FAU Institutional Repository http://purl.fcla.edu/fau/fauir

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

Notice: ©1983 American Society of Ichthyologists and Herpetologists. This manuscript is an author version with the final publication available and may be cited as: Gilmore, R. G. (1983). Observations on the embryos of the longfin mako, Isurus paucus, and the bigeye thresher, Alopias superciliosus. Copeia 2, 375-382.

/<""\ \

Copria, 1983(2), pp. 375-382

Observations on the Embryos of the Longfin Mako, Jsurus paucus, and the Bigeye Thresher, Alopias superciliosus

R. GRANT GILMORE

Four embryos of Alopias superciliosus and one of lsurus paucus were dissected and examined along with the reproductive organs of adults captured in the Florida Current off the east-central coast of Florida between latitude 26°30'N and 28°30'N. The embryos were found to contain yolk, demonstrating prenatal nutrition through intrauterine oophagy. Various proportions of embryo anatomy considered diagnostic for these species resemble those of adults. The general gonad morphology and presence of egg capsules containing multiple ova resem­ ble the described development stages of other lamnids, alopiids and Odontaspis taurus (Odontaspidae). This is the first documented observation of oophagy in these species.

OPHAGOUS embryos have been record­ As these species are rarely caught and examined O ed in three elasmobranch families, Odon­ by biologists, there are no documented obser­ taspidae (Odontaspis taurus, Springer, 1948; Bass vations of oophagy in Alopias superciliosus and eta!., 1975; Pseudocarcharias kamoharai, Fujita, lsurus paucus. For this reason I present the fol­ 1 981 ), Lamnidae (Lamna nasus, Lohberger, lowing embryonic description of Isurus paucus 191 0; Shann, 1911, 1923; Bigelow and Schroe­ and Alopias superciliosus with evidence of oo­ der, 1948) and Alopiidae (Alopias vulpinus, Gub­ phagy in these species. anov, 1972;A. pelagicus, Otake and Mizue, 1981). Although there has been much conjecture on METHODS the possibility of, and the nature of, oophagy in Isurus spp., few definitive observations have All specimens were collected on drift-set been published. Bass et a!. (1975) stated that swordfish longlines floating with the Florida the observations of Vaillant (1889) on the great­ Current in the upper 60-100 m between lati­ ly distended embryonic cardiac stomach con­ tude 26.30'N and 28•30'N and longitude taining yolk in Isurus oxyrinchus " . .. almost cer­ 79•30'W and 80•00'W. All captures were made tainly refers to a case of oviphagy rather than between 1400 hr and 1700 hr on a variety of to one gigantic ovum, and we can class Isurus tuna hooks baited with mackerel, Scomber scom­ with Lamna, Alopias and Odontaspis as far as em­ ber, or squid. A general description of longline bryonic nutrition is concerned." Guitart Man­ capture methodology is given by Stillwell and day (1975) illustrated a 650 mm TL I. oxyrinchus Casey (1976). embryo which has a distended abdomen greatly Both fresh and preserved reproductive or­ resembling the abdominal contour in oopha­ gans and embryos were examined and photo­ gous embryos of Lamna nasus (Shann, 1923) and graphed during and after dissection from the Odontaspis taurus (Gilmore eta!., in press) which adult. Numerical estimates of ovarian ova were have ingested large amounts of maternal yolk. made by weighing the ovary and a subsample Except for Nakamura's (1935) excellent illus­ in which the ova were counted. The weight of tration of a 43.5 em SL (96.5 em TL) embryo the known number of ova in the subsample was of the bigeye thresher, Alopias superciliosus then considered directly proportional to the (Lowe), descriptions of embryonic development number in the total weighed ovary. in this species are limited to the brief accounts All measurements of adults and embryos were of Springer (1943), Cadenat (1956), Bigelow and made while the shark was lying horizontally on Schroeder (1948) and Gruber and Compagno a flat surface. Terminology and measurements (1982). follow Basset al. (1975: Fig. 3). Standard length Present embryonic descriptions of the longfin (SL) was taken from the tip of the snout to the mako, Isurus paucus Cui tart Manday are limited center of the precaudal pit. All weights were to the single account of Guitart Manday ( 197 5). taken on a spring scale calibrated in pounds and

© 1983 by the American Society of Ichthyologists and Herpetologists 376 COPEIA, I 983, NO. 2

Fig. I. A) 97 em SL lsurus paucus embryo. Note long pectoral fins, folded 1st dorsal and damaged upper caudal lobe. B) Highly folded and vascularized inner uterine membrane at opening lO isthmus. The snout of the embryo was wedged into this portion of the uterus. C) Ventral surface of embryo showing lack of ventral pigmentation which is diagnostic in the adult. D) Opened abdominal cavity showing greatly enlarged liver extending from the transverse septum and pericardia! cavity (right) lO the cloaca (left). Note light color (actually orange) along the central portion of liver lobes. RL =right lobe; M = median lobe; LL = left lobe. converted to kg or on a scale balance calibrated Six of these were females, one of which con­ to 0.1 g. tained a single female embryo 77.0 em SL (97 Specimens were fixed in 10% formalin for a em TL; 5.2 kg) (Fig. 1). The pregnant female period of one to six months before being washed (303.5 em SL) was fortuitously caught (entan­ and preserved permanently in 70% ethanol. Ek­ gled) on a 16 km swordfish longline on 3 Dec. tachrome and Kodachrome transparencies were 1980. The embryo was found in the right uterus made of both fresh and preserved specimens. facing anteriorly with its tail protruding from the cloaca. The greatly expanded and vascular­

fSURUS PAUCUS ized left uterus indicated that a second embryo had been present but was apparently aborted The longfin mako, lsurus paucus, is a circum­ shortly before or during the process of capture. tropical pelagic species recorded from the In­ The head of the embryo was nuzzled into the dian, Pacific and western north Atlantic oceans highly convoluted and vascularized anterior (Guitart Manday, 1966; Garrick, 1967). In the portion of the uterus (where the isthmus ends, western Atlantic the species is most common off Fig. I B). Examination of the mouth, throat and the coast of Cuba, where it was first described, gut contents of the embryo revealed .08 g of and in the straits of Florida (Dodrill and Gil­ yolk on the gill arches and 28 g of yolk in the more, 1979) but may range as far north as Cape cardiac stomach. This was a relatively small Hatteras (Casey et al., 1980). quantity of yolk compared to descriptions of the From 1975 to 1980 13 Isurus paucus speci­ distended yolk-filled cardiac stomachs in Lamna mens (167.5 to 303.5 em SL) were examined. nasus and I. oxyrinchus. The right and left lobes GILMORE-SHARK EMBRYOS 377 of the liver extended back to the cloaca and TABLE I. COMPARISON OF BOD\' PROPORTIONS OF both were 300 mm in length (39% of SL). The THE EMBRYO AND PARENT IN Jsuru s paucus. central portion of the liver lobes contain ed a bright orange pigment but were otherwise the F.mbr)'O 9 Part'nf 9 typical dark brown color obse1:ved in adult spec­ Total length 97.0 em 372.8 em imens. The small amount of yolk in the digestive (both had damaged tract and the enlarged liver indicates that al­ upper caudal lobes) though nutritive material was not abundant in Fork length 86.2 336.6 the digestive tract at the time of examination, Standard length 77.0 303.5 it apparently had been but was presently stored Top of snout to: %. SL % SL in liver tissue. Ant. margin of eye 7 6 It was evident from small bits of unencapsu­ Front of mouth 6 jaw removed lated yolk present in the oviduct that maternal Nasal aperture 5 5 yolk supplies were declining and not playing a 1st gill opening 21 19 prominent role in embryonic nutrition during P, origin 26 24 this stage in pregnancy. No eggs, yolk or en­ D, origin 37 38 capsulated ova were present in the uterus. The P2 origin 54 52 ovary was not noticeably enlarged (300 X I50 Height of l st gill opening 8 8 mm, 1.6 kg) and contained approximately 5,200 Height of 5th gill opening 7 8 ova ranging in size from 3 to 5 mm. Most ova Horizontal eye diameter 2 were less than 4 mm in diameter. These obser­ Mouth width 8 jaw removed vations indicate that ovulation had ceased. P, base length 6 7 If the phases of gestation in/. paucus are anal­ P, free inner margin 5 5 ogous to those in 0. taurus (Gilmore et al., in P, anterior margin 24 23 press) then the 97 em embryo was in the ter­ D, base length 9 9 minal phase of gestation just prior to parturi­ D, free inner margin 3 2 tion. An enlarged ovary (to 8.5 kg, containing D, anterior margin 12 14 13,000 to 24,000 ova, many from 6 to I 0 mm D, height 7 II in diameter) in 0. taurus, characterizes the phase Upper caudal pit to tip in pregnancy when embryos are actively feeding of upper caudal lobe 21 22 on maternal yolk and yolk capsules. However, Lower caudal pit to tip prior to parturition, the maternal ovary and of lower caudal lobe 13 16 greatly distended yolk-filled stomach of the em­ Weight 5.2 kg 351 kg bryo decline in size (Gilmore et al., in press). Most of the body proportions of the embryo were similar to those of the adult, and would permit one to identify the embryos to species (Table 1). One of the principal diagnostic char­ ance; however, the difference between dorsal acters used to separate adult/. paucus from all and ventral caudal fin lobe lengths was similar other lsurus species is the length of the pectoral in both embryo and adult (Table 1). fins, which should be longer than the head length The embryo was black to gray dorsally, with (i.e., larger than distance from tip of the snout little or no pigment on the ventral surface from to first gill slit; Garrick, 1967). The pectoral fin the tip of the snout to the caudal fin. Small gray length was a greater percentage of SL in the blotches were present near the corners of the embryo (31% SL) than in the adult (28% SL) mouth, an area which is usually heavily pig­ presenting evidence for the taxonomic signifi­ mented in the adult. In contrast, the mother cance of this character even in identifying em­ lacked dark gray ventral pigment only between bryos (Guitart Manday, 1975). The pectoral fins the pectoral fin bases. were still longer than the head in the embryo A comparison between embryos of lsurus pau­ even though the embryonic head length is long­ cus and the sympatric species I. oxyrinchus re­ er in proportion to the body than in adults. The veals apparent differences in embryonic growth dorsal fin was proportionately smaller in the prior to parturition. Basset al. (I975) predict embryo than in adults and was folded down over the size at birth for /. oxyrinchus to be 60 to 70 the right side. The caudal fin was also folded em TL. The smallest free swimming specimen dorso-ventrally, giving a heterocercal appear- of/. oxyrinclws I have examined was 67 em TL. 378 COPEIA, 1983, NO. 2

Fig. 2. A) 32.0 em SL Alopias superciliosus embryo. B) 32.0 em SL A. superciliosus embryo within right uterus with uterine fluid and egg capsules. C) Head of 55.5 em SL A. superciliosus embryo showing well developed diagnostic groove on nape. Also note "denticle-less" smooth outer epithelial layer peeling away on gill slits and nape. D) Egg capsules from uterus (B) showing variety of ova numbers in each capsule. Ov = cluster of ova in tail membrane of a single capsule. Rye= reduced yolk capsule containing a few ova and a gelatinous albumin/mucous mixture.

Both my I. paucus embryo and that of Guitart was in Aug. 1941 when Springer (1943) de­ Manday measured over 90 em. Besides having scribed embryos from a specimen caught in the larger embryos the two gravid female/. paucus Atlantic near Salerno, Florida. This species is examined to date have contained only one em­ principally an offshore resident of the conti­ bryo per uterus while/. oxyrinchus may have up nental slope and open sea, having been record­ to five per uterus. Adult/. paucus may also reach ed to depths of 4 7 5 m (Compagno and Vergara, a relatively large size as the four largest (all 1978). females) of the 13 adults examined were 349 From April 1978 to Feb. 1981 seven bigeye em to 417 em TL, compared to 195 em to 301 threshers (155.3 to 221.0 em SL) were exam­ em TL for eight adult /. oxyrinchus also exam­ ined. Five of these specimens were females, two ined. The maximum length for I. oxyrinchus re­ of which contained embryos. corded to date is apparently 380 em (Gubanov, A 225.5 em SL female landed on 9 May 1979 1974; Applegate, 1966). contained two embryos, a 30.0 em SL (55.0 em TL), 0.27 kg female in the left uterus and a

ALOPIAS SUPERCILIOSVS 32.0 em SL (60.0 em TL, Fig. 2A, B), 0.39 kg male in the right uterus. Also in the uterine The bigeye thresher, Alopias superciliosus, is a cavity with both embryos were 18 and 35 yolk­ circumtropical pelagic species occurring in the filled egg capsules 15 to 19 mm in diameter and western Atlantic from Long Island to southern 45 to 65 mm in length; there were 8 to 60 ova Brazil (Compagno and Vergara, 1978). The first per capsule (Fig. 2D). Both the cardiac stomach capture of this species after its original descrip­ and valvular intestine of the female embryo tion in 1840 (based on specimens from Madeira) contained yolk. Only the mouth and throat of GILMORE-SHARK EMBRYOS 379 the male were examined and found to contain ered with a smooth epithelium covering the well yolk. The liver of the female embryo was yellow­ developed dermal denticles of the second epi­ orange in color and relatively small, measuring thelial layer. This pigmented outer epithelial a maximum of 17% of the SL (right lobe). The layer peeled easily from the body after preser­ teeth were well developed though not erect. vation (Fig. 2C). This outer layer probably pro­ They were folded in three rows and were not tects the highly vascularized uterine lining from sheathed below a membrane. In older embryos the sharp denticles of large active embryos and (53-55.5 em SL) described below, the teeth were may also aid in allowing the embryo to make a sheathed below a membrane. The body was flac­ smooth exit during parturition. The smooth cid and brown, countershading to cream. The outer epithelial layer has not been described for embryos were facing the highly vascularized and other alopiid embryos and may be a character folded opening to the oviduct isthmus and had only found in A. superciliosus (Nakamura, 1935; apparently fed on egg capsules entering the 'Gubanov, 1972; Hixon, 1979). The juvenile A. uterus from the oviduct. Both embryos had a superciliosus examined had erect spinous denti­ yolk stalk attachment scar on the ventrum for­ cles, some of which were enlarged. Spinous den­ ward of the pectoral fins. The ovary was en­ tides were well developed on all the alopiid em­ larged, weighing 2.27 kg and measuring 33.0 X bryos examined, therefore apparently 15.5 X 7.5 em, and contained approximately necessitating the presence of a protective smooth 52,000 eggs varying in diameter from 3.9 to 5.3 outer epithelium. mm. The oviduct measured 540 mm from the All alopiid embryos had body to tail lengths nidamental gland to the uterus. and other proportions resembling those of adult On 18 June 1979 another pregnant female bigeye threshers (Table 2). Head proportions ( 180.0 em SL) was captured. Each uterus con­ were higher in percent SL in embryos and the tained an embryo, a 53.0 em SL (105.5 em TL), eye was proportionately larger in the smaller 2.95 kg male and a 55.5 em SL (104.5 em TL, embryos. Except for the smaller pectoral fin in Fig. 2C), 2.50 kg female. The cardiac stomach the embryo, all other relative fin measurements and valvular intestine of both embryos con­ were similar to the adult. The lateral head tained yolk. The liver in the male embryo was groove on the nape, diagnostic for this species, tan-orange in color, and with a maximum length was present on all embryos. Considering the of 22% SL (right lobe), was proportionately prominence of this latter character in both the larger than the liver of the 9 May embryos. The adults and the embryos examined, it is surpris­ body was dark gray (rather than brown), coun­ ing that mention or illustration of this character tershading to white. The color pattern resem­ was omitted by Bigelow and Schroeder (1948) bled that of most of the dead adults examined. in their description of a 129.6 em TL Cuban Besides the dark gray color pattern, these em­ male. Other diagnostic characters presented by bryos differed from the 9 May specimens in that Bigelow and Schroeder ( 1948) fit Alopias super­ the body muscles were firm, not flaccid. Basset ciliosus, indicating that they were in fact describ­ al. (1975) stated that living 0. taurus embryos ing this species. A detailed description of the dissected from a dead female changed from flac­ lateral head grooves as a specific character in cid brown to firm gray as muscle tonus increased A. superciliosus is presented by Gruber and Com­ with swimming (after release in aquaria) and pagno ( 1982). hypothesized that the development of muscle tonus must take place before birth under nat­ SUMMARY AND DISCUSSION ural conditions. The 53 and 55.5 em SL em­ bryos could have changed color and developed Examination of a 97 em TL lsurus paucus muscle tonus in preparation for an ensuing par­ embryo documented the occurrence of ooph­ turition. agy in this species as remnants of yolk were Eight egg capsules were found in the oviducts found in the anterior digestive tract and mouth. but none in the uteri. The turgid dark brown The embryo was apparently near term as no capsules were filled with yolk and measured encapsulated ova were found in the oviduct, 5.7 X 2.7 em. The ovary was greatly enlarged, indicating that ovulation was declining or had weighing 7.5 kg, measuring 41 X 23 X 14 em ceased. The embryo had apparently consumed and containing 38,250 ova varying in diameter all external supplies of yolk as no encapsulated from 6.9 to 9.2 mm. ova or empty capsules were found free within All of the bigeye thresher embryos were cov- the uterus. The parental ovary was reduced in 380 COPEIA, I 983, NO. 2

TABLE2. COMPARISON OF BODY PROPORTIONS BF.TWF.EN ADULT AND EMBRYONIC A/opias suprrci/iosus EXPRF.SSF.D AS A PERCENTAGE OF THE DISTANCE FROM THE SNOUT TO THE DoRSAL PRECAUDAL NoTCH (SL).

9 May 18 June 9 May 18 June specimen spec1men speCimens speC!mellS

SL (em) 225.5 180.0 32.0 30.0 53.0 55.5 FL (em) 237.0 35.0 33.0 59.5 62.5 TL (em) 395.0 35.03 60.0 55.0 105.5 104.5 Mean from two adult Percent SL females

Total length 185 188 183 199 188 Snout to: Eye 7 10 8 14 II Mouth 8 II II 14 12 Nose 6 8 7 10 8 I st gill opening 24 32 30 34 29 P, origin 27 37 36 39 31 D, origin 61 63 62 67 61 P, origin 72 73 72 74 65 Height of: 1st gill opening 4 3 3 5 5 5th gill opening 5 4 4 3 4 Horizontal eye diameter 3 9 9 5 5 Vertical eye diameter 4 8 7 8 8 D, base 12 10 10 12 II D, height 13 10 10 12 II D, anterior margin 16 16 14 16 15 P, base 13 9 9 12 I 0 P, anterior margin 33 38 33 39 35 P, base 14 10 10 13 II P, anterior margin 16 15 15 17 14 C. upper lobe 85 88 79 99 88 C. lower lohe 13 12 II 14 12 Mouth width 8 II 10 10 8

size, further indicating that this embryo had just egg capsules examined varied in size, shape and passed through the period of maximum oo­ number of ova encapsulated as had been ob­ phagy and was nearing parturition. served in other oophagous species (Pseudoca r­ I. paucus embryos in late stages of develop­ charias kamoharai, Fujita, I 981; Odontaspis tau r­ ment can be identified to species using the same us, Gilmore et al., in press). As in Isurus paucus, diagnostic morphological characters that are bigeye thresher embryos attain a large size (i.e., definitive for adults. They also appear to be to 105.5 em TL) prior to parturition and exhibit further differentiated from the congeneric and many of the diagnostic anatomical characters sympatric species, I. oxyrinchus, in reaching a for the species. A smooth protective integument larger size at birth (i.e., I. paucus to 97 em TL; was observed to cover the dermal denticles in I. oxyrinchus to 70 em TL). A. superciliosus, apparently preventing damage A. superciliosus embryos examined had eaten to the uterine membrane as this species has ex­ yolk from yolk capsules also present in utero. ceptionally sharp and enlarged denticles (Big­ The parental ovaries were enlarged, weighing elow and Schroeder, 1948; Basset al., 1975). from 2.27 to 7.50 kg, and egg capsules filled The rarity of I. paucus in biological collections with ova were present in the uterus and upper has not permitted an adequate study of its life portions of the oviduct, indicating that the em­ history. The biology of A. superciliosus has only bryos were in an active oophagous stage. The recently been treated by Gruber and Compagno GILMORE-SHARK EMBRYOS 381

( 1982). Prior to this treatment there was no CASEY, j., H. W. PRATT AND C. STILLWELL. 1980. definitive evidence of oophagy in these species, The shark tagger I 980 summary. Newsletter, Co­ although it was expected and assumed (Com­ operative Shark Tagging Program, NOAA, Natl. pagno, 1977; Wourms, 1981). These observa­ Mar. Fish. Serv., Northeast Fish. Center, Narra­ gansett, Rhode Island. tions further verify the apparent universal em­ COMPAGNO, L. J. V. 1977. Phyletic relationships of bryonic nutrition through oophagy in lamnid living sharks and rays. Amer. Zool. 17:303-322. and alopiid sharks. Although adelphophagy has ---, AND R. VERGARA R. 1978. Sharks. FAO been recorded only in the odontaspid sharks species identification sheets for fishery purposes. (Wourms, 1977, 1981) it is likely to occur in Western Central Atlantic (fishing area 31). Vol. 5. lamnid and alopiid sharks also. I have observed W. Fischer (ed.). FAO Fish. Dept., Rome. blastodiscs on many encapsulated uterine ova DoDRILL, J. W., AND R. G. GILMORE. 1979. First in lsurus oxyrinchus, yet typically only three to North American continental record of the Iongtin five embryos survive to parturition in this species mako (Isurus paucus Guitart Manday). Fla. Sci . 42: (Bass et al., 1975). As the isurid and alopiid 52-58. FUJITA , K. 1981. Oviphagous embryos of the Pseu­ sharks are large, active pelagic predators, a re­ docarchariid shark, Pseudocarcharias kamoharai, from productive scenario in which a few (i.e., <5 per the central Pacific. Jap. J. Ichthy. 28:37-44. uterus) large embryos are produced may pre­ GARRICK, J . A. F. 1967. Revision of sharks of genus sent the greatest survival benefit. Chances of Isurus with description of a new species (Galeoidea, survival should be increased in a newborn that Lamnidae). Proc. U.W. Natl. Mus. 118:663-690. is large and has abundant hepatic nutritive sup­ GILMORE, R. G.,J. W. DoDRILL AND P. A. LINLEY. In plies. The pup has adequate size and energy not press. Embryonic development of the sand tiger only to pursue food actively, but also to escape shark, Odontaspis taurus Rafinesque. Fish. Bull. predators. GRUBER, S. H., AND L.J. V. CoMPAGNO. 1982. Taxo­ nomic status and biology of the bigeye thresher, Alopias superciliosus. Ibid. 79:6I7 -640. ACKNOWLEDGMENTS GuBANOV, YE. P. 1972. On the biology of the thresh­ er shark Alopias vulpinus (Bonnaterre) in the north­ Various fishermen helped immeasurably by west Indian Ocean. J. lchthyol. 12:591-600. bringing their valuable catch of longfin makos ---. 1974. Thecaptureofagiantspeciesofmako and bigeye threshers to shore for examination. shark (lsurus glaucus) in the Indian Ocean. Ibid. 14: 589-591. Particularly helpful were Wayne Mullinix, GuiTART MANDAY, D. 1966. Nueva nombre para una George Giannikopoulos, Fred Thibuult and especia de tiburon del genus Isurus (Elasmobranch: Raymond Hasselgrove. Jon Dodrill, Stewart lsuridae) de aguas Cubanas. Poeyana, ser. A: 1-9. Springer, Robert jones and Patricia Linley made ---. 1975. Las pesquerias pelagico-oceanicas de helpful comments on the manuscript. This con­ corto radio de accion en Ia region noroccidental de stitutes contribution 274 from the Harbor Cuba. Oceanogr. In st., Acad. of Sci., Havana, Cuba. Branch Foundation, Inc. Seria Oceanologica: 1-41. HIXON , M.A. 1979. Term fetuses from a large com­ mon thresher shark, Alopias vulpinus. Calif. Fish LITERATURE CITED Game 65:191-192. JosEPH, D. C. 1954. A record-sized thresher from APPLEGATE, S. P. 1966. A possible record-size bonito southern California. Ibid. 40:433-435. shark, Isurus oxyrinchus Rafinesque from southern LOHBERG ER, J. 1910. Uberzwei riesige embryonen California waters. Calif. Fish Game 52:204-207. von Lamna. (Beitrage zur Naturgeschichte Osta­ BAss, A.J.,J. D. D'AuBREYAND N. K1sTNASAMY. 1975. siens) Abh. Bayer Akad. Wiss. 4 (Suppl. 2): 1-45. Sharks of the east coast of southern Africa. IV. The NAKAMURA, H. 1935. On the two species of the families Odontaspididae, Scapanorhynchidae, Isu­ thresher shark from Formosan waters. Mem. Fac. ridae, Cetorhinidae, Alopiidae, Orectolobidae, and Sci. Agric. Taihoku Imp. Univ. 14:1-6. Rhiniodontidae. Oceanogr. Res. Inst. , Durban, 0TAKE, T., AND K. MIZUE. 1981. Direct evidence for South Africa. Invest. Rep. 39. oophagy in thresher shark, Alopias pelagicus. Jap. J. BIGELOW, H. B., AND W. C. SCHROEDER. 1948. Fishes 1chthy. 28:171-172. of the western North Atlantic, 1ancelets, cyclo­ SHANN, E. W. 1911. A description of the advanced stomes, and sharks. Sears Found. Mar. Res., Mem. embryonic stage of Lamna cornubica . Fish. Bd. Scot­ No. 1(1). land Ann. Rept. 28 :73-79. CADENAT, J. 1956. Notes d'ichthyologie ouest-afri­ ---. 1923. The embryonic development of the caine. XV. Sur un requin-renard nouveau pour Ia porbeagle shark, Lamna cornubica. Proc. Zool. Soc. faune d' Afrique Occidentale Francaise Alopias su­ (Lond.) 11:161-171. prrciliosus (Lowe) 1840? Bull. lnst. Fr. Afr. Noire, SPRINGER , S. 1943. A second species of thresher shark 18:1257-1266. from Florida. Copeia 1943:54-55. 382 COPEIA, I 983, NO. 2

1948. Oviphagous embryos of the sand WouRMs,J. P. 1977. Reproduction and development shark, Carcharias taums. Copeia 1948:153-157. in chondrichthyan fishes. A mer. Zoo!. 17:379-4 10. STILLWELL, C. E., AND J. G. CASEY. 1976. Observa­ ---. 1981 . Viviparity: the maternal-fetal rela­ tions on the bigeye thresher shark Alopias superci­ tionship in fishes. Ibid. 21:473-515. liosus, in the western North Atlantic. Fish. Bull. 74: 221-225. HARBOR BRANCH .FouNDATION, [Nc., RR 1, Box VAILLANT, L. L. 1889. Note sur un foetus gigan­ I 96, FoRT PIERCE, FLORIDA 33450. Accepted tesque d'Oxyrhina spallanwni Bonap. Bull. Soc. Phi­ 17 May I 982. lo rn . Paris (8) I :38-39.