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HERPETOLOGICAL
NATURAL HISTORY
VOL.9 2002 NO.
I
Herpetological l{atLtal Histort',
9(
I ), 2002,
pages
1-14.
02002 by La Sierra University
A REVIEW OF 30
YEARS
OF ECOLOGICAL RESEARCH
ON THE SHEDAO PITVIPER, GLOYDIUS SHEDAOENSIS
Richard Shine
Biological Sciences
A08,
University of Sydney, NSW 2006, Australia
Email: rics @ bio.usyd.edu.au
Li-Xin Sun
Snake
lsland Natural Protection District, Lushun, People's Republic of China
ErmiZhao
Chengdu
Institute of Biology, The Chinese Academy of Sciences.
Chengdu 610041. People's Republic of China
Email: zhaoermi@mail.sc.cninfo.nel
Xavier Bonnet
Conseil G6n6ral
Des Deux
Sdvres, CEBC, CNRS,
79360 Villiers en Bois, France
Email:
bonnet@cebc.cnrs.fr
Abstract. Although it remains virtually unknown to western
scientists, an insular
population
of pitvipers
in
northeastern
China
has attracted intensive study for > 30 yr. The small (< I km2) island of Shedao lies on a
migratory
pathway
for passerines.
and the regular spring and autumn migrations of these birds support a
remarkably dense
population
of endemic
pitvipers
(Glot'diu"
shedaoensis).
Adult pitvipers
of both sexes
average 60-70 cm snout-vent length and
prey
almost entirely on birds. Juvenile snakes
feed less
often than
adults, and consume invertebrates as well as birds. Reproductive output
is high,
perhaps
because the assured
food supply after
parturition
each
year
minimizes energy-based
"survival costs of reproduction." OfTspring
size is large,
presumably
as an adaptation to the paucity of small prey items on the island. The snakes
ambush birds from trees and shrubs as well as
from the ground;
arboreal ambush sites are
more frequent in
juveniles
than adults. Snakes are
inactive for most
of the
year
apart
from brief (6-wk) periods
of bird migra-
tion in spring and autumn. Even in peak periods,
only one-third of snakes are active each day. The snakes
display
high philopatry
and high energy-assimilation efficiency. Research on G. shedaoensis has stimulat-
ed major conservation
initiatives
to eliminate
illegal collecting, reduce fire frequency, increase water avail-
ability,
reduce
the
numbers
ofintroduced
weeds and rats, revegetate areas affected by landslides, and some-
times directly supplement
food
supplies
for the snakes.
Since
these management strategies commenced. the
numbers of pitvipers
have increased
substantially
and the age structure of the
population
has shifted.
Key Words. China: Conservation:
Foraging;
Gloydius
shedaoensis; Reproduction; Viperidae.
Studies
of snake ecology have increased dra-
matically in number over recent decades
(Shine
and
Bonnet 2000). Although this increase has involved
an expansion ofthe geographic
and taxonomic range
of study,
most research has continued to focus on a
relatively small number of taxa in a relatively small
proportion of the world. For example, North
American
garter
snakes
(Thamnophis
spp.) and rat-
tlesnakes
(Crotalus spp.) and European vipers
(Vipera
spp.) continue to be the subjects of a high
proportion
of all studies. Thus, much of the expan-
sion ofresearch on snake ecolosv has involved more
work on already-studied
taxa and
areas. Based
on the
contents
of recent issues
of hetpetological
or ecolog-
ical
journals,
or reviews
of snake
ecology
(Seigel
and
Collins 1993),
one could imagine
that there
have
been virtually no detailed studies
on the
ecology of
the snake fauna
over large
parts
of the
world.
This
apparent neglect
may tell us as much
about
the lack of communication
between
scientists
writ-
ing in diff'erent
languages.
as about
the actual
distri-
bution of research
eflbrt. In this
paper
we review
the
results
of a prolonged
and arnbitious research pro-
gram on the
pitviper
Glot'dius shedaoensis
(Fig. l),
a program
arguably rivaling even Henry S. Fitch's
herculean
eftbfts
(Fitch 1999) in some respects.
The
Shedao research
program
is surely
one of the most
Figure l. The Shedao
pitviper.
Gloydiu.s shetluoensis. in a typical arbo-
real
fbraging
pose.
Herpetological Natural History,
Vol. 9(1),
2002
ambitious conservation-oriented
ecological
studies
ever conducted
on snakes. Remarkably,
the species
involved
is one that most
professional
herpetologists
have
never
even heard of, let alone seen. Because
it
occurs in China. and most
publications
about it are
in
Chinese-language
journals,
the research
carried
out
on this taxon has
attracted very little attention
fiom
researchers
who publish in western-language
(English,
French,
etc.)
journals.
In an attempt
to bring the Chinese research
to
the attention
of western
scientists,
we review major
results
of studies
on this system.
This is not a
straightfbrward
task. Previous
English-language
publications
on this system
(Huang
1989;
Li 1995)
generally
provide conclusions
but not actual data
nor statistical
analyses.
For the raw
data, we have
gone
to the
original
pub-
lications. In cases where sufficient
detail
is available.
we have
carried out
statistical
tests
on appropriate
hypothe-
ses
(all such
tests in this paper
are our
own, rather than reporting of prior
analyses). Most of the Chinese
papers
do not include
such
tests, and often
they
provide only average values (albeit,
ofien with accompanying
SDs). It was
not always f-easible
to retrieve
original
data because numerous
workers have
been involved, many
of whom are now
retired or deceased. We also mention
major results
that were
simply reported
as conclusions
in the original studies.
Because
Chinese workers
have
tended
to measure
traits
other than those
tradi-
tionally quantified
by western
workers
(again
reflecting
the lack
ofinternation-
al communication),
we supplement
this
review with original data fiom our
recent
collaborative
studies.
MATERIALS AND METHODS
Study Area
Shedao
(literally,
"snake
island")
lies approximately
l3 km (7 nautical
miles) off the coast of the Liaodong
Peninsula
in northeastern
China. in the
Bohai
Sea
(38"57'N,
120"59'E). The
island
is 0.73 km2 in overall size.
and is
very steep-sided. The highest
peak
on
the island
is 215 m above sea level.
L)
EESFg€€.qu"sia
EEgEgi€aB8tE
Shine et al.-Ecology of Gloydius shedaoensis
Figure 2. Weather
records from Shedao, based
on a
meteorological
station
set up on the island. The
-eraphs
show mean
minima and maxinta
(upper
graph)
and mean
values
and standard deviations tbr daily records
(lower
graph)
over
the
years
1.990 91.
Several ephemeral watercourses
run in shallow val-
leys
on the southeastern
side of the island,
but there
is no permanent
water
except for that provided
by
human
activities
(see
below). The island is fbrmed
by sedimentary rocks
that have been
deeply fblded
and fractured, creating
many crevices
that provide
retreat sites for snakes. The island
was fbrrned
by
uplift about one million years ago, but was con-
nected
to the mainland
(Liaodong
Peninsula) inter-
mittently during Pleistocene
sea-level f-luctuations
(Li 1993: Zhao
1980).
The climate on Shedao is highly seasonal, with
an annual mean
temperature of about 10"C. Winters
are severely
cold. During the snakes' main activity
periods
(May and
September). air temperature
typi-
cally ranges from l0-20"C (Fig. 2). Rain falls pri-
marily in summer
(June-August).
The island
is fie-
quently
exposed
to strong winds,
typically fiom the
southeast from March-July but switching to the
north
in September. Despite
its small size,
cool cli-
mate
and
lack
of standing water,
the island supports
209 species
of plants.
Except for very steep areas,
most pafis of the island are covered by shrubs
or
trees. The species comprise plants typical of
Northern
China.
Surveys
have
revealed 143 invene-
brate taxa on Shedao,
primarily afihropods. Apart
fiom Shedao
pitvipers.
the only vertebrates
living
permanently
on the island are
one
microchiropteran
bat (Pipistrelltr.s
ubranttts'), the introduced
brown rat
(Rtrttus
rnn,egicus),
and seabirds
(blacktailed gull
Lanrs c'rassircstris'.
Chinese egret Egrctta eulo-
p
ltot e s
; noft hern
white-rumped sw ift A
p
Lr s
1t
uc ifi r: u s
).
Each
yeerr
the island is visited
by large numbers
of migratory
birds (at least
84 species total, -50 of
them
passerines:
Snake
Island
Survey Team 1973,
1974.
1976; Shine et al. unpubl. data). The migra-
tion
occurs in two discrete
seasons. in spring
(rnid-
April to the end of May) and autumn
(late
August
until the end of October). Most of these transient
birds probably
remain on the island
lbr only a few
days
(Snake
Island
Survey
Tearn
1974. 1976). The
peak
of the bird-migration periods
occurs
befbre
(in
spring)
and after
(in autumn) the major snake-acriv-
ity periods,
presumably
because thermal
conditions
restrict
snake lbraging more
than bird rnigration.
History of Ecological Research
Although
the island and its snakes must have
been known to local people
(fishermen
fiequently
visit
the island in small
boats in calm weather),
the
first scientiflc reports
of the extraordinary
density
of pitvipers on Shedao date from the Japanese
occupation
of Manchuria
(Hasegawa
1932; Koba
1933, 1938; Mori 1932).
Although
based on only a
single day's data
collection on the island,
Koba's
1938 paper provides
a
long
(20-page),
detailed. and
well-illustrated
account on topics such as the
snakes' morphology,
diet, and feeding
behavior.
Chinese scientists
began significant research
on Shedao
in the 1950s,
although most
papers
were
brief
and many were semi-popular
(Wu 1957, 1958,
l96l). The
initial stimulus tbr the work was
scien-
tific curiosity
but with increasing
understanding
of
this remarkable
system the emphasis
began to shifi
towards research
on conservation
issues.
Several
major papers
were published
in the 1970s
under
collective authorship
of the "Snake
Island
Survey
Team," including
a semi-popular synthesis
of major
results rn 1976. The research was broadly-based.
and included extensive
surveys and
analysis of the
island's
flora and fauna, not
simply the snakes
(e.g.,
Huang 1979).
For example, avian migration pat-
terns attracted
detailed
study.
Taxonomy
Early publications refer to the snake as
Agkistrodon
halys,but Zhao described it as a sepa-
rate
species ln 1919
(Zhao 1919')
based on morpho-
logical traits.
Zhao recognized
two disjunct
popula-
tions of Agkistrodon
shedaoensis,
one on Shedao
Island and one in mountainous
areas
of the main-
land (Quianshan
Mountain. 90 km S Shenyang;
Long-panshan
Mountain.
100
km N Dalian).
A sub-
sequent
paper
by Zhao
(1980)
examined
the taxo-
nomic distinctiveness
of the island
snakes in much
more detail using a wide array of data including
electrophoretic
analysis
of venoms, venom
toxicity,
immunodiffusion, and scalation
counts (see also
Chen et al. 1984). Zhao
(1980)
also
interprered
the
biogeographic
history of the taxon. The distinctive-
ness
of G. shedaoensi.r was
further demonstrated
by
Jiang and Zhao (1980), who compared G.
sltedaoensis
with mainland pitvipers in terms of
ecological
traits such
as habitat
use, food habits,
daily activity cycles,
seasonal
activity
patterns,
tol-
erance
to low temperatures,
and reproductive
biolo-
gy (dates
ofparturition,
litter sizes,
ofIspring
sizes).
Since those studies.
most authorities have
treated
G. sheduoensis
as a separate
species
lsee
Literature
Cited). However,
Ji et al.
(1989)
treated
G. shedaoensl.s
as a subspecies
of G. saxatilis,
based
on similarity
of coloration
and scalation.
Electrophoresis
of 23
presumptive
loci failed
to dis-
tinguish
between
G. snxatilis
and G. shedaoensis,
although
this technique
differentiated
all other taxa
investigated
(Murphy
et al. 1993).
Genetic
studies
indicate that the two G. shedooensis populations
are very similar
to each other,
but distinct from G.
saxatilis
(Shan
et al. 1993). The
overall
conclusion
fiom this work seems
to be that G. shetlaoensis is
indeed a distinctive taxon,
albeit
closely related
to
G. saxatilis.
Recent changes
to the
understanding
of
higher-level phylogenetic
relationships
within
pitvipers have led to division of "Agkistrodon,"
with the Asian species now allocated
to Clol'dius
(Gloyd
and
Conant 1990:
Parkinson
et al. 1997).
RESULTS AND DISCUSSION
Venom Composition, Toxicity, and Yield
The venom of G. shedaoensis
contains ncr
detectable
neurotoxins.
and hence is less toxic tnan
Herpetological Natural History, Vol. 9(1), 2002
the venoms
of most other Asian pitvipers (Zhang
1989;Zhang
and
Hsu 1985;Zhao
1980; Zhao
et al.
1979).
Interperitoneally
injected
LD5es in mice
aver-
aged
0.81 mg&g (Zhang
and
Hsu 198,5). In compar-
ison, LDr.,s averaged
0.38 fbr G. intermedius,
0.33-0.63
for G. ussuriensls,
0.49-0.88 tor G. bret'i-
cattdus,
and 0.83 for G. saxcttilis
(Zhang
and Hsu
1985).
A more recent
study supports
most of these
conclusions
(Chen et al. 1992).
Chinese scientists
envenomated
by G. shedaoensis
have developed
massive local
swelling
but few or no systemic symp-
toms
(LS,
pers.
obs.).
Hospitalization
for up to 2 mo
can occur
afier a very severe bite (LS,
pers.
obs.).
Fangs
of adult
G. shedaoensis
average 7.1 mm
in length (range:
4.5-10.0 mm) and rhe venom
gland
weighs
an average
of 163 mg (50-3
l0 mg:
Wu 1.977a). A single bite
yields
approximarely
96.5
mg of venom
(21
.5-156.6 mg). A snake
requires
about 10-15
d to fully replenish its venom supply
after emptying
the
glands
(Wu 1977a).
Morphology
Gloydius shedaoensis is a relatively large
species, with a maximum recorded
body length of
99 cm (Li 1995).
Adults average about
60-70 cm
total length.
compared to < 60 cm for most other
Chinese species
of Gloydius
(Zhao
1980).
General
body shape is similar
to that of congeneric
taxa
(Gloyd and Conant 1990). The dorsal scales
are
strongly keeled,
and the
overall color ofthe dorsum
ranges from dark gray to pale pinkish-gray.
Irregular light-colored
blotches break up the ani-
mal's outline.
such that
the snakes are
well camou-
flaged.
both in arboreal
and terestrial situations.
Early studies provided
data from dissection of
snakes to quantify relative masses of medicinally
important components
of the body such as fat
stores,
gall bladders
and
venom glands,
as well as
the gonads (Wu 1911a).
This work documenred
higher fat reserves in adult females
than in adult
males
(Wu 1977a). Li (1995)
provided
an English-
language
review of scalation.
body size, color and
skeletal
morphology.
Males and females attain similar adult body
sizes
(Table
l). Analysis
of our own data on SVLs
of adult
snakes confirms
that mean
adult body sizes
are very similar in the two sexes
(unpaired
/1a.3
=
1.11,
P = 0.25). Body sizes
at maturity are known
with confidence only for females; the smallest
f'emale
of 79 animals recorded
to give birth was
5ul
cm long
(Sun
et al.2002).
Shine et al.-Ecology of Gloydius shedaoensis
TABLE 1. Body sizes and sexual size dimorphism of Shedao
pitvipers,
Gloydius shedaoensis. Table shows values tbr
total body length,
except that the last row shows snout-vent
length
and
is based only on adult snakes
(estimated
at
> 50
cm SVL). All measurements in cm.
Males Females Reference
range mean (SD) range mean (SD)
9 48.0-78.4
87 61.2-82.0
19 53.3-73.0
4t 54.5-80.0
64 51.0-69.0
64.4
70.2
59.8
(4.5)
69.7-84.0
60.0-79.0
50.4-78.2
5t.2-76.1
50.0-74.0
69.3
68.3
60.7
(5.0)
1
78
28
4l
81
Koba
(1938)
Snake
Island
Survey
Team
(1973)
Zhao
(1980)
Ji et
al.
(1989)
Shine
et al., unpubl. data
Life History
Chinese researchers have classified snakes as
'Juvenile,"
"adult,"
or "old adult" based on body
size, color, scale
rugosity,
and the presence
and
number
of white spots on a snake's
head
and body
(Li et al. 1990;
Snake
Island
Survey
Team 1979).
These "white spots" are unpigmented scales.
Although long-term mark-recapture
programs
have
been a central feature of research on snake ecology
in western countries and in Japan (Fitch 1999;
Fukada 1992), they have not been employed in
China. Such a study has recently commenced on
Shedao, to clarify growth
trajectories and age struc-
ture of the Shedao pitviper population (Sun,
unpubl. data).
Demography has been well-studied, with sev-
eral short-term mark-recapture censuses to quantify
both absolute numbers of snakes and population
composition in terms of sex ratio and age structure.
Females
generally
outnumber
males in these counts
(53Vo
of 1638 snakes in Li et al. 1990 against a null
of 50Vo,
t = 4.52, df = l, p < 0.05). The
proportion
of the
population
composed ofjuvenile snakes has
decreased
through time because
heavy
commercial
harvesting removed many adult snakes during the
earliest
years
of study
(Huang 1990). With the ces-
sation of harvesting in 1980,
relative numbers of
adults
have increased. By comparing numbers of
offspring born to the rate of population
recovery,
Huang
(1990)
estimated an annual
survival rate for
neonatal
snakes of approximately 567c.
Seasonal Activity Patterns
The snakes hibernate through the colder
months of the year,
emerging in mid-April during
the first bird-migration
period (Huang 1989; Li et
al. 1993; Snake Island Survey Team 1914, 1916).
Juvenile snakes tend to emerge befbre adults, and
adult f'emales befbre adult males: such a pattern
is
quite unusual among snakes
(Sun et al. 1993,
2001). Even at the
peak
ofthe bird abundance, only
about one-third of snakes
in the population are
active on any
given
day
(Sun
et al. 1990). This
esti-
mate was derived by paint-marking
snakes
within
large field enclosures, followed by visual censuses
to determine the proportion of marked snakes
active at different times. During summer the snakes
are largely inactive, and remain hidden except after
rain ihowers
(Li 1995). The autumn bird-migration
period engenders a similar level of activity to the
spring migration, with the snakes disappearing to
their hibernation sites in late October. Detailed
analyses reveal subtle seasonal shifts in habitat use;
for example, the proportion
of snakes recorded in
grass
versus trees varies among months. The snakes
use both habitat types fairly equally in midsummer
(when there are no birds to eat), but tend to be
found more often in trees during the bird-migration
periods
of spring and autumn
(Snake
Island
Survey
Team l9l4; Yang 1986).
Such
shifts may, however,
reflect
seasonal biases
in observability
(due
to veg-
etation
growth in summer)
rather
than (or as well
as) actual changes in snake behavior.
Because
parturition
is highly seasonal, the age
structure of the population
shows
regular
seasonal
f-luctuations. Neonates
are most abundant
in late
autumn, soon after birth (Snake Island Survey
Team 1974).
Diel Activity Patterns
Within the main seasons of activity, the snakes
also display regular diel patterns of movement.
They typically spend the night on the
ground,
ofien
under rocks or grass.
They climb to their ambush
sites
early in the morning.
stay
there for a f'ew hours,
then retreat
to the ground
in the late mornin-e
(Sun
1990;
Shine
et al. 2002(1).
They return
to the trees
ln
the late
afternoon,
descending
at dusk.
Some
ani-
mals remain at their foraging sites
overnight,
and
others
move
about
actively
atter dark.
Home ranges
of individual snakes include an
overnight
retreat
site
(on or under
the ground)
plus
one or more foragin-9
sites.
These
are typically
close
together
(Sun 1
990). Individual snakes
usually
return
to the same fbraging
site over
long
periods
of
time. lf displaced
(even to the extent of being
removed
fiom the island
and released
in the
sea near-
by), they rapidly
return
to their
original
capture site
(Sun
1990).
Snakes displaced
500 m tiom
rheir usual
home ranges
returned
within a week
(Sun 1990).
Although
thermoregulatory
biology has
played
a central
role in the study
of snake
ecology.
it has
attracted little direct interest from Chirrese
researchers.
However,
they have noted
that diel
shifts in ambush-site
selection
(especially.
the ten-
dency
to spend
the middle
of the day
on the
ground
rather
than in the trees)
may be driven by therrnal
cues
(e.g.,
Li 199,5).
Also. the
snakes'
retreat
to deep
burows for the winter is presumably
fbrced
by the
fact that the ground
fieezes
to depths
of up to I m
(Sun 1990).
Burrows
used
during
winter
typlcally
have leaf
litter
blocking
the entrance,
thus providing
additional
insulation
against
severely
low air tern-
peratures
(Sun
1990).
Hibernating
snakes
typically
display
body
temperatures
between
2 and
5"C (Li et
al. 1993). Thermal
factors
may
also
explain
why the
snakes
do not commence
fbraging until after the
peak of the bird-migration
period
in spring.
and
cease
foraging prior to the end
of the
bird-migration
period
in autumn
(Shine
et a|.2002b').
Reproductive
Biology
Reproduction
by Shedao
pitvipers
has
attracred
substantial
study over a long period of time.
Seasonal
cycles
based
on sizes
and histological
examination
of the testes
and
ovaries were
reported
by Yang
(1983).
who int'ened
from these
data
that
most mattng occurred from August to October.
Testes
are largest
during
midsummer
(June-July:
Yang
1983).
Sperm are produced
fiom April to
July,
and testes
and epididymes
of adult
males
contain
mature
spermatozoa
tiom July-October.
Ovulatron
occurs in June, with parturition
from
late August
to
mid-October
(Sun
et al. 1993.
1994,
2002).
Most
births occur
during
September
(Sun
et al. 1993).
Herpetological Natural History, Yol. 9(l), 2002
Many papers
report litter sizes.
mostly fiom
dissections
of gravid
females
(e.g.,
Huang 1989;
Snake Island
Survey
Team
1974; Wu 1977a).
More
extensive
data came from a study in which near-
term females
were
captured
and rnaintained
in cap-
tivity until they gave
birth (Sun
et al. 1993,
199,1,
2002). Stillborn offspring are rare (5.3% ot
neonates
were
stillborn:
Sun et al. 1993).
The
pro-
portion
of reproductive
animals
in samples
of adult
females
averages
around
257c,
suggesting
a 4-yr
reproductive
cycle
(Sun
et al. l99zl).
For example,
Li et al. (1990)
reported
that72 of 323 adult-size
females
were gravid
during
summer
(23ch).
Of 64
females
with lengths
> 900 mm, only ten were
gravid (15.6'lc).
The authors
suggest
that
this may
represent
a significant
decline in reproductive
fie-
quency
with increasing
body size
(and
thus. per-
haps
with age) but
statistical
analysis
does not
sup-
port
this inf'erence
(t = 1.60,
df = I
, P = 0.25).
The
proportion of reproductive
animals may vary in
response
to year-to-year
variation
in fbod supply;
certainly,
f'emales
are in higher body condition in
some
years
than in others
(Sun
et
al. 1993. 2002).
Studies on reproductive
output show that
f'ernale
G. sheclooensl.r produce
a remarkably
heavy
litter relative to maternal
mass
and produce very
large
ofTspring
(Sun
et al. 2002).
In both respects.
they diff-er
substantially
tiom related
taxa (includ-
ing the mainland population
oI G. sheduoen.sis;Lt
pers.
comm. 2000).
The very high relative
clutch
mass
(0.80
vs. < 0.50 litter
mass
as
percent
f'emale
postpartum
body mass fbr most other pitvipers)
may reflect the fact that some
components
of the
costs
of reproduction
(post-parturition
rnortality?)
are low on Shedao. Because parturition
occurs
just
befbre the autumn bird rnigration. post-partum
f'emales
f'ace little risk of dying fi"om starvation
before
they can obtain
fbod (Sun
et al. 2002). The
large
offspring
size
on Shedao
(14
vs. < 7 g in other
Glot'dius) plausibly ref-lects
the scarcity of small
prey
on
the island. Neonatal
G. shetluoensi.l
that are
too small
to ingest
passerines
must feed
on inverte-
brates, thus enforcing strong selection
for larger
size
at birth
(Sun
et
al. 2002).
There are few published data on behavrors
associated
with reproduction,
because
courtship.
male-male combat and copulation are rarely
observed
on
the isiand
(LS.
pers.
obs.).
Copulation
can occur in both arboreal
and terrestrial
locations
(Li 1995),
and may be relatively
brief (18-min
duration:
Snake
Island
Survey Team
1974, l9l6).
Shine et al.-Ecology of Gloydius
shedaoensis
Food Habits
Adult Shedao
pitvipers
feed almost exclusive-
ly on birds. Of 8l prey items recorded
in adult
snakes by the Snake
Island
Survey
Team
(1974),80
were birds and the other
was a rat
(Rattus
uon-egi-
cas).
Analyses of stomach contents
have document-
ed predation
on 24 species of birds, all of thern
passerines
except fbr two species of quail
(Cotunti.r
cotunti.r,
Turnix tu*i). Warblers and buntings are
probably
the most important
prey groups
(Shine
1
unpubl. data). Gape-limitation
is important. with some birds
being killed but then rejected
because they are too large to
swallow (e.g..
doves). Shedao
pitvipers
are able to swallow
prey items
that
weigh as much
as the snake
itself
(Li 1995;Fig.
3). Juvenile snakes
take small
birds. but
also feed upon inver-
tebrates. Of 12
prey items fiom
juvenile snakes. seven were
birds. f
our were centipedes
(.Otostigmus
politu,s'),
and one
was an isopod (Meto1tonorthus
pruinosus'.
Snake Island Survey
Team 19711). Researchers
have
seen
pitvipers approaching
the
nests of seagulls
(presumably
to
feed on chicks), but the snakes
were attacked by the adult
birds
(LS,
pers.
obs.).
Shedao pitvipers require
3-7 d (depending
on the size of
the prey and weather condi-
tions)
1r.l fully digest their
prey
(Li et al. 1990), but they
do not
cease
foraging during this peri-
od. Some snakes
in ambush
poses contain fieshly-ingested
birds.
For example.
one sample
of adult snakes
included ten
snakes with empty
stomachs, 59
snakes with a single bird in
each,
nine snakes each contain-
ing two birds, and one with
three birds (Snake Island
SurveyTeam
1974).
Of l6juve-
nile snakes, six had empty
stomachs,
eight contained
sin-
gle prey, and two contained
two prey items each
(bird plus centipede; centipede
plus isopod: Snake
lsland Survey
Team 1974). ln other studies. the
pro-
portion of snakes containing
prey in autumn
aver-
aged about 20Vc
tn adults
and 10c/c injuveniles (Li
1995; Li et al. 1990).
Adult females typically con-
tain food more often than do adult males
(26c/o
vs.
22Vc tn Li et al. 1990). Statistical analysis
of the raw
data used
for these conclusions
reveals that the dif-
t'erence
in proportions
with tbod between
adults and
juveniles
is significant
(f =9.03.
d,f
= l. p < 0.003)
Figure 3. A Shedao
pitviper.
Cloydiu.s
.shedaoettsis, swallowing a bird,
Herpetological Natural History, Yol. 9(l), 2002
rl$u
s
Figure 4. A Shedao
pitviper,
Glol-dius shedaoensis,
in rypical
terresrrial fbraging pose.
whereas that
between males and females
is not (12
-
1.05,
df
= 1, P = 0.31). The lower rate
of f'eeding in
juvenile snakes may result from gape-limitation:
juvenile snakes
are unable to ingest most bird
species in the area
(Li et al. 1990).
Foraging Behavior
Snakes catch birds from ambush,
and foraging
snakes display distinctive postures
and patterns
of
habitat selection. Although some birds are taken
from the ground,
many are captured
on arboreal
perches.
Snakes lie with the head facing outwards
along a branch approximately I m above the
ground; the forebody
is formed into a concertina
shape to permit
a rapid strike when
a bird alights in
front of the
pitviper
(Fig.
a). The incidence of arbo-
reality changes with the size of the snake: approxi-
mately
907o ofjuvenile snakes are found above the
ground,
whereas this is true for only 637c of adults
(no raw data available;
Li 1995). This difl'erence
may be partly attributable to the lower visibility of
small snakes
on the ground
compared to in a tree
(Sun
et a1.2001;
Shine and
Sun 2002). The height
above
ground to which the snakes climb to adopt
their ambush posture also differs between age
groups
(adults
typically climb
to I
- I .5 m,
juveniles
to 0.5-1 m) and also varies with the time of day
(higher in the morning than the afternoon) (Li
1995; no raw data available).
Although most prey are undoubtedly taken
fiom ambush sites,
Shedao
pitvipers will also eat
dead
birds or those trapped
in mist nets
(Sun 1990).
Thus, they can forage
actively as well as ambush
their prey. Because
small snakes often strike and
kill birds that
are too large for them
to swallow, an
actively
foraging snake may well encounter
a dead
bird on the
ground.
The invertebrates
taken
byjuve-
nile pitvipers are presumably taken at night by
active foraging; it is common to see
small snakes
moving about
at this time
(RS,
pers.
obs.).
Some birds taken from arboreal
perches
are
retained
after the initial strike.
whereas others
are
struck and released
(RS,
pers.
obs.). In some cases,
the snake falls off its perch
either
at the time of the
strike
(as
it throws its body forward) or later,
as ir
struggles with a bird that it has seized.
In other
cases it retains its hold
on the branch
and may swal-
low the
bird without leaving
the tree.
Snakes also ambush birds from terrestrial sites.
These
usually involve a tightly coiled
posture,
often
with the head
t'acing towards
an exposed open
area
such as a rock. Commonly a snake will lie with
Shine et al.-Ecology of Gloydius shedaoensis
only its head
visible,
and the rest of the body hid-
den under leaf litter (Sun 1990).
Surveys suggest
that approximately
two-thirds
of snakes use arbore-
al rather
than terrestrial foraging
sites
(Snake
lsland
Survey Team
1974),
but this estimate
may
be sensi-
tive to diff'erential
observability
of snakes
in the
two environments.
Studies
on l7 captive snakes have quantified
the efliciency with which the snakes
can turn bird
biomass
into snake biomass
(Wu 1911a.b).
These
snakes
ranged in mass
from
53.5-188
g prior
to the
experiment.
They ingested 15.0-62.5 g of mice,
and gained
2.0-36.0 g in body mass.
The mass
gained
as a proportion
of mass ingested
averaged
33.47c,
and ranged from 7.0-72.77c.
Regression
analysis revealed no significant relationship
between
assimilation
efficiency
(mass
gained/mass
ingested)
and absolute
body mass
(n
= 17, r = -0.
13,
P
=
0.61).
CONSERVATION ISSUES
Research
by Chinese scientists
identified a
number
of potential
or actual
threats to the Shedao
pitviper population (reviewed
by Huang 1989
and
Tang 1990).
These
can be classified
into two major
types: threats
that involve human activities, and
"natural"
processes.
Etl'ects
of Human Activities
Commercial exploitation. Prior to the com-
mencement
of research,
the Shedao
pitviper popu-
lation was heavily exploited for commercial pur-
poses
(Tang
1990).
The snakes
were killed
ro make
snake
wine or snake powder,
or to feed
to domestic
pigs. Snake venom was used for medicine.
Research
to document
this threat involved a com-
parison
of population
estimates
from earlier work-
ers to assess
snake numbers
through
time. Although
the data were imprecise,
they suggested
a strong
decline from the 1930s (approximately 100,000
snakes: Koba 1933, 1938)
to the 1950s
(50,000
snakes)
and continuing
through the 1970s
(20,000
snakes)
to the early 1980s
(10,000
snakes)
(Tang
1990).
Regular
mark-recapture
studies
(using
short-
term paint-marking) were instituted, to provide
more robust
estimates
of actual
snake densities.
Introduction of feral plants and animals. The
leguminous
vine Pueraria
lobata
is the most
impor-
tant threat
in this category. lt is a strangling
creeper
that eliminates
or overgrows native
woody vegeta-
tion (Zhao
et al. 1990).
Its slender
branches
do not
provide suitable ambush sites fbr the snakes.
Surveys showed
that snake abundance
was lower
in
plots
covered by Pueraria
than in control
plots;
and
that the removal
of Puerctria
on these
plots
was fol-
lowed by a significant increase
in snake
numbers
(Zhao
et al. 1990). This experiment
involved
three
plots,
each 12 x 12 m2.
One was
covered by dense
tangled Pueraria
(typical
of 27c
of the island's
sur-
lace area);
one by Pueriara growing
over other trees
(typical
of 10Vc
ofthe island's
surface
area); and one
was a control
(Pueriara-free)
plot.
The first of these
sites contained few snakes
(mean - 0.3 snakes
recorded per day),
whereas
the other two contained
more
animals
(means
of 5.3-6.0 snakes). Following
removal
of Pueraria in spring 1989 and replanting
with natlve vegetation,
the numbers
of birds and
snakes in the experimental
plot increased
substan-
tially (to a mean
of 11.7 snakes/day
over a 7-d peri-
od). Unfortunately,
Pueraria is difTicult to kill
because
it is fast-growing
and resistant
to drought.
The other feral organism
of potential
concern
is the brown rat (Rattus
non'egicus);
one of these
animals was
observed
attacking a
juvenile snake in
the laboratory
(Tang 1990).
More importantly,
the
rats'
activities
may damage
plants
and
soil cover on
the island.
However.
rat numbers
on the island
are
low (average
capture rate < 5 rats per 100 trap-
days:
Li 1995),
perhaps
because
the snakes
readily
feed on these rodents. Thus,
rats may at times
pro-
vide a significant
prey resource.
Fire. Several fires
prior to 1980
destroyed
veg-
etation over significant areas
of the island (Tang
1990).
Threats Due to Natural Processes
Research
has identified a series of potential
sources
of mortality which might reduce
the rate of
population
recovery.
Food and water supply. Experiments
with arri-
ficial hibernacula
suggested
that > 407c
of neonatal
snakes die
during winter,
possibly
due
to low energy
reserves prior to hibernation (Wu 1977
a,b).
Laboratory
experiments
show
that neonatal
pitvipers
can survive for very long periods
without fbod, as
long as they have access
to water. In experimental
studies,
seven neonates
survived
an average of 148
d
(range = 30-392 d) under these
conditions
(Wu
1971a'). Another
eight neonates
survived an average
of 214 d (range 53-246 d) under similar circum-
stances
(Wu 1977a). However,
neonates
kept with-
l0
out water
died more
quickly (mean
= 78.2
d, range
34 101
d:
Wu 1977a).
Although there
is no standing
water naturally
on the island, the snakes frequently
drink dew on grass,
or directly fiorn the artificial
pools
now
in place
(Sun
1990).
However, rainf'all
is
rare
during the main
bird-migration periods
in spring
and autumn
(Fig.
2).
Food may
be limiting
in some
situations. It is
common
to see relatively
emaciated
snakes
on the
island
(RS.
pers.
obs.).
and the 4-yr delay between
successive litters
by a
given
f'emale
(see
above) sug-
gests
that replenishment
of energy stores
is a slow
process.
Long-term
observations
suggest that the
numbers
of migrating passerines
have
declined
over
the
years
(Tang
1990).
Because
this decline is like-
ly to reflect
broadscale
environmental
degradatron
over
the birds' summer
or winter
habitats,
any solu-
tion must
involve
a massive spatial
scale.
Ultimate-
ly, the population
density of pitvipers
on Shedao
will probably
depend
upon
processes
iit work over
a
vastly
greater
area
than the island itself.
Landslides.
A typhoon in August 1985
caused
l8 landslides.
covering
a total area
of 4000 ml
(Tang
1990).
Plants were
destroyed,
soil was lost.
and many snakes
were killed.
Predation. Birds of prey are frequently
seen
on
the island and have
been recorded
to eiit neona-
tal
pitvipers
(Koba
1938: Tang 1990).
Disease.
Ninety-six
of 225 snakes examined
on the island
exhibited inflammation
of the mouth.
presumably
due to injuries
sustained
during f'eeding
(Tang
1990).
In sevele
cases this may reduce
the
snake's
ability to continue
taking
prey.
MANAGEMENT INITIATIVES
The research
on Shedao
pitvipers
has been
accompanied
by a series of "hands-on"
manipula-
tions
to address
the
problems
listed
above.
Effects of Human Activities
Commercial exploitation. The island of
Shedao was declared a Nature
Reserve in 1980.
Protection was also afforded to a mountain
(Laotieshan)
on the rnainland nearby
that
selves as a
stopping-over point
fbr migrating passerines
on their
way to Shedao. The rnountain
was protected
tcl
ensure fbod supply fbr the island snakes. A two-
story
six-room house
was constructed
on the island
in 1986 to accommodate research tealns.
Researchers
have
been based on the island
fulltinre
Herpetological Natural History, Y
ol. 9
(l), 2002
since the early 1980s. For example.
one of the
authors
of this paper
(SL) spends up to 200 d each
year
on the island,
and has
been doing
so since 1982.
No snakes are removed
fiorn the island.
although
venom
is sometimes
taken lbr medical
research.
Faunal
resources
can also be conserved
by
marking
them valuable
in economic or other terms.
Venom
fiom G. shedaoensi.s is used to treat a wide
variety
of medical
conditions.
including
cerebral
thrombosis,
atrophic
gastritis.
tumors,
and
rheuma-
tism
(Tang
1990). A 100-bed hospital
has
been set
up in Dalian
in association with the Snake Island
orgiinization. Tourism also offers resources.
Visitors
are
brought to the island
during
appropriate
tirnes of year.
but are only
allowed
to remain
on
the
island
for < 30 min and
are restricted
to a small
area
near
the boat-ramp.
A small
fee fiom these tourists
helps
to defray
the cost
of rlainraining
the f-acilities.
Unsurprisingly,
the abundance
of G. .shedaoen-
srs has
stimulated
researchers
to use this
species for
a variety
of projects.
For example. recent
work has
measured
electrocardic'rgrams
in the laboratory
(Xu
et al. 1987)
and examined
the distriburion
of tr-ace
elements
within the
snake's body
(Xu et al. 199
l).
Removal of feral plants and animals. There
have been major atten.rpts
to eliminate the intro-
duced weed Ptteruria
using
herbicides.
direct cut-
ting. and replanting
with native
vegetation
(Zhao
et
al. 1990). Rodent-trapping
prograrns
have been
introduced
also.
Capture rates ranged
from 3.8-5.8
rats
per 100
trap-nights
ovel'a 4-yr period.
Fire. The control
over visitor
numbers
(and
the
restriction
of these
people
to a srnall area near
the
jetty)
substantially
reduces the risk
of fires
being lit
by humans.
The long-term
efTects
of this reduced
flre frequency
remain
unclear. The
snakes select rel-
atively
open habitats fbr ambush-sites
(Shine
and
Sun
2002),
so that
an increase in ve-getation
density
may
ultimately reduce
the
amount of optimal
habi-
tat. On the other hand,
an intense
fire at the wrong
time of year could cause
significant rnortality of
snakes. Thus,
seasonal timing of fires is important
in terms of the efl'ect on snake populations.
Natural Sources of Mortality
Food and water supply. 800 water-basins
were
placed
on the island
during
the 1980s, with
water
added or replaced
every l0 d during drought
conditions
(Tang
I
990). These
are no longer
used
affer
the 1988 construction
of fbur much
larger
con-
crete
bowls
(2 m wide.
2 m deep)
to provide
addi-
Shine et al.-Ecology of Gloydius
shedaoensis
Figure
5. Overall
trends in abundance
and age
structure
of Shedao pitvipers,
based on snakes recorded
during
regular
census periods.
See
Sun et al.
(2001
) fbr details
of survey methods.
Bars
show
one standard
error
on
either
side of
the mean.
tional
drinking
sites for snakes. These pools
also
enhance
snake f'eeding
rates by providing ideal
ambush
sites
(Huang 1989).
Beside
one of these
tanks. a l0-m deep
well generates
a constant water
supply. Pumps
and
hoses
allow water
to be moved
among
bowls.
In 1986
and 1987,
ibod supply was supple-
mented
directly
by bringing
several hundred
small
birds
(chicken,
quail,
etc.) from the mainland
and
ofl'ering them
to the snakes. A less
direct
method
to
enhance feeding
rates
was trialed
in 1992,
by tying
ears
of rice to branches
that were
in use
as fbraging
sites by snakes
(Zheio
et al. 1992).
The rate
of bird
visitation
and of snake abundance
and
f'eeding rate
was monitored
fiom 0100-0145 h over 3-day
pen-
ods befbre
and afier this manipulation.
Bird num-
bers increased
tiom 60-125. snake
numbers
liorn
approximately
17 87, and f-eeding
rate per snake
fiom approximately l0-20c/o (Zhao et al. 1992').
Statistical
analysis
is rendered
difficult, however.
because
of the lack of control plots monitored
over
the
same time
span. ln another series
of manipula-
tions, twigs on many of the trees in Shedao
have
been
pruned
such that very
slender
branches
(strong
enough
to support
birds but not snakes)
have
been
removed.
This procedure
reduces
the number of
available perching sites where the birds are saf'e
fiom snake predation.
To address the high rate
of neonatal
mortality,
a large
(800
rn:; garden
was
built on the mainland.
Neonates fbund active
on the island late
in autumn
were brought back to this enclosure
to hibernate,
and then returned
to the
island
the fbllowing
spring.
Construction
of an artificial hibernaculum
on the
island allowed investigators
to identify optimal
thermal,
and hydric conditions
during winter, and
hence
to mimic
these in the mainland
enclosure
(Li
and Diao
1993; Li et al. 1993).
Landslide. Areas aff-ected
by landslides
have
been replanted,
in an attempt
to stabilize
the soil.
Predation. There
has been
no attemDt
to con-
trol birds of prey.
Disease.
Mouth inf'ections
have been treated
by capturing
snakes
and applying potassium
per-
manganate
and
gentian
violet.
Effectiveness
of Conservation Initiatives
Periodic mark-recapture
studies,
using short-
term paint-marking,
indicate
that the population
of
pitvipers on Shedao
has been steadily increasing
since the area was protected.
From approximately
9000 snakes in 1982, the population grew to
approximately
121,000
by 1989
(Huang
1984, 1990;
Sun et al. 1994).
It is
currently
estimated
at approx-
imately
18.000
(Sun
unpubl.
data).
Changes in population
size and age structure
over the last decade are also evident
in data fiom
regular
census
activities
that do not
involve
marking
the
snakes.
On most days
throughout
the spring and
autumn
bird-migration periods
each
year,
scientists
walk the same
-540-m
path
and
count snakes
within
a 3-m-wide transect
(the path and l-m widths on
either
side). The snake's
sex and
size class
are also
recorded.
We
have analyzed
the raw data tiom these
counts for the
years
1990-97,
excluding 1995
(Sun
et al. 2001). Over this period total numbers
of
snakes
averaged 40.6 per
survey
(0.31
per
m):
thus.
the
data set contains
37,980 records
of sightings
of
snakes.
Analysis
clearly shows
that snake numbers
have increased
through
time.
with a concurrent
shifi
ll
o
q)
J
E 200
o
o
L
o
I 150
E
c
an
o
JE15
o
g
o
.i 10
s
year
1990 1991 1992 1993 1994 1996 1997
1990 1991 1992 1993 1994 1996 1997
12
in the proportion
of juvenile to adult animals
(Fig.
5). The shift in age structure
is characteristic
ofpop-
ulations recovering from intense harvesting
focussed
on adult specimens
(e.g.,
Caughley
and
Sinclair 1994;
Webb
1995).
In summary,
the
pitviper population
of Shedao
not only has attracted
intensive
study over many
years,
but also
has been
a focus
tbr the
development
and application
of conservation
initiatives.
Those
programs have been successful,
and the Shedao
studies may have much to tell western science
about innovative approaches
to issues of snake
biology and
conservation.
ACKNOWLEDGMENTS
We thank
John Weigel
for alerling
Shine
to the
existence
of Shedao;
our wives
and families
for tol-
erating
our absences
on fieldwork on the island;
M.
Kearney for photographs;
and the Australian
Research
Council for fundins our studies.
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