same species. Other reported variation may be due to artifacts. Live-bearing elasmobranchs are notorious for aborting pups, especially if they are in advanced stages of development, when the pregnant females are hooked, boated, handled, or otherwise stressed. Thus some reports of unusually small litter sizes probably represent only partial litters.

Likewise, there probably is “real” variation in birth size among individual females and distinct populations. In addition, there is size variation among individuals within a single brood of young that were all fertilized at about the same time. However, some data reported in the literature are undoubtedly based on the artifact of premature abortion of developmen-tally advanced embryos. Shark and ray embryos that appear to be “full term” in develop-ment may not necessarily represent the size at which they would have been born naturally. Finally, in some cases, birth size is estimated indirectly by back-calculation using equations employed in age and growth models. Such estimates are based on varied assumptions and may not agree with estimates derived from measurements of embryos or newborn young.

Determining the length of gestation is dependent on knowing the times of fertiliza-tion of the ova and parturition. The timing of fertilization is estimated from the appear-ance of fertilized ova or embryos in early stages of development in the uterus. However, the earliest cleavage stages of fertilized ova are not easily recognized without specialized techniques (Simpfendorfer, 1992; Morris, 1999), nor is the timing of mating necessarily


coincident with the time of fertilization. In many shark species, females mate immedi-ately after giving birth to young, but store sperm for up to 12 months before ovulating and fertilizing a second batch of eggs (Pratt, 1979). The timing of birth is estimated based on the occurrence of large “full-term” embryos and/or the appearance of small free-living neonates, with the same limitations noted earlier. Finally, the length of gestation is likely infl uenced by the speed of development, which may vary with water temperature or other environmental parameters. Given these limitations, the length of gestation reported for various elasmobranchs varies widely.

A signifi cant degree of variation in maturity sizes is also common. For males, clasper development and testicular maturation are not synchronous in some cases, and histologi-cal examination of the gonad and reproductive tract is more defi nitive (Pratt, 1979, 1996). In some maturing females, virgins may fi rst mate as much as 12 months before they ovu-late eggs and begin to carry young. The presence of enlarged yolked eggs in the ovary is suggestive of maturity, but only the presence of fertilized ova or developing embryos in the uterus is defi nitive. Evaluating the attainment of sexual maturity in females is further com-plicated if there is a resting period in a multiyear cycle, or if there is extensive migration or geographic segregation of females in different stages of reproduction. Furthermore, not all individuals of a species will necessarily become sexually mature at the same chronological age, and all individuals of the same age may not be the same size owing to growth rate dif-ferences. Finally, in some wide-ranging species, the size and age at which sexual maturity is achieved may vary geographically.

Estimating the age at which sexual maturity is attained is dependent on accurate aging techniques. In the case of pelagic species, vertebrae have been the only structures used to reveal growth rings. It is usually assumed that a pair of growth rings is laid down annu-ally, although there may be exceptions. Despite the wide use of vertebral aging in elas-mobranch research, there have been relatively few verifi cation studies, though there is an extensive literature on the details and limitations of vertebral aging (see Cailliet, 1990; Cailliet and Goldman, 2004, for reviews). Estimates of the age at which sexual maturity is attained are infl uenced by the accuracy of this method, as well as by natural variation among individuals and populations of a species.

Gathering accurate and comprehensive reproductive data from pelagic shark popula-tions is critical for enlightened fi shery management. Demographic models that utilize life-history parameters are commonly applied to elasmobranchs (Cortés, 2000, 2008; Simpfendorfer, 2004; Au et al., 2008; Smith et al., 2008a). The intrinsic rate of population increase (r), which is a measure of potential growth rate for a population, is commonly estimated by use of life tables or matrix models (age and stage based). Demographic mod-els commonly utilize these reproductive factors: mx, fecundity at age x; α, age at maturity; and w, maximum reproductive age.

The net reproductive rate (R0, the average total number of female offspring produced by a single female pup over its lifetime) and mean generation length (G, the mean period between birth of parent and offspring) are calculated from life table data (including number of pups and reproductive rate). R0 is utilized in calculating rm, the innate capac-ity for increase under particular environmental conditions. Matrix models utilize the fi nite rate of population increase (λ), which is calculated from reproductive and mortality data (Mollet and Cailliet, 2002). Rebound potential (r2m), or how fast a population will


increase after fi shing pressure has been removed from the population, is a modifi cation of the life table approach that uses, among other parameters, the mean number of pups per litter (b).

Because reproductive characteristics may vary between populations, it is very impor-tant to characterize these life-history traits throughout the natural geographic range of any species. Our understanding of the reproductive variability of pelagic elasmobranchs is still poor, and much more work is required to improve fi sheries models and predictions.

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sharks of the open ocean || the reproductive biology of pelagic elasmobranchs

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