SMITH and MERRINER: REPRODUCTIVE BIOLOGY OF COWNOSE RAY 



would be born the following summer when the adults 

 return to Chesapeake Bay, a gestation period of 

 11-12 mo beginning in July or August and ending 

 in June or July. 



The relatively large size of cownose ray embryos 

 in late September and early October suggests the 

 possibility of two 5-6 mo gestation periods. Partu- 

 rition might occur on the cownose rays' wintering 

 grounds followed by the gestation of another brood 

 of embryos destined for birth the following summer. 

 This hypothesis is not unprecedented, since the 

 presence of well-developed young in the spiny 

 butterfly ray, Gymnura altavela, during May in 

 Delaware Bay and during February off the coast of 

 North Carolina (27 fathoms) led Daiber and Booth 

 (1960) to propose two 5-6 mo gestation periods per 

 year for this species. Precise definition of the cow- 

 nose ray gestation cycle will require collecting 

 gravid female rays on their wintering grounds. 



Embryonic Development and Nutrition 



The shell capsule of the cownose ray, which we 

 observed twice in utero, is of a greenish amber, thin 

 diaphanous material, and is about 10 cm long. One 

 capsule held a single ovum, while the capsule from 

 a second female contained three ova. Ova are yellow, 

 extremely flaccid, and about 3-4 cm in diameter. 



The embryos in late summer and fall possess yolk 

 stalks and yolk sacs, although these often become 

 detached during collection (Fig. 3). The smallest em- 

 bryos we collected are about 20 mm wide, batoid in 

 appearance, and unencapsulated. Numerous exter- 

 nal branchial filaments (ca. 15-30 mm long), which 

 emerge from the gill slits, are highly conspicuous 

 on small embryos (18-75 mm). These filaments are 

 absent in embryos larger than 89 mm. 



Three-quarter term embryos are upright in the 

 uterus (ventral surface of the embryo on the ven- 

 tral wall of the uterus) with the rostrum pointed for- 

 ward. The pectoral fins are folded dorsally. The tail 

 and heavily sheathed spine are bent forward along 

 the dorsum of the disc. The yolk sac and stalk are 

 almost completely absorbed; only about 3 mm of the 

 umbilicus protrudes from the abdomen. 



Full-term embryos are similarly oriented. How- 

 ever, the umbilicus is completely absorbed, leaving 

 only a small scar that is evident on free-swimming 

 young. Pigmentation is that of the adults, i.e., 

 chocolate-brown dorsally, white ventrally, and black 

 caudally. Several tooth plates were discovered in the 

 left uterus from which a full-term young was re- 

 moved, confirming Bigelow and Schroeders' (1953) 

 report that tooth replacement begins in utero. 



During the early stages of gestation the uterus 

 is rigid and thick-walled, but it gradually expands 

 to accommodate the developing young. Just prior 

 to parturition, it is extremely distended (ca. 15 cm 

 at its greatest breadth), thin-walled, and flaccid. 



Myliobatoids overcome spatial restrictions in utero 

 by rolling the pectoral fins dorsally or ventrally, 

 along the anterioposterior axis (Gudger 1951), and 

 some studies report that larger than average 

 females carry more and larger offspring (e.g., Babel 

 1967). Although we observed multiple encapsulated 

 ova in cownose rays, and others have cited the oc- 

 currence of multiple embryos in utero (Smith 1907; 

 Gudger 1910; Bearden 1965), we never found more 

 than one embryo per gravid female. Setna and 

 Sarangdhar (1949) and James (1962, 1970) made 

 similar observations for the Javanese cownose ray, 

 R. javanica, from the Indian Ocean. Our data for 

 term embryos (n = 4) are insufficient to corrolate 

 embryo size with parent's size; however, we suspect 

 that in general only one cownose ray embryo is car- 

 ried to term. 



Embryonic nutrition is from yolk and histotrophe. 

 Yolk of the late summer and fall embryos (n = 33) 

 gradually diminishes between August and October 

 (Fig. 4), and most yolk reserves are probably util- 

 ized when embryos are about 20 cm. Histotrophe, 

 a viscid, yellowish secretion of the uterus (as also 

 cited by Schwartz 1967), also nourishes the embryos. 

 The amount of histotrophe, although not quantified, 

 increases considerably as gestation progresses. Tro- 

 phonemata, the uterine villi that produce histo- 

 trophe, are deep red, flattened in cross section and 

 spatulate distally. They attain their greatest length 

 (ca. 2-3 cm) in females with near full-term embryos. 

 The trophonemata occasionally invade the gill slits. 



In summarizing chondrichthyan, fetal-maternal 

 relationships, Wourms (1977) noted that the effi- 

 ciency of placental analogues, the villiform tropho- 

 nemata, far surpasses that of the yolk-sac placenta 

 exhibited by some carcharhinids. In cownose ray em- 

 bryos, yolk apparently provides initial nutritional re- 

 quirements. Embryos may augment yolk supplies 

 during the first month of gestation by absorbing 

 histotrophe via the external branchial filaments, as 

 was suggested for Urolophus halleri by Babel 

 (1967). After October, histotrophe supplies nourish- 

 ment for the remainder of the gestation period, 

 probably engulfed via the mouth, spiracles, and gill 

 slits. 



Viviparity and the use of nursery areas that are 

 relatively free of predators, e.g., Chesapeake Bay, 

 no doubt protect young cownose rays. Large car- 

 charhinids, of which batoids are purported to be a 



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