I

Asiatic Herpetological Research

June 1995

Vol. 6, pp. 53-61

Ecology and Conservation of Onychodactylus fischeri (Caudata, Hynobiidae)
in the Russian Far EastPaul C. Griffin And Vasili A. Solkin 2
1

1

Department of Forestry and Natural Resource Management, University of California at Berkeley, Berkeley,
California, 94720, USA^Pacific Institute of Geography, Far East Branch of Russian Academy of Sciences, Vladivostok, 690032,

RussiaAbstract. -Onychodactylus fischeri (Boulenger, 1886) is a lungless salamander with a larval development
time of over four years and lifespan that may extend over 18 years. O. fischeri develops and spawns only incold torrential brooks. In the Russian Primorski Krai of the Russian Far East O. fischeri lives in undisturbed
Ussuriland montane taiga forest. Adults migrate annually to breed. In homing experiments adults which wereready for breeding migrated over 800m of land to breeding sites. Homing experiments showed that sexuallymature adults may demonstrate stream fidelity. Males were more frequently encountered at surface waters thanfemales. There are seasonal peaks to breeding-adult activity. High-impact forest harvesting is now typical in
headwater forests and river valleys across the range of 0. fischeri, causing disturbance and siltation in

spawning brooks and surrounding forest habitat. Pinus koreansis trees comprised a dominant component of
the forest canopy in spawning drainages.

Key Words: Amphibia, Caudata, Hynobiidae, Onychodactylus fischeri, Russian Far East, Ussuri taiga,
conservation, ecology.

Introduction
This study set out to discover aspects of

Onychodactylus

fischeribiology bycollecting standardized morphological andcolor pattern data during the course of adultand juvenile mark-recapture surveys, bydocumenting microhabitat location, bydetermining ages of adults and larvae, bymoving marked sets of salamanders andrecording their return to home brooks, andby continuing early attempts at inducing
captive breeding, and to assess movement of

individuals between spawning streams.
Ussuri taiga has been heavily harvested

from plains and river valleys in this century
to the point that headwaters comprise someof the least disturbed examples of this forest
type.
High-impact, wasteful forest
harvesting is now occurring in theelevational range of O. fischeri range in an
inefficient manner, causing catastrophic

disturbance and siltation to its spawning
brooks and surrounding forest habitat. O.
fischeri is an endangered species in the Red
Data Book of the USSR but is afforded noprotection

undercurrent

Russianenvironmental law.

FIG. 1.

Map of Asia and the Russian Far East

showing study location in boxed area.

© 1995 by Asiatic Herpetological ResearchVol. 6, p. 54

Asiatic Herpetological Research

June 1995

FIG. 2. Dorsal Color Patterns of 0. fisc fieri.. Percent frequencies out of 351 salamanders in "Chinese"brook were: A, 1%; B and B2, 36.4%; C, 46.7%;D, 5%; F, 4.8%; L, 0.3%

Methods and Materials
Our studies were within the range of
Onychodactylus fischeri in the Sixote-Alin
Mountain Range of the Primorskii Krai,
Russia. These mountains are forested byUsuriland taiga.

We conducted our surveys

and experiments at elevations between 500
m and 1000 m., at a site 10 km west of the
Pacific Ocean in headwater brooks of the
Mysovka River (Lat. 135°, Long. 41°).
This river flows into the Tinfura River, atributary of the Ol'ga Bay (Fig. 1). Climate
is typical of the maritime Russian Far East,

Vol. 6, p. 55

Asiatic Herpetological Research

June 1995

with humid summer days averaging 25° C in
July and cold winters down to -30° C. The
summer monsoon and winter snows provide

approximately

120

cm

of

annualprecipitation (Fullard, 1972).

We surveyed the brook tributaries at the
headwaters of the upper Mysovka watershed
and gave them the following arbitrary
names: "Chinese," "Zapovednik," "Mutnii,""Himalayan," "Burned," and "Tetkin." We
characterized the forest canopy cover in theentire study site in terms of dominant tree
species and also inventoried subdominant
trees of the forest canopy in "Chinese"drainage. In 1993 we noted changes in soil
and forest structure that resulted from forest

FIG. 3. Timber harvest operations in the Mysovka
floodplain downstream from the study site.

harvest activity taking place in the Mysovka

skeletochronological analysis (Smirina,

watershed.

1972).

To estimate the sex ratio and age structure ina breeding population we marked and

To examine stream fidelity we released
20 breeding adults from "Zapovednik"
brook into "Chinese" brook in 1991. We
released 100 salamanders with a range of
secondary sexual characters from
"Zapovednik" brook into "Burned" brook.
In 1992 we released 31 breeding males, 43
breeding females, and 52 non-breeding"Chinese" brook into
adults from
"Zapovednik" brook. We searched formarked individuals in "Zapovednik" and"Burned" brooks on nights when we wererecorded data from all individuals
encountered in a one kilometer stream
transect of "Chinese" brook, divided into 20
sections, during measurements from 1990 to
1993. Between one and three people withheadlamps walked the transect once every
night for a two to three hour observation
period in June 1990, May and June 1991,
September 7-14, 1991, and June 3-13 1993.
We began each transect at a downstream
gauging station where we measured relative
humidity, brook depth and temperature.

Each individual yielded data forbiotope, transect section, fat condition, skintail

In 1993

thefollowing categories: sex, maturity class,pattern,

not surveying the "Chinese" brook transect.

wounds, and morphometriclengths for snout-vent, tail, head length andcourtship, egg-laying and
Their aquaria were plastic,
with rocks, moss, and 3 to 5 cm of standing
water. Air and water temperature in theaquaria were dependent on ambient stream
toinduceWe distinguished adult sex andfertilization.

reproductive stage by the secondary sexual
characters discussed in Serbinova andSolkin (1992).
assigned salamanders
unique identification numbers by toe-temperature.

head width.

Weclipping, and reclipped regenerating toes
only when we were sure of the original
mark.
designated the color pattern for

we collected three males andfemales that were ready for breeding from
"Chinese" brook. We injected synthetic
leutenizing and releasing hormone into themResultsWe

individuals according to our categorizationof light-colored spot placement on the neck,back and tail (Fig. 2). To determine exact
ages for some individual salamanders wesent a random subset of 118 clipped adultand larval toe bones

toMoscowfor

Onychodactylus fischeri spawn in "Mutnii","Zapovednik", "Himalayan", and "Chinese""Chinese" brook flows over a
brooks.
substrate of 1.5 meter deep rock cobble
which is covered by moss and shallow
rooted plant growth. "Zapovednik" brookhas much less rock cobble, with smoothVol. 6, p. 56

45

Asiatic Herpetological Research

June 1995

Number of individuals caught

40
35

30 -|
25

|

d 20
15

10
5

Oi

100
95
>>

I

40

50

60

40

50

60

T

?

a
'

T

70

80

Daily Relative

90

%

85

E

80 -

-

3 75
u 70

X
OS

65

60
55

>

-r'r-ii

1020——————

—

t—

i

i

30

i

i

i

i

|

70

80

count day
12
1 1

-

Daily Water Temperature

10 a.

9-

E

8

t 7S 6£ 54 3

i—

I

10

20

30

May

—i—i—r—i—I—

40

50

<—r-

60

70

June

80

September

FIG. 4. Daily number of salamanders captured, relative humidity and stream temperature in "Chinese" brookduring May, June and September 1991.

bedrock as the substrate for some sections.
In the study area predaceous fish only

fischeri does occur.

in "Burned" and "Tetkin"whichwere both affected by adrainages,
forest canopy-removing wildfire 40 years
ago and by ensuing landslides.

strongoccurredkoreansis

accounts for aofthedominant
significant portion
canopycover in the brook drainages where O.

slope

effect;Manchurian oak(Quercus mongolica ) and P. koreansis
dominate the southeast-facing slope while P.
koreansis, fir {Abies sp.), birches (Betula

maples (Acer spp.), elms (Ulmus
and linden (J ilia spp.) comprised
much of the canopy of the north-facingspp.),

Pinus

Dominant forest trees

in the drainage of "Chinese" brook reflects aspp.),

slope.

Asiatic Herpetological Research

June 1995"i

Individuals Caught in Water

Vol. 6, p. 57

outlawing harvest of that
Other harvested species included
Abies sp., Tilia sp. and Populus tremula.
The river channel was widened in 1992,
apparently as a subsequent outcome of
regulations

SO ?

S

60

3

40

species.

20

50

60

70

90

80

100

harvest activities.

Rel Humiditv"*

We first encountered breeding adults at

u "1 Individuals
caught ai water edge

spawning brooks during snowmelt in late
April and early May. Adult males captured
in surface waters outnumbered adult females
in all seasons. Breeding adult activity was
highest in May and June, when stream
temperatures were low (Serbinova andIn September 1991 theSolkin, 1992).

35 -

30
25

§20

5 15
10
5

40

50

60

70

80

90

Rel Humidity-ibreeding population rose during a small
peak composed of adults aged 6 to 9 years;
at that time 1 1 out of 20 males and 5 out of 9
females exhibited secondary sexual
characters and juveniles represented 45.3

Individuals caught in waterfall splash zone

6 -

%

2

-

of all captures.
50

60

70

80

90

100

Rel Humiditv

60 .

fischeri in pools and riffles, on dry and wet
rocks in the watercourse, on rocks in the
misty zone near waterfalls, and on the

Individuals caught on land

50 -

S 40
o 30 -

shore.

°20-

40

50

60

70

80

90

100

Rel Humidity

FIG. 5.

Around spawning brooks we found O.

Histograms divided according to ten-percent atmospheric relative humidity classes
showing number of salamander captures in water,water edge, splash zone and land biotopes. Note thatfew salamanders were active on land when relative
humidity was below 90%.

A six man work team from the local
forest production ministry harvested timber

downstream in 1993 with one tank- treaded
bulldozer and one rubber-tired loader
servicing a logging truck (Fig. 3). Theirroad building often crossed the small river inthe floodplain. The bulldozer skidded logs
down slopes of greater than 35 degrees.
There was severe disturbance to soil
structure caused by these activities. Soils
were brown podbels with an illuvial B
horizons ending less than 50 cm below thePinus
litter surface (Ivanov, 1976).
koreansis was being harvested from theriver plain and hills despite current

Salamanders were most active at thesurface during evenings of high relative
humidity (Fig. 4). 535 captures provided
founddata for biotope location.
salamanders most often in the water (54.0ofof total) and on the stream bank (16.4

We

%

%

On nights of low relative humidity
salamanders were often located on rocks inthe misty splash zone near waterfalls (6.0of total). On land salamanders were mostofoften within 50 cm of the water (11.3
total).

%%

Salamanders were rarely active on
total).
land if relative humidity was lower than 90
percent (Fig. 5). Juveniles were active onland markedly less than adults. In the brookchannel we uncovered 1 gravid female when
we dismantled a 0.5 cubic meter rock matrix
where brook water seeped through mosscovered rocks. We occasionally observed
O. fischeri on land between streams and on
ridges during times of rainfall and highrelative humidity.

We found abundant larvae in surface
waters during nocturnal transect surveys.
Larvae were also active diurnally. During
two one-hour periods in June 1993 weobserved Onychodactylus fischeri larvae

Vol. 6, p. 58

Asiatic Herpetological Research

95% Confidence Bands for Tail to Snout-vent Allometry

June 1995

Distribution of Captured Male Age. 1993

10

Males

!

Females

6-

u

4 -

jfh.
!5

5

7.5

15

It)

20

17 5

Distribution of Captured Female Age. 1991

50

55

60

65

70

75

80

85

90 95 100

Lsv

FIG. 6. Allometric relationship showing relatively
longer tail size (L cd) in adult males at given snoutvent length (L sv). The difference in the slopes issignificant

6

-

i

-

(ANCOVA; F = 18.21; df = 1; p <

xp.
2.5

5

,

10

7 5

0.0001).

15

m n
,

,

17 5

,

20

22.5

Age

hunting on flat rocks under 3 cm of water inthe late afternoon. By means of their limbs
the larvae locomoted to approach aquatic

Gammarid casings and lunged when the
invertebrates exposed their legs and head.

Itappeared that larvae used their forelimbs inconjunction with a gape-and-suck feeding
technique to apprehend the prey.

The number of transect captures was anindex of active adult population size,
generally decreasing over the course of thesummer except for a small increase in early
fall.

12 5

Analysis of our mark-recapture data by

the Jolly-Seber stochastic method (Donnely

and Guyer, 1994) yielded standard errors
too large for individual population estimatesof males, females, and juveniles.

FIG. 7. Histogram showing relative abundance ofages in a subset of captured males and females.

designation of color pattern 351 individuals
in "Chinese" brook, the dominant patternsof bright flecking on grey to brownof total) and B
backgrounds were C (46.7(36.4% of total).

%

Our data on age and development times
support the hypothesis that Onychodactylus
fischeri is a slow developing, long-lived
salamander. Cross sections of larval bones
indicate that larvae may develop up to four
years before metamorphosis to terrestrial
juveniles. The mean age of breeding males
in 1991 was 8.65 years (Std Dev. 2.87);
mean breeding female age was 8.75 years

Maximum ages were at(Std. Dev. 2.34)
least 16 years for males, and 18 years for.

Males had significantly longer tails than
did females once the effect of snout to ventlength was accounted for (ANCOVA; F =8.99; df = 1; P - 0.003). Also, tail length
increased more rapidly with body size inmales than in females (ANCOVA; F =18.21; df =p < 0.0001) (Fig. 6). We
observed tail wounds on 23 out of 350
males and 19 out of 166 females.
It
that
in
females"Chinese"brookappeared
had a thinner fat layer than females in"Mutnii" brook, where the brook substrate
includes more bedrock. According to our
1;females (Fig. 7). Ages approximated bycounting winter rings may underestimate
true age because of endosteal resorption(Leclair 1990).

In

1991

at

"Zapovednik" brook werecaptured one of the 20 salamanders that
we had taken from there for release into

"Chinese" brook; we recaptured none of
In 1991 wethese in "Chinese" brook.
salamanders
none
of
the
100
recaptured
which we had released into "Burned" brook
We alsofrom "Zapovednik" brook.

June 1995

Asiatic Herpetological ResearchVol. 6, p. 59

FIG. 9. Onychodactylus fischeri male grasps andfertilizes egg sacs with hind limbs.

reproduction

and development.

Theseasonal activity pattern which we observed

FIG. 8. Onychodactylus fischeri female lays eggs
in two gelatinous sacs.

inadults seems limited by watertemperatures over 10° C. The burst of
breeding activity observable in late spring
may signify the most strategic time for egglaying in view of the short warm season in
the Russian Far East; it is logical thateggs
laid in the late spring develop faster thanrecaptured none of these in their original
stream. In 1992 at "Chinese" brook werecaptured 8 of 31 breeding males, 15 of 43
breeding females and none of the 52 nonbreeding adults out of the total 126
salamanders which we moved in 1991 from
"Chinese" brook to "Zapovednik" brook.

in early fall because watertemperatures drop below 5° C in the winter.
The higher proportion of males caught inour surveys suggests that males may wait on
the surface rocks and waters to seek
females. Egg sacs and larvae seem to be

The breeding adults which we caught had

located most often in intersticial rock habitat,

returned within a month to "Chinese" brookover 1 km of land or by a longer route along

sheltered from surface predators in areas ofcontinuous water flow (Regel and Epshtein,1975). Iwasawa and Kira observed that O.
japonicus eggs developed slowly for 143
days in water of 10° C (1980). Longer
winters may cause the larval stage in O.
fischeri occasionally to extend longer than
the three years observed in O. japonicus

the Mysovka river.

Hormoneininjection
captives
inducedsuccessfully
courtship, egg-laying
(Fig.

8)

and fertilization(Fig. 9).

One

female produced a clutch of two egg sacs in
1993. Eggs were 6 to 8
in diameter,with 5-10 eggs in each sac. We observed
deflation of female cloacal labia in the six
days after egg-laying. Egg death probably
resulted from a severe rise in pH of available

mmwater.

Discussion
Onychodactylus fischeri is limited by theavailability of suitable torrential streams for

eggs laid(Hayase and Yamane 1982).

Lunglessness is a synapomorphy ofsalamanders in the Onychodactylus clade,which have a long larval period in torrential
streams as a requisite portion of their
ontology. Bruce et al. (1992) supported the
hypothesis that lunglessness in amphibians
is a larval
adaptation to torrential streams byshowing that experimentally lunglesssalamander larvae were displaced

Vol. 6, p. 60

Asiatic Herpetological Researchdownstream less when released in

fast-

flowing water than were control larvae withlungs.

June 1995

of seasonal employment in fur,mushroom, honey, berry, ginseng, andgame meat gathering and preparation(Schumacher, 1973). The best conservation
loss

The reproductive potential of anindividual Onychodactylus fischeri seems

strategy for Onychodactylus fischeri appears
to be exclusion of high-impact timber

low, despite their long lifespan, consideringthat a female living 12 years may only
produce 140 eggs. Additionally, many of
the adults we found did not have secondary
sexual traits indicative of reproduction.
Akita (1989) notes that not all adult O.
japonicus breed every year. The low clutch

harvest activity from key spawning
watersheds, given that regional timber
harvesters, Hyundai and other multinationaltimber interests generally ignore existing
rules of the Russian Federation's Ministryof Forests. It would be informative tomass suggest that eachto assess the adequacy of existing preserves.

size and large egg

delineate metapopulation boundaries in order

egg is a significant reproductive investment
relative to other hynobiids.

Kuzmin showedthat the sympatric hynobiid Salamandrella

keyserlingii is more general in its feeding
and breeding habitat preferences (1990).

Our 1992 experiments suggest thathoming was only by adults

successfulwhich were ready for breeding, indicatingthat adults may have a preference for
It is also
particular spawning brooks.
possible that non-breeding adults may also
have returned to their original brooks andnot been recaptured, or that the breeding
adults that did not return may have spawned
in a different stream.

Onychodactylus

Onychodactylus fischeri is an indicatorspecies of high-quality old growth forest
habitat in upper slopes of Ussuri taiga.
Because eggs and larvae develop in coldrunning water year round under the cover ofrocks, undisturbed stream substrate and a
specific hydrological regime are critical for
quality spawning habitat.
Long-term

stream hydrology, which isneeded to support O. fischeri breeding anddevelopment, is dependent on undisturbed
complex forest structure. Shade and large
woody debris affect stream temperature andriffle-pool ratio. Extensive root systems
retain soil structure and decaying logs on thestability ofWe speculate that theforest floor regulate soil moisture. The deeproots of conifers provide more soil stability

connectedness of suitable habitat between
large watersheds is important for dispersal

on slopes than shallow-rooted deciduous
Acid soils locally associated withtrees.

after landscape level disturbances.

Pinus koreansis litter may regulate stream
pH and nutrient availability. We observed

fischerimay

migrate over land throughforested corridors.

The pressure to harvest trees

in thefragile taiga is promoted by an international

wood and fiber market that devalues natural
capital by not factoring in negative
externalities such as anthropogenic fire,landslides and species loss.
Repeatedhighgrading is the most widespread harvest
method in the Russian Far East and haslasting effects on forest ecology. Forested
slopes and floodplains are exposed tocatastrophic erosion for years after tractors
are used to skid out widely spaced trees.
Reduction of canopy cover to levels to
below 40% alters the evapotranspiration
regime in a way which allows catastrophic

The hard currency that goes to the
Primorskii krai in return for the Ussuri taigalogs does not compensate for the permanent

wildfire.

that catastrophic disturbance tospawningbrooks occurred through natural processesof wildfire and landslides and throughanthropogenic road building and logging in
the watercourse, upslope, and downstream.
Tree harvest on slopes above watercourses
causes stream sedimentation of finematerials and organics.
Such increased
sediment loads associated with logging havenegative effects on aquatic amphibians(Corn and Bury, 1989). As is the case on"Burned" creek, siltation eliminates thespaces between rocks which are critical foregg deposition and larval development.
Disturbed brooks may be suitable to O.
fischeri spawning only after adequate forest
structure regenerates and interstitial spaces
filled with silt and sand are cleared.

June 1995

Asiatic Herpetological Research

HAYASE, N. AND S. YAMANE.

Acknowledgments
The authors would like to thankVladimir Aramilev for his invaluableassistance in Vladivostok and in the field;
Dmitri Pikunov for support from theLaboratory of Wild Animals of the Pacific
Institute of Geography; Irina Olenicheva forher assistance with theVol. 6, p. 61

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Salamander, Onychodactylus japonicus (Houttuyn),
at Mts. Tsukuba, Ibaraki,
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IVANOV, G. I. 1976.
south of the Far East],

Formations[Soilin theMoscow. Science.

200

pages. (In Russian).

skeletochronologicalwork; and David Wake and Mario GarciaParis for their constructive criticism of themanuscript.

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Y.
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Breeding Cycle of
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