I

Asiatic Herpetological Research

June 1995'

Vol. 6, pp. 114-119

Reproductive Behavior in the Long-tailed Salamander (Onychodactylus
fischeri Boulenger).
I.

A. Serbinova

12and V. A. Solkin'Moscow Zoo, B. Gruzinskaya 1 Moscow 12342 Russia,

2

Pacific Ocean Institute of Geography, Far East Branch of Russian Academy of Sciences, Vladivostok,

690032, Russia

We studied reproductive behavior in wild and captive Onychodactylus fischeri. Reproductive
behavior and physiology is triggered by warming water temperatures in the spring. Pair formation begins at7° C and spawning at 9° C water temperature. Fertilization is external. The development of distinctive
femoral musculature and skin on the posterior surface of the hindlimbs in the male is for grasping the eggs

Abstract. -during fertilization. Pairs of salamander experimentally injected with a synthetic analogue of gonadotropin
releasing hormone exhibited typical mating behavior and produced fertile clutches of eggs.

Key words: Onychodactylus fischeri,

salamander, reproduction, external fertilization,

courtship, gonadotropin releasing hormone.

directed to the time of maximum diurnal
All captured salamanders wereactivity.

Introduction

Thelong-tailedsalamander,

Onychodactylus fischeri is one of the mostpoorly known amphibians in Russia.
Emeliyanov (1947) noted that spawning
takes place from the time salamanders
appear in the spring until the middle of July.
Regel and Epshtein (1975) concluded that,

reproduction in this species is not restricted
to a specific season. The discovery of aclutch with some hatched larvae indicatedindividually numbered by toe-clipping using
standard techniques.
total of 601

Asalamanders were captured of which 102
were recaptured. All salamanders weremeasured and weighed on a triple beam
We noted the degree ofbalance.
development of such male secondary sexual
characters as the distinctive femoral
musculature and skin development on theWeposterior surface of the hind limbs.
recorded such female characteristics as theprobably occurred in therelative size of oocytes observed through theIt is difficult tospring (Kozik, 1991).
establish the precise time of oviposition
since the length of embryonic development
for this species is unknown. The length ofembryonic development for the related

abdomen, their passage into the oviductsthat oviposition

species O. japonicus is 120 days (Hayaseand Oseki, 1983) and it breeds in the winterThe absence of precise1989).
information on the timing and method ofreproduction of the long-tailed salamander
prompted us to undertake this study.
(Akita,Methods and Materials
This study was conducted from May
through July, 1991 on the Primorsky krai atributary of the Mineral'naya River.
Daylight observations of the location andreproductive state of salamanders in nature

were made along a 1000m transect along
Kitaisky Spring.

The search effort was© 1995 by Asiatic Herpetological Researchand the condition of the ventral opening tothe cloaca.

The long-tailed salamander has secretive
habits and we determined that observation ofnatural oviposition was unlikely. Therefore,

wereproductive behavior
captive individuals.
Salamanders were housed outdoors in theshade of an awning in 8 liter aquaria with 35 cm of running water and shelters.
Aquarium water was changed daily. Eachof seven males and seven females wereinjected with 1-5 |ig/individual/day of astimulated

hormonallyin

synthetic analogue of gonadotropin releasing

hormone for 7-12 days.

All individuals

were determined to be ready for breeding
before injection. Males and females werekept separate until ovulation began; thenthey were paired.

Vol.6, p. 115

Asiatic Herpetological Research

June 1995

number of animals

41——

710temperature

1316

may
water temperature

2225

—B~

non-breeding animals

1928

31

3

6
June

-*- breeding animals
FIG. 1.

Pattern of Onychodactylus fischeri activity and water temperature during the spring..

number of males-*-

non-breeding—s—breedingFIG. 2. Frequency occurrence of breeding and non-breeding male Onychodactylus fischeri.

9Vol.6, p. 116

Asiatic Herpetological Research

June 1995

number of females

8521

may

14

June

with opened cloaca

body cavity oocytes

oocytes in oviducts

spawned

FIG. 3. Frequency occurrence and reproductive state of female Onychodactylus fischeri.

May when the last stretches of the stream
Results and Discussion

The first observations of active
salamanders were made in late April to early
May at a water temperature of approximately
3° C and while sections of the stream werestill covered with ice.
The number ofanimals active each day increased as
temperatures
(Fig.

1).

warmed during the spring

The first salamanders observed

did not exhibit readiness for breeding.
Oocytes were not visible through theabdomen wall of females and males did notexhibit hindlimb muscle and skindevelopment. All animals were in a poor
nutritional state. The peak number of nonreproductively ready salamanders occurred
on 12 May when water temperature reached
6° C. Not all salamanders leave their wintershelters simultaneously due to differential
warming rates along the slopes and this is

After 12 May thenumber of non-reproductive salamanders
decreased to a constant level by 20 May.

reflected in Fig.

1.

The peak number of reproductively
ready salamanders was encountered on 17

were ice free. These animals appeared to bewell nourished. From 15 May to 15 June amajority of the males encountered were inbreeding condition (Fig. 2).

By

20May

post-hibernation

aggregations of salamanders began todisintegrate and the individuals dispersed
This marked thealong the stream.
beginning of the breeding season.

By 10 May we began encountering
females with opened cloacas (Fig. 3). By
the end of May females with ovulated
oocytes in the body cavity were observed
and by 10 June we found salamanders withoocytes in the oviducts. We first observed afemale that had spawned or oviposited hereggs on 9 June. In early June we observed
3 male-female pairs of salamanders with atleast one member in reproductive readiness.
These observations agree with previous
accounts (Regel and Epshtein, 1975).

In the hormonally treated females thecaudad displacement of oocytes usually tookApril 1995

Asiatic Herpetological ResearchVol. 6, p. 117

FIG. 5. Comparison of the male Onychodactylus
in normal posture and infischeri hindlimbs and tailthe pre-fertilization posture with the legs extended.

Note the distinctive heavy femoral musculature andskin development on the posterior of the hindlimbs.

male then extends his rear legs and holds
this position (Fig. 5).

When spawning begins
FIG. 4. Courtship behavior of Onychodactylus
fischeri with the male (light salamander)
approaching the female's (dark salamander) vent,rubbing against the female's abdomen and straddlingthe female.

three days later they filled the oviducts.
From hormone injection to readiness forspawning usually took from six to 10 days.
observed 6 cases of spawning, two ofWe

which were followed by spermatophore
deposition.

hormonally treated animals
approximately one to two days before
spawning the female salamander ceased
most activity and assumed a typical prespawning posture on a stone with the rear
third of the body in the water. At this timethe male moves about the aquarium,
theperiodically approaches the female touchinghis snout to her vent, rubbing his body onhers and resting beside her (Fig. 4).

femalemmthat of Salamandrella
Ranodon sibiricus. Duringandkeyserlingii
egg deposition (30-40 min.) the maleremains sitting beside and in contact with thefemale. When the egg sacs appear the maleenters the water and approaches the female's

strong unlike

two to four days after injection. In anotherday oocytes appeared in the body cavity andIn

theattaches a mucous cord to the stone with a
one to eightpair of egg sacs each containing
intosix
fiveareTheeggseggs.
diameter. The mucous capsule is thick andThevent with his snout. In this position themale's body begins to undulate. When themale nudges the egg sac with his snout thiscauses a burst of excited thrashing from side
to side by his snout. This dislodges the egg
The male moves
sac from the female.
immediately over the egg sac with his legs
extended and grasps the egg sac with his

forelimbs, positioning it between hishindlimbs. The male then grasps the egg
sac with the hindlimbs and pulls the base ofthe sac against his vent and deposits thespermatophore (Fig. 6).

June 1995

Asiatic Herpetological Research

Vol.6, p. 118

Thesesalamanders are sparsely
distributed and do not form breeding
aggregations. Male salamanders seem toseek out females well before spawning (i.e.
15-20 days), perhaps by olfaction. TheF IG. 6.

Male Onychodactylus fischeri grasping

the egg sac with the hindlimbs in apposition withthe vent during spermatophore deposition. Note theheavy femoral musculature and skindevelopment on the posterior of the hindlimbs.
distinctive

Those individuals that are ready forbreeding emerge from hibernation later thanWe

those that are not reproductively ready.
believe that the triggering mechanism forbreeding is the elevation of the stream
temperature as can be seen in the increased
activity of reproductively ready salamanders
when the water temperature reaches 6 to 7°

C (Fig. 1).

males initiate courtship behavior at this timeand it may continue for up to 10 days thus
assuring that the male is likely to be inattendance to fertilize the eggs when thefemale spawns. This lengthy courtshipperiod is the longest known of our nativeamphibians. This pattern contrasts with thatof Mertensiella caucasica, the Caucasiansalamander, a species with a similar ecology
but different reproductive pattern from thatof O. fischeri. The Caucasian salamander
has internal fertilization that induces
ovulation. Courtship and copulation takemuch less time and the pair is together for amuch shorter time than are long-tailedsalamanders. These represent two very
different reproductive strategies for two
distantly related species living in similar
habitats.

Summary
Our studies have demonstrated thatAt this time females with open
When watercloacas begin to appear.
temperatures have reached 8° C mostfemales have opened cloacas and many haveoocytes in the body cavity. At 9° C watertemperature some females have oocytes in

reproduction in O. fischeri is triggered bywarming water temperatures in the spring.
Pair formation begins at 7°C and spawningat 9°C water temperature. Fertilization isexternal. The development of distinctive

By the time water temperatureand holding the eggs during fertilization.

the oviducts.

reaches 10° C most females have oocytes inthe oviducts and some are beginning tospawn (Fig. 3). We believe increasing
temperature is the primary triggering
mechanism for reproductive readiness,courtship behavior and spawning.

We found very few post reproductive
females on the surface (n=3 in 1990; n=5 in1991). Very few males were observed on
the surface with their legs extended in thereproductive posture. Spawning activity
coincided with the period of optimum

temperature for activity and low waterlevels. Salamanders generally remain near
the area of spawning until the next
reproductive season.

femoral musculature and skin is for grasping
Pairs of salamander experimentally injectedwith a synthetic analogue of gonadotropin
releasing hormone exhibited typical matingbehavior and produced fertile clutches ofeggs.

June 1995

Asiatic Herpetological Research

Literature Cited

A KIT A,Y.

1989.
Breeding cycle of
Onychodactylus japonicus on Mt. Hodatsu, withspecial reference to biannual spawning. Pp. 305 In

Proceedingsof

Herpetological

theSecond Japan-China
Symposium, Kyoto, Japan,

Herpetological Society of Japan.

EMELIYANO A. A.

1947.

[On the biology of thelong-tailed salamander]. Zoologichesky
56(1): 65-70. (In Russian).

HAYASE, N. AND K. OSEKI.

Zhumal1983. [Spawning andembryology of the salamander Onychodactylus
japonicus (Houttuyn). Collect, and Breed 45(3): 122123. (In Japanese).

KOZIK, S. S.
tailed1991. [The discovery of the longsalamander clutch]. Zoologichesky Zhurnal

70(5): 159-160.

(In Russian).

REGEL, E. D. AND S. M. EPSHTEIN.

1975.

[Some peculiarities of the long-tailed salamander
biology]. Zoologichesky Zhumal 54(10): 15151524.

(In Russian).

Vol. 6, p. 119