Proceedings ofthe United StatesNational MuseumSMITHSONIAN INSTITUTION ? WASHINGTON, D.C.
Volume 115 1964 Number 3476ADDITIONAL INFORMATION ON THE MORPHOLOGYOF AN EMBRYO WHALE SHARK
By J. A. F. Garrick^
An embryo whale shark, Rhincodon typus Smith, kindly loanedby the Marine Laboratory, Texas Game and Fish Commission, Rock-port, shows several notable differences in proportional dimensionsand other features as compared with accounts of adult specimens.To describe these differences is the purpose of this paper.The embryo, 350 mm. in total length, is one that has been removedfrom an egg-case trawled from 31 fathoms in the Gulf of Mexicoabout 130 miles south of Port Isabel, Texas, on June 29, 1953. Thisspecimen, believed to be the only embryo whale shark available,has been reported previously by Breuer (1954), Baughman (1955),and Reid (1957), who published dimensions of it and discussed itstrunk ridges and oronasal groove. Reid also presented a figure ofthe underside of the head, while Breuer's and Baughman's accountseach included a photograph of the specimen and its egg-case. Tosupplement these abeady published figures, I submit here five addi-tional illustrations of the embryo whale shai'k and its dermal denticles.For these drawings I am greatly indebted to the skill of Mrs. FanuyPhiUips.
' Division of Fishes, U.S. National Museum. This research was supported by contracts between theSmithsonian Institution and the Atomic Energy Commission (A EC (30-1) 2409) and the Office of NavalResearch (NONR 1354 (09)).
2 PROCEEDINGS OF THE NATIONAL MUSEUM vol. 115Proportional differences.?In the following account the fea-tures of the embryo whale shark are compared for the most partwith those of the adult (total length 17' 3") from Acapulco, Mexico,figm-ed in Bigelow and Schroeder (1948). As dimensions of boththese specimens are already available in their respective accounts,there is no need to reproduce such measiu-ements here. Instead,I shall give, in general terms, the major differences between theembryo and adult, followed in each case by a figm-e in parentheseswhich is the proportional difference expressed as a percentage of totallength.The differences are: the adult is slightly broader headed (0.5), longerheaded (1.4), and noticeably shorter tailed (6.3); the adidt eye is strik-ingly smaller (0.9), but the gUl-openings are longer (0.3 to 2.2); the firstdorsal (2.6), second dorsal (8.4), anal (7.8), and pelvic fins (3.2)are fm-ther rearward in the adult; the first dorsal fin is proportionatelyhigher (1.2), but its base is shorter (0.9) in the adult (however, thereverse is the case for both height and base length?about 2.0 and 0.3respectivel}^?in the second dorsal and anal fins); the distance betweenthe fu'st and second dorsal fins and between the anal fin and subcaudalorigin are longer in the adult (4.8 and 3.4 respectively); the pectoralfin of the adult has a much longer distal margin (5.5) than that of theembryo, though the anterior margins are comparable; the lengths ofthe upper and lower lobes of the caudal fin are considerably shorter(7.3 and 4.2 respectively) in the adult than in the embryo.The above differences are indicative of the growth change whichthe whale shark undergoes. Understanding such growth change isimportant in studying sharks because of the frequent need to rely onproportional dimensions to distinguish species. The pattern of growthchange is by no means identical in aU sharks, but there do appear tobe conmion featm-es (Beebe and Tee-Van, 1941, p. 107; Maschlanka,1955, p. 12; S. Springer, 1960, p. 9; Garrick, 1960, p. 546), such asaccelerated growth in the trunk region, as compared to the head andtail, which thus proportionately decrease with increasing total length;a tendency for the pectoral fin to increase its relative length or atleast remain stable (though Carcharhinus longimanus (Poey) showsa relative shortening of pectoral fin from juvenile to adult, as notedby S. Springer, 1960, p. 9); a broadening of the head region; and anoticeable decrease in eye diameter. Dorsal fin heights tend toincrease relatively in the galeoid sharks (but C. longimanus is againan exception), while in the squaloid sharks the reverse generallyholds true (Garrick, 1960, p. 548).The indicated growth change of the embryo whale shark fits theabove pattern reasonably well except that the head length in theembryo is relatively shorter than that of the adult. This may be
EMBRYO WHALE SHARK?GARRICK 3
only ail apparent difference for the following reason. The dorsal lobeof the caudal fin of the embryo is raised only slightly from thehorizontal axis of the body; hence, the posterior margin between thedorsal and ventral lobes is deeply notched, the angle being less than90?, In the adult the caudal fin is lunate, the dorsal lobe being raisedsteeply from the horizontal axis, with the result that the posteriormargin is only slightly concave. It follows that the change leadingfrom the slightly raised dorsal lobe in the embryo to the steeplyraised lobe in the adult woidd yield relative total lengths which arenot strictly comparable, and thus this difference woidd provide biasin proportional lengths of structures, such as head length, if calculatedin terms of the total length. Accordingly, one would expect the headlength of the embryo to have a lower relative value in terms of totallength than is the case for the adult. Better comparison is affordedby examining the head length in terms of the length to the uppercaudal origin?this shows the relative head length in embryo andadidt to be the same, which is nearer to the actual situation in mostother sharks.The need for caution in extrapolating proportional dimensions ofsmall specimens is demonstrated by the different growth rates oper-ating on the first dorsal fin of the embryo as compared with the seconddorsal and anal. Dimensions of the first dorsal fin in the embryoand in the adult indicate that the rate of vertical growth is proportion-ately faster than that of horizontal, whereas in the second dorsaland anal fins the horizontal growth is faster. A similar situationhas been described for Etmoptertis baxteri Garrick (Garrick, 1960,p. 548) and it may be relatively common. The lengths of the freerear tips of the dorsal and anal fins compared with theh bases alsoshow considerable change with growth. In the embryo, these freetips are relatively short (about 4.0 in base in the first dorsal fin) butin the adidt they are much longer (about 1.4 in base in the first dorsal).Another change affecting the comparison of all fins is the usualtendency for fin tips to become relatively pointed in the adidt, whereasin the embryo they are more rounded or blunt tipped (V. G. Springer,1961, p. 480, gives an example of this in Mustelus norrisi Springer).The tip of the dorsal lobe of the caudal fin in the embryo is distinctlynotched, presumably representing the subterminal notch, which isnot evident in the adult.Dermal ridges.?As noted by Reid (1957, p. 158), the embryowhale shark has a longitudinal dermal ridge originating on each sideof the head and dividing, above the end of the pectoral fin, into tworidges which continue posteriorly. Reid identified this ridge as onecorresponding to an upper divided ridge in the adult. Tiie adulthas, in addition, a lower ridge which extends the whole length of its
4 PROCEEDINGS OF THE NATIONAL MUSEUM vol. iisbody and forms a keel on the peduncle and anterior part of the caudalfin. I interpret the lower half of the divided ridge in the embryo tobe the same as the lowermost ridge in the adult, since posteriorlythe lower ridge forms the keel on the peduncle and caudal fin.This means that, at a later date, a third ridge must appear above thelower one in the embryo. Similar longitudinal ridges occur in somemembers of the family Orectolobidae. The embryo also has a mid-dorsal ridge which extends from the level of the first gill-opening tothe origin of the first dorsal fin and possibly is present between thefirst and second dorsal fins. Adults have been described with andwithout a middorsal ridge.Precaudal pits.?The embryo has a prominent upper precaudal pit,with a notably wide, transverse front margin. There is also a smallbut distinct lower precaudal pit. Adults are described as having theupper pit but lacking the lower.Nostrils.?Reid (1957, p. 158) reported that each nostril in the em-bryo is connected to the mouth by a distinct furrow?a character fre-quently used to support the view that the whale shark is closely relatedto, or belongs in, the family Orectolobidae.On the basis of an adult specimen, Barnard (1935, p. 649) disputedthis view. Without wishing to enter the controversy, I confirm Reid'sdescription that, in the embryo, there is no doubt that the nostril isjoined to the mouth by a naked or nearly naked furrow (pi. 4). How-ever, in view of the close proximity of the nostril to the mouth, I won-der if any significance can be placed upon this connection. Also, inpassing, I would mention that, in the embryo, the distance (in percent-age of total length) from snout tip to outer nostril (0.6) is about halfthat of snout tip to mouth (1.0). Bigelow and Schroeder (1948, p.189) give the reverse of these figures for the adult they describe.Dermal denticles.?The dermal denticles of the embryo (pi. 3)closely resemble those of the adult in having ovoid blades, each Aviththree posterior marginal teeth and a strong median longitudinal keel.Some denticles from the lower longitudinal dermal trunk ridge, how-ever, are distinctly larger and are arranged in longitudinal pairs, withthe anterior denticle overlapping the one posterior to it. These pairsare clearly visible not only because of their larger size, but also becauseof their darker pigmentation. The posterior denticle of each pair issimilar in shape to the surrounding body denticles, but usually it has abroader topped longitudinal ridge. The anterior denticle is of thesame size, but it is more nearly oval in shape, with only a median pos-terior tooth; its longitudinal ridge is broadly expanded and roundtopped, and usually it bears several minor ridges which convergeposteriorly to form a single ridge.
ROC. U.S. NAT. MUS . VOL. 115 GARRICK?PLATE 1
(J
Q<
PROC. U.S. NAT. MUS . VOL. 115 GARRICK?PLATE 2/
Rhincodo7i typus, enihij-o: \ cntral and dorsal \icus (note veilk sac in upper figure).
PROC. U.S. NAT. MUS . VOL. 115 GARRICK?PLATE 3
Rhincodon lypus, embryo: jL-inial denticles from in front of, and a little below, first dorsalfin. The two pairs of enlarged denticles, overlapping lengthwise (left center and upperright), are on the lower dermal ridge.
PROC. US, NAT. MUS., VOL. 115 GARRICK -PLATE 4
Rhincodon typus, cmbino: left nostril with nasal flap reflected to show naked furrow leadingfrom nostril to month.
EMBRYO WHALE SHARK?GARRICK 5
I do not know if similar pairs of enlarged denticles occur on the longi-tudinal dermal ridges of adults. However, Ford (1921, p. 493) de-scribed the first denticles to erupt in Scyliorhinus canicula, S. stellaris,and Galeus melanostomus as being conspicuously larger than the nor-mal body denticles and "symmetrically arranged in a sequence oftransverse pairs forming two longitudinal rows, one on either side ofthe midline in a dorsolateral position." At a later stage, these largerdenticles "lose their individuality eventually owing to the presence ofequally large and similar scales which have grown up around them"(p. 494).Teeth.?In the embryo, the teeth are for the most part still coveredby membrane, but those that are visible show little difference from theteeth of adults.GiLL-RAKERS.?The plankton-sieving apparatus of the adult whaleshark consists of transverse cartilaginous bars (representing gill-rakers)which join one gill-arch to the next; these transverse bars are furtherconnected, one to the other, by a secondary grid of slenderer crossmembers. The entire structure is covered on its internal (pharyngeal)surface by a fine, spongelike lattice or veU derived from dermal den-ticles. This structure forms the sieving apparatus, with interstices1 to 3 mm. in diameter.In the embryo the sieve is still in a very early stage of development,comprising only the gill-raker elements. These project forward fromeach arch to the next, but their tips are still free. On the first archthere are about 26 rakers on the upper limb and 34 on the lower. Therakers are comparatively stout rods, closely arranged, with virtuallyno space between them. Each raker shows faint indications of beingbipinnate, having very short processes developing along the sides.These processes are presumably the rudiments of the secondary gridmembers. There is as yet no obvious sign of the spongy tissue whichwill later line their inner surface.Reid (1957, p. 157) suggests that the relatively advanced stage ofdevelopment of the embryo whale shark and the extent to which itsexternal yolk sac has been absorbed are indications that it is approach-ing the size at which it would hatch. This is probably correct.On the other hand, the abdomen is filled almost completely with yolk,forming an oval mass about 80 mm. long, 50 mm. wide, and 40 mm.deep. This yolk supply seemingly would allow sufficient reserve tocomplete development of the pharyngeal sieve either before or afterhatching. Only further specimens will establish whether the juvenilewhale shark feeds from the beginning in the same manner as theadults.Color and pattern.?The color of the embryo when firstremoved from the egg-case was "bluish grey with white spots, the
6 PROCEEDINGS OF THE NATIONAL MUSEUM vol. us
undersurface white" (Breuer, 1954, p. 29). After preservation, theembryo is brownish rather than bluish grey, but with the dermalridges dusky. Adults have been described as being variously darkgrey to reddish or greenish brown above and white or yellow below.The color pattern of small spots and narrow transverse bars on theembryo (pis. 1-2) is remarkably similar to that of adults.Vertebrae.?Radiographs of the embryo whale shark showvertebral centra very clearly in the body region and the anteriorfour-fifths of the tail. The centra are widely spaced, presumablyfrom incomplete calcification. In the body region anterior to the levelof the origin of the upper caudal lobe, there are 81 vertebrae, whileposteriorly on the caudal axis there are 72 countable vertebrae.The total number of caudal vertebrae is probably much higher, butthose in the terminal fifth of the caudal axis are calcified or developedinsufficiently to show on the radiographs.
Literature CitedBarnard, K. H.1935. Notes on South African marine fishes. Ann. South African Mus., vol.30, no. 5., pp. 645-G58, pis. 23-25, figs. 1-7.Baughman, J. L.1955. The oviparity of the whale shark, Rhineodon typus, with records ofthis and other fishes in Texas waters. Copeia, 1955, no. 1, pp.54-55, pi. 1.Beebe, W., and Tee-Van, J.1941. Fishes from the tropical eastern Pacific, Part 2: Sharks. Zoologica,vol. 26, no. 2., pp. 93-122, pis. 1-2, figs. 1-34.Bigelow, H. B., and Schroeder, W. C.1948. Fishes of the western North Atlantic, Part I: Cyclostomes and sharks.Mem. Sears Found. Mar. Res., no. 1, pp. 29-257, figs. 4r-106.Breuer, J. P.1954. The littlest biggest fish. Te.xas Game and Fish, vol. 12, no. 2., pp.4-5, 29, 3 figs.Ford, E.1921. A contribution to our knowledge of the life histories of the dogfisheslanded at Plymouth. Journ. Mar. Biol. Assoc, new ser., vol. 12,no. 3, pp. 468-505.Garrick. J. A. F.1960. Studies on New Zealand Elasmobranchii, Part XII: The species ofSqualus from New Zealand and Australia, and a general accountand key to the New Zealand Squaloidea. Trans. Roy. Soc. NewZealand, vol. 88, no. 3, pp. 519-577, figs. 1-6.Maschlanka, H.1955. Die Proportionsanderungen beim Wachstum der Katzenhaie {Scyllio-rhinus canicula und Sc. stellare). Pubbl. Stazione Zool. Napoli, vol.26, pp. 12-27, figs. 1-14.Reid, G. K.1957. External morphology of an embryo whale shark, Rhineodon typusSmith. Copeia, 1957, no. 2, pp. 157-158, 1 fig.Springer, S.1960. Natural history of the sandbar shark Eidarnia milherli. U.S. FishWildlife Serv., Fishery Bull. 178, vol. 61, pp. 1-36, figs. 1-5.Springer, V. G.1961. Notes on and additions to the fish fauna of the Tampa Bay area inFlorida. Copeia, 1961, no. 4, pp. 480-482. 7
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