Francis and Stevens: Reproduction, embryonic development, and growth of Lamna nasus 



59 



of a female in the South Atlantic in March and stated: 

 "The shark had recently spawned, to judge by external 

 characters (an inflamed area of the body around the 

 anus) and the state of the ovaries." He did not elaborate 

 further on the ovaries, so it is difficult to assess his re- 

 port. If the female was postpartum, the timing is one 

 month earlier than our suggested parturition period for 

 Southern Hemisphere porbeagles. Another possibility 

 is that the inflammation around the cloaca may have 

 been the result of recent mating. 



If the gestation and rest periods combined last one 

 year, and females reproduce every year, annual fecun- 

 dity is 3.85 young per female. If there is a resting pe- 

 riod of just over one year between pregnancies, an- 

 nual fecundity would be half that amount. It is there- 

 fore important to determine whether Aasen's (1963) 

 suggestion of a one-year cycle is valid for both hemi- 

 spheres. The gestation period in shortfin makos is 

 thought to be 18 months, with a reproductive cycle of 

 three years (Mollet et al.^M. Interestingly, the greater 

 average fecundity of makos would result in an annual 

 fecundity of about four per female (Mollet et al.^M, 

 which is similar to the reproductive output of porbea- 

 gles assuming a one-year cycle. 



For Southern Hemisphere porbeagles, the length at 

 birth was estimated to be 58-67 cm (68-79 cm TL), 

 based on the lengths of the largest embryos and the 

 shortest postnatal juveniles. In the North Atlantic, 

 the largest reported embryos were 60-64 cm (Pen- 

 nant, in Shann, 1911) and 65 cm (Gauld, 1989). Big- 

 elow and Schroeder (1948) reported a 55.7-cm speci- 

 men (66.0 cm TL; USNM 47528), but it was an em- 

 bryo rather than a postnatal juvenile (Williams^'^). 

 The embryo would have been about 58 cm before pres- 

 ervation. Postnatal porbeagles of 66 and 70 cm were 

 reported by Imms and Day respectively (in Shann, 

 1911). These observations indicate that porbeagles are 

 bom at about the same length in both hemispheres. 



Embryonic development 



We assembled a comprehensive series of porbeagle 

 embryos ranging from early gestation (9.6 cm long) 

 to full-term, enabling us to describe the main mor- 

 phological changes that occur during gestation. Pre- 

 vious studies that described and illustrated embryos 

 were based on only a few embryos, most of which 

 were midterm (Swenander, 1906, 1907; Shann, 1911; 

 Nordgard, 1926; Bigelow and Schroeder, 1948; Tem- 

 pleman, 1963). The following review of embryonic de- 

 velopment is derived from our observations, supple- 

 mented by literature reports. 



13 Williams, J. T. 1997. National Museum of Natural History. 

 Washington DC 20560-0159. Personal commun. 



Embryos 4.3^.7 cm long have external gills and 

 well-developed branchial regions (Swenander, 1907). 

 They have nearly absorbed their yolk sacs and have a 

 large spiral valve, but there is no yolk in the digestive 

 system. Swenander ( 1907) stated that "these embryos 

 are too small to be able to swallow entire egg capsules 

 and their teeth are not sufficiently developed to tear 

 open the egg capsules." They have not begun to feed 

 at this stage, despite the large number of egg capsules 

 present in the uteri, but precocial teeth have already 

 formed. At 10 cm, the lower jaw contains two rela- 

 tively massive fangs (Fig. 9A) that appear capable of 

 tearing open egg capsules. The upper teeth are much 

 less developed and there is only one functional tooth 

 on each side of each jaw. Lower jaw teeth also de- 

 velop earlier than upper jaw teeth in sandtiger sharks 

 (Hamlett, 1983). The abdomen is swollen and the em- 

 bryos have presumably begun feeding (the stomachs 

 were not dissected). Large numbers of egg capsules 

 are present in the uteri. The external gills have been 

 resorbed. By 15 cm, the abdomen is distended, and the 

 head and branchial region are gelatinous and grossly 

 enlarged (Bigelow and Schroeder, 1948). 



Between 20 and 42 cm, development is dominated 

 by the consumption of large numbers of egg capsules, 

 leading to a great increase in the relative size and dis- 

 tension of the yolk stomach (Swenander, 1907; Shann, 

 1911, 1923; Bigelow and Schroeder, 1948; Templeman, 

 1963; Moss''; Fig. 8). Large fangs are present in both 

 jaws (Swenander, 1907; Templeman, 1963; Moss'^; Fig. 

 9) and are used to open the egg capsules before re- 

 moval of the contents; how this is accomplished is un- 

 known. At 30-42 cm, yolk accounts for up to 81% of 

 total weight (Fig. 11; Templeman, 1963). The stomach 

 yolk in midterm embryos of shortfin makos peaks at 

 about 60-70% of total weight (Mollet et al." ). Relative 

 and absolute amounts of yolk in porbeagles and other 

 oophagous sharks decline during the rest of gestation 

 (Fig. 11; Molletetal.il). 



Porbeagle embryos shed their fangs at about 34—38 

 cm. Embiyonic fangs (the "emb" teeth of Gilmore, 1993) 

 have also been reported in salmon sharks, common and 

 bigeye thresher sharks (Alopias vulpinus and A. su- 

 perciliosus), shortfin makos and sandtiger sharks (Loh- 

 berger, 1910; Bass et al., 1975; Gruber and Compagno, 

 1981; Gilmore et al., 1983; Hamlett, 1983; Gilmore, 

 1993; Chen et al., 1997). They probably occur in all 

 oophagous species, and in at least some species, they 

 are shed part-way through gestation. In bigeye thresher 

 sharks, fangs appear at about 11 cm TL and disappear 

 at about 60 cm TL (Chen et al., 1997). In sandtiger 

 sharks, they appear at 4-5 cm TL, and are lost some 

 time before birth (Gilmore et al., 1983; Hamlett, 1983). 



We suspect that female porbeagles cease ovulation 

 at about the time the embryonic fangs are lost, as 



