J. Zool., Lond.

(2001) 253, 141155 # 2001 The Zoological Society of London Printed in the United Kingdom

The reproductive strategy of giant pandas (Ailuropoda

melanoleuca): infant growth and development and mother
infant relationships
Xiaojian Zhu1, Donald G. Lindburg2*, Wenshi Pan1, Karin A. Forney2 and Dajun Wang1
1
2

Department of Environmental Biology and Ecology, College of Life Science, Peking University, Beijing 100871, P.R. China
Centre for Reproduction of Endangered Species, Zoological Society of San Diego, P.O. Box 120551, San Diego, CA 92112-0551, U.S.A.

(Accepted 18 January 2000)

Abstract
Reproductive activities of six giant panda females (Ailuropoda melanoleuca) living in the Qinling
Mountains of China (Shaanxi Province) were recorded from 1989 into early 1995. Data on mating and
birth dates, litter size, cub sex and den use were collected for three of the pandas. At this site, pregnant
females migrated to lower elevations in advance of other pandas to seek dens for birthing. One dam was
videotaped in the den with her cub from birth to the end of the denning phase at 94 days of age. This cub
was repeatedly handled during the dam's absences to obtain data on development and weight. During the
early part of the denning phase, the cub was maintained on the dam's body virtually continuously. Postpartum fasting for up to 3 weeks was noted. Dams invariably moved cubs to new dens three or four times
during the birth season. By the time cubs left the den at about 3 4 months, they were fully furred and
capable of surviving winter temperatures without further shelter. Reproductive parameters for the wild
population fell within the range of values for captive pandas, based on information in the literature and in
the giant panda studbook. The combined data on length of gestation, intervals between births, litter size
and weight, infant development, and reproductive life span reveal a range of life-history variables that
strongly resemble the Ursidae.
Key words: Arctoidea, Mammalia, Ailuropoda melanoleuca, giant panda, reproduction, life histories, China

INTRODUCTION
An understanding of reproductive biology in the giant
panda (Ailuropoda melanoleuca) has been hampered by
limited effort and, in the wild, difcult observational
conditions. Schaller et al. (1985) provided general information on the timing of mating and birth seasons and
observed a small number of copulations in his study of
the Wolong Reserve population, but most other information derives from studies of captive-living pandas.
Descriptive accounts of selected aspects of infant development and interactions between dam and infant in captive
situations have been published by Celma Villares et al.
(1985), Hoyo Bastien, Schoch & Tellez Giron (1985),
Schaller et al. (1985), Tellez Giron & Gomez Llata
(1990), Hu & Wei (1990) and Schaller (1993).
Giant pandas were rst brought into captivity in 1936
(Sowerby, 1936), but a captive birth did not occur until
27 years later (Auyang & Tung, 1964). By the end of
1997, a total of 133 litters had been born in captive
facilities worldwide, from which 90 cubs survived to
*All correspondence to: Donald G. Lindburg.
E-mail: dlindburg@sandiegozoo.org

30 days, according to the international studbook (Xie &

Gipps, 1997). A low conception rate and even lower
survival rate of infants over this 34-year period indicate
that factors which would contribute to a self-sustaining
captive population are not yet clearly discerned.
A long-term eld study of giant pandas living in the
Changqing Forestry District (Yangxian County) in
China's Qinling Mountains began in 1985. In 1989, for
the rst time, a female was followed through an entire
sequence of courtship, copulation, parturition and cub
rearing. In this report, we present data on various aspects
of reproduction for three females from the mating season
of 1989 through that of 1994. In addition, we describe
behavioural interactions between a wild-born male cub
and his mother during the rst 33 weeks of life in the
1994 95 season. Our objective is to provide the rst
detailed information on these events outside the captive
context, and thereby contribute to the understanding of
the reproductive strategy of giant pandas.
STUDY AREA
The Qinling Mountains of Shaanxi Province extend for
500 km from east to west across the central part of

X. Zhu ET AL.

142

CHINA

radio collars (Telonics MOD-500 with S6B Mortality/

Motive Sensor; further described in Schaller et al., 1985,
and Pan et al., 1988) to facilitate tracking. All were
believed to be sexually mature, but were of an unknown
age. The timing of seasonal shifts in elevation by radiocollared females (estimated from range maps), changes
in their activity levels, and documentation of the time of
mating led to predictions of which ones were pregnant
and the approximate time they would give birth.
Parturient females were subsequently located by
triangulation, using signals from their radio collars.

Xian

2093m

Video recording of motherinfant behaviour

1961m

O JIA GOU

125m

1971m

SH
UI

DO
N

LIA

U
GO
Den
Lair
Peak
Ridge
River

Fig. 1. Map of the Qinling Mountain study area, Shaanxi

Province, China.

China. In its northsouth dimensions, this range

extends for 100200 km (Fig. 1). The highest peaks
reach to more than 3000 m. Tai Bai Peak, situated in the
middle part of the range, is 3767 m above sea level, and
is the highest peak in eastern China. Its eastward extension blocks the cold wind currents from the north,
thereby providing a natural divide for the climate of
north and south China. The southern slopes of the
Qinling Mountains are gentle and broad, and permit the
south-eastern monsoon to move along the Hangjiang
River into the high mountain areas. Therefore, the
climate on the southern aspect is warm and humid, and
botanically diverse. The vegetation can be divided into a
number of vertical zones. Two of these, the coniferous
deciduousbashania bamboo (Bashania fargesii ) mixed
forest at middle elevations and the dark coniferous
fargesia bamboo (Fargesia spathacea) forest at
subalpine levels, form suitable habitat for giant pandas.
On the southern slopes, a division into warm temperate and temperate zones occurs at about 1350 m. This
is the highest point of human cultivation, and separates
human agriculture from the giant panda bamboo forest
ecosystem in the mid-to-high elevations of the range
(Pan et al., 1988). Despite human encroachments, the
panda population in the study area has remained stable
over the past two decades (Pan, Lu & Zhu, 1994).
MATERIALS AND METHODS
Field data
Observations on the giant panda population inhabiting
the Qinling Mountains (Shaanxi Province) began in
1985, and 8 females and 7 males in 1987 were tted with

In August, 1994, the birth den of female Jiao Jiao, who

was strongly habituated to the observers from follows
beginning in 1989, was located for purposes of recording
activities inside the den by video camera. An infra-red
camera (Minitron MTV-1881) equipped with a 20 mm
lens (Avenir f/1.4) and microphone attachment
(Sennheiser K3U) was placed inside a modied metal
container and wedged into an out-of-the-way rock
crevice near the entrance to the birth den, with full view
of its inner chamber. Cables linked this camera to a
video recorder (Sony Hi-8 CCD-V99) about 30 m away.
An on/off switch at the recording site permitted activation of the camera without having to approach the
entrance. During recording periods, the female occasionally raised her head and glanced at the container
holding the monitoring equipment, but otherwise
ignored it.
Video records were obtained intermittently from the
second day (August 19, 1994) to the 33rd week (March
31, 1995) of infant life. During the rst 14 weeks, the
infant was transported by the dam to a new den on
3 occasions, necessitating the repositioning of all
monitoring and recording equipment in each case.
During Week 15, the infant was taken into the forest by
the dam, after which it was left by itself in a secluded
location (lair) whenever the dam foraged for food. By
this time, the ground had a permanent snow cover of
several centimetres and minimum daily temperatures
averaged < 0 8C. Dens were no longer used, and videotaping sessions occurred less frequently.
Over the course of the study, about 40 trips were
made into the forest to videotape. Although capable of
monitoring either day or night, power limitations and
the distance of den sites from camp of about a halfday's climb and intervening rugged terrain rendered
continuous monitoring impossible. Recording times
were concentrated in the hours after arrival at den sites
at about mid-day, but sometimes continued into or
throughout the night hours to past daybreak and over
much of the following day. Recording periods were
structured according to the following hierarchy: (1)
recording cycles, containing multiple recording sessions
and lasting from 1 or 2 h to as much as 80 h of
continous presence at a den site; (2) recording sessions,
containing multiple recorded segments; (3) recorded

Reproduction in giant pandas

143

Table 1. Summary of video records for infant male panda (Ailuropoda melanoleuca), Sun, 199495 (birthdate: 17 August, 1994)
Week of life

Dates

Age (days)

Cave no.

No. full minute scans

Min of activity recorded

12
34
56
714
1533

19 Aug30 Aug 94
31 Aug13 Sept 94
16 Sep27 Sep 94
4 Oct26 Nov 94
11 Dec 9431 Mar 95

213
1427
3041
4894
98226

1
1&2
2
24
Lair

263
154
190
243
93

313
209
224
288
117

segments which covered a continuous bout of mother

infant activity within a session.
During each session, the motherinfant pair was
continuously monitored for activity, using 2 different
methods: (1) a rapid pulse signal from the mother's
radio collar indicating activity; or (2) if no rapid pulse
was detected, the video monitor was turned on every
15 min to view the animals. If there was an indication of
activity, and the animals were visible, the video recorder
was activated. The recorder was turned off (to conserve
power) when both mother and infant were again inactive. During periods of maternal absence from the den,
i.e., when no radio-collar signal was available, the
recorder was turned on every 15 min to sample infant
activity. Recorded segments generally ranged from
about 30 s to 3 or 4 min of continuous taping, but
occasionally the camera was left on for as long as 10 to
15 min. Over 60% of taped segments (n = 461) were
1 min or less in duration. For 25 sessions having
records of exact start and end times, the mean duration
was 4 h, 38 mins. The recorder was activated an average
of once every 15 min within these 25 sessions.
Video scoring methods
Tapes were viewed with a Panasonic video editor
(Model AG-A650) in the second author's laboratory in
San Diego, California (USA). From these tapes, individual behaviours, postures and states for both mother
and infant were scored separately for each recorded
segment. Segments were treated as real observation
times, and intervals within segments were generated
from a continuously recycling Timex stopwatch programmed to emit an auditory tone at the end of each
minute. Mother and infant behaviours were recorded
continuously within each segment. States and postures
were scored as instantaneous scans (Altmann, 1974) at
the end of each full minute. The total duration of each
recording segment was calculated, based on video start
and stop times. Rates for behavioural activities were
based on number of occurrences/time in segments in
which an activity occurred. Data were entered on a
score sheet, using an ethogram developed from observations of both captive (Kleiman, 1983) and wild (W. Pan
and X. Zhu, pers. obs.) pandas, then were computerized
for analysis.
Daytime sessions, extending from 06:00 to 18:00,
were separated from night time sessions for purposes of
analysis. Night time recording took place on 3 dates in

August, 1 in September, 3 in October, and 1 in

November. These sessions ranged from as little as
30 min in length during the early evening to vigils
extending from midnight to dawn. The cumulative
number of full minute scans over all nights was only
214, and thus too infrequent for meaningful analysis.
However, a visual review of the data suggested enough
difference between night and day in some activities to
warrant separate analysis of the 2 data sets. Unless
otherwise indicated, the information presented is for
daytime sessions only.
The day of birth (August 17) was designated as Day
`0'. Data from the videotapes were initially grouped by
week of infant life, but small and variable sample sizes
resulted in some spurious patterns. Therefore, weekly
data were further combined to provide roughly equal
sample sizes while maintaining sufcient temporal resolution during the early weeks of life (Table 1). Thus,
during the rst 6 weeks, video samples were grouped by
2-week intervals, and after 6 weeks, data were combined
for the periods during which the cub remained in dens
(weeks 714) and in lairs (weeks 1533). Alternate
groupings were investigated and did not qualitatively
change the results.
The results of the video recording can be divided into
3 main categories: (1) behaviour rates during periods of
the mother's activity; (2) scan-based porportions of time
spent in various states during periods of the mother's
activity; (3) rates and proportions for the infant when
the mother was away from the den. No conclusions can
be drawn from these data regarding complete 24-h
behaviour rates or time budgets.
Measurements of infants
Two of the offspring of female Jiao Jiao, a female born
in 1992 and a male born in 1994, were weighed and
measured periodically during times when the dam was
away from the den. The female cub (Xi Wang) was
handled on 9 occasions between the ages of 52 and
90 days, and the male cub (Sun) on 14 occasions
between 28 and 102 days of age. A third infant, a female
born in 1993 (Gui Ye) to a different dam (Mo Mo), was
handled on a single occasion, at 80 days of age. In
addition to weighing and measuring, changes in external
appearance were noted for each cub from birth to the
end of the period of handling.
Cubs were placed in a small basket attached to a
25-kg spring balance for weighing. For body measure-

X. Zhu

144

ET AL.

Table 2. Summer-time elevation changes and activity levels of pregnant and non-pregant giant panda females
Pregnant females
Date

Female name

30 Jul-89
4 Aug-89
9 Aug-89
15 Aug-89
16 Aug-89
17 Aug-89

Jiao Jiao

24 Jul-93
3 Aug-93
8 Aug-93
9 Aug-93
21 Aug-93

(birth of Hu Zi)

Rui Xue

(birth of Shi Gen)

Non-pregnant females

Approx.
elevation (m)

Percentage
activity

2450
2100
1800
1950
1900
1850

52
47

21
10
12

2000
1900
1850
1850
1850

20
14

ments, cubs were restrained by hand and a tape used for

measurements of girth and length of extremities. Joints
were palpated through the skin and the measurements
taken from articulation points. Measurements were
taken from either side of the body.
Captive demographics
Comparative information from the captive population
was drawn primarily from the latest version of the
international studbook (Xie & Gipps, 1997). However,
data on 11 cubs born in 1997 after publication of the
studbook were obtained by personal communication
with studbook keeper Xie Zhong, and are included in
the totals given as studbook data. Thus, the captive data
are complete through December 31, 1997.
RESULTS
Seasonal activity of pregnant and non-pregnant females
Initial studies (Pan et al., 1988; Lu, 1991) indicated that
pandas in the Qinling Mountains ascended from their
OctoberMay range (below 2000 m) to elevations up to
3100 m, where they remained from June through September. Pregnant females, however, may deviate from
this pattern (Table 2). In the 1989 season, a radiocollared female was seen with other pandas at an elevation of 2450 m on July 30. However, by her August 9
parturition date she had descended to 1800 m. A nonpregnant control female was sighted at 2400 m or higher
during this same period. A second pregnant female was
located at 2000 m on July 24 during the 1993 season,
nearly a month before she gave birth. She descended
even lower subsequently, and remained below 2000 m
during the time of parturition and early lactation.
Again, however, a non-pregnant control female was
recorded at > 2200 m during the same period. Considering all data for the four females, the two pregnant
pandas descended to below 2100 m more than 6 weeks

Approx.
elevation (m)

Percentage
activity

Yang He

2450
2600

2400
2460
2500

54
51

55
56
52

Jiao Jiao
or
Nu Xia

2350
2250
2200
2500

51
56

Female name

before their non-pregnant controls, and were at elevations averaging about 430 m lower in subsequent
sightings.
In addition, radio-collar signals with > 10 tonnes per
10 s, indicating activity, averaged 28.4% and 17.0% of
all signals in pregnant females, compared to 53.6% and
53.5% in non-pregnant controls at the higher summer
elevations (Table 2). Reduced activity appeared to
precede parturition by as much as a month, at a time
when females were conning their foraging to the near
vicinity of a den site (see also Lu, 1991).
Matings and births
Fifteen oestrous periods involving eight different
females were observed. In all but two of these, a female
was accompanied by three to ve males who competed
for the opportunity to copulate. A female observed in
1993 and 1995 was accompanied by a single but different
male during these two seasons. Male associations with
females during oestrus could last for up to 1 month,
beginning in early March and ending shortly after
copulation had occurred.
Here, we report on six episodes for which information
on copulation and birth dates, den usage, litter size
and sex of cubs is available (Table 3). Between 1989 and
1994, copulation dates (n = 6) for three females in
4 different years fell within a 30-day period beginning
on March 11 (Table 3). The birth dates of the six infants
were determined by radio-tracking of females to their
birth dens. Despite the 30-day variability in mating dates,
the six births were tightly clustered within a 10-day
period in the second half of August. By counting the
days from copulation to birth, an average gestation of
146.3 11.5 (sd) days (range = 128 161) was calculated.
All but one of the births were of single cubs, and of
ve that could be sexed, three were males. Female Mo
Mo gave birth to twins, one of which was found dead
2 days after parturition. The carcass weighed only 60 g,
and examination showed that a portion of the internal
organs was missing. The second cub of this litter was

Reproduction in giant pandas

145

Table 3. Records of mating, parturition, and cave use for the pregnancies of giant pandas followed in this study
Date rst
observed
with male

Mothers'
name
Jiao Jiao
Jiao Jiao
Jiao Jiao
Rui Xue
Mo Mo

8 Mar-92

23 Mar-93

19 Mar-94

Mo Mo
Summary

Copulation
date

Birth date
of litter

11 Mar-89
12 Mar-92
10 Apr-94
27 Mar-93
31 Mar-93

19 Aug-89
15 Aug-92
17 Aug-94
21 Aug-93
24 Aug-93
24 Aug-93
16 Aug-94

27 Mar-94

Mar 8early Mar 11Apr 10 Aug 1524

April

Gestation
period
(days)
161
156
128
145
146
142
Av. 146.3

Cub's
name

Sex

Present
status

Hu Zi
Xi Wang
Sun
Shi Gen
Gui Ye
(twin)a
Cub 1

M
F
M
?
F
?
M

Alive
Alive
Alive
?
Dead
Dead
Alive

M:F:U
3:2:2

No. caves
and lairs
used
>3
9
6
>4
>4
>3
39

No. days
in caves
117
125
94

Av. 112

a
This twin was found dead.
?, Birth date unknown, but infant observed later in season; Av., average; M, male; F, female; U, unknown.

Weight (kg)

Sun (Jiao Jiao)

7
6

Xi Wang (Jiao Jiao)

Giu Ye (died; Mo Mo)

5
4
3
2
1
0
0

10

20

30

40

50 60 70
Age (days)

80

90 100 110

Fig. 2. Growth curve for two wild-born giant panda infants

(names in parentheses refer to the dam).

less than half the weight of two other cubs when

weighed at 80 days of age (infant Gui Ye, Fig. 2). Later,
this cub was no longer seen, and was assumed to have
died. The dam mated and gave birth to an infant in the
following year.
Denning activities
A total of 13 different naturally formed rock caves were
used as maternity dens for the six births and cub rearing
events. Within a season, the number of caves used by a
female ranged from three to six. Occasionally, a cave
was used twice in the same season, and more than one
female was observed to use the same cave, although in
different years.
For all six births listed in Table 3, caves were located
at elevations between approximately 1800 and 2000 m.
Details on seven caves used by female Jiao Jiao are
presented in Table 4, and may indicate a general pattern
of den site selection for all. This female selected a
different cave for the birth of each of her three cubs,
and remained in these initial locations for 3, 5 and 19
days, respectively. Caves used for birthing tended to be
of simple construction, with very little bedding. During
the period August 2731, 1994, the average minimum
temperature inside one birth cave (Cave A3 in Table 4)
was 16.2 8C, compared to 13.9 8C outside. Maximum

temperatures inside and outside were 18.3 and 20.8 8C,

respectively.
Cave B1 was the second cave used by this female in
two of her three seasons. It had a smaller and more
concealed entrance, but a wide interior. Because of its
more enclosed design, this cave provided a warmer and
more secluded environment for the infant (no temperature data are available). It was occupied for roughly the
next 2 to 4 weeks of infant life. For the later stages of
cub development, female Jiao Jiao used three different
caves (C1, D1, and D2 in Table 4), with occupation
beginning from as early as the 15th to about the 70th
day of cub life. These caves were more open, but facing
south-eastward, seemingly leading to increased warming
by the sun during a time when ambient seasonal
temperatures were in decline.
An increase in the amount of material, including large
branches and sticks, placed in the cave entrance with the
rst two or three shifts in location following parturition,
suggested an effort to hide the cub or prevent it from
crawling outside the den. In the late stages of denning,
Jiao Jiao's caves were near ridge tops, with wide
entrances and the least amount of concealment, but
with the entrance facing the sun for long parts of the
day. From these, the mother changed to the infant's rst
period of life outside dens, when cubs were left in dense
patches of bamboo (called lairs) while she fed nearby.
The time from birth to abandonment of last dens for the
three cubs averaged 112 days (Table 3).
Physical characteristics and development of cubs
At birth, the infants were pinkish in colour, with very
short, white, sparse hair covering the entire body. By
about 8 to 10 days of age, the skin in the areas where
black hair would eventually grow turned grey. At the
age of 2325 days, the pelage had achieved the typical
black and white markings of the adult panda. The eyes
began to open in a narrow slit at 40 to 49 days, and
some long, white hairs had grown in areas of the pelage
that would eventually be entirely black. By about 72 days
the eyes were half open, and in another 3 or 4 days were

146

Table 4. Caves used by Jiao Jiao for rearing of cubs Hu Zi (1989), Xi Wang (1992) and Sun (1994)
Year(s) Elevation
used
(m)
Direction Brightness Structural/construction

Size
L6W6H
(m)
Bedding

Slope of
the cave
oor

Frequency
of use
Total days
(times/cub) of use

Early stage A1

1989

1800

Flat

A2

1992

to

Nothing, or some dry

bamboo or pieces of
bark

308, inclining
downward

Cave
No.

SE

Relatively
bright

Simple. Under an inclined rock

or in a space between two
connecting rocks. The
entrance opens wide

Space under two closely connected 2.961.3

rocks, with a small triangular
60.7
entrance. Spacious inside
Space among three big rocks, with 1.861.2
a small triangular entrance which 60.8
is 8 m above the ground

Fresh bamboo inside,

and a large dry wood
branch at entrance
Bamboo, pine and birch
branches, dry or fresh

Space under cliffs with a large

entrance

Thick layer of fresh

Flat
bamboo and a large
wood stick at entrance
Dry bamboo
Flat

1994

1960

B1

1992
1994

1950

Dark

(late)

C1

1989
1992

1920

SE

Bright

Late stage D1

1989
1992

1900

SE

Bright

D2

1992
1994

2000

Space under cliffs with a large

entrance (18.661.6)

In 1992, cave B1 was occupied a second time during the mid-stage (after cave C1).

1
1

3.061.0
60.7

12a

158, square
1
80 cm lower than
entrance

1730
4976

48

25

X. Zhu ET AL.

A3
Mid-stage
(early)

319

Table 5. The physical measurements of three panda cubs: Sun (birthdate: 17 Aug-94, mother: Jiao Jiao), Xi Wang (birthdate: 15 Aug-92, mother: Jiao Jiao), and Gui Ye (twin,
birthdate: 25 Aug-93, mother: Mo Mo)
Body
length
(cm)

Body
weight
(kg)

Foreleg
(cm)

Hindleg
(cm)

Forepaw
(cm6cm)

Hindpaw
(cm6cm)

Girth at
neck
(cm)

Girth at
chest (cm)

Girth at
belly
(cm)

Head
length
(cm)

Tail
length
(cm)

Sun
16 Sep-94
22 Sep-94
27 Sep-94
2 Oct-94
7 Oct-94
12 Oct-94
18 Oct-94
24 Oct-94
29 Oct-94
3 Nov-94
9 Nov-94
17 Nov-94
22 Nov-94
28 Nov-94

28
34
39
44
49
54
60
66
69
76
82
91
96
102

34.5
35.5
37.5
39.5
42.0
44.5
49.0
50.0
51.0
52.0
53.0
58.5
59.5
61.5

1.35
1.70
2.00
2.35
2.65
2.93
3.35
3.62
3.95
4.23
4.54
5.08
5.45
5.83

14.0
14.5
15.0
15.0

17.0
19.5
19.0
22.5
22.5
26.5
26.5
27.0

8.0
9.0
11.5
12.0

14.5
13.0
14.0

18.0
18.0
20.0

3.762.4
4.062.8
4.363.0
5.363.3

5.363.8
5.563.6
6.164.7

7.264.9
7.864.9
7.464.9
8.065.4

3.162.4
3.562.7
4.062.9
5.063.0

4.763.4
6.563.4
7.064.0

9.164.5
7.864.8
10.064.7
9.964.9

16.5
19.0
19.5
22.0

28.0
28.0

27.0
29.0
31.0

33.0

41.0
40.0

37.0
40.0
43.0

44.5

32.5
35.0
35.0

44.0
44.5

48.0

53.5
53.1
51.0

10.5
12.0
13.0
13.0

16.0
19.0
20.0

17.5
19.5
21.5
23.5
23.5

6.0
6.0
6.0
6.0
6.0
6.0
6.0
6.0
8.0
8.0
8.0
7.8

7.8

Xi Wang
6 Oct-92
14 Oct-92
19 Oct-92
23 Oct-92
28 Oct-92
1 Nov-92
5 Nov-92
8 Nov-92
13 Nov-92

52
59
65
69
74
78
82
85
90

43.0
52.0
52.0

52.0
55.0
55.5

3.00
3.30
3.70
4.00
4.25
4.55
4.85
5.10
5.35

18.0
21.0
20.0

15.0
16.0
16.0

4.065.5
6.064.0
7.563.3

7.064.3
9.064.0
7.064.8

7.063.5
7.263.5

8.864.4

8.564.3

33.0
36.0
41.0

41.0
42.5
44.0

8.4
8.0
8.0

7.0
8.0

Gui Ye
13 Oct-93

80

35.0

1.90

23.0

4.062.5

4.562.5

7.3

Reproduction in giant pandas

Cub name and

date of
Age
measurement (days)

147

60
50

80%

40

60%

30

40%

20

20%

10

0%

0
12

34
56
714
Week of infant life

15+

On mother
(a)

(b)

Fig. 3. Time spent by the giant panda dam in successive dens

(caves) by week of infant life, and rate of infant vocalization
during the denning phase.

100%

Off mother

75%
50%
25%
0%
12

34

56

714

15+
20

80%

% Hold/Cradle
Lick

60%

Mouth Carry

15
10

40%
5

20%

0%
12
40

(c)

34

56

Scratch
Crawl

30
Rate/h

completely open. At this time, the rst appearance of

canine teeth was noted. Incisors rst appeared at about
90 days, and infants were clearly able to move their eyes
in focusing by this time.
Measurements of various parts of the body are presented in Table 5. It is of interest to note that tail length
in the male cub increased by less than 2 cm during the
same period in which body weight underwent a fourfold
increase. Gains in weight are given in Fig. 2, and show a
virtually identical increase in two cubs, despite a difference in sex. As adults, males weigh on average 1020%
more than females (Schaller et al., 1985).

100%

Not visible

Rate/h (lines)

Liar

Cave 4

Mother absent
during all sampled
periods

Cave 3

Percent of visible scans

Cave 2

Percent of scans (bars)

Cave 1

100%

Infant vocalization rate/h (line)

X. Zhu ET AL.

Percent of scans mother was

present (bars)

148

714

15+

Shiver
Comf. Mvmt.

20
10
0
12

34

56

714

15+

Motherinfant behaviour at dens

Fig. 4. Denning activities of mother and infant by week of

infant life: (a) time infant was on mother, using only scans in
which the infant was visible; (b) maternal activities while in the
den; (c) rates per hour for selected infant behaviours.

Information on interactions between mother and infant

were obtained primarily from the videotaped records of
female Jiao Jiao and her male infant (Sun). The rst
videotaping session occurred on the evening of August
19, beginning at 20:15, and lasted for about 30 min. At
this time the infant was in his second day of life. Except
for brief glimpses during bouts of maternal licking, the
infant was largely obscured from view by the mother's
arms as she held him rather tightly to her ventrum. No
vocalizations were detected during this initial session.
Figure 3 shows the percentage of scans during which
the dam was present at dens during the rst 14 weeks
following parturition. She was rst seen leaving the
birth den on the 13th day of infant life, at about 18:00,
for a period of about 2 min. Later that evening,
however, she was away for 40.4% of scans (23 of 57).
Five additional departures were seen over the next
2 days (i.e. in Week 3), of which four were during the
daylight hours. Most of these absences were brief. Three
days after her rst departure, the infant being at 16 days
of age, the female gently grasped him in her mouth and
transported him to a new cave site.
During Weeks 36, the dam was present during 79
89% of scans (Fig. 3), and not until Day 41 (6th week of
infant life) was she absent for an entire observation
session. From this time onward to the end of the 14th
week, the dam was away for all or most of each
observation session on eight of 13 visits to the den.

Because more full minute scans were taken on the days

when she was present, the time shown for the dam's
presence during Weeks 714 is inated by an unknown
amount. Clearly, her absences were increasing during
this period, and from the 15th week onward, after the
last den had been abandoned, the female was not seen
again in the immediate presence of the infant.
Although the infant was often not visible when the
dam was in the birth den (Fig. 4a), neither was he visible
on the ground, leading to the conclusion that he reposed
on her ventrum at these times. When combined with
scans in which the infant could be seen, these data
indicate that from birth to the end of Week 6, resting on
the dam's body occurred in 99 100% of scans. As the
dam sat semi-erect or lay in a rocked-back position, the
tight cradling of the infant with her arms (Fig. 4b)
frequently precluded seeing any kind of neonatal
activity, especially during the rst two weeks of life.
Although the frequency of suckling could not be determined under these conditions, modest repositioning of
the infant was commonly seen, often in response to his
vocalizations. Because it involved tongue movement
and occasional repositioning by the dam, maternal
licking of the infant was also more readily documented
(Fig. 4b). This activity, essential to stimulate the voiding
of body wastes, was highest in the early weeks of infant
life, but occurred to the end of the denning period

Reproduction in giant pandas

(Week 14). Repositioning the infant on her ventrum by
gently picking him up with her mouth was highest
during the rst 2 weeks (Fig. 4b). Thereafter, as the dam
began to leave the den to forage, on return she invariably retrieved the infant from the ground with her
mouth to place him on her body. Whenever the dam
was in the den, the infant was rarely seen on the ground
until he reached about 60 days of age. From this time
onward, until the last den was abandoned at 94 days,
the dam sometimes lay on her side with the infant
resting quietly beside her.
Vocalizations were highest in the rst 2 weeks of life
(Fig. 3), often heard whenever it seemed the infant was
seeking nipple contact or was disturbed by movements
of the dam. Vocalizations declined in subsequent weeks,
except during three of the rst four periods of videotaping while the dam was away from the den, beginning
at the end of Week 2. On the rst of these (Day 13), a
loud squawk-like vocalization was heard on average
over four times per min for a 25-min period. This event
took place in the late evening. Vocalizations ceased
when the dam returned at 11:48, picked up the infant
and placed him on her ventrum. The same high
frequency of vocalizing was seen again during the dam's
absence on Days 15 and 20, but during daytime taping.
The infant was noticeably less vocal during the next
observed absence of the dam on Day 31. After Day 40,
when she was often away for 100% of recorded sessions,
vocalizations were rarely heard.
In all sessions preceding the rst observed maternal
departure from the den on Day 13, the infant lay rather
quietly on the dam's body, always in a prone position,
alternately nursing and resting. Thereafter, this pattern
was interrupted by the increased frequency of maternal
departures, with the infant lying prone on the oor of
the den, vocalizing vigorously as noted earlier, or
asleep. Modest shifts in position initiated by the infant
(comfort movements) and scratching were rst seen at
about 3 weeks of age (Fig. 4c), the latter occurring
either while at rest on the dam's body or alone on the
den oor. The rst attempts at crawling occurred while
still on the dam's ventrum, at approximately 2 months
of age (Fig. 4c). The infant was rst seen to rise
unsteadily on all four limbs on Day 36, but actual
walking was not seen until the 17th week. Shivering was
rst seen at 19 days, and occurred regularly on subsequent days, even when on the dam's ventrum (Fig. 4c).
This activity was also commonly seen during periods
when the infant was alone in the den. After Week 14,
shivering was no longer seen.
The infant was last seen inside the den (Den 4) on
Day 94. At the next contact, on Day 98, he was found
in a patch of dense vegetation, with the dam foraging
nearby. There were only two sightings in December,
and none in January. During the two December visits
the infant was on the ground, occasionally resting
quietly but also crawling or walking for short distances.
Only two vocalizations were heard during these visits.
When contacted on February 1, at 168 days of age, the
infant climbed a tree and remained there during most of

149

the observation period. He was quite active, biting at

twigs and leaves, and moving about in a playful
manner. On all three visits in March, ending with Day
226 of life, the infant spent the entire time above
ground, climbing and playing. No vocalizations were
heard during these visits.
DISCUSSION
The elucidation of reproductive strategies inevitably
entails a discussion of life-history variables (Boyce,
1988a). The critical variables for giant pandas stem
from reliance on a bamboo niche that affords access to
plentiful food of relatively even but low nutritional
quality on a year-round basis (Schaller et al., 1985, 1989;
Johnson, Schaller & Hu, 1988). Although bamboo is
subject to periodic owering and die-off, these cycles
differ between species and might therefore be too variable to have been a factor in shaping the reproductive
patterns of the giant panda. Furthermore, the recovery
phase for bamboo of 510 years (Johnson et al., 1988;
Schaller et al., 1989) seems too long to constrain
seasonal reproductive phenomena such as delayed
implantation or the length of gestation (and thus, such
variables as the infant to dam size ratio at parturition).
In the only careful studies of pandas during a die-off,
Johnson et al. (1988) and Reid et al. (1989) found that,
despite an 82% decline in the preferred food source,
pandas at the Wolong Nature Reserve were able to
maintain adequate nutritional intake either through
adjustments in use of remnants of the preferred food or
by switching to other species of bamboo. Loss of the
latter option as a result of reduced habitat may account
for more recent reports of massive starvation during a
die-off cycle (Reid et al., 1989).
Although the phylogenetic status of pandas is for
some an unresolved issue, their similarity to ursids in a
number of traits, for example, body size relationships of
neonate and dam, the occurrence of delayed implantation of the embryo and relatively slow maturation of the
young, make comparisons with this taxon particularly
useful. Such considerations may help to resolve
questions about the taxonomic afnities of giant pandas.
The female giant panda typically has a single oestrus
in the spring of the year and, according to data summarized by Schaller et al. (1985), sexual maturity is attained
at about 5.5 6.5 years of age. Four of 19 females
captured as infants or young juveniles (whose ages are
therefore more accurately estimated), and > 20 years of
age, produced infants at the presumed ages of 18 19
years, but none thereafter (Xie & Gipps, 1997).
Birth intervals
The data of Table 3 indicate interbirth intervals of 2 and
three 3 for a female (Jiao Jiao) whose offspring survived
to weaning age. A second female in the study area
(Rui Xue in Table 3) took 3 years to rear a cub prior to

150

X. Zhu ET AL.

the birth of Shi Gen in 1993, and had another infant

2 years later. Yong (pers. comm.) recorded a 3-year
interval for one female in the Foping Nature Reserve.
Three-year intervals may be exceptional, however, and
are undoubtedly counterbalanced by known cases of
mating in successive seasons when a litter is lost prior to
gonadal recrudescence in the spring. Schaller (1993), for
example, tracked a female in the wild who mated in
3 successive years following early loss of her offspring,
and it is common practice in Chinese facilities today to
wean offspring from their dams at about 3 to 5 months
of age in order to obtain litters annually (Zhang et al.,
1996). Given the clear indications from both captive and
wild sources that females nursing young born in late
summerearly fall will not come into oestrus in the
following spring, and that weaning in the wild ususally
occurs at 18 24 months, we are condent that 2 years is
the usual birth interval for giant pandas.
Timing of births relative to oestrus
For the six oestrus/birth episodes reported here, copulation dates were spread over a 30-day period in the
spring, but births were condensed into a 10-day period,
on average, 146 days later (Table 3). For example,
although female Jiao Jiao mated nearly 30 days later in
1994 than in the two prior seasons, gestation in the 1994
season was 33 days shorter, bringing parturition dates
within a range of 6 days for this female over the three
seasons. Captive births (n = 133) have ranged from May
to November, with 75.9% occurring in August and
September (Xie & Gipps, 1997).
Our sample of females in the wild indicates a mean
gestation length of 146.3 11.5 (sd) days (Table 3).
Schaller et al. (1985) reported an average of 135.4 18.0
(sd) (recalculated) for 19 pregnancies (range 97163),
and Song et al. (1994) gave a gure of 139 21.0 (sd)
days (range 84 163) for 23 pregnancies at the Chengdu
Zoo. To these we have added data from six pregnancies
at the Wolong Centre (He, 1997) and three from the
National Zoological Park (Montali, 1997), having an
average of 138.1 25.7 (s d) and a range of 96184
days. For all sources combined (n = 57), mean length of
gestation is 138.6 19.8 (s d) days, in close agreement
with the estimate of 135 days originally reported by
Schaller et al. (1985). Although our average for wild
females is longer than for those in captivity, this
difference is not signicant (P = 0.318; d.f. = 55,
unpaired t-Test, 2-tailed). Given the extremes in range
for the composite sample (84 184 days), giant pandas
may be unique in the amount of variance shown in
this trait.
Low levels of progestogens in the urine of giant
pandas until several weeks after conception, when a
major increase occurs, is regarded as evidence for a
delay in embryonic implantation and thus of the onset
of foetal growth (Hodges et al., 1984; Monfort et al.,
1989). Adjustment in gestation length resulting in
increased synchrony of births in the wild is likely to be

achieved by adjustments in the length of this early phase

of pregnancy (Sandell, 1990). Synchronization of births
is posited as one of several hypotheses used to account
for the evolution of delayed implantation (Mead, 1989),
and in pandas it might be one mechanism for avoiding
seasonally late parturitions and consequent exposure of
young to life outside the den during cold winter
temperatures.
On the other hand, delayed implantation is regarded
as an ancient trait, since it is found in all extant bears
(Sandell, 1990). If the phyletic afnities of pandas are
with bears (O'Brien et al., 1985; Wayne et al., 1989;
Bininda-Emonds, Gittleman & Purvis, 1999), delayed
implantation may be an example of phylogenetic inertia
(Gould & Lewontin, 1979; Gould & Vrba, 1982) rather
than an adaptation to current circumstances. The temporal mismatch of scales between delayed implantation
(seasonal) and variations in food availability based on
the long-term owering cycles of bamboo with 5 10
years for recovery lends support to the ancient trait
theory.
Denning
Giant pandas in the Qinling Mountains may differ from
those in the Qionglai Mountains of Wolong Reserve in
their preference for foraging at higher elevations during
the summer months. The data in Table 2 indicate,
furthermore, that in the fall pregnant females descended
to elevations below 2000 m in advance of non-pregnant
females. It is possible that pregnant females were
seeking den sites at lower altitudes to incur the benet
of warmer temperatures during the post-partum phase.
It is more likely, however that parturition marks the
beginning of a denning phase of about 4 months'
duration, and parturient females might pose unusual
hypothermic risk to their offspring if they attempted to
complete this phase at altitudes forsaken for the winter
by the population in general. It is of some interest that
female Mo Mo (Table 3) lost a litter of twins born at a
site between 2350 and 2500 m in 1993, but successfully
reared a litter born between 1850 and 2000 m in the next
year. Schaller et al. (1985) found dens well above 2000 m
at Wolong; however, the more southerly latitude of
Wolong could have lessened the impact of temperature
on den selection at that location.
Denning is mandated by the altricial state of cubs at
birth, and it is possible that the use of several different
dens within a season reduces parasite load or predation
on the young. Notably, rock caves were used exclusively at our study site, undoubtedly because trees large
enough to accommodate an adult female (see Schaller
et al., 1985) were absent. It appeared that dens used for
parturition differed in size, seclusion and duration of
occupancy from those used at later stages, suggesting
that the initial site is adequate for times when the dam
is continuously present, but perhaps not for later stages
when she begins to leave the offspring behind to
forage.

Reproduction in giant pandas

Post-partum fasting
Having access to a food resource that varies little in
availability and nutritional value throughout the year
(Schaller et al., 1985, 1989), giant pandas have no need
to hibernate. They do, however, use dens for the birth
and protective care of their highly altricial neonates. Of
further interest is the fact that dams also appear to
undergo a post-partum fast of sorts. The female whose
videotaped activities were analysed for this report began
leaving the den when the infant was 13 days of age, and
following two previous parturitions she fasted for 9 and
25 days (Lu, Pan & Harkness, 1994). Data from captive
females also appear to support the notion of a fasting
phase. In a detailed description of post-partum
behaviour at the Madrid Zoo, Celma Villares et al.
(1985) noted repeated refusals of food and water for at
least the rst 5 days (the point at which their report
ends). Some captive females at the Chengdu Zoo
(R. Snyder, pers. comm.) and the Wolong Centre
(R. Swaisgood, pers. comm.) also refused food and
water, despite frequent proffers, in the days following
parturition. Schaller et al. (1985) described post-natal
activities of a female, Mei Mei, at the Chengdu Zoo and,
although they present no data on feeding, noted that
latrine trips averaged 0 to 0.4 per h, a remarkable decline
from the passage rate for faeces reported for wild
pandas, and clearly indicative of reduced food intake.
Why do parturient dams fast, particularly when food
is plentiful at the time? One could argue that giant
pandas have not quite shed themselves of the seasonal
dormancy carried forward from a common ancestry
with bears. More likely, however, is that fasting is
mandated by the extremely altricial state of cubs at
birth. Mrosovsky & Sherry (1980) hypothesized that
periods of anorexia may occur when feeding by a parent
would compete with activities of greater importance,
and in support cited numerous cases involving
incubating and hibernating species. We suggest that an
early disruption of panda care-giving behaviour to
forage would place infant survival in jeopardy. The
scantiness of infant body hair at birth and rapid
achievement of a dense pelage roughly coinciding in
time with the rst departures of the dam from the den
suggest that the mother's warmth is essential to the
prevention of hypothermia, even though births occur in
late summer and early fall. The high frequency of
suckling (6 14 times per day, Schaller et al., 1985) may
also preclude the absence of dams for the time required
for a bout of foraging (initially 1 6 h in length,
according to Lu et al., 1994). It is of interest to note that
when the dam at the Madrid Zoo was nally enticed to
leave her infant to feed, she quickly returned to it when
it began to cry loudly (Celma Villares et al., 1985).
Litter size
One of six pregnancies in our eld sample (Table 3) was
known to yield twins, but only one infant survived.

151

Twinning is difcult to measure in the wild because

panda females routinely raise only one cub, leaving the
other to die within hours of parturition. For 133 captive
birth events listed in the current international studbook,
twin births occurred in 64 (48.1%), yielding an average
litter size of 1.48. Chinese sources (Liu, 1988; Hu, 1990)
noted the birth of a litter of triplets at the Shanghai Zoo
during the 1960s, and a litter of three occurred in 1999
at the Wolong Centre, but neither occurrence has yet
been included in the studbook. Cubs from twin litters
often have great disparity in birth weight (up to 48%;
Tellez Giron & Gomez Llata, 1990), and necropsy
reports indicate that in some instances the smaller cub is
less developed and may be predisposed to die at parturition (Montali et al., 1990; Tellez Giron & Gomez Llata,
1990). However, when there appears to be little or no
disparity in weight or vigour between litter mates, the
dam nevertheless takes only one for rearing (Celma
Villares et al., 1985; Schaller et al., 1985; Tellez Giron &
Gomez Llata, 1990). Only one captive female in the 64
known cases of multiple births has successfully reared
twins without human assistance (R. Snyder, pers.
comm.), and reports of twin rearing by wild dams
(Schaller et al., 1985) lack convincing documentation.
Thus, although close to half of all veriable litters have
consisted of two cubs, the nearly absolute practice of
abandoning one in effect establishes one cub as the
norm for giant panda litter size.
Early litter pruning through action of the dam, in
contrast to loss through littermate competition for teats
or other forms of juvenile wastage (Tait, 1980; CluttonBrock, Albon & Guinness, 1989; Clutton-Brock, 1991)
is uncommon in mammals. An average litter size of 3.0
(n = 211) is reported for black bears (Ursus americanus),
and cub mortality in this species is not a result of
maternal abandonment at parturition (Alt, 1989). Similarly, size of litters whelped by 77 marked or otherwise
recognizable grizzly bear females (Ursus arctos) in the
Yellowstone ecosystem averaged 2.1 cubs and, like
black bears, all littermates received maternal solicitude
(Craighead, Sumner & Mitchell, 1995). In contrast to
giant pandas, ursid dams routinely attempt to rear the
entire litter, regardless of its size.
Our data on the investment in cub rearing by giant
pandas, particularly during the initial weeks of more or
less actively and continuously supporting the highly
altricial neonate on her body (see section on `Maternal
solicitude'), suggests that bestowing the same level of
care on two neonates would be virtually impossible (see
also Schaller et al., 1985, on this point). It remains
unclear why twinning in this species should occur in
nearly half of all litters, given the high probability that
only one will survive.
Infant mortality
Of six infants in our sample, two died at or shortly after
birth (Table 3). Schaller (1993) provided records of a
female who produced only one surviving infant out of

152

X. Zhu ET AL.

four known parturitions. Although there are additional

suggestions in the literature of unusually high infant
mortality in the wild (Johnson et al., 1988; Hu, 1990;
Gittleman, 1994), the information available at this time
is too scanty to permit rm conclusions. Studbook data
(Xie & Gipps, 1997) indicate survival to 30 days of
68.1% for litters of a single cub (n = 69), and of 54.7%
for at least one cub in twin litters (n = 64). However,
captive data are unlikely to be a reliable guide to
survival rates in the wild.
Birth weights and altriciality
Among eutherian mammals, it is well known that the
ursids are exceptional in the extent to which they
deviate from the regression of newborn weight on
maternal weight (Leitch, Hytten & Billewicz, 1959). For
example, in a study of American black bears, Alt (1989)
gave an average birth weight for individual cubs of
363.7 g (n = 33) and an average litter (n = 10) weight of
1162 g. For parturient dams the average body weight
was 101.2 kg. Thus, individual cubs averaged 0.36% and
litters 1.14% of female body weight.
Giant pandas take this trend even further. Schaller
et al. (1985) reported an average birth weight of 104 g
(range 75 175), and we assume these are for individuals
from both single and twin litters. Our search yielded
birth weights for 26 cubs, including 10 sets of twins
(Celma Villares et al., 1985; Tellez Giron & Gomez
Llata, 1990; Huang, 1994; Liu et al., 1994; Song et al.,
1994; Zhong et al., 1994; Montali, 1997). Individual
weights averaged 112.3 36.3 g, whereas litter weights
(n = 16) averaged 165.5 75.1 g.
Captive panda females may tend toward obesity, with
weights  150 kg known to have occurred (Morris &
Morris, 1966). From our observations of wild females
and those by Schaller et al. (1985), including two which
were actually weighed, we estimate a range of about
75 110 kg and an average of about 90 kg for fully
mature females. Based on the observed weights for
captive-born offspring, individual cubs averaged 0.12%
and litters 0.18% of female body weight. Alt (1989) used
the Leitch et al. (1959) regression equation to obtain a
predicted weight of 7924 g for litters of American black
bears, but found them to be 6.8 times lighter than
predicted. Using the same procedure for giant pandas,
we found litters to be 43.4 times lighter than predicted.
These values differ somewhat from those presented
for giant pandas in comparative studies of carnivore life
histories (Gittleman, 1986; Gittleman & Oftedal, 1987;
Oftedal & Gittleman, 1989), in which mean weights for
dams as high as 120 kg were used, but nevertheless
clearly establish that pandas deviate substantially more
than bears from the regression of newborn weight on
maternal weight.
Ramsay & Dunbrack (1986) attribute the unusually
small size of ursid cubs at birth to the need to shift from
transplacental to mammary nourishment during the
dam's winter dormancy which, in turn, is mandated by

the seasonal scarcity of food. A period of uterine

growth of only 68 weeks shortens the transplacental
phase of litter nourishment, and avoids the potentially
fatal depletion of maternal protein. Cub growth following birth is sustained by mammary nourishment to
the end of the dormant phase 4 6 weeks later, at which
time the cubs are at the weight predicted by regression.
The same constraints obviously do not apply to the
giant panda, for which dams have year round access to
adequate food resources. The very small size of panda
infants could be part of a larger pattern of economy in
pre-natal investment in reproduction (including delayed
implantation and short gestation), due to the pandas'
subsistence on a diet which Schaller et al. (1985: p. 235)
describe as `extraordinarily limited', and thus an independently evolved life-history trait. However, if panda
cub size at birth is a reection of the phylogenetic
conservatism of life-history patterns (Harvey & Read,
1988) for a species whose afnities are with the ursids,
subsistence on a low quality diet may be at best a
secondary factor accounting for further reduction in
size of an already small infant.
Given its short life as a foetus and small size at
parturition, it is not surprising that panda cubs surpass
the majority of canids, felids and ursids in altriciality
(Oftedal & Gittleman, 1989). The descriptive data compiled for this report on physical state at birth and for
such landmarks as opening of the eyes and emergence of
the dentition (Table 5) are in general agreement with
those summarized by Schaller et al. (1985: table 6.9,
p. 196) for captive-born neonates. Apparently, dietary
differences between the two milieux have little effect on
these traits.
Maternal solicitude
The counterpart of a high degree of altriciality is a high
degree of maternal investment in care-giving behaviour
(May & Rubenstein, 1984; Harvey & Read, 1988).
Hibernating ursids are an exception, being in a state of
dormancy during the initial weeks of the post-partum
phase. Although very little information on behaviour in
the den is available, semi-popular accounts (Rogers,
1981; Lynch, 1993) indicate that black bear dams lie in a
semi-circle within which the cubs nd warmth and,
through their own efforts, locate the teat by detection of
its higher temperature (Lynch, 1993). Although in a
dormant state, the dam does stimulate the voiding of
cub excreta and apparently is responsive to their loud
vocalizations as needed. Oftedal et al. (1993), for
example, noted a case in which the litter died from
exposure to the cold, suggesting cubs' vocalizations may
have been ignored by the dam.
Panda dams, in contrast, support the infant on their
bodies more or less continuously for the rst 1 to 2 weeks
of life. Not only do they forego feeding and drinking
during this phase (see section on post-partum fasting)
but, as results from this study indicate, are actively
engaged in facilitation of suckling, thermoregulation,

Reproduction in giant pandas

grooming and bowel and bladder stimulation. In fact,
the amount of support provided by the dam in holding
the neonate to her body meant that we could only get
occasional glimpses of it during videotaping sessions
(Fig. 4a). Schaller et al. (1985) described a captive
female who did not let the infant off her body during
the rst 26 days post-partum, and Celma Villares et al.
(1985), who conducted a 24-h watch at the Madrid Zoo,
noted that the dam rarely separated herself from the
infant during the rst weeks of life, even carrying it in
her mouth when she moved out of the nest to urinate.
Captive females might be overly protective in the
presence of humans, but the striking similarity of these
observations to ours for the wild female Jiao Jiao
suggests that a high degree of maternalinfant contact
during the rst 2 or 3 weeks of life is typical of panda
dams.
Although Jiao Jiao began leaving the den 13 days
after parturition, and did so at an increasing rate over
subsequent weeks (Fig. 3), on those occasions when she
was present she held the infant on her body in excess of
80% of taped segments to the end of the denning period
at 94 days of age (Fig. 4a).
Cub growth and development
Weight gains for two wild-born cubs, beginning at 28
and 52 days respectively (Fig. 2), proceeded at a rate of
about 60 g/d. We know of no other reports of repeated
weights for wild-living cubs. In a captive study, Zhang
et al. (1996) reported an average daily gain of 71.4 g
(n = 4), but rates increased from an average of 47.1 g/d
during the rst month to 110.4 in the 6th month.
Although starting out at a lighter weight at parturition
than black bear cubs, it is of some interest to note that
at 4 weeks of age the male cub in this study weighed
1.35 kg, compared to 0.94 kg for 13 black bear cubs at
the same age (Alt, 1989). The weight disparity was even
greater at 10 weeks, i.e. 3.9 kg vs. 2.2 kg. Comparisons
based on a single individual are unconvincing; however,
the similarity in weight gains between the two wild-born
individuals (Fig. 2) and their rough agreement with
captive data (see also growth curves for three cubs in
Davis, 1964) adds condence to the conclusion that in
the initial months giant panda cubs grow at a faster rate
than black bear cubs. Even so, according to Gittleman
& Oftedal (1987), giant pandas t the pattern of large
bodied felids and ursids in having relatively slow
growing offspring.
Preliminary analysis of giant panda milk reveals it to
be much lower in fat content than that of polar bears,
but probably equivalent to that of black bears (Oftedal
& Gittleman, 1989). According to Schaller et al.
(1985), cubs begin to ingest bamboo leaves at about
56 months of age, and appear to be fully weaned at
8 9 months. At the time of den abandonment at
94 days of cub life, the infant in this study (Sun) neared
6 kg in weight. By this time, giant panda cubs are
tolerant of low winter temperatures and snow. They are

153

unable to locomote efciently until 35 months of age,

however, and are thus unable to accompany the dam as
she forages. Safety at this time is found in resting in lairs
of dense vegetation or in the trees. Eventually, however,
panda cubs resemble bears at breakout from the den in
maintaining contact with the mother during travel.
CONCLUSIONS
To summarize, the picture that emerges for giant
pandas is of a short gestation which includes delayed
implantation of the embryo until about 2 months before
parturition; the birth of twins in nearly half of all litters
but with maternal interest in and nurturance of only one
cub; cubs that are of greater altriciality and smaller size
relative to adult dam size than any other eutherian
mammal; a variable period of fasting as the dam
remains in the den after parturition; an active role by
the dam in caring for the young; a denning period of
about 4 months' duration and emergence in early
winter; production of milk which is relatively high in fat
content; slow infant growth and development compared
to most other mammals; a transition to solid food
beginning at about 56 months of age; complete separation from the dam at 2 or sometimes 3 years of age; rst
reproduction for females at about 6 years; production of
a litter of one surviving cub every 2 years on average;
and maximum lifetime contribution of 7 8 cubs by the
end of dams' reproductive life span at about 19 or 20
years of age.
There are two competing hypotheses which may be
advanced to account for the reproductive strategy of the
giant panda. One of these is an extreme conservatism in
reproductive expenditures which is mandated by a
carnivore relying on a continuously available but nutritionally poor food source, as favoured by Schaller et al.
(1985, 1989). We agree that the giant panda's approach
to reproduction is undoubtedly constrained by adaptation to a way of life that fossil material indicates began
at least 3 million years ago (Pei, 1974). Thus, birth
weight is even smaller relative to adult dam size than in
bears, gestation is somewhat shorter, litter size is
typically smaller, and lactation cannot be sustained for
more than a few days without signicant nutritional
intake. However, carnivore life-history traits do not
generally correlate well with ecological ones (Gittleman,
1993, 1994) and, for that matter, need not be entirely
accounted for as adaptations to current circumstances
(Gould & Lewontin, 1979; Gould & Vrba, 1982; Boyce,
1988b).
Alternatively, some aspects of giant panda reproduction may be more judiciously seen as expressions of a
common phylogeny with the Ursidae. Although the
subject of the giant panda's true afnities still generates
controversy (Schaller et al., 1985; Zhang & Shi, 1991;
Schaller 1993; Zhang & Ryder, 1993; Waits et al., 1999),
there is an emerging concensus, based largely on
molecular data (O'Brien et al., 1985; Wayne et al., 1989,
Bininda-Emonds et al., 1999), that they very likely

154

X. Zhu ET AL.

shared a common ancestry with bears. Although we

cannot yet conrm the extent of constraints imposed by
reliance on bamboo as the principal food source, some
aspects of panda reproduction seem to us to reect the
conservatism of phylogeny. Why, for example, should
pandas have twins at all, given that dams appear unable
to care for more than one? Despite apparent low cost of
foetal production, investment in an offspring which
appears in many cases to lack viability at birth, yet
occurs in nearly half of all births, seems to us to be poor
insurance against reproductive failure should one cub
not survive, as suggested by Schaller et al. (1985).
Although litter pruning occurs in other mammals in
seasons having poor prospects for rearing (Tait, 1980;
Clutton-Brock, 1991), giant pandas do this routinely, in
good years and bad, and do so at the very start of life
outside the womb. Although it is theoretically possible
that giant panda females evaluate the viability of their
offspring immediately after birth and select the cub with
the greatest chance of survival, there are insufcient
data available to substantiate this hypothesis. An alternative scenario is that twinning is an ancient trait
stemming from membership in a phylogenetic line in
which litter size of two or more is the norm. Other traits
such as delayed implantation and extremely small birth
weight may be additional examples of phylogenetic
conservatism as opposed to adaptation to a frugal
nutritional niche.
Acknowledgements
We thank Drs. John Gittleman and Ronald Swaisgood,
and an anonymous reviewer, for providing comments
on this manuscript.
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