Download The Development of the External Features of Xenopus lvis, based

THE EXTERNAL FEATURES OF XENOPUS LBCVIS.
516
The Development of the External Features of Xen,opm lmvis, based on Material
collected by the late E. J. Bles. By Prof. KARLPETER,University of
Greifswald, Germany. (Communicated by G. R. DE BEER,M.A., B.Sc.)
(F’LATES35-39 *.)
[Read 23rd October, 1930.1
INhis excellent paper, ‘‘ The Life-History of Xenopus levis,” the late Edward J.
Bles described the development of this remarkable Aglossan. He treated
in extenso of the earrliest stages-fertilization, segmentation, gastrulationand more briefly of the development, after hatching, of the mature larva and
of the metamorphosis. The communication was “ intended to be the first of
a series dealing with observations on the life-history of the Anura Aglossa
and their anatomy at different stages of development.” Bles obtained by breeding in captivity a large collection of the eggs and larva of each stage, which
is now preserved in the Embryological collection of the Department of Anatomy
in Cambridge. There are also some fine pictures, of which a number are
unfinished, of larva of Xenopus from the master-hand of Mr. Maxwell.
Impaired health, unfortunately, prevented Dr . Bles from completing his
scheme of investigation, and his Trustees have asked me to give a description
of Maxwell’sd r a w i n g e m invitation which I have accepted with great pleasure.
But these drawings do not repreaent the entire development of X e m p u s :
a few only of the larva had been depicted in various aspects with great skill
and delicacy.
To complete the description of the development of this interesting species,
I found it necessary to have the lacking stages dram after Bles’s material.
Therefore I add to the drawings of Maxwell a fifth Plate in the manner of a
‘‘ Normentafel ” containing the larvs from the atage just before hatching
up to that of the young frog. The youngest stages are represented in Bles’s
own paper. Bles’s fig. 14 is almost the mme stage as our fig, 1, PI. 39.
The larva of PI. 39 are drawn by Herr Levin under my direction. They ere
well preserved, except that a few of the older ones are a little shrunken.
These deformations are corrected.
The Iarvse of Pls. 35-38 are pictured a t a higher magnification than thorJe
of P1. 39, and were drawn after the living specimens. They show more details
than the preserved tadpoles. As Bles WYS in his paper, the living larva are
very transparent ; in the head-region almost all of the complicated structure
of the vertebrab head can be studied in the living animal.
* Ple. 35-38 drawn under the direction of E. J. Blee.
616
PROF. KARL PETER ON THE DEVELOPMENT
OF
The larvae of figs. 1-12, PI. 39,are seen from the left side, the little frog fig. 13
from the dorsal side. Figs. 1 a-12 a show the anterior end of the larva:
1 a-5 a from beneath, ventrally ; 6 a-12 a from above, dorsally.
The drawings of Maxwell represent older larvae and frogs. The tadpolc
of PI. 38. fig. 3 and PI. 35 is a little younger than PI. 39. fig. 6. It is drawn
from the right side, from below, and from above. The figures of PI. 36 show
a larva in the same aspects; it is a little younger than PI. 39. fig. 7. I n P1.37
a tadpole between stages 7 and 8 of P1.39 is represented. P1.38 shows a young
frog, older than that of fig. 12, and the anterior end of a full-grown frog.
The description of the Maxwell drawings is interpolated between the corresponding stages of PI. 39.
Before entering on the description, I have to thank Professor Wilson and
Mrs. Bles for the confidence they have shown me by entrusting me with this
work and for the munificence which has enabled me to utilize the whole material.
I made a preliminary survey of it in the Anatomical Dept. in Cambridge,
and am under obligation to Dr. Shearer for kindly assisting me in this labour.
At Greifswald I studied the material intensively, chiefly with regard to the
development of the external features, and had the figures drawn which form
the “ Normentafel ” in P1. 39. I hope later to be able to supply further papers
illustrating the internal development of Xerwpus.
Description of the Larvae.
PLATE
39. FIGS. 1 & 1 a.
The larva has a length of 4.7 mm. It is at the same stage of development
as the larva represented on fig. 14 of Bles’s paper. It is still enclosed within
the egg. The tail is short, only one half of the length of the body of the larva ;
the fin-fold is well developed.
The exterior shows very few differentiated features. The head is separated
from the body by a slight constriction (fig. 1 a). The swelling in front of this
constriction shows three tubercles, the buds of the external gills. The dorsal
protuberance contains the eye.
I n the front of the head protrudes the cement-organ (the ‘‘ Haftnapf ”) ;
it consists of a pigmented ovoid area. Dorsally from the cement organ,
separated by the slight depression of the stomodaeum, lie the frontal glands,
the “ Stirnstreifen ” of German authors, the organs which soften the eggmembrane during hatching. Beneath the lateral side of this dark stripe are the
small nasal pits.
In the living specimen the eye and the myotomes of body and tad are better
visible than in the preserved one (cf. Bled8 fig. 14).
RATE
39. mas. 2 t 2 a.
Fig. 2 represents a larva of 6 mm. length after hatching. The tail has grown
lower, up to one-third of the length of the whole larva ; its end is not yet
THE EXTERNAL FEATURES OF XENOPUS LBVIS.
517
sharp ; the fin-fold is broader. In the body and tail the myotomes are visible,
although not very distinctly.
The head is further developed and shows more details. Two stumps of
external gills are developed ; the pigmented eye and the nasal groove are visible.
The still imperforate stomodaeum, which is a deeper depression than a t the
earlier stage, lies ventrally from the nasal pit. The cement-organ protrudes
sharply ; its glandular area shows a short bifurcation ; it is bilobed, and the
surrounding region is pigmented. Bles says that the form of the glandular
area is crescentic. The frontal gland is almost invisible, only a delicate
pigmentation shows its position.
PLATE
39. FIGS. 3 & 3 a.
The larva of fig. 3 is 7.6 mm. in length, three-fifths of it belonging to the tail.
The end of the tail is more acute than in the former stage ; the fin-fold is much
broadened. The myotomes are distinctly pronounced. From the dorsal
side of the head black pigment-cells extend to the tail.
The body of the larva has become thicker, shorter, and better delimited
from the tail. The cloaca ending in the anus is visible at the postero-ventral
end of the body.
Three gills are developed, short and without bifurcation. Behind them a slight
protuberance indicates the position of the pronephros.
The mouth is now perforated. It lies dorsally from the bilobed cement-organ,
which is well developed.
PLATE
39. FIGS. 4 & 4 a.
Fig 4 shows a well developed tadpole. The tail has lengthened, both
absolutely and relatively. It occupies two-thirds of the whole length, and
has reached its definitive sue.
The pigmentation spreads out over the body and the entire tail, leaving free
the ventral side of head and body.
The gut begins to curl up, the cloaca has become longer. Through the
transparent skin the heart is visible in front of the gut.
The external gills are a t the height of their development ; three threads,
simple, without branches, are to be seen. A? the ventral view (fig. 4 a) shows,
the operculum begins to grow over the gills.
On the top of the head are to be seen the very prominent cement-organs,
the stomodaeum and the nasal pits. The pigmented area of the cement-organ
has a pronounced crescentic shape. The mouth is perforated and has a curved
form. On its edge a little white spot is to be seen, the place from which the
tentacles grow out.
PLATE
39. figs. 5 & 6a.
The stage of fig. 6 is characterized by the reduction of the external gills
and the cement-organ. The length of the tadpole is 9.5 mm. ; head andbody
~ c c u p yone-third of it,
518
PROF. KARL
PETER ON THE DEVEJXPMBNT OF
The tail with the fin-fold has not altered its relative length and its shape,
except that the dorsal fin-fold has no longer the breadth of the ventral one,
I n this specimen the pigment-cells are expanded. They spread out over the
dorsal side of the body and root of the tail ; the rest of the tail is pigmented
all over.
The gut is arranged in several coils ; its antero-dorsal point is covered by the
bud of the pronephros, which is better visible than in the former stage.
The external gills are very much shortened ; they are partly covered by the
operculum. Only two short stumps appear from under the spiraculum. The
heart is situated between the gill-regions.
The anterior end of the head becomes broader. The mouth is also broad,
and a t its sides there are sharp edges ; these little points are the beginnings
of the tentacles. The mouth lies on the upper side of the head. The cementorgan is in regression and is only faintly pigmented.
PLATE35. FIGS. 1 & 2 ; PLATE
38. mu. 3.
I n P1. 35 and in PI. 38 is drawn a larva of the stage between figs. 5 & 6 of
P1. 39.
PI. 38. fig. 3 shows the fore end of the tadpole from the right side under
higher magnification ; P1.35. figs. 1 & 2 represent the same specimen from the
dorsal and the ventral sides. The figures, drawn from ti living larva, show very
well the external features and the transparency of the body ; almost all the
organs of head and body are visible through the skin, with vessels, nerves, and
muscles.
The head has now the shape of a chisel. It is broad and flat. The lower lip
overlaps the upper, the mouth lies on the dorsal face of the snout. A t the
edges of the mouth protrude short stems, the buds of the tentacles.
The side view shows the ears, the heart, and the spiracle. No external
gills are visible ; they are completely atrophied. The filters of the gill-chamber
shine through the skin. Of the extremities there is no trace. The gut is full
of iridescent material ; a t its dorsal anterior edge lie the curved tubules of the
pronephros. The myotomes of the tail are well pronounced.
The distribution of the pigment-cells is similar to that in P1. 39. figs. 5 & &
I n the skin they are contracted, in the brain-membranes expanded (cf. the dorsal
aspect, P1. 39. fig. 1).
This figure shows the breadth of the head and the short rudiments of tentacles
widely distant one from another. The lobi olfactorii, with the nervi olfactorii
which diverge towards the pigmented nostrils, are distinguishable in the brain,
and further back the epiphysis with its pedicle, the mid-brain, and the rhombencephalon. On both sides of the latter &rethe ear-vesicles, partly covered
by pigment-cells.
The tubules of the pronephros are situated laterally from the gut. The
vesicle behind them is probably the l y m p h - h a .
THE EXTERNAL FEATURES OF XBNOPUS LAVIS.
519
The ventral aspect (Pl. 35. fig. 2) shows the gut, and in front of it the heart.
From the bulbus emerge the aortic arches, which spread out laterally. They
lie over the gill-chamber,whose filters are faintly visible.
PLATE
39.FIGS. 6 & 6 a.
The larva of fig. 6 shows several differences from fig. 5 ; the end of the tail
sharpens, the gut curls up, the gills dirwtppear, the head flattens dorso-ventrally.
The length of the tadpole is 14 mm. The specimen of fig. 6 is a little shrunken
(see the folds of the submental lymph-sac).
The head has the shape of a chisel, flattened dorso-ventrally and broadened
transversely, as fig. 6 a shows. In this figure the larva is seen from the dorsal
side, the ventral side exhibiting no interesting detail after the disappearance of
the cement-organ. The broad mouth is dorsally situated ; at its edges are two
short threade, the tentacles. The circumference of the nostrils is pigmented,
likewise the brain.
The external gills are completely atrophied ; no trace of them is viaible.
The gut is disposed in several coils. Between the cloaca and the tail a little
knob represents the first rudiment of the posterior limb. The bud of the
anterior extremity is a rounded thickening at the anterior end of the gut.
The point of the tail is thinned ; the dorsal fin-fold is narrow, the ventral
one much broader.
h A T B 36. FIGS. 1-3.
This tadpole, a little older than that of PI. 39.fig. 6,ispicturd i n three aspectsfrom the left (fig. 3), from the dorsal (fig. 2) and from the ventral side (fig. 1).
Fig. 3 shows the larva in full length from the left aide. The shape of the body
has not altered ; the ventral fin-foldof the tail is very broad for the greater part
of its extent, but becomes rapidly narrower towards the hinder end. The
end of the tail iS very acute.
The tentacles are but short. The limbs are little protuberances without
further differentiation. Ventrally from them are the coils of the gut, in front
of them the gill-chamber.
The dorsal aspect shows the same organs in head and body as P1. 35. fig. 1.
Note the little lymph-heart dorso-mediallyfrom the pronephros.
Seen from the ventral side (fig. 1) the larva shows the curled-up gut, and in
front is the heart with the aortic arches. The filter-processesin the gill-chamber
are distinctly visible.
PLATE39. FIGS. 7 & 7 a.
The larva acquires the outlines characteristic of a Xe?mpus tadpole. It has
become a great deal longer-the length is 29 mm.
The pigmentation shows the charmtenstic distribution found by Bles ;
it covers the dorsal half of the animal, except for a dorso-lateral stripe on each
. side of body and hil. But the end of the fin-foldS ~ O W Eh e b h k pigment-oeh.
520
PROF. EARL PETER ON THE DEVELOPMENT O F
The skin shows a new feature : the sense-organs are faintly visible in the skin
covering the gut and in the fin-fold between the gut and cloaca.
The head is broad and dorso-ventrally flattened. The mouth is a little
widened. The tentacles have been growing out of its edges ; they are longer
than in fig. 6 and bifurcate a t their ends.
The dorsal side (fig. 7 a ) shows the broad expanse of the snout and the brain
shining through the skin. From the anterior end of the brain emerge the
olfactory nerves to the nasal pits. A white spot indicates the position of
the epiphysis.
I n the lateral aspect note the open spiracle.
The buds of the extremities are more conspicuous. The anterior one appears
as a short stem under the skin, the posterior one is well developed ; neither is
yet differentiated into leg and foot.
PLATE
37.FIGS. 1 & 2.
This tadpole drawn by Maxwell and represented in P1. 37 from the left and
from the dorsal sides is to be placed between fig. 7 and fig. 8 of P1. 39.
The head is very broad and flat, like a chisel. The mouth-region between the
tentacles shows a straight contour (fig. 1). The body is broad and flat too ;
in the region of the extremities it suddenly becomes narrower. The tail is very
flat from side to side and sharpens a t the end.
The tentacles are long ; the left one is apparently broken off ; the right one
bears a short branch. From the dorsal aspect (fig. 1) one sees the brain shining
through the skin. The olfactory nerves grow out from the olfactory bulbs and
reach the pigmented nasal grooves. Nerves, vessels, and muscles are visible
through the transparent skin. The pigmentation is well developed ; its
distribution is the same as in P1. 39.fig. 7. The large pigment-cells of the skin
are clearly pictured, also the little black spots in the membranes of the brain
and of the labyrinth, lying very close together and seen through the skin.
The well dev:loped coils of the gut are visible in the side view.
The limbs are differentiated into leg and foot. The anterior one is covered
by a thin membrane, and is bent a t the elbowjoint.
PLATE
39.FIQS. 8 & 8 a.
The larva represented in fig. 8 has a length of 35 mm. and like that of fig. 7
shows the features of a fully developed tadpole ; the characteristic peculiarities
are still more accentuated. The pigment-cells of this larva are contracted
into little black spots ; their distribution is as usual.
The tentacles have grown to double the length compared with fig. 7 ; in this
specimen they bear no branches.
The extremities are longer and more differentiated ; they are divided into
hand (or foot) and arm (or leg). The anterior one is not yet free.
No other difference of importance is to be remarked,
THE E X T E B N U FEATURES OF XENOPUS LIEVIS.
52 1
PLATE
39. mas. 9 & 9 a.
The tadpole measures 40 mm. in length. The differences between this
larva and the specimen shown in fig. 8 are confined to the tentacles and the
extremities. Note also the open spiracle, and the sense-organs in the skin
over the gut.
The tentacles show several branches. The extremities are further developed,
especially the posterior one. The rays of the digits are visible in the foot,
and the knee-joint in the leg. The anterior limb, covered by the skin, is much
amaller than the posterior ; it is a curved appendage of the trunk with small
digits.
PLAm 39. FIGS. 10 BE 10 a.
The larva represented in fig. 10 is remarkably small ; it measures only 32 mm.
in length. It differs from fig. 9 only in the development of the extremities.
The head is still broad and flattened (fig. 10 a).
The hind leg has become longer and projects beyond the margin of the
fin-fold. The knee is very clearly to be seen, and its joint is bent, as shown
in fig. 10 a. The toes are well differentiated. The arm is bent at the elbow.
joint, but not yet free.
PLATE 39. FIQS. 11 & 11 a.
The larva of fig. 10 is a well developed tadpole ; that of fig. 11 is in course
of metamorphosis to the frog.
Head and body are transformed in shape. The head is no longer flattened,
but rounded. It is higher dorso-ventrally and narrower from right to left,
but still relatively broader than in the adult frog. The mouth lies on the lower
side of the head, no longer on the upper side. At its edges are the tentacles,
now somewhat reduced-short threads with little branches. The spiracles
are not yet closed.
The caudal portion of the body is b r o a d e r 4 result of the development
of the legs.
The sense-organs are conspicuous, not only over the gut but also on the back
of head and body (fig. 11 a). The skin loses its transparency and assumes
the adult character.
The tail is very long and shows no eign of degeneration. The fin-fold is still
well developed, in the tail itself and also in front of the cloaca.
The extremities are further developed. The anterior one is free, with elbow
and fingers, the posterior is very long. The toes are united by a swimming
membrane ; the claws of the first three toes have begun to develop.
PLATE
39. FIGS. 12 & 12 a.
Fig. 12 represents a little frog with a long tail.
Head and body are still rounded, especially the snout. The mouth is shifted
&l”.J0URN.-ZOOLOQY,
VOL. XXXVII.
36
522
PROF. KARL PETER ON THE DEVBLOPMENT OF
still further ventrally. The tentacles are atrophied to short black stumps
a t the edges of the mouth.
The spiracle is still open. It lies under the insertion of the arm.
The fin.fold of the tail is shorter ; it has almost disappeared between the
llody and the anus.
The leg is B powerful swimming-organ with large toes, three of which bear
horny claws. The anterior extremity is bent in the definitive position.
PLATE
38. FIG. 1.
Fig. 1 of P1. 38 shows from the dorsal side a frog in a more advanced stage
of metamorphosis. It is fully developed, but has still a tail, now atrophied
to a short appendage.
The snout, the nostrils, and the eyes are like those of an adult frog.
I could not observe the closure of the spiracle, because neither the actual
specimen nor any other of the same stage was found in the material.
The skin has made an advance : one sees a new pigmentation, dark spots
on a light ground. The lateral line sense-organs are visible.
PLATE
39.FIG. 13.
Fig. 13 represents a young frog from the dorsal side.
The external features are in all respects those of a frog, the metamorphosis being
now completed. The frog has its definitive coloration and sense-organa.
The tentacles have entirely disappeared. Only a small white spot with a few
pigmented cells OIL the edge of the upper jaw of the broad crescentic mouth
shows the place from which the tentacles projected in the tadpole.
Beneath the eye a short tentacle has developed.
The three claws of the toes are well developed. A fourth has grown out a t the
basis of the first toe.
The frog grows still further, but does not change in shape and appearance.
PLATE
38. FIG. 2.
The anterior half of a fully developed adult frog is shown in fig. 2 from the
right side.
The artist has represented the mottled skin with the lateral sense-organs
in colour.
The nostrils are prominent, as also the large eyes with the brown iris. The
tentacle under the eye is very short and thin. The mouth is situated on
the ventral side of the snout.
The short feeble arms bear four fingers without claws.
THE EXTERNAL FEATURES OF XENOPUS LBVIS.
623
On surveying the whole development of the external features of Xenopiis
and comparing it with that of a species of Ram, we perceive that we have
to deal with a very remarkable form.
The peculiarities of the Xenopus larva are often referred to ; I propose to put
them together once more with reference to the figures.
Naturally the peculiarities are correlated with t,he mode of life of the larva,
especially with the feeding habits. Bles describes in an interesting manner how
the food, consisting of little planktonic organisms such as Chlamydomonas, is
carried in with the stream of water and filtered off in the gill-chamber. This
explains the absence of horny teeth and the persistence of the opercular opening.
The shape of the larva is extraordinary, and is reminiscent of that of fishes.
The long tail with the broad fin-fold which occupies two-thirds of the length
of the whole animal is hardly to be found in any other tadpole. The broad
flat head is very characteristic, especially the long tentacles which project
a t the edges of the mouth. These tentacles, along with the fish-like hotly,
have led some authors to compare the Xenopus larva with a Siluroid form.
As already said, we find no horny teeth in the mouth at any stage in the
X e n q u s larva. All the tadpoles of Ram bear these teeth for rasping the
flesh etc.
The development of the gills is remarkable too. There are three external
gills which remain rudimentary: at the height of their development they
are only short simple threads. I have never seen bifurcation nor branches.
They evidently exist but a short time, and are soon grown over by the
operculum.
There are no internal gills at all ; where they would normally be situated
filter-processes are developed for filtering the water entering through the
mouth. Small organisms are held back in the gill-chamber and the water
leaves the body through the spiraculum. For this reason the spiraculum is still
open in the young frog with a long tail at the end of the metamorphosis.
Correlated with the frog's life in the water is the fact that the sense-organs
of the lateral line do not atrophy a t the metamorphosis, but pergat as functional
organs in the adult.
Bles called attention to the strange pigmentation of the larva, which is absent
from special parts of body and tail, and suggested a biological explanation
for this distribution.
The development of Xenopus is sufficiently peculiar to merit extended
treatment, not only as regards the external features but also the internal organs.
The latter portion of the task I intend either to undertake myself or to entrust
to one of my assistants.