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THE STRUCTURE OF THE SPERM ATOPHORES OF
AMBYSTOMA PUNCTATUM



BERTRAM G. SMITH



[Reprinted from Biological Bulletin, Vol. XVIII., No. 4, March, 1910. |



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I Reprinted from Biological Bulletin, Vol. XVIII., No. 4, March, 1910.]



THE STRUCTURE OF THE SPERMATOPHORES OF
• AMBYSTOMA PUNCTATUM.

BERTRAM G. SMITH.

Since the recent paper of Wright and Allen ('09) has again
directed attention to the breeding habits of Amby stoma puncta-
turn, it has occurred to me that a more careful description of the
spermatophores than has yet been given might be of value in a
comparative survey of the habits of the urodeles. No adequate
figures of these spermatophores have yet been published.

The spermatophores of Amby stoma punctatum studied by me
at Ann Arbor (Smith, '07) were not freshly deposited, and were
not in the best possible structural condition for study; hence
only a brief description, illustrated by a photograph, was at-
tempted. Since then I have been able to study these structures
in abundance under the best possible conditions. As evidence
that the spermatophores were freshly deposited, there may be
cited the fact that the spermatozoa of some of them were found
to be active when examined in the laboratory seven hours after
their collection. The results of this study have confirmed the
description previously given by me, in regard to distribution and
general structure, but have revealed the common occurrence of
compound spermatophores, a condition previously unnoticed.

In the early spring of 1909, when the snow had nearly all dis-
appeared, I found specimens of Ambystoma punctatum and A.
jeffersonianum, under rocks on the hillside near "Branchipus
Pond," about two miles from the campus of Syracuse University.
The study of the habits of these animals was undertaken in
order, if possible, to determine by direct observation the exact
procedure in the process of fertilization by means of spermato-
phores in the case of A. punctatum , and to obtain data in regard
to A. jeffersonianum , in which the manner of fertilization is
entirely a matter of conjecture.

Conditions made it impossible to keep a very close watch of
the pond during the breeding season, and the abruptness of the
weather changes caused me to miss the few opportunities for direct

204



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BERTRAM G. SMITH.

r ation of the activites of the animals in the field, by means
lantern at night. Specimens of both sexes were trans-
l to the laboratory and kept under observation in aquaria;
1 males of A. punctatum, and one of A. jeffersonianum,
ted masses of seminal fluid on the floor of the aquarium,
othing resembling the formation of -true spermatophores
ed. The largest of these masses was nearly 2 cm. long,
he quantity of sperm deposited by each individual was
sufficient to form a group of spermatophores. The be-
• of the sexes toward each other presented nothing that
be interpreted as normal breeding behavior.
:he pond large numbers of spermatophores were deposited,
lese were carefully studied, both in situ and in the labora-
but all the specimens collected were identified, with con-
ble certainty, as the product of A . punctatum. The failure
re the main problems caused me to lay my notes and draw-
side, awaiting an opportunity to continue the investigation;
le conclusive results of Wright and Allen ('09) have made
nnecessary so far as regards A. punctatum.
itification of Species. — The fact that A. jeffersonianum
;, though less abundantly, in the same region with A. punc-
made necessary a determination of the species of the sper-
>hores found. The only available method seemed to be
%h a study of the spermatozoa. The material available
ted of spermatozoa from a considerable number of individ-
f A . punctatum, taken both at Syracuse and at Ann Arbor,
Dermatozoa from one specimen of A: jeffersonianum, taken
racuse. Material from each individual was fixed by a
y of methods, stained, mounted and carefully measured
high powers of the microscope. The average measure-
were as follows:

Acrosome Head. Middle Piece. Tail. * Total Length.

-Aatum 20/* n6/* 15.0/* 480/' 631.0/i

'sonianum 17/* 114^ 11.3^ 348," 490.3 /*

rill be seen that the sperm of A. jeffersonianum is in general
r than that of A. punctatum. The middle piece is most
and accurately measured, and affords the readiest means



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*F^5?^*V



SPERMATOPHORES OF AMBYSTOMA PUNCTATUM. 206

of differentiating the two species. The range of variation in
the length of the middle piece of A. punctatum (in several in-
dividuals) is 14//-16/*; in A. jeffersonianum (in one individual)
11. 2 /i-11.9 /i.

The fact that only one individual of A. jeffersonianum was
considered of course militates against the acceptance of these
results as absolutely conclusive; but since material was taken
from several individuals of A. punctatum, and in all of these
there was a decided difference from the results obtained from the
single individual of A. jeffersonianum, it is highly probable that
the species may be distinguished in this way.

Spermatozoa were then taken from a dozen or more spermato-
phores, each from a different group and presumably deposited
by a different individual. This material was treated precisely
as in the case of the spermatozoa described above. Somewhat
to my surprise and disappointment, all the specimens conformed
to the dimensions of the sperm of A. punctatum.

Structure of the Spermatophores. — Two general types of sperma-
tophores are recognizable: simple and compound. The com-
pound spermatophores may be roughly divided into the vertically
serial, and the Y-shaped types, the former by far the most com-
mon; but both these conditions maybe found combined in one
compound spermatophore.

A spermatophore of the simple type is illustrated in Fig. 1.
It consists of an expanded hummocky base and a stout stalk,
of very clear, transparent, gelatinous material, surmounted by
a dome-shaped mass of snowy-white seminal fluid.

While to the naked eye the stalk of a simple spermatophore
is perfectly clear, under a low power of the microscope it is seen
to possess a delicate network of fibrous material. Under high
power this is found to be made up of sparsely distributed sperma-
tozoa, interlaced to form a meshwork. In some spermatophores
the strands of this network assume considerable regularity.
There may be distinguished regular parallel strands extending
in the direction of the axis of the stalk, distributed at about
equal intervals through its substance ; these strands are connected
by more irregular cross-strands.

Evidently a few spermatozoa are present in the cloaca at the



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BERTRAM G. SMIT^

the stalk of the spermatophore is laid down, and these
Da owe the regularity of their distribution to the
ridges of the cloaca.

iparison a drawing (Fig. 2) of a spermatophore of
is viridescens, obtained from a specimen in captivity,
alongside the figure of the simple spermatophore of




Camera drawing of simple spermatophore of Ambystomo punctatum,
\ and in the following figures the blackened portion is in nature snowy

Camera drawing of a spermatophore of Diemyctylus viridescens, X 5.

a punctatum. (The spermatophore of Diemyctylus
previously described and figured by Jordan, '93.)
>ermatophores of Diemyctylus viridescens were avail-
lis study, but none of these differed essentially from
ured. The average dimensions of twelve simple sper-
ts of Amby stoma punctatum taken at random, and of
ured spermatophores of Diemyctylus viridescens, are



Total


Longest Diameter


Smallest Diameter


Breadth.


Height.


of Sperm Mass.


of Stalk.




6.2 mm.


3.7 mm.


2.5 mm.


6.4 mm.


8.0 "


2-5 "


0.3 "


12.0 "



plest and most common case of compound spermato-
lat in which one spermatophore is deposited directly
another (see Fig. 3). In the process of deposition of
i spermatophore the sperm ball of the first one is
to the form of an inverted cup covering the stalk of the
:he sides of this cup are stamped with a characteristic



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BERTRAM G. SMITH.

X)und spermatophores are not all so regular in form as
£ured. Sometimes successive spermatophores are packed
r so closely that is it difficult to distinguish individuals
implex; but while the first impression obtained from some
i spermatophores was that of great irregularity, closer
[lowed that all of them might be reduced to the vertical-
r pe, the Y-shaped type, or a combination of these,
of the sperm masses of the simple spermatophores, or
ninal one in the case of a compound spermatophore, were
onsiderably frayed as if from being taken up into the
>f a female ; rarely, the entire ball of sperm was missing,
course possible that either condition might be accidental,
e hundred spermatophores taken at random, the number
kind was as follows:

mple type 23

>mpound, two in vertical series 45

>m pound, more than two in vertical series 21

shaped, or combination of this type with (2) or (3) _ii

otal 100

me of the spermatophores examined was there any ap-
to the complexity of structure shown in European urodeles
>r ('05). Zeller's drawings appear to me highly conven-
ed.

ssion. — Of the various kinds of spermatophores of
oma punctatum, the simple type is functionally the most

yet even this is not so highly differentiated and struc-
so well adapted for its purpose as the spermatophore of
tylus viridescens. In case the of Diemyctylus, I have seen
the entire ball of sperm removed from the very slender
y the female cloaca. In Amby stoma, on account of the
ss of the stalk affording a large surface for contact with
>s of spermatozoa, this would be more difficult, and ac-

to the observations of Wright and Allen ('09) does not
-only a very few sperms, comparatively, are detached
lined by the cloaca.

>nly mention of compound spermatophores that I find in
rature is in the case of the axolotl, described by Gasco
While in many cases the spermatophores deposited were



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SPERMATOPHORES OF AMBYSTOMA PUNCTATUM. 2IO

single, in one case the male was observed to return repeatedly,
at intervals of several minutes, to the same spermatophore and
deposit another on top of it, thus building up a compound sper-
matophore consisting of seven simple spermatophores. Whether
the compound spermatophore of Amby stoma punctatum is built
up in this way I have no means of deciding; it would seem quite
as probable that the spermatophores were deposited in rapid
succession, while the animal remained in one place — a condition
not far removed from what occurs in external fertilization, in
which a large amount of seminal fluid is discharged at once.
In any case it is difficult to see that any advantage is gained by
depositing one spermatophore on top of another and thereby
destroying the efficiency of the one previously deposited. As
already noted in the case of Amby stoma punctatum, the spermato-
zoa of these spermatophores retain their vitality in water for
many hours. The formation of compound spermatophores of
the vertical-serial type seems to me a useless and wasteful pro-
cedure, and the large proportion of such spermatophores indicates
that the spermatophore-forming habit is not highly evolved nor
perfectly adapted to its purpose.

In my previous paper (Smith, '07) on the breeding habits of
Ambystoma punctatum, I ventured the prediction, based on the
large number of spermatophores and the manner of their distri-
bution, that the behavior of the adults in the fertilization process
would be found to be simpler than in the case of Diemyctylus
viridescens. In the latter case only a very few spermatophores
are formed by each male, and particular safeguards are necessary
in order to insure the delivery of at least one of them to the fe-
male cloaca: these safeguards are furnished by the complicated
but definite series of acts on the part of the adults which precedes
and conditions the deposition of a spermatophore. Just as in
the higher vertebrates economy of egg production is correlated
with care of the young, so in Diemyctylus economy in the pro-
duction of spermatophores is accompanied by a considerable
amount of certainty as to their fate. This prediction as to the
relative simplicity of the behavior of the adults of Ambystoma
punctatum, the recent observations of Wright and Allen ('09)
have abundantly justified. In the light of the observations on



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BERTRAM G. SMITH.

cture of the spermatophores recorded in the present

e can go further and say that the entire process of secur-

lization by means of spermatophores is in Ambystoma

m more primitive, less highly adapted to secure its ob-

i economy of material, than in Diemyctylus viridescens.

gical Laboratory,
niversity of wisconsin,
Madison, Wis.

LITERATURE.

Amours des Axolotls. Zool. Anz., 4.
Iwin O.

: Habits and Development of the Newt (Diemyctylus viridescens).
rn. Morphol.. Vol. VIII.. No. 2.
tram G.
: Breeding Habits of Ambystoma punctatum Linn. Am. Nat., Vol. XLL,

486. (Includes a more extensive bibliography of earlier literature.)
en, W. Docters *

>er die Aufnahme der Spermatophoren bei Salamandra maculosa Laur.
1. Anz., 31, pp. 649-653-
bert Hazen

:es on the Breeding Habits of Ambystoma punctatum. Biol. Bull., Vol.
V., No. 4.

bert H., and Allen, Arthur A.

: Early Breeding Habits of Ambystoma punctatum. Am. Nat., Vol.
III., No. 513.
7.

:ersuchungen tlber die Samentrager und die Kloakenwulst der Tritonen.
Lschr. wiss. Zool., Bd. 79.



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THE NESTS AND LARV^ OF NECTURUS.



BERTRAM G. SMITH.



[Reprinted from Biological Bulletin, Vol. XX., No. 4, March, 191 1. 1



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(Reprinted from Biological Bulletin, Vol. XX., No. 4. March, 1011.]



THE NESTS AND LARV/E OF NECTURUS.

bertram g. smith.
The Nests.

1. Nests in a Lake Habitat. — Through the courtesy of Professor
Bennet M. Allen I recently became acquainted with the spawning
grounds of Necturus maculosus Rafinesque in Lake Monona, Wis.
During the latter part of June and the early part of July, 1910,
several trips were made to the locality for the purpose of ob-
taining embryological material.

The "nests" were found in water about 3-5 feet deep and
about 50-100 feet from the shore, in a locality where the bottom
was strewn with loose flat stones of various sizes. The largest
of these stones, about 1^-2 feet in diameter, frequently served as
cover for the eggs of Necturus. The eggs are attached by the
slender stalks of the gelatinous envelopes singly to the under
sides of these stones, distributed over an area about 8-10
inches in diameter (see Fig. 1). The presence of minute algae,
etc., in the water made it so opaque that it was impossible to
see the bottom ; the eggs were obtained by wading in the water,
feeling about with the feet for a large flat stone, then bringing
it to the surface.

Eycleshymer (*o6) describes nests of eggs attached to the
under sides of logs, boards, pieces of tin, canvas, etc., but does
not mention finding nests under stones. Doubtless any con-
venient object may be selected as cover.

The number of eggs present in a nest was determined in five
cases as follows: 18, 61, 80, 84, 87. The average is 66. The
nest photographed contained 84 eggs.

The first embryos were obtained on June 22 ; these were in
an advanced stage of development, with head well formed and a

191



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THE NESTS AND LARViE OF NECTURUS. 1 93

hardly be inferred from the text, my experience shows that the
collecting season may be much later than Eycleshymer recorded.

A noticeable feature of the development as compared with
other amphibians that I have studied, is the uniformity in the
stage of development of embryos found in different nests in the
same locality. On each of the following dates from four to seven
nests were secured : June 22, 25, 29, July 5. On each date all the
eggs were found so nearly in the same stage of development that
only slight differences could be detected in eggs from different
nests. This uniformity points to a very short spawning season —
perhaps two or three days — in this locality; it would seem that
all the eggs in a restricted area are laid at nearly the same time.
But Eycleshymer fo6) says: "The eggs are first deposited in
those localities where the water is shallow and exposed for the
greater part of the day to the rays of the sun. The period of
egg-laying usually covers two or three weeks. There is no foun-
dation whatever for the statement made by Hans Virchow that
the animals deposit their eggs so to speak at the same hour."

I had no success in keeping embryos of Necturus alive in the
laboratory, although later in the year larvae of Cryptobranchus
thrived under the same conditions.

2. Nests in a Stream Habitat.— I am not aware of any published
observations on the nesting of Necturus in streams, hence the
following notes on the subject may be of interest.

During the late summer and early autumn of the past five
years, while searching for adults, eggs and larvae of Cryptobran-
chus, I have had occasion to overturn numberless stones in the
bottom of a large creek tributary to the Allegheny River, in
northwestern Pennsylvania. This has resulted in the frequent
finding of specimens of Necturus.

All the specimens found were small, none exceeding 20 cm.
(8 in.) in length and most of them were much smaller. The
smallest, taken September 13, 1906, was 35 mm. long (see Fig. 6).
This specimen was one of a group of six or seven found under the
same stone; the others, aided by the swift current, escaped.

These circumstances led me to suspect that the stream was
a spawning ground for Necturus. This suspicion received con-
firmation when, on August 24, 1910, I found attached to the



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I96 BERTRAM G. SMITH.

Specimens preserved July 31 (see Fig. 3) average about 25
mm. long. As compared with Cryptobranchus larvae of the same
age after hatching, in Necturus the general form of the body is
more slender, except that the yolk sac is of relatively greater
size. The absolute size of the Cryptobranchus larva is much
greater. The pigmentation in Necturus is less intense, and the
general appearance is that of a less advanced stage of develop-
ment.

These specimens show the beginning of the dorso-lateral
stripes, which attain great prominence in later stages and will
be described in the stage in which they are most marked.

In the larvae preserved during the latter part of August, the
yolk sac still persists, though its size is so reduced that the
abdomen is only slightly distended by it. The lateral stripes
are quite distinct, though not so conspicuous as in slightly later
stages. The larvae average about 30 mm. in length. In Crypto-
branchus larvae of the same age after hatching, the yolk sac is
so reduced that- the abdomen is no more distended than in the
adult; the color is much darker than in Necturus, the form of
the body stouter, and the absolute size nearly twice as great.

For a larval specimen 34 mm. long, I am indebted to Mr.
L. W. Harrington, formerly an assistant in the Zoological Labora-
tory of the University of Michigan. This specimen was obtained
by Mr. Harrington from fishermen in the Detroit River on
November 24, 1906, and was examined by me on the same day,
before preservation. The transparency of the ventral abdominal
wall enables one readily to note that the yolk has been entirely
absorbed. Since the coloration conforms accurately to that of
the Lake Monona specimens, a description of the color pattern
will serve for all the western larvae examined by me.

As contrasted with the adult, the most striking feature of
the 34-mm. larva is the presence of a conspicuous dorso-lateral
longitudinal stripe, light yellow in color, on each side of the
body. The lateral margin of each stripe is metamerically crenate.
The body stripes continue unbroken and without fusion to the
tip of the tail; anteriorly, they are separated by a slight break
from similar stripes along the margin of the dorsal surface of the
head ; these latter are sometimes connected at their anterior ends
by a faint transverse bar over the tip of the snout.



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THE NESTS AND LARYiE OF NECTURUS.

The ground color of the dorsal and lateral surfaces is
brown, with small scattering spots of lighter color es
noticeable along the sides of the body and tail. As co
with the earlier stages the pigmentation is much more
but this merely serves to accentuate the light-yellow
It is to be particularly noted that in all the western larvs
have examined, the dark color of the dorsal surface of tl
is continued along the dorsal edge of the tail between th<
stripes (see Fig. 4). The ventral surface is pale yellow,
transparent.



Fig. 4. Fig. 5.

Fig. 4. Caudal portion of a 34-mm. Necturus larva taken from tl
River, showing color pattern of the tail. The specimen is somewhat
from partial drying before preservation; in particular the ventral margin
is upturned. Photographed after preservation in formalin. ( X 3 H)

Fig. 5. Caudal portion of a 35-mm. larva of Necturus taken from a
northwestern Pennsylvania, showing color pattern of the tail. Photogra
a formalin specimen. (X 3HO

Mention has already been made of larvae taken from a
habitat in northwestern Pennsylvania. No attempt w?
to capture all the specimens found, but a series was pi
representing a gradation in size from the smallest, 35 mi
to the largest, 20 cm. in length. Of these the fourteen s
all under 15 cm. in length, show larval characteristics
color pattern.

The smallest specimen, 35 mm. in length (see Fig.
taken on September 13, 1906. This larva is younger ai
phologically less advanced than the slightly smaller la
tained from the Detroit River; but on account of an im
difference in the color pattern its description has been d



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198



BERTRAM G. SMITH.



By dissection it was found that the yolk sac, though reduced
almost to the form of a digestive tube, still contained a small
amount of yolk. Assuming that this larva had been hatched
about 8-IO weeks, we find a similar condition of the yolk sac
in Cryptobranchus larvae of the same age after hatching.



Fig. 6. Living larva of Neclurus, 35 mm. long. (X J.)

This specimen differs from the western larvae in that the dorso-
lateral stripes unite in the median line at the base of the tail,
to be continued as a single stripe along the dorsal edge of the
tail (see Fig. 5). Since this peculiarity is present in all the
fourteen larvae that I have examined from the eastern habitat,
it would appear to be a constant difference between the eastern




Fig. 7. Larva of Neclurus, 55 mm. long, photographed after preservation in
ormalin. Nearly actual size.

and western forms. Otherwise the color and color pattern of
both eastern and western larvae are the same.

The larger specimens may be described as follows: A 42-mm.
larva taken on August 29, 1907, differs morphologically from
the 35-mm. larva in its slightly greater yolk content; evidently
it is younger, though of greater size. A specimen 55 mm. long



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THE NESTS AND LARVAE OF

(Fig- 7)» taken on August 20, 1906, agree
pattern with the 35-mm. larva; the yolk
sorbed. Another 55-mm. larva taken Sej
the same condition. A 60-mm. specimen
shows a slight loss in the distinctness of tl

The striped pattern characteristic of
culmination in specimens of about 55 mn
this time on it gradually disappears, tl
being obscured by dark pigment; during
large black spots, which give the mottled z
pattern of the adult, become established,
of a body length of 15 cm. the larval cc
replaced by that of the adult. Several s
length of 20 cm. were dissected and found

Eycleshymer (*o6), after describing th<
the adult, continues: "It is probable th
color are responsible for a number of s]
instance I might state that some years
described a small Necturus, taken from th
now Rivers in Ontario, to which he gave t
lateralis, var. latastei. 'The coloration
abdomen sooty and the gular fold white,
of 1904 the writer was fortunate enough
animals which measured about 4 and 6 inc
smaller corresponds closely to the des<



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