On the Presence and Disappearance of theHind Limb in the Cetacean Embryos
By
TEIZO OGAWA(Received Feb. 10, 1953)

LA Historical Sketch

G. Guldberg of Norway reported for the first time the unquestionable
existence of the hind limb protrusion in the f etal Cetacea. That is, hespoke on May 14, 189.4, at the 8th meeting of the Anatomical Associationof Germany opened at Strassburg upon a 7 mm long embryo of the harbor
porpoise, Phocaena communis, which showed comparatively well developed
hind limbs. At the same occasion Guldberg introduced two other embryos,
17 mm and 18 mm long of the same species, in which he could observe
lateral to the genital tubercle very low eminences, representing to his mind
the rest of the hind limbs.
Soon afterwards a large monograph (1894) on the development of thedolphin was published from Bergen Museum under the joint names ofGuldberg and Fridtjof Nansen, the famous explorer of the North Pole,and Guldberg reported then his findings in details on the hind limbs of
the three Phocaena-embryos, together with a number of clear drawings.
The 7 mm and 17 mm embryos were said to have been obtained fromGreenland.
Shortly later (1895) W. Kukenthal of Germany, assuming that thelow eminences seen by Guldberg in 17 mm and 18 mm embryos might be
the anlage of the mammary glands, opposed partly to Guldberg's opinion.
He added that he had written already in 1893 on the rudimentary hindlimb in a 25 mm long embryo of Phocaena. The originality requested by
Kukenthal was not fully accepted by Guldberg, chiefly because the former
mentioned the eminence in a height between the navel and the genitalorgan, namely, its position was different from the latter's finding.
Later Guldberg wrote again in 1899 another paper dealing with thesame research materials as before, in which he laid stress on the microscopical proofs to indicate that the low eminences in 17 mm and 18 mm
long embryos can never be the anlage of mammary glands, but nothing
than the rest of the hind limbs. It is also to be noted in this paper, thatGuldberg revised his earlier drawing on the external appearance of the7 mm long Phocaena-embryo. Compare his pictures of 1894, Taf. IV,

T. OGAWA

128Fig.12andof1899,Taf. XX,Fi
g.1.
The presentauthordeems,the very inter
estin
gd
iscu
ssion
sbetweenthes
etwoEuropeana
uthor
itie
scametotheendin1899witht
hev
i
ctor
yo
ft
heNorwegiancetologist. AfterwardsKukenthalh
imsel
fmadei
n1914
agr
eatc
ontr
ibutiontothi
sproblem,as he found inthre
eembryos(32mm, 28mm, 30mm di
rekt
e kりr
per
fange） of Megaptera theex‑istenceo
f rudimentary h
i
ndl
i
mbs,t
h
a
ti
s,fort
h
efi
r
s
tt
i
mea
stot
he
balee
nw
hales. The 32m mem‑bryo, whichwithr
elat
i
v
elyl
ess
marked cu
rv
atur
eo
fthebody‑axiswasestimatedastheyoung‑estofthet
hree, showedonbothsidesoftheg
enitaltuberclethehind limb elev
ation,1.
2m m inheight and 0.
9m m wide att
hebase. I
twasconicalbutroundedatthetip,papilla‑like, and flatlaterally, andcaudall
ydir
ected.
Also in two other embryos,
28m m and 30mm, the restoftheh
ind limb was recognized,
thoughles
sremarkably. Inthe(a)samepaperKukenthaladdedh
isobservationonthehindlimbofa
11m mlon
gembryo ofP
hocae‑e).
noide
sdalli (TγuII. PersonalObserv
ations(b)Fig.1. Fourteenmillimete
rembryoofProdelphinus caeru
leoalbus. (a)lefts
ide,(b)rights
ide.

Recently Icouldaf
firmina
14m m long embryo ofProdel‑
Meyen)co
l
‑
ph
inu
scaer
u
leoalbus(lectedatArar
i on thew
ester
ncoas
tofIzuPeninsu
fa,thepre‑senceo
fthehindlimb,asshownintheaccompanyingphotographs(Fig.1a,b). The body‑axi
softheembryo isstronglyb
ent,sot
helength(14mm)wasmeasured
st
r
aigh
tfromthe nucha totheOnthePresenceandDisappearanceo
ftheHindLimbi
ntheCetaceanEmbryos 129cau
dalf
lexur
e. Thiswayo
fmeasurementi
sappropr
iatesoasnottospoilthedeli
catem
ater
ialafterf
ixationinformalin, and besidesto compare
igures,ast
hi
saut
ho
rmeasureda
lsot
he Nacken‑
steiss‑with Guldbergsf．
Hinge
Theformo
ftheh
indlimbprotr
usionobserv
ed by me int
hisP
ro‑rentfromGuldber
ず sdescr
iption. Indelphi
n
u
s‑
embr
yoi
scon
si
der
ab
l
yd
i町e
myc
asei
ti
smorec
on
i
ca
landp
oin
t
ed,t
h
eapex b
e
i
n
gd
i
r
ec
t
e
dc
au
dall
yずsp
ic
t
u
r
eso
ft
h
e7m mlon
gembryoand laterad. Though the Guldbe1
r
en
ta
smen
t
ion
edabov
ebetween1
894and1899,oneshouldtakear
ed
i庁e(a)Genitaltubercle(b)Left hindlimb(c)Fig.2. Twentymillimete
rembryoof Megapteranodosa. (a)leftside, (b)rightside, (c)fromrightdorsal, theprotrusiono
fthehind limbw
ellnoti
cable.

T. OGAWA

130

naturally the later published picture for more accurate. Anyway, in hisspecimen the limb in question must have been more rounded and relatively
fan-like.
The difference of the form between Guldberg's and mine is probably
due to the ontogenetic stage of the embryos. It is very conceivable thatin my specimen the retrogression of the hind limb has proceeded further oThe difference according to the species of animals seems to be less plausibk
In two other more developed embryos of Prodelphinus caeruleoalbus
collected recently by Dr. M. Nishiwaki at Arari, which are respectively
20 mm and 24 mm in body-length, I could recognize rudiments of the hindlimb as a very low eminence on each side, exactly at the place, whereGuldbe,rg saw the rudimentary hind limb in the 17 mm and 18 mm embryosof Phocaena. But in my cases it appeared to the naked eye as a single
eminence, though Guldberg found "on each side two small tubercles, which
are connected at their origin". The body-length of these fetuses (20 mmand 24 mm) was measured not from the nucha, but from the head to thetail flexure, as the head is more erected and the neck flexure is less marked
than in the 14 mm embryo. Guldberg also calculated the length of 17 mm
and 18 mm from the head to the tail.
As the next, I wish to mention another finding of the hind limbs ina 20 mm long embryo of the Humpback, Megaptera nodosa. This embryo
has been pre:served for several years in formalin in the Whales ResearchInstitute, Tsukishima, Tokyo, and its state of preservation is very good.
On opening the fetal membranes the existence of the hind limb elevation
is clearly visible (Fig. 2 a, b, c), though not so marked as in the 14 mmlong Prodelphinus. To compare with Kiikenthal's description on the fetusesof Megaptera, the hind limb elevation in my case is a little lower inheight but broader at the baseo Fig. 9, Taf. 1 of his paper, showing a28 mm long embryo, seems to resemble my own observation in a highgrade, as to the hind limb.
UL

Relation with the Caudal Flukes

My attention was further given to the chronological relation between
the disappearance of the hind limb and the formation of the caudal
flukes. For this purpose I examined several other fetuses of Prodelphinus, a little larger than the above mentioned, and reached theopinion that a certain synchronism exists between these two phenomena.
In the 14 mm long embryo, which has the easily observable hind limb,
no lateral widening of the flukes can be recognized, the tail tapering quite
gradually to the tail-end (Fig. 3 a). Keeping pace with becoming smaller

On the Presence and Disappearance of the Hind Limb in the Cetacean Embryos

131of the hind limb protrusion in the 24 mm and 25 mm long Prodelphinus,
the elevation of the flukes makes appearance (Fig. 3 b, c), at first so
faintly that one may fail to find it, if not with special care. In larger
embryos, in which the flukes can be seen at ease, there remains no traceof the hind limb elevation at all (Fig. 3 d).
The same circumstance applies probably also to Megaptera, though
I have examined till today only two embryos of this species small enoughfor this problem. We can recognize scarcely any elevation of the flukesin the 20 mm long embryo (Fig. 3 e), while the other embryo, 51 mm
long (from the head to the tip of the tail, as the caudal flexure is herenearly absent), shows pretty(e) 20mm(a) 14mm
well developed flukes, but
no trace of the hind limb
protrusion (Fig. 3 f).
This relation may be(c) 25mm
merely a matter of coincidence without any important~significance. But if one con- (b) 24mm
siders the hind extremities
of Pinnipedia, above all ofPhocidae, being shifted far
caudally and functioning inswimming rather as themain portion of the tail, thechronological agreement bet(f) 51mm(d) 39mm
ween the disappearance oft
the hind limb and the apMegaptera nodosa
Prodelphinus caeruleoalbus
pearance of the caudal flukes
Fig. 3. Schema showing the tail and the hinddeserves our special notice.
limb in small embryos of the Cetacea (seen fromI won't discuss here thecaudal direction).
validity of E. Hackel's famous thesis, that the ontogenesis recapitulates the phylogenesis, nor any
phylogenetic relationship between Pinnipedia and Cetacea. But in myopinion the disappearance of the paired hind limbs in the Cetacea seems
to have an intimate causal nexus with the appearance of the paired caudal
flukes of them.

vIV. Summary
In a 14 mm long embryo of the dolphin, Prodelphinus caeruleoalbus,
and in a 20 mm long embryo of the Humpback, Megaptera nodosa, the132

T. OGAWA

paired elevations of the hind limb are pretty well developed. Photographsof them are shown. Further consideration was given to the simultaneousness of the disappearance of the hind limb elevation with the first
appearance of the caudal flukes in the Cetacean embryos.
Literature
1) G. Guldberg: Uber temporare aussere Hinterflossen bei Delphin-Embryonen. Verhandl.
d. anat. Gesell. auf der 8. Versamml. in Strassburg am 13.-16. Mai, 1894. Anat.
Anz. Bd. 9, 1894, Erganz. S. 92-95.
2) G. Guldberg and F. Nansen: On the Development and Structure of the ~Whale. Part
1: On the Development of the Dolphin. Bergen, 1894.
3) G. Guldberg: Neuere Untersuchungen iiber die Rudimente von Hinterflossen und
die Milchdriisenanlage bei jungen Delphinembryonen. Internat. Monats. f. Anat.
u. Physiol. Bd. 16, 1899, S. 301-321.
4) W. Kukenthal: Vergleichend-anatomische und entwicklungsgeschichtliche Untersuchungen an Waltieren. II. Jena, 1893. (cited by Guldberg)
5) W. Kukenthal: Uber Rudimente von Hinterflossen bei Embryonen von Walen. Anat.
Anz. Bd. 10, 1895, S. 534-537.
6) W. Kukenthal: Untersuchungen an Walen. Zweiter Teil. Jenaische Zeit. f. Naturwissenschaft. Bd. 51, 1914, S. 1-122.
(Department of Anatomy, Medical Faculty,University of Tokyo)