Reproductive Seasonality of Myanmar Long-tailed Macaque (Macaca fascicularis aurea)

2009·0.29 MB·

by  San, Aye Mi

The Natural History Journal of Chulalongkorn University 9(2): 223-234, October 2009
©2009 by Chulalongkorn University

Reproductive Seasonality of Myanmar Long-tailed Macaque
(Macaca fascicularis aurea)

AYE MI SAN1 AND YUZURU HAMADA2*

1Department of Zoology, Yangon University, University Avenue Road,
Kamayut, Yangon, Union of Myanmar.
2Evolutionary Morphology Section, Primate Research Institute, Kyoto University,
41-2 Kanrin, Inuyama, Aichi, 484-8506, Japan.

Abstract.– The Myanmar long-tailed macaques (Macaca fascicularis aurea)
are distributed to coastal regions in Myanmar, ranging from 10˚ to 21˚N.
Reproductive pattern was studied on a troop of long-tailed macaque
inhabiting the steep limestone-rock Bayin Nyi Naung Mountain (16˚ 58.2' N),
in Southern part of Myanmar, where the climate is seasonal. Bayin Nyi Naung
Mountain troop shows the reproductive seasonality which appears to be
related with the seasonal food availability. Birth season occurs from March to
July that coincides with the food abundance season and mating occurs during
November to February that during the lean season. There are positive
correlations between rainfall and fruit availability, mean temperature and
frequency of birth, fruit availability and lactation. There is a highly
significant correlation between rainfall and lactation. The rainfall is critical
determining food abundance and the rainy season is the best period for
females to lactate to grow up their infants.

KEY WORDS: Macaca fascicularis aurea, Myanmar, food availability, reproductive
seasonality

fascicularis aurea. This subspecies is
INTRODUCTION
distributed to the area along coastal regions

and is continuously from Southern end
The long-tailed macaques (Macaca
(Thanintaryi Division, 10˚ N) to the
fascicularis) are widely distributed in the
Northwestern end in Myanmar (Rakhine
insular and peninsular Southeast Asia
State, border with Bangladesh, 21˚ N; Aye
ranging from ca 10˚ S to 21˚ N (Fooden and
Mi San, 2007 and Nwe et al., 2005) with
Albrecht, 1999). Fooden (1995) classified
some populations inhabiting the Andaman
long-tailed macaques into 10 subspecies, of
sea coastal localities in Thailand and the
these the Myanmar subspecies is M.
southeastern-most area of Bangladesh
(Fooden 1995; Malaivijitnond et al., 2005).
*Corresponding author: This subspecies has rarely been reported.
Tel: [phone]
Every primate species is considered to adapt
Fax: [phone]
to its own habitat in general, and the
Email: [email protected]
224 NAT. HIST. J. CHULALONGKORN UNIV. 9(2), OCTOBER 2009
Myanmar subspecies (M. f. aurea) should to 21˚ N, is considered as the good model to
have adapted to their specific habitat, elucidate the relationship between
particularly to the habitat in rather higher environment and reproductive seasonality.
latitude for the species. The climate in higher We evaluated fluctuations in the food
latitude tends to be seasonal in rainfall and availability, rainfall, and temperature across
temperature, which is reflected by the seasons and their effect on the pattern of
phenology of food plants. Primates living in reproduction of a troop in Bayin Nyi Naung
seasonal environment with respect to food Mountain (16˚ 58.2' N, BNNM), which
availability, rainfall, and temperature, appear locates the intermediate in the range of this
to respond to different environmental signals subspecies. The climate in BNNM shows
to determine the timing of reproductive clear seasonality; hot, rainy and cool seasons
events (Crockett and Rudran, 1987; Gevaerts, with seasonal precipitation and temperature
1992; Lancaster and Lee, 1965). pattern. Our goal was to examine the role of
Annual fluctuations in food abundance food availability and environment factors that
undoubtedly affect the time of female effect on the reproductive patterns of M. f.
fecundity and reproduction. In Old World aurea.
monkeys, birth season and birth peak
(Butynski, 1988, Lindburg, 1987; Nakagawa,
MATERIALS AND METHODS
2000), conception period (Koenig et al.,

1997), or period of lactation (Lee, 1987)
Study Area
appear to be determined by the food
A population of long-tailed macaques
abundance. van Schaik and van Noordwijk
inhabiting Bayin Nyi Naung Mountain
(1985) stated that in an environment with
(BNNM), Kayin State, Southern part of
unpredictability in the height of the annual
Myanmar is the subject. The habitat locates
food peak, pregnancy rather than lactation
at the right bank of the Thanlwin River, at
coincides with the period of food abundance.
16˚ 58.2' N and 97˚ 29.6' E. The BNNM is a
The long-tailed macaques (M. f.
natural limestone steep mountain with wild
fascicularis) distributed to the lower latitude
vegetation of evergreen lowland forest. The
do not exhibit distinctive reproductive
area is surrounded by river, wetlands,
seasonality, as Furuya (1965), Chiang
agricultural fields, and human settlements.
(1968), and Mah (1980) reported for the wild
Thus, the population is isolated from
long-tailed macaques distributed in
neighboring conspecific populations. BNNM
Peninsular Malaysia and Singapore.
is low in altitude, and the highest peak of the
Fittinghoff (1978) and Wheatly (1978)
mountain is 122 m above sea level (a.s.l),
mentioned that M. f. fascicularis in Borneo
however, the slope is so steep that it is
produce infants in 10 months of the year at
difficult to walk around the mountain. There
least. However, M. f. fascicularis in Sumatra
are two major study sites; site No. 1 is
showed birth peaked in the second half of the
situated near the entrance of the cave at 16˚
calendar year (van Schaik and van
58' 16.5" N, 97˚ 29' 37.4" E and 39 m a.s.l;
Noordwijk, 1988). Although it is supposed
site No.2 is situated at the south-western foot
that the reproduction becomes definitive in
of the BNNM along the walking pass to the
higher latitude, no study was made.
cave at 16˚ 58' 11.7" N, 97˚ 29' 36.4" E, and
The Myanmar subspecies (M. f. aurea),
3 m to 34 m a.s.l., with three ha of area. We
which ranges widely in latitude, from 10˚N
SAN AND HAMADA — REPRODUCTIVE SEASONALIFY OF MACAQUE 225
observed macaques from the stairways and characterized by three defined seasons: a hot
paths connecting the two study sites. Long- dry season from March to May, rainy season
tailed macaques spent most of their day time from June to October and a cool dry season
in these sites. from November to next February. July and
August are the two wettest months,
Climate and Vegetation contributing 56% -58% of the total annual
Based on climatology data recorded at the rainfall. The mean monthly rainfall and
Meteorological Department, Tha-ton city temperature during January 2004 to May
situating 7.7 km from the BNNM, between 2007 were shown in Fig. 1.
January 2005 and May 2007. The climate is
1600 32
1400
30
1200
)
mm) 1000 28 re (C
ainfall ( 800 26 mperatu RTeaminfpaellr a(tmumre)(˚C)
R
an 600 24 n te
e a
M e
400 M
22
200
0 20
J F M A M J J A S O N D
Month

FIGURE 1. Monthly temperature and rainfall at the Meteorological Station of Tha-ton.

Although the wild vegetations cover the Subject Population
whole mountain, vegetation in the two study The subject macaques were classified as
sites were changed by humans, which are the Macaca fascicularis aurea by their
dominated by Ficus sp., Litsaea sp., morphological traits, that is, infrazygomatic
Artocarpus sp., Mangifera indica, Xylia sp., pattern of cheek hairs and no hair-crest at the
Annona sp., Carica papaya and Stephania vertex of the head (Fooden, 1995; Aye Mi
venosa. The food plants were identified and San, 2007). Individuals were classified into
phenological states, that is, presence or six sex-age classes based on their
absence of young leaves, ripe or unripe fruits, morphological characteristics:
and flowers, were determined. The
percentage availability of fruits were monthly Adult Male (Ad-M): secondary sexual traits
calculated. completely developed, such as muscular
226 NAT. HIST. J. CHULALONGKORN UNIV. 9(2), OCTOBER 2009
body, distinct cheek hair and fully r red coloration (without swelling)
erupted canines around the genitalia
Adult Female (Ad-F): parous with nipples + slight swelling under the tail root
elongated by suckling ++ medium-sized swelling under the tail
Sub-adult Male (Sub-M): fully grown linear root
body size with suspension of testicle +++ large swelling under and sides of the
Sub-adult Female (Sub-F): reproductively tail root continuous to the genitalia
mature but nulliparous indicated by the
shorter nipples All socio-sexual behaviors, including
Juvenile (Juv): weaned and reproductively sexual solicitation, copulation, interference in
immature copulation, and rejection of copulation were
Infant (Inf): blackish pelage and carried by recorded. In addition to the recording of
the mother. The color gradually changed sexual interactions, mating partners were
during development. Neonates (age less identified and consortships were recorded
than 1 month) were determined by size, with the focal animal sampling method.
blackish pelage, pinkish skin, forehead The pregnant females and neonates and/or
hair pattern, and uncontrolled behavior. small infants were counted. Although the
exact dates of births could not be determined,
Individual Identification and observation we assigned a birth month to each infant
Seven adult males and eleven adult based on monthly census data (From
females were selected as focal animals. All January, 2005 to May, 2007) and the
these individuals were identified by their developmental states (body size, pelage
natural marks on the body (scars, lack of color, and positional behavior).
finger, wart, and so on), physiognomic
differences, pelage color pattern, body size Data Analysis
and habit. Feeding activity data were summarized by
diet category and percentage of food
Observation of Behavior availability was calculated for each month.
Behavioral observation was made bi- Fruit availability (%) was calculated by the
monthly in four consecutive days on 18 focal division of number of fruit species with the
animals. We visited the BNNM two times total number of plant species and
per season, and totally 15 times of multiplication of 100. The Simpson’s
observations were made during January, Diversity Index (Levins, 1968) was used to
2005 to May, 2007. Instantaneous focal evaluate seasonal variation in dietary
animal sampling (Martin and Bateson, 2000) diversity. The index was calculated as
was used to record the activity (rest, feed, follow: D=1/∑P2, where P was the observed
i i
travel and social) of each focal animal in 3- feeding frequency of i-th plant species.
min intervals. Focal samples lasted for 15 According to Eisenberg et al. (1981), annual
min, were conducted between 07:30 and birth rate [b] was obtained by b= I/F, where
t t
17:30 hr daily. During the study period we I is the number of births observed in a year
t
completed 2,160 (15 min) focal samples (t) and F is the number of adult females
t
totaling 540 hr of focal observations. observed during the same period. All
Swelling states were recorded for focal analyses were performed using SPSS
animals as follows (Engelhardt, et al. 2004); statistical software version 13.5.
SAN AND HAMADA — REPRODUCTIVE SEASONALIFY OF MACAQUE 227
RESULTS shows the mean numbers for age and sex
classes. The sex ratio was 1: 1.2 (male:
Population Structure female), and the mean number of adult male
The population size of the long-tailed was significantly smaller than that of adult
macaque in BNNM was found to range from female (t= -3.595, P= 0.003).
29 to 49 animals (mean 39.7±4.9). Fig. 2

FIGURE 2. Population structure of Bayn Nyi Naung Mountain troop: Mean number and standard deviation in
each age and sex class.

Food Availability and Diet fluctuated seasonally from 9 to 17.
Based on the individual activity Availability of fruits (number of species) in
records of feeding, the long-tailed macaque the BNNM peaked from June to July, that is,
used at least 23 plant species from 15 during the rainy season; and reached the
families in two study sites of BNNM (Table nadir during the cool season (Fig. 3).
1). The number of natural food plant species
228 NAT. HIST. J. CHULALONGKORN UNIV. 9(2), OCTOBER 2009
TABLE 1. List of Plant Species Utilized as Food in BNNM

Scientific Name Myanmar Name Family Status* Fruit Leaf Flower Stem
Ficus glomerata Thapan Moraceae T √ √ √
Ficus sp. Nyaung Moraceae T √ √ √
Artocarpus
Peinne Moraceae T √ √
heterophyllus
Mangifera indica Thayet Anacardiaceae T √ √ √
Zizyphus jujuba Zi, Zi-daw Rhamnaceae T √
Moringa oleifera Dant-tha-lon Moringaceae T √ √ √
Carica papaya Thinbaw Annonaceae T √ √ √
Annona sp. Awza Annonaceae T √ √ √
Eugenia Taung-thabye Myrtaceae T √ √
Averrhoa carambola Zaung-ya Averrhoaceae T √ √
Dipterocarpacea
Shorea cinerea Kadut T √ √
e
Cedrela serrata Taung-tama Meliaceae T √ √ √
Tamarindus indica Magyi Caesalpiniaceae T √ √
Phyllanthus urinaria Taung-zi-phyu Euphorbiaceae T √
Litsaea sp. Ondon Lauraceae T √
Cynodon dactylon Myesa-myet Graminae G √
Paspalum distichum Sinngo-myet Graminae G √
Convolvulus arvensis Kyauk-yo-nwe Convolvulaceae C √ √
Ipomoea sp. Kazun Convolvulaceae C √ √
Hinnu-nwe-
Amarantus spinosus Amarantaceae H √
subauk
Citrus sp. Than-ba-ya Rutaceae Sh √
Citrus decumana Kywe-gaw Rutaceae Sh √
Dendrocalamus sp. Hmyin-wa Graminae B √

*: Status of plant, T for Tree, G for Grass, C for Climber or Creeper, H for Herb, Sh for Shrub, and B
for Bamboo.
SAN AND HAMADA — REPRODUCTIVE SEASONALIFY OF MACAQUE 229

FIGURE 3. Availability of natural plant foods and percentage of fruit species eaten.

Simpson’s diversity index (D=1/∑Pi2) Fluctuation of mating and birth
ranged from 7.17 in cool season to 8.08 in Although the occurrence of estrous cycle
rainy season, and the overall average was is spread rather evenly over the year, the
7.61. In all seasons four species of plants highly frequency of the mating occurred in
were most frequently used by macaques, that November to February (cool season), which
is Ficus sp., Ficus glomerata, Mangifera is the period of low plant food availability
indica and Artocarpus sp. or heterophyllus. (Fig. 4).

18 45
)
16 40 an
e
vailability 111024 3305 uency (M MF(Mraeetqiaunneg)n cy
A 25 eq
nt 8 Fr
Pla 6 20 ng Plant
ti Availability
4 15 Ma
2 10
J F M A M J J A S O N D
Month

FIGURE 4. Relationship between the ratio of females (%) showing mating behavior and availability of food plants.
230 NAT. HIST. J. CHULALONGKORN UNIV. 9(2), OCTOBER 2009

Seasonality of Birth and 0.31 – 0.46 in 2007 (according to the
Early pregnancy could not be discerned result of the two pregnant females).
visually, however, mid or late pregnancy Birth dates, which were determined from
could be noticed by the body profile of the focal observation of pregnant females and
females. At least four females were pregnant the developmental states of neonates and
in the year 2005 and seven in 2006 and six infants, were confined to the period from
in the year 2007 (observation was made until March to July. The greatest number of
May). A total of 15 births and two pregnant births per month, four, was recorded in
females (in May 2007) occurred in study March out of seven births in the year 2006.
group. Live births were found for these Neonates carried by their mothers were not
females showed pregnancy. The birth rate found in September to February during the
(b) from year to year ranged from 0.36 study three years (Fig. 5).
infants/female/year in 2005, 0.54 in 2006,

FIGURE 5. Number of neonates in the study period from 2005 January to 2007 May.

Relationship among Climate, Food highly significant one between mean
Availability and Reproduction temperature and availability of leaves (Rs =
We calculated Spearman’s coefficients of -0.630, P = 0.000). There is a positive
correlation among climate (monthly means of correlation between mean temperature and
rainfall and temperature), food availability birth (Rs = 0.471, P = 0.010) in the BNNM
(leaves and fruits) and reproduction (births and group. However, there is no relationship
lactation). We found significant correlations between rainfall and birth (Rs = -0.021, P=
between rainfall and availability of fruits (Rs 0.921). There is also a highly significant
= 0.509, P = 0.005) and a negative correlation correlation between rainfall and number of
between mean temperature and availability of lactating females (Rs = 0.812, P= 0.000) and
fruits (Rs = -0.566, P = 0.001). There is a no relationship between mean temperature
positive correlation between rainfall and and number of lactating females (Rs = 0.181,
young leaves (Rs = 0.417, P= 0.029) and a P= 0.347).
SAN AND HAMADA — REPRODUCTIVE SEASONALIFY OF MACAQUE 231
A negative correlation was found between young leaves at BNNM begins just prior to
birth and availability of leaves (Rs = -0.405, or at the early stage of the rainy (wet) season.
P= 0.029) and no relationship was found There is a positive correlation between
between birth and fruit availability (Rs = - rainfall and fruit availability and negative
0.198, P = 0.303). The positive correlation correlation between mean temperature and
was found between availability of fruits and fruit availability.
number of lactating females (Rs = 0.472, P = Correlation between birth and food
0.010) and there is no relationship between availability has also been confirmed in many
number of lactating females and availability species of primates, including Cercopithecines
of young leaves (Rs = 0.0204, P= 0.289). in Asia (Andelman, 1986). BNNM population
follows the ordinary reproductive
seasonality. Field studies have shown that
DISCUSSION
the yearly pattern of reproduction is related

to rainfall and food availability in squirrel
Reproductive Seasonality
monkey (Saimiri, Boinski and Fowler, 1989),
The primates distributed to the higher
so that the birth season occurs during the
latitude tend to be seasonal breeders. Long-
time of the year when fruit production is the
tailed macaques (Macaca fascicularis),
greatest (Boinski, 1987).
which are distributed to the lower latitude,
The seasonality of foods is the
have been studied to show the spectrum from
determinant of reproductive seasonality.
non-seasonal to partially seasonal breeders
Most colobine monkeys in Africa, which are
(Fooden, 1995). The long-tailed macaques in
mainly folivores, breed throughout the year
Myanmar (Macaca fascicularis aurea) are
with a variable pattern of birth peaks
distributed to the higher latitude for the
(Struhsaker and Leland, 1987), and baboons,
species, and therefore, are good subject for
which are omnivores (graminivores), are also
elucidating the relationship between
non-seasonal breeders. On the other hand,
environment and the reproduction. In
long-tailed macaques at BNNM are primarily
Myanmar, there are three different seasons in
folio-frugivores and utilize at least 23 species
general, hot (March to May), rainy (late-May
of trees and shrubs. Among them, they
to October) and cool season (November to
frequently used four species of tree plants.
next February), and accordingly food
The Ficus glomerata, that is the major food
availability is highly seasonal. The weather
fruits, offers not only fruits but also leaves
in BNNM also exhibits seasonal variation in
and buds which are exceptionally available
temperature and rainfall (Fig. 1), with the
throughout year. Yeager (1989) stated that
majority of rain occurring in June through
dietary necessity is the most highly satisfied
mid-October. Although we controlled neither
during the period of high fruit availability
availability of plant species nor quantity of
and the least during periods of fruit scarcity.
food items, the results indicate that the
The BNNM long-tailed macaques had
BNNM forest is characterized by greater
definite season of birth restricted to five
temporal variability in the availability of
months in a year, from March to July (hot
fruits and leaves. Fruit abundance shows
and rainy season), just before the peak of
seasonal fluctuation which is shown by
fruits and leaves (June and July) (Fig. 6).
Simpson’s diversity index, the highest in
Mating and conception occurred during cool
rainy season (8.08) and the lowest in cool
season (November to February) when
season (7.17). The peak in flowers and
232 NAT. HIST. J. CHULALONGKORN UNIV. 9(2), OCTOBER 2009
animals are in good nutritional condition occur in hot and early rainy season (March to
after feeding on abundant fruits and young July), when fruits and young leaves are
leaves (June to October) (Fig. 4). Pregnancy flourishing, which fulfilled the nutritional
lasted the whole cool season when the troop requirements of lactating females.
only relied on poor food resources. Births

FIGURE 6. Relationship between the number of birth and availability of natural plant.

The lactation may be the major rising and high food availability, and another
determinant of the reproductive seasonality. In is that the period of pregnancy is during a
BNNM, the birth season starts from the rise in the availability of food to store
March (hot season) and the mid or late- reserves. Myanmar long-tailed macaques
lactation which necessitates mother to greatly followed the first strategy.
invest coincides with the timing of higher What environmental cue starts mating is
rainfall and higher fruit availability, in June not known for the long-tailed macaques (M.
to October (rainy season). There is a positive f. aurea). Temperature (and daytime) seemed
correlation between the fruit availability and to have the greatest impact on the initiation
number of lactating females. The period from of mating season. As temperature decreased,
mating (conception) to the birth coincided number of mating per month increased.
with that of the low availability of fruits and Births (parturitions) occurred when it was
young leaves in BNNM. hotter. This is the pattern that was expected
Van Schaik and van Noordwijk (1985) and also is in agreement with Dumond’s
suggested that there are two different (1968) observation of mating during winter
strategies in which monkeys tune their and births during summer. Thus, BNNM
reproductive cycle to the food availability; troop follow the ordinary reproductive
one is that the conception coincides with the seasonality.
lean season and lactation with the period of