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FAU Institutional Repository This 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).
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