Effects of group size on birth rate, infant mortality and social interactions in Formosan macaques at Mt Longevity, Taiwan

 Effects of group size on birth rate, infant mortality

and social interactions in Formosan macaques

at Mt Longevity, Taiwan

M.J. Hsu 1, J.F. Lin 1,2 and G. Agoramoorthy 3,4

1 Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung 804,

Taiwan

2 Shi-Pu Junior High School, Kaohsiung 840, Taiwan

3 Department of Pharmacy, Tajen University, Yanpu, Pingtung 907, Taiwan

Received 5 October 2004, accepted 16 November 2005

In social animals, the influence of life-history traits on group structure and

size is potentially important in the context of the evolution of social systems.

Birth rate and infant survival have been differently predicted as a function of

group size by models of the evolution of group living in primates. A wild population

of the Formosan macaque, Macaca cyclopis that inhabits Mt Longevity,

Taiwan has been monitored since July 1993 to collect demographic, reproductive

and social behaviour data. Little is known about the effects of troop size

on population growth in Formosan macaques. In this paper, we have presented

for the first time 5-years of data (1997-2001) on the troop dynamics of 14 social

troops. We also examined the effects of troop size on birth rate, infant mortality

and inter-troop social interactions.

The annual average troop size increment fluctuated from 1.94% to 10.97%.

The annual average troop size of 14 groups was 43.57 ± 15.88 individuals in 1997,

and increased to 55.97 ± 16.86 individuals in 2001. The per-capita rates of troop

size increase was negatively correlated with troop size without infants (F1,12 = 5.57,

P < 0.05). The average birth rate (birth per adult female) was 0.78 (± 0.07, n = 14)

and it was not linearly related to troop size, nor the number of adult females (P >

0.33). The average infant mortality was 0.16 (± 0.09, n = 14), which was relatively

constant regardless of the troop size category (small, medium or large). Intertroop

dominance was closely dependent on the number of adult males and females

rather than group size. Thus larger group size imposed an advantage on habitat

utilization without the appearance of low birth rate or high infant mortality. On

the other hand, infant mortality increased and infant survival per adult female

decreased when the percentage of adult females increased in troops. Therefore,

competition among adult females plays an important role partially supporting the

predation — intra-group feeding competition hypothesis.

key words: Formosan macaque, Macaca cyclopis, Taiwan, troop size, infant mortality,

birth rate, social interaction.

Ethology Ecology & Evolution 18: -17, 2006

4 Corresponding author (E-mail: agoram@mail.nsysu.edu.tw).

M.J. Hsu, J.F. Lin and G. Agoramoorthy

Introduction . . . . . . . . . . . . . . . . . 4

Materials and methods . . . . . . . . . . . . . . 5

Results . . . . . . . . . . . . . . . . . . 7

Troop size and growth rate . . . . . . . . . . . . . 7

Natality . . . . . . . . . . . . . . . . . . 9

Infant mortality . . . . . . . . . . . . . . . 10

Inter-troop interactions . . . . . . . . . . . . . . 11

Discussion . . . . . . . . . . . . . . . . . . 13

Troop size and effect on demography . . . . . . . . . . 13

Social interactions . . . . . . . . . . . . . . . 15

Acknowledgments . . . . . . . . . . . . . . . . 15

References . . . . . . . . . . . . . . . . . 16

INTRODUCTION

Most diurnal primates exhibit a wide range of social grouping patterns. The

groups may vary widely in size, age and sex classes and cohesiveness. The benefits

that result from group living and the extent to which animals of different ages

and sexes share these benefits, remain an area of contention (Chapman et al. 1995,

Lefebvre et al. 2003). Macaques are an excellent taxonomic group to address such

issues since most species form cohesive groups and exhibit variation in group size

and structure. Birth rate and immature survival rate have been differently predicted

as a function of group size by models of the evolution of group living in primates.

According to Wrangham’s (1980) inter-group feeding competition hypothesis, large

groups have an advantage in accessing resources. This hypothesis predicts that birth

rate may exhibit a humped curve against group size of female-bonded primates,

and it indicates that the infant per female rate is expected to be higher in medium-

sized groups and lower in large- and small-sized groups (van Schaik 1983). In

contrast, the predation — intra-group feeding competition hypothesis proposed by

van Schaik (1983) suggests that the birth rate may decrease with group size when

intra-group competition becomes very intense (Sterck et al. 1997). This hypothesis

predicts that infant per female rate should decrease when group size increases.

In addition, when natural predators occur, mortality among immature individuals

should be higher in smaller-sized groups of social primates (van Schaik 1983). Nevertheless,

the controversy continues concerning the interpretation of the correlation

between reproductive parameters and troop size in female-bonded primates (Janson

& Goldsmith 1995, Kumar 1995, Takahata et al. 1998a).

Among the 21 extant species in the widespread genus Macaca, the Formosan

macaque, Macaca cyclopis, is one of the least known. It is endemic to the island

of Taiwan (area 36000 km2) and only a few field studies have attempted to understand

its population dynamics, reproduction and ecology (reviewed in Hsu & Lin

2001). Despite its wide distribution at various altitudes ranging from 100 to 3300

m, hunting pressure was substantial with mass captures of about 1000 macaques

annually for the purpose of medical research, the preparation of skeletons, Chinese

medicine (skeletal jelly), and the pet trade in the past (Peng et al. 1973, Masui et

al. 1986). Illegal poaching still continues despite the fact that this species is listed

in the IUCN (2003) Red List of Threatened Animals and protected by Taiwan’s

Wildlife Conservation Law (1989). Information on troop dynamics, life histories,

social behavior and reproduction are therefore important for the conservation of

this endemic species in Taiwan.

Effects of group size in wild Formosan macaques

We have been monitoring a population of M. cyclopis that inhabits the lowland

rainforest at Mt. Longevity, southern Taiwan since July 1993 (Hsu et al. 2000, 2001,

2002; Hsu & Lin 2001). The majority of the troops have a multi-male/multi-female

structure, which makes the population interesting for socio-ecological studies. Data

on birth seasonality and inter-birth intervals of this population were published

(Hsu et al. 2001), but little is known about the effects of troop size on population

growth. The aim of this paper is to present data on the demographic parameters

of multi-male/multi-female social troops of wild Formosan macaques that inhabit

Mt. Longevity, Taiwan. We examined the effects of troop size on birth rate, infant

mortality and inter-troop social interactions based on the predictions of the existing

hypotheses concerning the evolution of group living in primates (Wrangham 1980,

van Schaik 1983). We attempted to test whether intra-group female competition

reduced birth rate or increased infant mortality in social troops of wild Formosan

macaques.

Materials and methods

Study site

Mt Longevity (22°39’N, 120°15’E) is located in Kaohsiung City adjacent to the Taiwan

Strait and it has been isolated from other mountains over the last 50 years by to urban development.

Its natural forest has been preserved since the beginning of the last century mainly

because it was an active military base during the Japanese occupation of Taiwan (Hsu et al.

2001). The public has had access to this mountain only since 1989 and the northern part is

still an active military base to which civilians including researchers have no access. The protection

of the natural forest by the Taiwan military has left the habitat less disturbed. The

flora includes 215 species in 73 families and 176 genera. The total surface area of Mt Longevity

has been estimated as 35 km2. We used a topographic map to calculate the total area used

by all macaque troops that includes several raised coral reefs, undulating hillocks and valleys.

The study site, excluding the restricted area occupied by the military, covers about 25 km2.

According to the records of the Central Weather Bureau in Kaohsiung, the average

annual precipitation between 1997 and 2001 was 2288 mm (SD ± 465), concentrated from

June to August. The wet season, with monthly average above 100 mm, was from May to October

(Fig. 1). The dry season started in November and ended in March with a monthly average

rainfall below 50 mm. This pattern fits the characteristics of the seasonal variations in rainfall

demonstrated by Walter & Leith (1967). The average monthly temperature was coldest in

January (19.8 oC) and highest in July (28.8 oC). The average monthly humidity was above 75%

throughout the year.

Data collection

A thorough search of the forest, using trails, footpaths and line transects, enable us to

identify and follow 14 troops from 1997-2001 (Table 1). Some of these troops had also been

monitored since 1994 (Hsu & Lin 2001). We classified individuals into broad age and sex

classes based on direct measurement of chronological age from known birth year or based on

physical characteristics and body size (National Research Council 1981, Hsu & Lin 2001).

Most females give birth to their first infants around 5 years of age and we considered adult

females were equal to, or older than, 5 years. Subadult males were between 5-6 years, and

their secondary sexual characteristics not as fully developed as they are in adult males. Adult

males were equal to, or older than, 7 years. Individuals aged between 1 and 4 years were

M.J. Hsu, J.F. Lin and G. Agoramoorthy

considered juveniles. Infants of both sexes were typically nursing, cared for by their mothers,

and weaned at around six months of age (Hsu et al. 2000). Artificial feeding of monkeys at Mt

Fig. 1. — Monthly variations in rainfall and temperature at Mt Longevity

Taiwan between 1997 and 2001.

Table 1.

Demographic parameters including troop size, birth rate and infant mortality in Formosan

macaques at Mt Longevity (1997-2001). Data were indicated as mean (± SD).

Troop

name

No. adult

males

No. adult

females

Troop size

(without

infants)

Troop size Birth rate

(%)

Infant mortality

(%)

E 4.2 ±1.0 10.8 ±3.5 28.1 ±6.5 32.7 ±8.5 79.2 ±16.0 28.7 ±29.9

Ia 4.4 ±0.7 8.4 ±1.4 29.4 ±2.1 33.1 ±2.5 77.1 ±16.7 17.7 ±26.7

N 4.7 ±1.0 9.3 ±1.8 31.0 ±1.6 34.9 ±1.6 64.1 ±18.4 5.0 ±11.2

M 3.9 ±1.3 9.5 ±1.0 31.8 ±3.6 36.4 ±3.4 73.7 ±14.9 3.3 ±7.5

A 5.2 ±1.4 9.6 ±0.4 34.1 ±1.2 38.3 ±1.5 83.3 ±8.4 22.1 ±18.4

D 5.0 ±0.5 10.3 ±2.2 35.4 ±8.1 40.6 ±8.5 85.5 ±13.5 6.0 ±13.4

O 6.9±0.9 12.6±1.5 42.0±6.5 47.8±7.1 73.3±18.1 4.4±9.9

J 5.4 ±1.0 13.5 ±2.7 43.1 ±6.1 49.5 ±7.2 90.8 ±8.6 21.8 ±11.8

C 7.3 ±1.2 16.1 ±2.2 46.5 ±3.2 51.6 ±3.5 68.7 ±9.4 27.3 ±14.9

B 8.7 ±1.1 16.2 ±3.4 48.5 ±6.7 54.8 ±8.6 79.2 ±10.2 26.0 ±15.5

K 9.3 ±1.8 16.8 ±3.1 52.8 ±5.1 61.0 ±5.8 80.5 ±18.8 20.3 ±11.9

F 8.1 ±1.7 18.7 ±4.1 59.2 ±4.9 67.2 ±6.8 77.1 ±5.2 25.6 ±12.7

G 7.2 ±1.7 18.9 ±2.6 60.7 ±4.4 69.8 ±5.9 79.1 ±9.2 10.2 ±6.6

I 7.8 ±1.5 20.0 ±4.4 66.7 ±9.6 77.1 ±10.7 85.0 ±10.2 12.5 ±12.0

Effects of group size in wild Formosan macaques

Longevity is legally prohibited but some troops have home ranges that overlap with tourist

trails and receive occasional food items from visitors.

We conducted a systematic census to record troop composition changes twice a week

between January 1997 and December 2001. We included a temporary all-male group in the

troop with which it was most closely associated. We used focal animal sampling and scan

sampling (Lehner 1996) to record data on social interactions. We recorded inter-troop interactions

that included fight, chase, and displacement during close encounters between 1998

and 2001 to determine winner-loser or uncertainty and to establish an inter-troop dominance

hierarchy (Lehner 1996).

Calculation and analysis

Troop size at the end of each year was compared with that at the beginning by calculating

the annual per-capita rate of troop size increase. The mean annual per-capita rate of troop

size increase from 1997 to 2001 was calculated as the average annual growth rate. The mean

size of a troop for 5 years was the average of the annual average troop sizes from 1997-2001.

The time of conception was backdated from birth, assuming a gestation length of 163 days

(Hsu et al. 2001). All means are presented as the values ± 1 standard deviation. Birth rate was

calculated as the total number of births divided by the availability of sexually mature females

(? 5 years) in a troop, which is the crude birth rate. Infant weaning rate was the number of

infants weaned divided by the available number of sexually mature females (? 5 years) in a

troop. We calculated the percentage of winning events during aggressive conflicts as the total

number of winning events plus half of the counter attack events divided by the total number

of aggressive interactions of a troop.

We conducted all statistical analyses through Statistical Analysis System software (SAS

Institute Inc. 2000). We calculated Spearman rank correlation coefficients among demographic

parameters (Table 1). The Spearman correlation coefficient indicated that the mean

number of adults (males and females), troop sizes with or without infants, were significantly

correlated to each other (P < 0.001). Therefore, we used only one independent variable (base

on the higher R2) in various regression analyses to test the relationships with dependent variables.

Dependent variables included the number of births, the number of surviving infants,

the birth rate, the infant mortality, the infant survival rate, the number of infants weaned per

adult female, and the percentage of winning shown by the troop.

We used analysis of variance (ANOVA F test) within various General linear models to

test the effects of the independent variables (troop size with or without infants, number of

adult females or proportion of adult females) and categories (troop, year) on the dependent

variables.

Results

Troop size and growth rate

The annual average troop size for 14 troops fluctuated from an increment of

10.97% to as little as 1.94%. In 1997, the troop size was 43.57 ± 15.88 individuals

(range 20.4-78.3) but it increased to 48.35 ± 16.96 by 1998. Subsequently, a slight

increased was recorded between 1998 and 2000 (2.61 % to 1.94%), but it stayed as

49.61 ± 12.01 to 50.57 ± 12.65 in 2000. Nonetheless, the annual average troop size

was 55.97 ± 16.86 individuals (range 34.8-88.4) during 2001, which was an increment

of 10.68% compared to the previous year. Most troop sizes were between 30

and 70, which included 85.7% of troop sizes (Fig. 2). The largest troop (I) recorded

in our study had 100 individuals in July 1998.

M.J. Hsu, J.F. Lin and G. Agoramoorthy

All the 14 troops had a multi-male/multi-female structure with an average

adult sex ratio (AM/AF) of 0.48 (± 0.07, range 0.38-0.57). When subadult males,

juveniles and infants were included, the mean ratio of total males to females per

troop was 1.02:1. The mean proportion of adult females in 14 troops was 27.4% (±

2.2, range 25.2-32.6%). Even though it was the highest in the smallest troop (E), the

mean proportion of adult females was not linearly correlated (P > 0.51) with mean

troop size (range 32.7 to 77.1, Table 1).

The per-capita rate of troop size increase fluctuated widely, from 1.61 to 0.80

(Fig. 3). It was negatively correlated with troop size (with and without infants) in

1997-1999 (P < 0.05) and the relationship did not change significantly within years

(P > 0.05). Troop size without infants (F1, 55 = 36.79, P < 0.001) and troop (F13, 55 =

2.55, P < 0.01) accounted for 52.0% of the variations of per-capita rate increase.

Therefore, we further used mean troop size without infants as an independent variable

and found the significant effect of that on mean per-capita rate increase in

troops (F1, 12 = 5.57, P < 0.05). The regression model to estimate the per-capita rates

of troop size increase was 1.22867-0.00316 multiple (troop size without infants).

The annual mean per-capita rate of troop size increased in 1997/1998 (1.12 ± 0.11)

but slowed down during 1998/1999 (1.04 ± 0.11) and 1999/2000 (1.03 ± 0.08). Nevertheless,

it later increased to 1.11 ± 0.08 in 2000/2001. Overall, the average percapita

rate of troop size increase was 1.07 (± 0.05, n = 14) during 1997-2001. The

relation of per-capita rate of troop size increase was not consistently related to the

number of adult females; the relationship correlated negatively in 1997 (rs = – 0.73,

P < 0.01) but positively in 2000 (rs = 0.61, P < 0.05). The per-capita rate of troop

size increase was not significantly correlated with the troops’ birth rate from 1997-

2001 (P > 0.18, n = 14 for each year).

Fig. 2. — The frequency distributions of troop sizes in the Mt Longevity Formosan macaque as of

December each year between 1997 and 2001.

Effects of group size in wild Formosan macaques

Natality

The birth peak occurred in May (47.7% of 705 births), and the majority of

births (81.1%; n = 519) occurred within a period of 2 months (April 15-June 15).

The overall mean birth date was May 11 ± 3 days and the average median date was

May 8 ± 5 days. The mean spread for five birth seasons was 142 ± 28 days. Only

two births occurred in February and three in August. The earliest birth date was

recorded on 17 February (1999) and the latest was on 15 August (2001). The conception

period ranged mainly from November to December (80.3%).

The mean number of births per troop was significantly correlated with the

mean number of adult females (F1, 12 = 208.3, R2 = 0.95, P < 0.001) and mean troop

size without infants (F1, 12 = 112.4, R2 = 0.90, P < 0.001). Since the intercept did

not significantly differ from zero, the best regression line to estimate the number of

births was: = 0.7905 ‧ (number of adult females).

The mean birth rate was neither significantly related to average troop size with

or without infants (both rs = 0.24, P > 0.40), nor with the number of adult females

(rs = 0.28, P > 0.33). In addition, the mean birth rate did not show a humped curve

against group size and the variations in birth rates were larger in small and medium-

sized troops (Fig. 4). The average birth rate (birth per adult female) was 0.78 (±

0.07, Table 1).

Furthermore, the mean proportion of infants within a troop did not correlate

with neither the number of adult females (P > 0.51) or the troop size without

infants (P > 0.88). The average proportion of infants in 14 troops was 16.7% (± 1.8,

range 13.3-19.5%). The mean proportion of infants was not significantly correlated

with the mean birth rate (P > 0.07).

Fig. 3. — The relationship between average troop size and the per-capita rates of size increase in 14

troops of Formosan macaques at Mt Longevity during the period 1997 to 2000.

10 M.J. Hsu, J.F. Lin and G. Agoramoorthy

Infant mortality

A total of 88 infants died within 6.5 months of age with 39.8% of deaths

occurring on the day of parturition and a further 21.6% occurred within 2 weeks

of age. In total, 69 infants died within 2 months of age and 1/3 of them (n = 23)

could be associated with an alpha male change during the previous mating season.

However, the alpha male change in troops did not itself increase infant mortality.

The annual infant mortality between 1997 and 2001 were not correlated with

troop size. Even after we separated troop sizes into three categories (small, medium

and large), the relationships between troop size and infant mortality were not consistent.

Infant mortality was highest in medium-sized troops in 1997, but it became

the lowest in 2000 (Fig. 5). However, no significant difference was found in mean

infant mortality among these three categories of troop sizes (Wilcoxon test, P >

0.10). The average infant mortality for 14 troops was 0.16 ± 0.09 (Table 1).

Mean infant mortality from the 14 groups was significantly correlated with

the percentage of adult females per troop (rs = 0.635, P < 0.05; Fig. 6), but not correlated

with troop size (P > 0.77), number of adult females (P > 0.25) nor number

of adult males (P > 0.32). The regression line to estimate infant mortality equals

– 56.28 + 2.651 multiple (percentage of adult females in a troop) and infant mortality

was not linearly correlated with mean birth rate (P > 0.48, n = 14).

The average number of infants weaned per adult female (infant weaning rate)

was 0.65 ± 0.08 (n = 14). It did not linearly correlate with mean troop size (with or

without infants) in 14 troops (P > 0.51). The mean infant weaning rate was nega-

Fig. 4. — The relationship between mean birth rate and the average number of individuals in the

troop expressed in terms of the number of adult females, troop size without infants, and total troop

size for 14 troops of Formosan macaques at Mt Longevity between 1997 and 2001.

Effects of group size in wild Formosan macaques 11

tively correlated with the mean percentage of adult females (rs = – 0.71, P < 0.01)

and adult males (rs = – 0.55, P < 0.05, Fig. 7). The best regression model to estimate

infant weaning rate was 1.3454 - 0.02522 ‧ (percentage of adult females per troop)

(F1, 12 = 12.34, R2 = 0.51, P < 0.005). The proportion of adult males per troop also

had negative effect (Fig. 7) on the mean infant weaning rate (F1, 12 = 4.79, R2 = 0.28,

P < 0.01), but the effect was not significant when the percentage of adult females

was included in the regression model (P > 0.08).

Inter-troop interactions

Between 1998 and 2001, we recorded 3050 troop interactions among 14 social

troops. The average number of troops interacted with was 6.6 ± 2.5 troops (n =

14). Direct aggression accounted for 78.5% to 88.5 % of all interactions. Counter

attacks occurred on only a few occasions (1.55-8.3%), and no winning troop was

determined. Occasionally, two troops were seen close to each other peacefully without

apparent aggression (11.5-21.5%).

At Mt Longevity, the dominance rank in troops changed periodically depending

on the year, location and number of individuals involved. In 1998, troop I was

the most dominant troop in the southern part of Mt Longevity and it displaced

other troops in 89.8% of the aggressive inter-troop interactions. The following year,

the number of adults in troop K was larger than troop I, and K became the dominant

troop in the southern part displacing other troops in 83.3% of the aggressive

interactions. However, in 2001 the situation in the southern part reversed when

troop I, with more adults than troop K regained the dominant status. On the other

hand, in the northern part of Mt Longevity, troop B was dominant in 1998 while

troop G held the dominant status during 1999 and 2001 respectively.

Small troop size, i.e. troops that had few adult males and females, imposed

some disadvantages in inter-troop interactions (Fig. 8). The percentage of winning

Fig. 5. — The average infant mortality of small, medium and large-sized troops of Formosan

macaques at Mt Longevity from 1997 to 2001.

12 M.J. Hsu, J.F. Lin and G. Agoramoorthy

and number of adults (troop size) were significantly correlated with each other (P

< 0.001). Therefore, we used one independent variable each time in a regression

to estimate the percentage of winning. The combination of adults (adult males and

females) within a troop best explain variations in the percentage of winning (R2 =

0.54-0.70) in 3 out of 4 years. However in 2000, the number of adult males best

Fig. 6. — The relationship between average infant mortality and the mean proportions of adult

females in 14 troops of Formosan macaques at Mt Longevity from 1997 to 2001.

Fig. 7. — The relationship between the mean number of infants surviving per adult female and the

mean percentage of adult females or adult males in 14 social groups of Formosan macaques at Mt

Longevity between 1997 and 2001.

Effects of group size in wild Formosan macaques 13

explain the variations in the percentage of winning (R2 = 0.72), but, it was not a

good indicator in 1998-1999. Therefore we chose the mean number of adults as the

best indicator to estimate the percentage of winning during inter-troop interactions

(Fig. 8, F1, 13 = 31.6, R2 = 0.72, P < 0.001). Since the intercept of this regression (Y =

– 27.37 + 3.53 * X, Fig. 8) did not significantly differ from zero (P > 0.07), a regression

model without intercept was calculated as the prediction for the percentage of

winning = 2.3719 ‧ (number of adults of a troop).

Discusion

Troop size and effect on demography

The general theoretical context used to explain primate group size variations

is associated with individuals maintaining group size to maximize inclusive fitness

(Wrangham 1980). However, short-term seasonal stress may intermittently alter

the cost associated with optimal group size (Pride 2005). Even though birth rate

in mammals plays a key factor in determining reproductive output, which is influenced

by both ecological and social components (Dunbar 1988, Hill et al. 2000),

troop size may also influence reproductive parameters (Takahata et al. 2005). The

per-capita rate of troop size in M. cyclopis at Mt Longevity fluctuated widely and,

in general, it was negatively correlated with troop size without infants, indicating

that large troop size was related to small or negative increments. Although troop

size ranged widely, it did not increase above 100 individuals per troop. The emigration

of both males and females and a decrease in infant weaning rate contributed

Fig. 8. — The relationship between the average percentage of winning during interactions and the

average number of adult females and males in 14 social groups of Formosan macaques at Mt. Longevity

from 1998 to 2001. Dotted line: Y = – 27.37 + 3.53 * X.

14 M.J. Hsu, J.F. Lin and G. Agoramoorthy

to limiting troop size increase between 1997 and 2001. However, the widely variable

range of troop size recorded in our study is consistent with other species such as

Macaca nemestrina (Caldecott 1986), M. sylvanus (Menard & Vallet 1996), and M.

mulatta (Southwick & Sidd iqi 1988).

Troop size exceeding 70-80 individuals is not common among Macaca cyclopis.

A large wild troop of M. cyclopis with 70 individuals was reported once in another

site, Chichi Dashan in Taiwan (Liu 1997). At Mt Longevity, the troop size seldom

exceeded 80 individuals and is not as large as the provisioned troops of M. mulatta

at Cayo Santiago (Berman et al. 1997), at Kowloon, Hong Kong (Burton & Chan

1996), and of M. fuscata at Mt Ryozen, Japan (Sugiyama & Ohsawa 1982).

Recent studies of M. fuscata and M. silenus found no significant relationship

between infant mortality and either troop size or the number of adult females

(Takahata et al. 1998a, Kumar 1995), which is consistent with our study. Neither

troop size without infants nor number of adult females in M. cyclopis at Mt Longevity

had significant effects on the ratios of infants to adult females (crude birth rate)

and infant mortality. However, the proportion of adult females had a significant

effect on both infant mortality and infant weaning rate. In contrast, the crude birth

rate of wild M. fuscata was positively correlated with troop size at Yakushima and

at Kinkazan (Japan) and negatively correlated with the number of adult females

(Takahata et al. 1998a). While smaller troops had a disadvantage in inter-troop

competition, the rate of troop size increase was high, possibly due to the smaller

denominator. However, the proportion of adult females in a troop has an important

influence on infant mortality and infant weaning, indicating that adult female competition

has negative effects on the rate of infant weaning. Our data further indicate

the negative effect of a large proportion of adult females on infant weaning

rate, partially supporting the predation — intra-group feeding competition hypothesis

proposed by van Schaik (1983). Our data suggest that the population density of

Formosan macaques is not extremely high at Mt Longevity because the birth rate is

not negatively correlated with group size.

Predator avoidance behaviour has been known to function as a selective pressure

to favor group living in primates and influencing group size (Treves & Chapman

1996). According to van Schaik (1983), the survival ratio of immature individuals may

increase with larger group size because predation pressure is predicted to be low in

large groups. During our study, we did not observe natural predation at Mt Longevity

since the only probable natural predator of monkeys in Taiwan, the clouded leopard,

has not been sighted for 15 years. This large cat is believed to be extinct in the wild

(Hsu & Agoramoorthy 1997). However, poaching and illegal trapping remain a threat

for monkeys at Mt Longevity (Agoramoorthy 2002). In addition, feral dogs have been

observed to chase and attack monkeys (M.J. Hsu unpublished data).

Food provisioning has been observed to influence troop size and birth rate in

M. fuscata in Japan. The birth rate of M. fuscata was reported to be high in provisioned

troops (0.54-0.59) compared to wild troops (0.27-0.35, Sugiyama & Ohsawa

1982, Wolfe 1986, Koyama et al. 1992, Takahata et al. 1998b). However, the birth rate

(0.78 infants per adult female per year) and overall annual growth rate (7%) in our

study of M. cyclopis were actually less than those of non-provisioned troops reported

previously in a similar eco-region of Taiwan (0.8 and 25.2%, respectively, Wu & Lin

1992). As a matter of fact, the birth rate of M. cyclopis is similar to that of the closely

related M. mulatta (0.77-0.90, Southwick et al. 1980; 0.78, Jiang 1988).

Food provisioning has been legally prohibited at Mt Longevity, but visitors

sometimes provide small amount of food to monkeys during weekends and holidays

Effects of group size in wild Formosan macaques 15

along tourist trails. In fact, the forest at Mt Longevity harbours plant species such

as Broussonetia papyrifera, Ficus microcarpa, F. septica, Malaisia scandens (Moraceae),

and Passiflora suberosa (Passifloraceae), which constitute the main natural

food source for monkeys throughout the year (M.J. Hsu unpublished data). Thus

food provisioning has no significant effects on troop size and birth rate regardless

of whether tourists have less or more frequent contact with monkeys.

Social interactions

Inter- and intra-troop competitions appears to play a major role in limiting

troop size increase in M. cyclopis. In large troops, competition among females (different

matrilineal) for resources, and competition among males to improve mating

access usually increase aggression. Our study found that troops containing over

20 adults usually had a higher percentage of winning in inter-troop interactions.

In small-sized troops, the intra-troop competition among females may be reduced

but their infants might be extremely vulnerable to attacks during alpha male changes

and inter-troop interactions. Thus our data suggest that inter-troop dominance

tends to closely depend on the number of adults rather than group size as reported

in M. mulatta (Vessey 1968) and M. fuscata (Kawanaka 1973, Sugiura et al. 2000).

Infanticide in macaques has been rarely observed, but aggression from newly

established alpha males or dominant males towards infants leading to death has

been reported in the closely related M. mulatta (Ciani 1984), and M. fuscata (Soltis

et al. 2000) in the wild. Although infanticide occasionally occur in this population

(G. Agoramoorthy unpublished data), we did not record infanticide during

this study of 14 social troops between 1997 and 2001, and infant mortality did not

increase in troops as a consequence of alpha male changes. While we did not find a

relationship between birth rate and troop size changes, a higher variation in birth

rates occurred in small and medium-sized troops. This might have been due to a

reduced availability of food resources for low-ranking females as well as inter-troop

competition since home range is usually related to troop size in non-human primates

including macaques (Takasaki 1984, Maruhashi et al. 1998).

Inter-troop resource competition appears to favor group living and influence

troop composition among non-human primates (Treves & Chapman 1996). In

general, the per-capita growth rate of troops decreased as a function of troop size

(without infants) increases. This indicates that the annual growth rate of large-sized

troops decreased through low immigration and possibly high emigration but not

necessarily through high infant mortality, which is not consistent with the predation

(van Schaik 1983). However, if the proportion of adult females exceeds 28% of

troop size, the troop will suffer higher infant mortality. More field studies are needed

to investigate the birth rate differences among females of various social ranks to

further test the predation — intra-group female competition hypothesis.

Acknowledgments

The field research was partially funded by the Republic of China’s Council of Agriculture

and National Science Council (NSC88-2313-B-020-023, NSC94-2311-B-110-003) through

research grants awarded to M.J. Hsu and G. Agoramoorthy.

16 M.J. Hsu, J.F. Lin and G. Agoramoorthy

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