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This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute.

Notice: ©1993 Springer. This manuscript is an author version with the final publication available at http://www.springerlink.com and may be cited as: Gilmore, R. G. (1993). Reproductive biology of lamnoid . Environmental Biology of , 38(1‐3), 95‐114. doi:10.1007/BF00842907

Environmental Biology of Fishes 38: 95-114,1993. O 1993 Kluwer Academic Publishers. Printed in the Netherlands.

Reproductive biology of lamnoid sharks

R. Grant Gilmore Division of Environmental, Coastal and Sciences, Harbor Branch Oceanographic Institution, 5600 US. 1 North, Fort Pierce, FL 34946, U.S.A.

Received 31.1.1991 Accepted 1.3.1993

Key words: Embryonic development, , Embryophagy, Adelphophagy, Migration, Elasmobranchs

Synopsis

The capture of recently inseminated or pregnant specimens of taurus, Isuruspaucus, I. oxyrinchus, Alopias superciliosus and A. vulpinus has allowed new information to be obtained on the reproductive biol- ogy of these . Oophagy and embryonic (adelphophagy) have been documented in C. taurus, but only oophagy in other lamnoid species. The occurrence of up to nine embryos of similar size per in and no indication of functional erect teeth in embryos leaves considerable doubt that embryo- phagy occurs in this . Considerable data has been collected on Carcharias taurus which allows a lamnoid reproductive model to be developed and tested, in spite of the obvious differences between the reproductive biology of this species and other lamnoids. Gonad structure, ovarian development, fertilization, early em- bryonic differentiation, embryonic nutrition and parturition, in C. taurus and other lamnoids differs signif- icantly from other elasmobranchs.

Introduction further on oophagy in L. nasus (Shann 1923). Dur- ing this period oophagy was described for the great Five to seven families have been placed in the order white , carcharias (as C. rondo- (Compagno 1977, 1984, Eschmeyer letii Miiller & Henle), by Sanzo (1912), for embryos 1990). In addition to a variety of anatomical charac- taken from a female captured in the Straits of Mess- ters, the order is unified by a common reproductive ina 31 March 1905. Documentation of oophagy in style: embryos examined from nine of the sixteen other species has only occurred during the past few species within the order have been found to be oo- decades (Table 1). phagous (Table 1). The first detailed description of Most lamniform species are inhabitants of deep lamnoid embryos and documentation of oophagy oceanic waters and are typically pelagic or meso- was made by Swenander (1907) for the pelagic. However, the sand , Carcharias shark, nasus (as L. cornubica). Lohberger taurus' and C. tricuspidatuslcommonly inhabit shal- (1910) followed Swenander with the most detailed low neritic waters. The accessibility of C. taurus has anatomical study of a lamnoid embryo yet publish- allowed its capture and study on a routine basis, ed. Shann (1911) published a description of Lamna thus giving us most of our present information on nasus embryos without knowledge of the studies of the reproductive biology of lamnoids. For this rea- Swenander (1907) or Lohberger (1910) and mis- identified the stomach, describing it as a yolk ' Taxonomic nomenclature follows Compagno 1984, and Esch- sac. Shann later corrected his error commenting meyer 1990. Table 1. Summary of lamnoid shark reproductive information.

SpeciesIReference Parturition size, Parturition Smallest free Female mat. Total no. Oophagy TL (cm) period swimming, size, TL (cm) embryos documented n (cm)

Carcharias taurus Springer (1948) winter Bass et al. (1975) winter Gilmore et al. (1983) winter Sadowsky (1970) Cadenat (l956a) Taniuchi (1970) Cetorhinus maximus Sund (1943) summer Matthews (1950) Bigelow & Schroeder (1948) Pseudocarcharias kamoharai Bass et al. (1975) Fujita (1981) variable Abe et al. (1969) Carcaharodon carcharias Klimley (1985) summerlfall Smith (1951) Bass et al. (1975) Scattergood (1962) Fitch (1949) Randall (1973) Bigelow & Schroeder (1948) Casey & Pratt (1985) summer Sanzo (1912) Uchida et al. (1987) springlsummer Norman & Fraser (1948) Cailliet et al. (1985) spring/summer Isurus oxyrinchus Cadenat (1950) Gilmore (data) springlsummer Bigelow & Schroeder (1948) Stevens (1983) winterlspring Garrick (1967) Bass et al. (1975) Vaillant (1889) Guitart-Manday (1966) Uchida et al. (1987) spring Branstetter (1981) winterlspring Gubanov (1978) Depperman (1953) Gohar & Mazhar (1964) Pratt, Casey, Castro, Gilmore (data) (1992) winter Isurus paucus Guitart-Manday (1966) Table I. Continued.

SpeciesIReference Parturition size, Parturition Smallest free Female mat. Total no. Oophagy TL (cm) period swimming, size, TL (cm) embryos documented TL (cm)

Garrick (1967) 123 Gilmore (1983) winter Casey & Pratt (pers. comm.) winter

Lamna nasw Bigelow & Schroeder (1948) summer 74 Bass et al. (1975) 70-75 Aasen (1966) spring 85-87 Shann (1911,1923) spring 82.5 Templeman (1963) Dunlop (1892) Swenander (1907) Nakaya (1971)

Lamna ditropis Otake (pers. comm. 1985) Alopias superciliosus Osipov (1968) Gruber & Compagno (1981) variable Bigelow & Schroeder (1948) 130 Cadenat (1 956b) Nakamura (1935) Fourmanoir (1961) Bass et al. (1975) Gilmore (1983) Springer (1943) Gubanov (1978) Stillwell & Casey (1976)

Alopias vulpinus Hixon (1979) summer Bigelow & Schroeder (1948) 117 Vaillant (1885) Gubanov (1972,1978) Leim & Scott (1966) Strasburg (1958) summer

Alopias pelagicw Nakamura (1935) Otake & Mime (1981) Strasburg (1958)

'Prior to or during adelphophagy; *= FL.

son, it has been used as a model species for repro- tive characters throughout the order, there are also ductive styles in lamniform sharks. However, more differences in the reproductive biology between the thorough analyses of the meager information avail- various genera and species. able for other lamniform species and critical exam- More pregnant specimens of Carcharias taurus ination of recently acquired specimens demon- have been captured on a world wide basis than any strates that, even though there are shared reproduc- other lamnoid. In every case, only a single embryo Fig. I. Photo of one of two uteri with six oviphagous embryos 43.0-49.2cm TL per uterus from Isurus oxyrinchus (HBOM 103:0025G 00253). has been found in each uterus at parturition (Bass et (Fig. 2) (Sanzo 1912, Uchida et al. 1987). Informa- al. 1975, Gilmore et al. 1983). Intra-uterine canni- tion on embryonic development is rudimentary or balism (embryophagy or adelphophagy) has been totally lacking for the Indian , Car- documented in this species by the same authors. charias tricuspidatus, , Odon- Recent captures of pregnant thresher sharks, Alo- taspis ferox, shark, C. noronhai pias vulpinus (Gubanov 1972), , A. (Odontaspididae), , Cetorhinus maxi- pelagicus (Otake & Mizue 1981) and bigeye thresh- mus (Cetorhinidae), , ow- er shark, A. superciliosus (Gruber & Compagno stoni () and , 1981, Gilmore 1983) have also documented no more pelagios (Cetorhinidae [Maisey than a single embryo per uterus. However, although 19851). oophagy has been documented in all alopiid spe- It is the objective of this paper to review some of cies, embryophagy has not. Multiple embryos per the recent discoveries illuminating embryonic re- uterus at parturition, or near term, have been docu- productive development in lamnoid sharks, com- mented in isurid sharks: Lamna nasus (maximum of ment on inaccuracies presently in the literature, and twoluterus, Bass et al. 1975); , Lamna present a variety of hypotheses on the function and ditropis (twoluterus, Tsuguo Otake, personal com- evolution of lamnoid reproductive systems. The munication, June 1985); mako, Zsum oxyrinchus need for further cooperative studies on a worldwide (Fig. 1) (ma. of nineluterus, Bass et al. 1975, Bran- basis is stressed, particularly for cosmopolitan pe- stetter 1981, Stevens 1983); longfin mako, Isurus lagic and mesopelagic species often captured in paucus (ma. of twoluterus, Harold Pratt & Jack oceanic longline fisheries. Not only should speci- Casey NMFS, personal communication, 1988) and mens be obtained, but there should be careful docu- shark, Pseudocarcharias kamoharai mentation of basic environmental information tak- (max. of twoluterus, Fujita 1981). Though definitive en at the time and place where the shark was cap- documentation is lacking, multiple embryos (7-30) tured. have been recorded for Carcharodon carcharias Fig. 2. Sketch of a Carcharodon carcharias embryo. Redrawn from Sanzo (1912).

Study material These specimens included male Alopias supercili- osus, Zsurus oxyrinchus, I. paucus and Carcharias All study material is curated in the Harbor Branch taurus, immature and in reproductive condition. Oceanographic Museum (HBOM). The following Their reproductive anatomy was very similar to material was examined: Isurus oxyrinchus, HBOM that of Cetorhinus maximus, though differing in the 103:00079,00111,00118,00154,00185,00190,00202, relative size of various organs. Paired testes were 00219,0025040253,00310; Isurus paucus, HBOM always associated with the epigonal organ and are 103:00078,00080,00109,00121,00177,00191,00192, of the radial type described by Pratt (1988). The ger- 00208, 00213, 00291; Alopias vulpinus, HBOM minal zone is located at the center of each of several 103:00303, 00320; Alopias superciliosus, HBOM lobes, from which radiate seminiferous follicles 103:00108,00147,00156,00157,00163,00171,00176, ending in the surrounding efferent ductules (Pratt 00187, 00203-00206, 00211, 00218, 00223, 00226- 1988). This testis type described for the lamnoids is 00232,00240,00319; Carcharias taurus (as Odontas- unique among the sharks and is only seen elsewhere pis taurus) HBOM 103:00065,00069,00101-00104, in the batoid order, Myliobatiformes. The relative 00133-00139, 00141-00145, 00162, 00170, 00179, position, size and development of the epididymus, 00183, 00199, 00220, 00221, 00225, 00227, 00242, ductus deferens and seminal vesicle were similar in 00244-00249, 0025440257, 00260-00265, 00267- all species. The seminal vesicle structure in Carcha- 00290, 00292-00302, 00304-00309; Carcharodon rias taurus resembles that described for C. maximus carcharias, HBOM 103:0020040214. in that it is divided into several chambers which are then subdivided by smaller membranous septa. These chambers are turgid with spermatophores in Comparative reproductive anatomy individuals in mating condition. The spermatophore structure differs significantly Male anatomy. - Cetorhinus maximus is the only between Isurus oxyrinchus and C. taurus. The sper- lamniform species whose male reproductive anato- matophores of C. taurus are nearly identical to my has received comprehensive detailed descrip- those described for Cetorhinus maximus by Mat- tive treatment (Matthews 1950), although Pratt thews (1950). No discrete form was observed as the (1988) has recently described testicular structure sperm were immersed in a semitransparent hyaline for various lamnoid species in a review of elasmo- matrix. As the sperm laden matrix extrudes through branch gonad structure. Specimens were examined the urogenital papilla, the 'spermatophores' break from the Harbor Branch Oceanographic Museum into cylindrical bodies of various lengths (Fig. 3a). collections and from material collected from the These bodies gradually dissolve in sea water, releas- Straits, donated by commercial fishermen. ing the sperm which then undergo rapid swimming movements. In Isurus oxyrinchus the seminal ves- al. 1983). Hamlett (1983) estimates that embryos of icle contained white opaque spermatophores with C. taurus may ingest 17000 ova during gestation. discrete form and size, resembling lx 2.5mm rice The maximum ovarian weight presented for C. grains (Fig. 3b). The sperm were closely packed in a maximus by Matthews (1950) was 12.2 kg with an es- matrix with little hyaline material relative to the timated six million ova having diameters ranging spermatophores in C. taurus (Fig. 3c-d). These from 0.5 to 5.0mm. As this latter specimen was not spermatophores did not dissolve as readily in sea in gestation, the may not have reached maxi- water and sperm release could only be elicited by mum size. However, the maximum ova diameters mechanically opening the spermatophore within observed by Matthews could represent the largest sea water. The urogenital papillae and clasper diameters attained for C. maximus as there was evi- structure in C. taurus, A. supercilliosus and I. pau- dence of recent copulation, and therefore ovulation cus were as described for L. nasus (= L. cornubica, was proximate. Maximum ovarian weights and ova Jungerson 1899) and C. maximus (Matthews 1950). diameters at ovulation are not known for I. paucus or I. oxyrinchus as pregnant specimens examined Female anatomy. -Female larnniform sharks have a were near parturition, a period when ovulation has single functional right ovary situated at the anterior ceased and the ovary begins to atrophy (Fig. 4c) end of the epigonal organ and suspended from the (Gilmore 1983, Gilmore et al. 1983). Maximum ova dorsal abdominal cavity by a mesovarium (Fig. 4a- diameters are around 5.0mm in Alopius supercili- d). Specimens examined revealed this general ana- osw (Gruber & Compagno 1981, Gilmore 1983). tomical pattern in A. superciliosus, Isurus paucus, I. After ovulation, the ova pass through the effe- oxyrinchus, C. taurus and C. carcharias. The same rent ovarian pore, over the mesovarium, and enter general lamnoid reproductive morphology has the ostium situated near the central confluence of been documented in L. nasus, A. vulpinus, A. pelag- the paired lobes of the and the paired oviducts. icus, C. maximus and P kamoharii by other authors The ova are apparently alternately shuttled to (Shann 1911,1923, Nakamura 1935, Matthews 1950, either oviduct as they pass through the anterior ovi- Gubanov 1972, Fujita 1981, Otake & Mizue 1981). A duct from the ostium, pass through a bifurcation in smooth fibrous coat from the anterior epigonal or- the oviduct (Fig. 4d) and then to either right or left gan covers the ovarian follicles thus creating an ova- oviducal glands. The oviduct bifurcation point ante- ry of the 'internal type' described by Pratt (1988). rior to the oviducal glands must have a gating mech- As Pratt (1988) states, 'this ovary type presents a anism which allows alternate movement of ova to 3-dimensional surface area' associated with the el- either oviduct. Evidence for the alternate move- lipsoidal interior lumen surrounding the oocyte ment of ova to each oviduct is the synchronous for- mass, therefore, giving 'much more available sur- mation of capsules containing a similar number face area to generate yolked oocytes than the rela- of ova in each oviducal gland. tively planar ovary found in other [elasmobranch] Fertilization is assumed to occur in the anterior orders'. A pocket, or efferent ovarianpore (Fig. 4c), oviduct in the vicinity of the ostium. This is based on opens to the abdominal cavity and allows ovulated the capture of recently mated C. taurus females on 8 ova to escape to the ostium. This pocket, situated and 12 May 1986 (off Daytona Beach, FL) which anterior and dorsally on the right side of the ovary, contained active sperm throughout the oviduct up enlarges as the ovary matures and reaches maxi- to the ostium. The 12 May specimen contained mum size when ovulation peaks. The ovary reaches sperm throughout the oviduct and within the first maximum size and ovulation rate during the oopha- capsule formed. This capsule did not contain ova, gous interval of embryonic development in C. tau- only ovalbumin and sperm (meI capsule of Gil- rus (Fig. 4a). During gestation the ovary in C. taurus more et al. 1983) indicating oviducal gland activity may reach a maximum size of 36.0 to 45.5cm in and capsule formation prior to the arrival of ova. length and weight of 8.5 kg, containing over 22000 Serial sections of the oviducal gland of pregnant C. ova, 1.3 to 10.0mm in diameter (Fig. 4b) (Gilmore et taurus have not demonstrated sperm storage in this Fig. 3. a - Spermatophores of Carcharias raum. b - SEM of spermatophore of Isurus oxyrinchus. c - SEM of internal exposure of sperrnatophore of I. oxyrinchus showing sperm aggregations. d - SEM detail of (c). species (our observations and Pratt 1993). The first head which contains ova andlor ovalburnin. In C. capsule to contain ova, only contains a single ovum. taurus, six basic capsule types have been identified Multiple ova occur in increasing numbers in succes- ranging from those containing no ova and only a sive capsules. Initial observations indicated that al- gelatinous ovalbumin/mucoid material, to those though multiple blastodiscs may be seen on several containing numerous fertilized or unfertilized ova ova in a single egg capsule, only one embryo devel- (up to 23 ova per capsule, Gilmore et al. 1983). Egg oped per capsule (Gilmore et al. 1983). However, capsules leave the oviducal gland and pass through recent observations reveal that up to three embryos the isthmus and enter the uterus typically in syn- may develop within a single capsule in C. taurus. A chrony in both oviducts. The capture of a series of pregnant C. taurus captured in mid June 1985 (off pregnant C. taurus in succession reveals a temporal Daytona Beach, FL) contained capsules with two pattern in the number and position of capsules in and three embryos in each of two capsules, respec- each oviduct over a 24 h period. This pattern reveals tively. that ova encapsulation occurs on a 24 h interval with As egg capsules leave the oviducal gland, a mem- newly formed capsules typically occurring within branous (collagen) tail forms behind the capsule Fig. 4. a - Ovary, paired oviducts with egg capsules and oviphagous embryos of Carcharias taurus captured off Stuart, Florida, September 1989. Note nearly identical position and number of capsules in each oviduct. Photo courtesy of Jose Castro. b - Ova up to lOmm in diameter in ovary with membrane excized for exposure, C. taurus. c - Ovary of pregnant Isurus oxyrinchus (HBOM 103:00253) showing efferent ovarian pore (eop) and oviduct including the oviducal gland (ovg). d - Anterior oviduct of Carcharodon carcharias showing bifurcation (bif) of oviduct a few centimeters posterior to the ostium (to the right) at the liver. the oviducal gland in specimens captured near Embryonic development in C. taurus has been dawn. well documented from early development to partu- Although fewer specimens of Alopias spp., Zsurus rition (Gilmore et al. 1983). Embryos of this species spp., Pseudocarcharias kamoharii and Lamna nasus pass through at least six nutritive phases during ges- have been examined, capsule formation and varia- tation. The first two occur while the embryo is en- tion in capsule morphology resembles that found in capsulated. During early cellular differentiation, C. taurus (Gubanov 1972, Fujita 1981, Gruber & encapsulated 13mm embryos utilize endocoelomic Compagno 1981, Gilmore 1983, Gilmore et a1.1983). yolk within the cardiac stomach, valvular intestine, Capsules produced early in the ovulation cycle do pericardial and coelomic cavities and do not con- not contain ova, whereas capsules produced during sume yolksac yolk supplies. This phase resembles the major oophagous interval in embryonic devel- the early development in amphibian embryos. opment contain the largest number of ova. Encapsulated embryos larger than 13mm TL (= total length) appear to consume or absorb materials that the ovary reaches its maximum size, ovulation such as albumin, mucous or other ova within the rates are high, embryonic growth rates are maximal capsule after their oral cavities,jaws and alimentary and the distention of the cardiac stomach ('the yolk tracts have developed sufficiently. The yolksac de- stomach', Shann 1911) occurs. Embryos in this latter clines in sue in embryos near hatching (= embryo phase have been documented in Lamna nasus emergence from the capsule), approximating (Swenander 1907, Shann 1911, Lohberger 1910), Zsu- 60mm TL. rus oxyrinchus (Stevens 1983, Uchida et al. 1987, The uterine epithelium is highly vascularized and Fig. I), and Carcharodon carcharias (Sanzo 1912). folded, particularly at the isthmus, and villiform Extensive abdominal cavity distention, due to yolk structures can be observed throughout the remain- consumption, has not been observed in alopiid em- der of the uterus (Fig. 5,6). This large surface area bryos to date (Otake & Mime 1981, Gruber & Com- and proximity of maternal blood supplies apparent- pagno 1981, Gilmore 1983). However, oophagy has ly insures oxygenation of the uterine fluid and may been documented in A. vulpinus (Gubanov 1972), enhance fluid secretion. Oxygenation of uterine A. pelagicus (Otake & Mizue IN),A. superciliosus fluid, which is undoubtedly a major source of respi- (Gilmore 1983),Isurus oxyrinchus (Stevens 1983),I. ratory oxygen, is necessary as lamnoids produce ve- paucus (Gilmore 1983) and Pseudocarcharias ka- ry large embryos without placentation. moharii (Fujita 1981). It is likely that all lamnoid A functional embryonic dentition (embryonic sharks are oophagous yet not necessarily embryo- teeth= emb), not resembling adult dentition (adult phagous. teeth= adl), develops between 40 and 60mm TL, Development of functional dentition, emb teeth, and apparently aids the embryo to escape from the in larnnoid embryos may give some indication of the capsule in addition to puncturing other capsule capacity to hunt and consume other embryos in ute- membranes after hatching (Fig. 7,8) (Gilmore et al. ro (Fig. 7,8). Erect functional teeth have been well 1983, Harnlett 1983). After hatching at lengths ap- documented in C. taurus embryos starting at a TL of proximating 60mm TL, the embryo obviously con- 40mm (Gilmore et al. 1983, Hamlett The em- sumes yolksac yolk supplies and possibly uterine bryonic dentition of A. pelagicus, A. superciliosus, fluid. At lengths of 100 to 334mm, hatched embryos C. carcharias, I. oxyrinchus, I. paucus and I? kamo- actively search for and attack egg capsules contain- hari have been found to be variously non-function- ing other embryos to the exclusion of capsules con- al, consisting of folded, not erect, soft or covered taining only unfertilized ova. Smaller encapsulated (with a membrane) adult teeth or microscopic emb embryos are either killed during capsular attacks by teeth (Sanzo 1912, Nakamura 1935, Fujita 1981, Ki- the larger hatched embryo, or are ripped from their yoshi Fujita personal communication 1985, Gil- capsules into the uterine cavity. Adult females cap- more 1983, Gilmore et al. 1983, Tsuguo Otake per- tured during July and August have contained dead, sonal communication 1985, Uchida et al. 1987). mangled embryos within the uterine cavity along However, Gruber & Compagno (1981) describe with a single living larger embryo (100-334mm TL), 'functional' teeth in a 20.6cm TL embryo of A. su- which may have within its mouth and digestive tract perciliosus. Two 59.0-61.5 cm TL embryos of A. vul- up to four embryos (Gilmore et al. 1983). This can- pinus taken from a female captured off Daytona nibalistic phase has only been documented in C. Beach, Florida on 19 January 1989 were found to taurus. have small emb teeth along the edge of the mouth. After the C. taurus embryo reaches a total length These teeth do not resemble the adult teeth which over 330mm and has consumed all siblings, it begins were forming under a membranous sheath in the to consume the large number (60-90) of turgid egg mouth of the same embryos. Several egg capsules capsules within the uterus that contain unfertilized found with these embryos were sliced open indicat- ova. These capsules can contain up to 23 unfertil- ing that these teeth were capable of opening cap- ized ova/capsule and are produced daily through- sules and possibly killing and consuming other em- out this period of gestation. It is during this period bryos. However, no smaller dead or consumed em- Fig. 5. a - Uterine membrane at isthmus (ist) with isthmian folds readily differentiated from remainder of uterine wall (uwl) with tropho- nemata in pregnant lsurus oxyrinchus (HBOM 103:00250).b -Scanning electron micrograph (SEM) enlargement of microfolds located on the isthmian folds photographed in (a). c- SEM enlargement of (b) showing ridges on microfolds. d - SEM enlargement of (c) showing detail of microfold ridges. bryos have been found to date in this species or any noids, particularly those that consistently produce other lamnoid except C. taurus. A more detailed single large embryos per uterus (e.g. alopiids). Em- study of the ontogeny of embryonic dentition may bryophagy occurs in C. taurus embryos when they demonstrate two distinct types of dentition, an em- are between 10 and 30cm TL. Although other lam- bryonic set and a set similar to the adult form. The noid embryos have been captured in the same in- predicted level of consumption of egg capsules in C. terval of development, the only ones which have taurus during a single pregnancy (1000-1700 cap- been examined for cannibalism and oophagy are sules containing 17000 ova, Hamlett 1983), may re- the alopiids. All three alopiid species have been ex- quire continual embryonic loss and replace- amined: A. pelagicus (42.1-52.1 cm TL, Otake & Mi- ment while within the uterus. Associated with this zue 1981), A. superciliosus (20.6cm TL, Gruber & loss would be an ontogenetic transition in tooth Compagno 1981, Gilmore 1983), and A. vulpinus morphology and function. (8.9-114.0cm TL, Gubanov 1972, Gilmore examin- Although embryophagy has only been docu- ation). Only yolk has been found, demonstrating mented in C. taurus, it may also occur in other lam- oophagy, not embryophagy. Late embryos of A. su- Fig. 6. a- SEM of trophonemata of uterine wall in a prep).b - SEM enlargement of (a). c - SEM enlargement of (b) showing epithelium of trophonemata. d - SEM enlargement of (c) showing terminal microvilli on epithelium of trophonemata of uterine wall. perciliosus, near 105 cm TL, have been found to con- erect teeth when approaching parturition (Gilmore sume egg capsules intact, swallowing them whole 1983, Fig. 7,8). (Gilmore 1983). Larger embryos are undoubtedly Embryos of all species typically have metabo- capable of swallowing egg capsules whereas smaller lized all intrauterine yolk supplies during the last embryos may find it necessary to mutilate the cap- two months of gestation. These late term embryos sule prior to consumption. Embryonic teeth in Alo- do not have distended cardiac stomachs, and as a pias spp. may be an for capsule con- percentage of body weight, may have considerably sumption and oophagy, not embryophagy. How- enlarged or livers with similar proportions as ever, the lack of specimens and data means that em- adult livers. During this period, ovulation has bryophagy cannot be entirely ruled out in other ceased and the maternal ovary atrophies. At partu- lamnoid species. rition, the embryos are large, and may function as Embryophagy is also questioned in Isurzu and active predators soon after (Table 1). Lamna due to the common occurrence of multiple embryos at term in each uterus. These embryos lack Fig. 7. a - Mouth of 48cm TL embryo of Zsurus oxyrinchus (HBOM 103:00250) showing lack of erect dentition. b - SEM of lateral view of 50cm embryo of Carcharias taurus showing embryonic (emb) teeth which do not resemble the adult dentition. c - Frontal view of dentition of a 91cm TL embryo of Carcharias taurus (HBOM 103:00182) which died at birth showing adult dentition type with well developed lateral denticles (lad) on either side of the major cusp.

Migration and reproduction NMFS, personal communication 1987, Steve Bran- stetter personal communication 1990).From Spring The only lamnoid species which has been studied to September adult females with embryos 13 to consistently in all life history stages is C. taurus. The 600mm TL have been recorded primarily from location of mating, gestation, parturition and juve- south of Cape Hatteras to Jupiter Island, Florida, or nile development can now be documented with in the northern Gulf of . Females carrying some degree of certainty. Figure 9 depicts the move- embryos over 800mm TL, or that have recently giv- ments of C. taurus in the Western Atlantic off the en birth, have been captured consistently dtliing the east coast of North America. Historically, adult cooler months from November to February off males and juveniles 1to 2m TL have typically dom- Florida (Springer 1948, Clark & Von Schmidt 1965, inated the catch of C. taurus in shallow nearshore Gilmore et al. 1983). Recently spent females and fe- waters of the mid-Atlantic bight during the summer males nearing first maturation have been caught on months (Bigelow & Schroeder 1948, Jack Casey the same shark longline from January to March Fig. 8. a - SEM of dentition of 53.6cm TL embryo of C. taurus (HBOM 103:00264) revealing multiple tooth rows of anterior-most teeth (symphysis to upper right) and change in tooth morphology between rows. b - SEM of dentition of 48cm TL I. oxyrinchus embryo (HBOM 103:00250) showing multiple rows of anterior teeth (symphyseal teeth to right) and membranous sheath over teeth partially exposed by SEM preparation. c - SEM of (a) showing posterior lateral tooth rows. d - SEM of (b) showing posterior lateral tooth rows.

(Springer 1948, Gilmore unpublished data). Males on courting males and a hierarchal social status in caught during this period were all mature and with courting males (Gordon 1993). Mating activity oc- seminal vesicles full of spermatophores. Mating curs in relatively shallow water, at depths less than scars were apparent Qn one February male cap- 30m off the Florida east coast (from 29'00' to tured off Ft. Pierce, Florida (Gilmore et al. 1983) 27'00'N) in late February to April, just after partu- and on several males observed in mixed sex aggre- rition. In North Carolina, mating apparently occurs gations off the coast of North Carolina during May in late April and early May. Females in early gesta- 1988 (Gilmore unpublished data). Major scarring tion typically occur inshore while males virtually around the nape and pectorals in males and females disappear from the inshore catch during the late has been commonly observed in mating aggrega- spring and summer in Florida waters (Gilmore et al. tions of sand tigers off North Carolina and Florida. 1983). Off North Carolina the males remain on the Recent observations of mating behavior in captive mating grounds until July. Male migration out of the Australian C. taurus have documented female bites mating and gestation grounds is probably both off- shore and northward as mature males are often caught north of Cape Hatteras. The characteristic seasonal developmental pat- tern for C. taurus has been observed through speci- mens collected for 37 years (Gilrnore et al. 1983, personal observations and capture notes). The de- velopmental stages of the embryos within a gravid female can now be predicted within a few weeks. Embryonic development is synchronous for all in- dividuals captured in one region of the species range. The synchronous development observed in Florida embryos over many years indicates that a very predictable environmentalcue governs mating activity and gonadal condition. Males and females rendezvous at the same location at the same time each year, both off Florida and North Carolina. There appears to be a delay of two weeks to amonth in development between C. taurus specimens from the Carolinas and Florida (based on capture re- cords maintained by JosC Castro and R.G. Gil- more). @ Mating grounds Few other lamnoids have been studied in enough Female gestation grounds detail to determine migratory patterns relative to a Juvenile nursery grounds -I reproduction. However, extant data from certain mature male population locations around the world allow some predictions <~uvenile male migratory to be made. Pregnant I. oxyrinchus have only been routes captured between 20" and 30°N or S latitude in the Fig. 9. Map of eastern seaboard of United States showing gesta- Pacific, Atlantic, Gulf of Mexico and northeastern tion grounds (black: spring-winter),parturition sites (white: win- (Vaillant 1889, Depperman 1953, Gohar & ter), neonateljuvenile migration (arrows: springlsummer),nurs- Mazhar 1964, Guitart-Manday 1975, Branstetter ery grounds (stipple: several years), mating sites (black: spring) 1981, Stevens1983, Uchida et al. 1987). Data are lim- and southward migration of males and recently mature females (winter). ited, but parturition in I. oxyrinchus appears to oc- cur either during the spring, or summer, at most lo- cations (Table 2). Its congener, I. Paucus, is equally tropicaYtropica1western Atlantic between 20" and lacking in reproductive information as only four 30°N in the Gulf of Mexico, or in the vicinity of the pregnant specimens have been captured, two with Florida Straits, it is likely that this region is a loca- multiple embryos (Casey & Pratt NMFS personal tion for parturition in makos or at least a maternity communication 1986, John Randall personal com- site. The capture of three ripe males I. paucus in the munication 1985) and two with two or fewer em- northern Gulf of Mexico on 16 April 1985 on the bryos (Guitart-Manday 1975, Gilmore 1983). Three same set line (27'35'N, 89"55'W, Steve Branstetter pregnant I. paucus specimens were taken in the personal communication 1990, Killam & Parsons Florida Straits and north of Puerto Rico (Guitart- 1986) and a single large mature female (342cm FL) Manday 1975, Gilmore 1983, Casey & Pratt NMFS on 1 April also in the northern Gulf of Mexico personal communication 1986) and one off (28"55'N, 85"35'W, Killam & Parsons 1986) may in- (John Randall personal communication 1985). dicate malelfemale syntopy within weeks and pos- Since all of the pregnant makos, short or longfin, sible mating activity in the northern Gulf from the have come from the sub- Extensive collections of the white shark, Carcha- rodon carcharias, made in North American waters and adult mating ground. However, the location of have failed to yield pregnant females. However, parturition may be further south based on winter1 sexual syntopy and free swimming young of the spring occurrence of juvenile and adult white year have been documented both off the west coast sharks in the Florida Straits over the past few years and the northeast (Casey & Pratt 1985, Klirnley (Gilmore unpublished data). The routine occur- 1985). Female C. carcharias apparently give birth rence of juvenile C. carcharias off Daytona Beach, off the coast south of Point Conception Florida, during the winter suggests that the nursery during the summer (smallest specimen 122 cm TL in ground for this species is broadly the western North July, Klimley 1985). Most adult male-female synto- Atlantic with the distribution of py occurs north of Pt. Conception, indicating mat- the species influenced by water temperatures ing most likely occurs in the vicinity of the principal (around the 15°C isotherm range ll-24"C, Casey & adult feeding grounds off the coast of northern or Pratt 1985). A similar occurrence of juveniles in- central California, possibly during the fall. In the shore in the warm latitudes of South during northeastern U.S. mating apparently also occurs in the winter and adult male-female syntopy at cooler the feeding grounds in the Mid-Atlantic Bight with latitudes during the summer (Bass et al. 1975) in- most records of syntopy in large adults coming from dicates that the seasonal distribution observed off late summer (Casey & Pratt 1985). The smallest free the North American coast may be a generalized swimming specimens were taken during the sum- pattern for C. carcharias. mer (to 122cm TL, Casey & Pratt 1985). The Mid- Little is known of migration relative to reproduc- Atlantic Bight apparently acts as a nursery ground tion in Lamna spp. though they appear to be con-

Table 2. Reproductive seasonality and pregnancy in Isurus spp. Authors are: 1= Depperman (1953); 2= Gilmore data; 3= Branstetter (1981);4= Uchida et al. (1987); 5= Stevens (1983); 6= Gilmore (1983); 7= Casey & Pratt personal communication; 8=Pratt, Casey, Castro, Gilmore personal observation (1992).

Isurus oxyrinchus (size at birth: 60-70cm TL,free swimming 64-77cm TL) Date Author Location Embryo number (size in cm TL) Estimated parturition period

Embryos Northern hemisphere Jan. Puerto Rico winter Feb. Florida Straits springlsummer April Florida Straits summer Aug. N. Gulf of Mexico winterlspring Nov. Okinawa, spring

Southern hemisphere Sept. New S. , Aust. winterlspring Sept. New S. Wales, Aust. winterlspring Oct. New S. Wales. Aust. winterlspring Juveniles June N. Gulf of Mexico spring* June Florida Straits summer** August Florida Straits summer*

Isuruspaucus (size at birth: 122cm TL;free swimming 123crn TL) Dec. 6 Florida Straits l(97) winter Jan. 7 Puerto Rico 4(113-122) winter

*Based on 70cm parturition size (Stevens 1983). **Based on 27.9cm yr-' growth for 81-198cm makos (Casey et al. 1986). fined to cool temperate waters with parturition oc- species.' Captures of pregnant Alopiaspelagicus al- curing during the spring (Aasen 1966, Templeman so indicate a variable mating period. 1963). Although accounts and fisheries of Cetorhinus Pregnant alopiids have been captured from a va- maximus date back to the last century, little life his- riety of locations throughout the world (Table 3). tory data exist. Basking sharks are most apparent in Alopias vulpinus embryos have been taken from the British Isles during the summer. They are easily specimens captured off New York and Florida and observed at the surface during this period. Mating embryo length data indicates spring or summer par- behavior and direct evidence of recent mating turition at most locations and spring mating in the (sperm in oviducts, Matthews 1950) demonstrates northwestern Red Sea. Gubanov (1972) presents that C. maximus mates off the British Isles during capture data which indicate a spatial and temporal the summer. However, the location of parturition, separation of A. vulpinus based on ontogeny and which apparently occurs during the winter or spring sex with most pregnant females and juveniles oc- remains a mystery. curing in the northwestern portion of the Indian Nothing has been published on the periodicity of Ocean from February to May (93% females were reproduction in Pseudocarcharias. pregnant), while sexual syntopy was greatest in the and Chagos islands during summer and fall. Most pregnant A. superciliosus have been cap- tured in the Florida Straits and both winter and summer parturition periods are indicated in this Recent captures of A. superciliosus embryos are from the west- em Atlantic (Moreno & Mor6n 1992).

Table 3. Reproductive seasonalityand pregnancy in Alopias spp. Authors are: l=Gilmore data; 2= Gubanov (1972); 3 = Gohar & Mazhar (1964); 4= Stillwell & Casey (1976) or Strasburg (1958); 5= Hixon (1W9); 6= Gruber & Compagno (1981); 7= Nakamura (1935); 8= Guitart-Manday (1975); 9= Otake & Mime (1981).

Alopias vulpinus (size at birth: 111-149m TL,free swimming 115-153cm TL) Date Author Location Embryo number (size in cm TL) Estimated parturition period

19 Jan. 1 Florida Straits 2(59-61) springlsummer 19 Feb. 2 N.W. 2(8.9) summer April 2 N.W. Indian Ocean 2(114) springlsummer 23 April 3 N.W. Red Sea 4-5 capsules ? mating in April 4 June 4 Christmas Island 2(114) summer 3 June 5 Ventura, California 4*(139-142) summer

Alopias superciliosus (size at birth: 1Wl05cm TL; free swimming 130cm TL) Mar. 7 Suo, 2(37) summerlfall 9 May 1 Florida Straits 2(55-60) summer 18 June 1 Florida Straits 2(105-106) summer 29 June 6 Florida Straits 2(21-21) winter Sept. 1 Florida Straits 2( 1 most Aug. thru-Sept. 8 Florida StraitsICuba 2(near term) summerlfall

Alopias pelagicus March 7 Suo, Taiwan 2(44) summer April 4 Fanning Is., Pac. 2(unknown) 9-12 Sept. 9 E.Indian Ocean 212(4245/5@-52) winterlspring

*Unverified number of embryos, lengths are for two embryos examined. Discussion more food, abundant predators in a variety of size ranges, more physiological stress) than deep water The mechanisms of viviparity differ significantly ecosystems (i.e. patchy food availability, low preda- between the lamniform and the galeiform sharks. tor density, little environmental instability, and However, both groups produce relatively large em- therefore less physiological stress). Given these dif- bryos at parturition which have been nourished fering environmental scenarios, large precocious throughout gestation by various maternal nutritive embryos with few siblings may be selected for in sources, including ovulation, uterine fluids or pla- highly productive and competitive shallow near- centation. If the various mechanisms of viviparity shore environments. The smallest embryos and evolved independently in several taxa of chondrich- largest litters in both lamnoids (18 embryos, 60- tyan fishes, then similar evolutionary pressures may 70cm TL in Isurus oxyrhinchus, Table 2) and car- be acting on all of these groups. Since both the lam- charhinids (up to 135 embryos, 35-44cm TL in Prio- noids and galeoids are typically large aggressive ap- nace glauca, Pratt 1979) have been recorded from ical predators, the rapid growth of embryos and the pelagic species. The largest embryos have been re- production of a large neonate at parturition would corded from estuarine and coastal species (2 em- allow a decided predatory advantage with very low bryos, 100cm TL in the lamnoid species Carcharias progeny mortalities relative to oviparous species, taurus or 7 embryos, l40cm TL in Careharodon car- particularly teleostean fishes. The production of a charias, Uchida et al. 1987) and the galeoid species large embryo is particularly important if growth (7-12 embryos, 70 cm in Carcharhinus leucas or 5-12 rates after parturition are not as fast as sympatric embryos, 85-100cm TL in C. obscurus, Dodrill teleostean predators. Large teleostean predators 1977). There may be exceptions with pelagic species such as the mackerals, (Scombridae) and the that give birth at location or during periods in which (Istiophoridae and Xiphiidae) have fe- food availability is high. The abundance of juvenile cundities ranging from several hundred thousand to and pregnant A. vulpinus (typically two embryos, 16 million , typically spawn several times within 11-149cm TL) in the northwestern Indian Ocean one year, grow rapidly (maturation in less than four during the upwelling season, a period of increased years for many species) and have relatively short aquatic productivity (Gubanov 1972), insures re- life spans (i.e. generally less than 10 years) relative source availability for both embryos and immature to the lamnoids and galeoids which may take two threshers. decades to mature (Manooch & Raver 1984, Bran- The higher incidence of young C. taurus in estu- stetter & McEachran 1986, Branstetter 1990). aries of the Mid-Atlantic Bight and C. carcharias in- Consistent differences in embryo size and fecun- shore on the east and west coast of North America dity in lamnoid sharks appear to have some associ- are undoubtedly responses to both food availability ation with the neonatal environment. Parallel re- and predatory pressures. Sand tiger sharks mate productive patterns in embryo size and fecundity synchronously each year in the late winter and observed in galeoid sharks further demonstrates spring after parturition, which allows the juveniles the potential impact of neonatal environments on to utilize estuaries of the Mid-Atlantic Bight during reproductive biology. Evolutionary pressure from a period of optimum food availability, the summer environmental sources impact reproductive mecha- and early fall. Abundant food resources insure rap- nisms which may then vary with the organisms' hab- id growth to a size that will eliminate most preda- itat and niche preference, in addition to its' phyletic tory mortality. history. Selection for the number and size of em- Abundant food resources allow rapid neonate bryos differs between pelagic and nearshore hab- and juvenile growth. Larnnoid growth rates and itats in both lamnoids and galeoid sharks. High en- time to maturation appear to be shorter than for ergy, environmentally unstable and heterogenous carcharhinid sharks of similar adult body size estuarine or nearshore continental shelf ecosystems (Branstetter 1990). It is estimated that male C. tau- would present a different challenge to survival (i.e., rus may mature within four or five years, females 112 within eight years (190-220cm TL, Gilmore et al. may play some role in explaining the observations 1983), while C. carcharias may mature within 9-10 made to date. Detailed analysis of these hypotheses years (366-427cm TL, Cailliet et al. 1985), Alopias will have to wait until sufficient study material is superciliosus in 3.5 to 4.5 years (300-350cm TL, available with the isolation of reproductive loca- Gruber & Compagno 1981). tions and capture of pregnant females. Oophagy has been documented in nine of the six- Another important area of study is the functional teen species of lamniform sharks. This reveals com- significance of embryophagy and oophagy in the plementary reproductive styles within the order development of lamnoids. Why do lamnoids, par- Lamniformes. Several authors have stated that em- ticularly C. taurus, have a low fecundity rate and bryophagy apparently occurs in lamnoid species embryonic cannibalism while carcharhinids which other than C. taurus (Compagno 1984). However, produce young of similar size to lamnoids have universal occurrence of embryophagy in the order higher fecundity without cannibalism? The only is questioned, based on the occurrence of multiple lamnoid we know in detail, C. taurus, reproduces embryos within a single uterus at parturition in six annually and mature females are pregnant through of the same nine species (Table 1). Several hypoth- at least 75% of their adult life, whereas carcharhi- eses have been proposed to explain this differential nids often skip a year between pregnancies. How- fecundity, but the paucity of early embryonic stages ever, the production of two pups a year does not in lamnoid collections worldwide has not allowed match a fecundity rate of 1045 pups every other these hypotheses to be tested. year in many of the carcharhinids within the same The mechanism for differential fecundity in lam- adult size range. Is the fitness of the lamnoid em- noids may be explained by the following hypotheti- bryo greater than the carcharhinid in regard to prey cal reproductive scenarios: (1) Lamnoids with mul- capture or energetics as a result of oophagy and em- tiple embryos per uterus release multiple ova bryophagy? Do lamnoids have better success in throughout pregnancy, therefore, insuring fertiliza- prey acquisition and capture immediately after par- tion of multiple embryos. C. taurus initially releases turition due to prior hunting experience in utero? a single fertilized ova which is followed by a gradual Or does embryonic cannibalism in C. taurus elim- increase in number of ova encapsulated, ranging inate embryonic competition for food resources in from 1to eventually 23 ova per capsule, though cap- order to produce a larger embryo in the shortest pe- sules produced after two weeks are not fertilized. riod of time on an annual basis? Stribling et al. (2) In lamnoids with multiple term embryos, several (1980) demonstrated that C. taurus embryonic embryos may occur in the first capsule produced. growth rates supersede that recorded for all other These embryos then hatch synchronously and con- elasmobranch species examined with a 1.2~lo6 in- sume other embryos which either remain in their crease in dry weight during gestation. capsules, or have only recently hatched, all of which These questions need to be treated in a serious are smaller than the first group to hatch. Those first study of the life histories, behavior and ecology of to hatch synchronouslyrefrain from consuming one both lamnoids and carcharhinids in the field and in another due to size similarity. (3) Differential sperm captive systems through careful descriptive studies viability allows for extended (2 weeks) fertilization and well designed experiments. of ova in C. taurus, while short term sperm viability in species with multiple embryos per uterus only permits fertilization of the first group of ova to ar- Acknowledgements rive in the anterior oviduct. (4) Multiple matings with short sperm viability account for extended fer- I thank my research assistant Douglas Scheidt for tilization of ova in C. taurus, while single short term aiding in the preparation of data used in the manu- encounters in pelagic species allow a single transfer script and D. Scheidt, H. Pratt, Patricia Linley and of sperm which fertilize multiple ova released dur- William Lellis for reviewing the manuscript. John ing mating. All of these representative scenarios Wourms and Wes Pratt furnished translated copies of critical literature. JosC Castro allowed use of his 14. In: G. Sibley, J. Seigel& C. Swift (ed.) Biology of the White photo of C. taurus embryos. I thank Tris Colket, Er- Shark, Mem. S. Cal. Acad. Sci. 9. ic Sander, Kenneth Cheatham and John Krall for Clark, E. & K. von Schmidt. 1965. Sharks of the central Gulf coast of Florida. Bull. Mar. Sci. 15: 13-83. furnishing invaluable specimens of various lamnoid Compagno, L.J.V. 1977. Phyletic relationships of living sharks species. Patricia Linley prepared EM specimens. and rays. Amer. Zool. 17: 303-322. This constitutes contribution number 852 to the Compagno, L.J.V. 1984. Sharks of the world: an annotated and Harbor Branch Oceanographic Institution. illustrated catalogue of shark species known to date. FA0 spe- cies catalogue, Vol. 4, Part 1, Hexanchiformes to Lamni- formes, U.N. Dev. Prog., FAO, Rome. 249pp. Depperman, B. 1953. Maternity model mako. Sports Afield, References cited March 1953: 8H7. Dodrill, J. 1977. A hook and line survey of the sharks found with- Aasen, 0.1966. Brugde, Cetorhinus maximus (Gunnerus), 1765. in five hundred meters of shore along Melbourne Beach, Bre- Saertrykk av Fishets Gang 49: 909-920. vard County, Florida. M.S. Thesis, Florida Institute of Tech- Abe, T., A. lsokawa, K. Aoki, T. Kishimoto, Y. Shimma & H. nology,Melbourne. 304pp. Shimma. 1969. Notes on some members of Osteodonti (class Dunlop, J. 1892. The habits and anatomical structure of the por- ) 11. Bull. Tokai Reg. . Res. Lab. 60: 1-3. beagle shark (Lamm cornubica Cuv.). Nat. Hist. Soc. d~as- Bass, A., J. D'Aubrey & N. Kistnasamy. 1975. Sharks of the east boro Trans. 4: 134-137. coast of southern Africa. IV. The families Odontaspididae, Eschmeyer, W.N. 1990. Catalog of the genera of recent fishes. Scapanorhynchidae,Isuridae, Cetorhinidae, Alopiidae, Orec- Cal. Acad. Sci., San Francisco. 697pp. tolobidae and Rhiniodontidae. Oceanogr. Res. Inst. (Dur- Fitch, J. 1949. The Carcharodon carcharias ban), Invest. Rep. 39.102~~. (Linnaeus) in California waters during 1948. Calif. Fish Game Bigelow, H.B. & W.C. Schroeder. 1948. Lancelets, cyclostomes, 35: 135-138. and sharks. pp.98-177. In: J. Tee-Van, C. Breder, S. Hilde- Fourmanoir, P. 1961. Requins de la cBte ouest de . brand, A. Parr & W. Schroeder (ed.) Fishes of the Western Mem. Inst. Scient. Madagascar 4: 1-81. North Atlantic, Part 1, Mem. Sears Found. Mar. Res., Yale Fujita, K. 1981. Oviphagous embryos of the pseudocarchariid University, New Haven. shark, Pseudocarcharias kamoharai, from the central Pacific. Branstetter, S. 1981. Biological notes on the sharks of the north Jap. J. Ichthyol. 28: 37-44. central Gulf of Mexico. Contrib. Mar. Sci. 24: 13-34. Garrick, J. 1967. Revison of sharks of genus Isurus with descrip- Branstetter, S. 1990. Early life-history implications of selected tion of a new species (Galeoidae, ). Proc. U.W. Natl. carcharhinoid and lamnoid sharks of the Northwest Atlantic. Mus. 118: 663-690. pp.17-28. In: H.L. Pratt, Jr., S.H. Gruber & T. Taninchi (ed.) Gilmore, R.G. 1983. Observations on the embryos of the longfin Elasmobranchs as Living Resources: Advances in the Biology, mako, Isurus paucus, and the , Alopias super- Ecology, Systematics, and the Status of the Fisheries, NOAA ciliosus. Copeia 1983: 375-382. Tech. Rep. 90. Gilmore, R.G., J. Dodrill & P: Unley. 1983. Reproduction and Branstetter, S. & J.D. McEachran. 1986. Age and growth of four embryonic development of the sand tiger shark, carcharhinid sharks common to the Gulf of Mexico: a sum- taurus (Rafinesque). U.S. Fish. Bull. 81: 201-225. mary paper. Indo-Pacific Fish Biology: 361-371. Gohar, H. & F. Mazhar. 1964. The elasmobranchs of the north- Cadenat, J. 1950. Poissons de mer du Senegal. I.EA.N., Initia- western Red Sea. Publ. Mar. Biol. St. Ghardaqa 13: 1-144. tions Africaines, 111.345~~. Gordon, I. 1993. Pre-copulatory behaviour of captive sandtiger Cadenat, J. 1956a. Note d'ichtyologie ouest-Africaine. XIV. - shark, Carchurias taurus. Env. Biol. Fish. 38: 159-164 (this vol- Remarques biologiques sur le requin-sable Carcharias (Car- ume). charias) taurus Rafinesque 1810. Bull. Inst. Fr. Afr. Noire 18: Gruber, S.H. & L.J.V. Compagno. 1981. Taxonomic status and 1249-1256. biology of the bigeye thresher, Alopias superciliosus. U.S. Cadenat, J. 1956b. Note d'lchtyologie ouest-Africaine.XV. - Sur Fish. Bull. 79: 617-640. un requin-renard nouveau pour la faune d'Afrique Occiden- Gubanov, Y.P. 1972. On the biology of the Alopias tale Frangaise Alopias superciliosus (Lowe) 1840? Bull. Inst. vulpinus (Bonnaterre) in the northwest Indian Ocean. J. Ich- Fr. Afr. Noire 18: 1257-1266. thyol. 12: 591-600. Cailliet,G.M., L. Natanson, B. Welden & D. Ebert. 1985. Prelimi- Gubanov, Y.P. 1978. The reproduction of some species of pelagic nary studies on the age and growth of the white shark, Carcha- sharks from the equatorial zone of the Indian Ocean. Voprosy rodon carcharias, using vertebral bands. pp. 49-60. In: C. Sib- Ikhtiologii 18: 781-792. (In Russian). ley, J. Seigel & C. Swift (ed.) Biology of the White Shark, Guitart-Manday, D. 1966. Nuevo nombre para una especie de Mem. S. Cal. Acad. Sci. 9. tihuron del genro Isurus (: Isuridae) de aguas Casey, J. & H.L. Pratt, Jr. 1985. Distribution of the white shark, Cubanas. Poeyana 15: 1-9. Carcharodon carcharias, in the western North Atlantic. pp. 2- Guitart-Manday, D. 1975. Las pesquerias pelagico-oceanicas de corto radio de accion en la region noroccidental de Cuba. Sadowsky, V. 1970. On the dentition of the , Odon- Oceanogr. Inst., Acad. of Sci., Havana. Seria Oceanologica 31: taspis taurus, from the vicinity of Cananeia, . Bol. Inst. 1-41. Oceanogr. S. Paulo. 218: 37-44. Hamlett, W.C. 1983. Maternal-fetal relations in elasmobranch Sanzo, L. 1912. Embrione di Carcharadon rondoletii M. Hle. con fishes. Ph.D. Dissertation, Clemson University, Clemson. particolare disposizione del sacco vitellino. R. Comitato Ta- 228pp. lassografico Italiano, Memoria ll: 3-9. Hixon, M.A. 1979. Term from a large Scattergood, L. 1962. White sharks, Carcharodon carcharias, in shark, Alopias vulpinus. Calif. Fish Game 65: 191-192. Maine, 1959-1960. Copeia 1962: 446-447. Killam, K. & G. Parsons. 1986. First record of longfin mako, Isu- Shann, E.W. 1911. A descriptionof the advanced embryonicstage ruspaucus, in the Gulf of Mexico. U.S. Fish. Bull. 84: 748-749. of Lamna cornubica. Fish. Board Scotland Ann. Rept. 28: 73- Klimley, P. 1985. The areal distribution and autoecology of the 79. white shark, Carcharodon carcharias, off the west coast of Shann, E.W. 1923. The embryonic development of the porbeagle North America. Mem. S. Cal. Acad. Sci. 9: 15-40. shark, Lamna cornubica. Proc. Zool. Soc. London 11: 161-171. Leim, A.H. & W.B. Scott. 1966. Fishes of the Atlantic coast of Smith, J.L.B. 1951. A juvenile of the man-eater Carcharodon car- Canada. Bull. Fish. Res. Board. Can. 155: 1-485. charias Linn. Ann. Mag. Nat. Hist. 4: 729-736. Lohberger, J. 1910. Ober zwei riesige Embryonen von Lamna. Springer, S. 1943. A second species of thresher shark from Flor- Abh. Bayer Akad. Wiss. 4 (Beitrage zur Naturgeschichte Os- ida. Copeia 1943: 54-455. tasiens Supp. 2): 1-45. Springer, S. 1948. Oviphagous embryos of the sand shark, Odon- Manooch, 111, C. & D. Raver, Jr. 1984. Fisherman's guide: fishes taspis taurus. Copeia 1948: 153-157. of the southeastern United States. N.C. St. Mus. of Nat. Hist., Stevens, J.D. 1983. Observations on reproduction in the shortfin Raleigh. 362pp. mako. Copeia 1983: 126-130. Matthews, L.H. 1950. Reproduction in the basking shark, Cetor- Stillwell, C. & J. Casey. 1976. Observations on the bigeye thresh- hinus maximus (Gunnerus). Philos. Trans. Royal Soc. Lond. er shark Alopias superciliosus, in the western North Atlantic. 234b: 247-316. U.S. Fish. Bull. 74: 221-225. Moreno, J.A. & J. Mor6n. 1992. Reproductive biology of the bi- Strasburg, D. 1958. Distribution, abundance, and habits of pelag- geye thresher shark, Alopias superciliosus (Lowe, 1839). Aust. ic sharks in the central Pacific Ocean. U.S. Fish. Bull. 58: 355- J. Mar. Freshwater Res. 43: 77-86. 361. Nakamura, H. 1935. On the two species of the thresher shark Stribling, M.C., W.C. Hamlett & J.P. Wourms. 1980. Develop- from Formosan waters. Mem. Fac. Sci. Agric. Taihoku Imp. mental efficiency of oophagy, a method of viviparous em- Univ. 14: 1-6. bryonic nutrition displayed by the sand tiger shark (Eugom- Nakaya, K. 1971. Descriptive notes on a porbeagle, Lamna nasus, phodus taurus). Proc. So. Carol. Acad. Sci. 42: 111. from Argentine waters, compared with the North Pacific Sund, C. 1943. Et brugdebarsel. Naturen 67: 285-286. salmon shark, Lamna ditropis. Bull. Fac. Fish. Hokkaido Univ. Swenander,G. 1907. tiber die Ernahrung des Embryos der Lam- 21: 269-279. nu cornubica. Zoologiska Studier Tillagn T. nllberg, Uppsala: Norman J. & F. Fraser. 1948. Giant fishes, whales and . 283-288. Putnam, London. 376pp. Taniuchi. T. 1970. Variation in the teeth of the sand shark, Odon- Osipov, V. 1968. The biology and fishing of and other pelagic taspis taurus (Rafinesque) taken from the East Sea. Jap. fishes in the northeast Indian Ocean. Trudy Vesesoiuznogo J. Ichthyol. 17: 37-44. Naughno Issledovatel'skogo Inst. Morskogo Rybnog. Kho- Templeman. W. 1963. Distribution of sharks of the Canadian At- ziaistra I. Okeanografii 64: 300-322. (In Russian). lantic (with special reference to Newfoundland waters). Bull. Otake, T. & K. Mizue. 1981. Direct evidence for oophagy in Fish. Res. Board Can. 140: 1-77. thresher shark, Alopias pelagicus. Jap. J. Ichthyol. 28: 73-79. Uchida, S., F. Yasuzumi, M. Toda & N. Okura. 1987. On the ob- Pratt, H.L., Jr. 1979. Reproduction in the , Prionace servations of reproduction in Carcharodon carcharias and Isu- glauca. U.S. Fish. Bull. 77: 445-470. rus oxyrinchus. Rep. of Japanese Group for Elasmobranch Pratt, H.L., Jr. 1988. Elasmobranch gonad structure: a descrip- Studies 24: 5-6. tion and survey. Copeia 1988: 719-729. Vaillant, L. 1885. Sur les dimensions comparatives des adultes et Pratt, H.L., Jr. 1993. The storage of spermatozoa in the oviductal des jeunes chez un poisson Blasmobranche, 1'Alopias vulpes. glands of western North Atlantic sharks. Env. Biol. Fish. 38: Bull. Soc. Philom. Paris 10: 41-42. 139-149 (this volume). Vaillant, L. 1889. Note sur un foetus gigantesque d'oxyrhina Randall, J.E. 1973. Size of the great white shark (Carcharodon). spallanzani Bonap. Bull. Soc. Philom. Paris 1: 38-39. Science 181: 169-170.