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: 3-17, 2006 4 Corresponding author (E-mail: agoram@mail.nsysu.edu.tw). 4 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 5 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 6 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 7 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. 8 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 9 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 negaFig. 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). Discussion 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 & Siddiqi 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 References Agoramoorthy G. 2002. Formosan macaques in crisis at Mt. Longevity, Taiwan. IPPL News: 12-13. Berman C.M., Rasmussen K.L.R. & Suomi S.J. 1997. Group size, infant development and social networks in free-ranging rhesus monkeys. Animal Behaviour 53: 405-421. Burton F.D. & Chan L. 1996. Behavior of mixed species groups of macaques, pp. 389-412. In: Fa J.E. & Lindburg D.G., Edits. Evolution and ecology of macaque societies. Cambridge: Cambridge University Press. Caldecott J.O. 1986. An ecological and behavioural study of the pig-tailed macaque. Contribution to primatology. Vol. 21. Basel: S. Krger. Chapman C.A., Wrangham R.W. & Chapman L.J. 1995. Ecological constraints on group size. An analysis of spider monkeys and chimpanzee subgroups. Behavioral Ecology and Sociobiology 36: 59-70. Ciani A.C. 1984. A case of infanticide in free-ranging group of rhesus monkeys (Macaca mulatta) in the Jackoo forest, Simla, India. Primates 25: 372-377. Dunbar R.I.M. 1988. Primate social system. London: Croom Helm. Hill R.A., Lycett J.E. & Dunbar R.I.M. 2000. Ecological and social determinants of birth intervals in baboons. Behavioral Ecology 5: 560-564. Hsu M.J. & Agoramoorthy G. 1997. Wildlife conservation in Taiwan. Conservation Biology 11: 834-836. Hsu M.J., Agoramoorthy G. & Lin J.F. 2001. Birth seasonality and interbirth intervals in freeranging Formosan macaques, Macaca cyclopis, at Mt. Longevity, Taiwan. Primates 42: 15-25. Hsu M.J. & Lin J.F. 2001. Troop size and structure in free-ranging Formosan macaques, Macaca cyclopis at Mt. Longevity, Taiwan. Zoological Studies 40: 49-60. Hsu M.J., Lin J.F., Chen L.M. & Agoramoorthy G. 2002. Copulation calls in male Formosan macaques: Honest signals of male quality? Folia Primatologica 73: 220-223. Hsu M.J., Moore J., Lin J.F. & Agoramoorthy G. 2000. High incidence of supernumerary nipples and twins in wild Formosan macaques at Mt. Longevity, Taiwan. American Journal of Primatology 52: 199-205. IUCN 2003. 2003 IUCN Red List of Threatened Animals. Gland: IUCN. Janson C.H. & Goldsmith M.L. 1995. Predicting group size in primates: foraging costs and predation risks. Behavioral Ecology 6: 326-336. Jiang H. 1988. The rhesus monkey (Macaca mulatta) population dynamic and distribution at Nanwan peninsula of Hainan Island. Acta Ecologica Sinica 8: 86-94. Kawanaka K. 1973. Intertroop relationships among Japanese monkeys. Primates 14: 113-159. Koyama N., Takahata Y., Huffman M. A., Norikoshi K. & Suzuki H. 1992. Reproductive parameters of female Japanese macaques. Thirty years data from the Arashiyama troops, Japan. Primates 33: 33-47. Kumar A. 1995. Birth rate and survival in relation to group size in the lion-tailed macaque, Macaca silenus. Primates 36: 1-9. Lefebvre D., Menard N. & Pierre J S. 2003. Modelling the influence of demographic parameters on group structure in social species with dispersal asymmetry and group fission. Behavioral Ecology and Sociobiology 53: 402-410. Lehner P.N. 1996. Handbook of ethological methods. Cambridge: Cambridge University Press. Liu G.C. 1997. Monkey-watching at Chichi dashan area. Nature Conservation 18: 55-61. Maruhashi T., Saito C. & Agetsuma N. 1998. Home range structure and inter-group competition for land of Japanese macaques in evergreen and deciduous forests. Primates 39: 291-301. Masui K., Narita Y.S. & Tanaka S. 1986. Information on the distribution of Formosan monkeys (Macaca cyclopis). Primates 27: 123-191. Menard N. & Vallet D. 1996. Demography and ecology of Barbary macaques (Macaca sylvanus) in two different habitats, pp. 95-106. In: Fa J.E. & Lindburg D.G., Edits. Evolution and ecology of macaque societies. Cambridge: Cambridge University Press. Effects of group size in wild Formosan macaques 17 National Research Council 1981. The Techniques for the Study of Primate Population Ecology. Washington, DC: National Academy Press. Peng M.T, Lai Y.L., Yang C.S. & Chiang H.S. 1973. Formosan monkey (Macaca cyclopis). Present status in Taiwan and its reproductive biology. Experimental Animal 22: 447-451. Pride R.E. 2005. Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta). Behavioral Ecology 16: 550-560. SAS Institute Inc. 2000. SAS/ETS software: changes and enhancements, release 8.1. Cary, NC, U.S.A. Soltis J., Thomsen R., Matsubayashi K. & Takaenaka O. 2000. Infanticide by resident males and female counter-strategies in wild Japanese macaques (Macaca fuscata). Behavioral Ecology and Sociobiology 48: 195-202. Southwick C.H. & Siddiqi M.R. 1988. Partial recovery and a new population estimate of rhesus monkey populations in India. American Journal of Primatology 16: 187-197. Southwick C.H., Richie T., Taylor H., Teas J. & Siddiqi F. 1980. Rhesus monkeys in India. Patterns of growth, decline, natural regulation, pp. 151-170. In: Cohen M. et al., Edits. Biosocial mechanisms of population regulation. New Haven: Yale University Press. Sterck E.H.M., Watts D.P. & van Schaik C.P. 1997. The evolution of female social relationships in nonhuman primates. 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Takahata Y., Suzuki S., Okayasu N., Takahashi H., Yamagiwa J., Izawa K., Furuichi T., Hill D., Maruhashi T., Saito C., Sato S. & Sprague D. 1998b. Reproduction of wild Japanese macaque females of Yakushima and Kinkazan islands. a preliminary report. Primates 39: 339-349. Takasaki H. 1984. A model for relating troop size and home range area in a primate species. Primates 25: 22-27. Treves A. & Chapman C.A. 1996. Conspecific threat, predation avoidance and resource defense. implications for group living in langurs. Behavioural Ecology and Sociobiology 39: 45-53. van Schaik C.P. 1983. Why diurnal primates living in groups. Behaviour 87: 120-144. Vessey S.H. 1968. Interactions between free-ranging groups of rhesus monkeys. Folia Primatologica 8: 228-239. Walter H. & Leith H. 1967. Klimadiagramm-Weltatlas. Jena: VEB Gustav Fischer Verlag. Wildlife Conservation Law 1989. Republic of China’s Wildlife Conservation Law I-3266. Taipe, Taiwan: ROC. Wolfe L.D. 1986. Reproductive biology of rhesus and Japanese macaques. Primates 27: 95- 102. Wrangham R.W. 1980. An ecological model of female-bonded primate groups. Behaviour 75: 262-300. Wu H.Y. & Lin Y.S. 1992. Life history variables of wild troops of Formosan macaques (Macaca

 CORRESPONDENCE CURRENT SCIENCE, VOL. 90, NO. 3, 10 FEBRUARY 2006 275 Primate polythelia puzzle The term ‘polythelia’ comes from Greek and means ‘many nipples’. In 1150 BC, King Chow Man in China was reported to have two supernumerary nipples, a condition then considered as a gift of divine power1 . In the West, polythelia could be traced back to the Romans; Lynceus described a woman with four breasts. Also, Julia, the mother of Alexander Severus and Anne Boleyn, the wife of Henry VIII of England had supernumerary nipples1 . Geoffroy-Saint-Hilaire and Darwin suggested that humans descended from animals with multiple breasts and polythelia could be regarded as atavistic or reversionary manifestations, in which remote ancestral characteristics unexpectedly appear2,3 . Polythelia is medically described as a minor congenital malformation that consists of nipples and/or related tissue in addition to the two nipples normally appearing on the chest4 . They are located along the embryonic milk line. In humans, the embryonic milk line extends bilaterally from a point slightly beyond the axillae on the arms, down the chest and the abdomen toward the groin, and ends at the proximal inner sides of the thighs. When Figure 1. An adult female Formosan macaque with four supernumerary nipples located anterior and posterior to the normal nipples. (Photo: G. Agoramoorthy). they are complete with breast tissue and ducts, they are called ‘polymastia’4 . Polythelia occur in 1–5% of humans; range varies in countries from 0.22% in Hungary to 1.63% in USA, and from 2.5% in Israel to 5.6% in Germany5 . In India, polythelia has been reported as a cutaneous marker of mitral valve prolapse, a common heart disorder6 . They are usually expressed asymmetrically, and are associated with increased risk for urogenital malignancies – the nature of possible causal relationships between gene defects, polythelia and urogenital disease is not clearly known7,8. Interestingly, polythelia has been anecdotally linked to multiple births in human but confirmatory data are lacking9 . Polythelia in non-human primates has been occasionally reported in species such as chimpanzee, orangutan, chacma baboon, rhesus macaque, Japanese macaque and Formosan macaque10. Nonetheless, the incidence of polythelia among the Formosan macaque, which is endemic to the island of Taiwan, was reported to be 33%, and the twinning rate was 1% – both are much greater than those reported for any other Cercopithecids and apes10 . Between January 2001 and October 2005, we examined a total of 244 adult female Formosan macaques in 18 social groups that inhabit Mt. Longevity, Taiwan to document infant twin birth and polythelia. We recorded 125 adult females (51.2%) with polythelia and the number of supernumerary nipples was two (23.8%) followed by one (17.2%) and three (8.6%) respectively, with a maximum of four (1.6%, Figure 1). We observed four cases of twin births, of which three multiparous mothers had polythelia (Table 1). Only one infant survived till weaning out of every twin birth. In one out of four cases (Troop B 12, Table 1), two offspring had polythelia (2, 3) like their mother, while the rest did not follow this trend. However, in one case (Troop Kc 5, Table 1), the mother had none but her daughter had two supernumerary nipples. The percentage of adult females with polythelia among the 18 social groups was not evenly distributed and ranged from 10 to 81.8% (Figure 2). So far we have recorded ten cases of twinning in Formosan macaques at Mt. Longevity (including six cases from an earlier study10) and 90% of females had polythelia. Besides, twinning rate was significantly higher in females with polythelia than those without polythelia (c 2 test, P < 0.01). The ultimate cause for the high occurrence of polythelia in Formosan macaques is unknown. However, isolation and inbreeding, including developmental by-products reinforcing selection simultaneously may have caused this genetic trait to spread in the population of monkeys. The twinning rate correlated with the occurrence of polythelia in Cercopithecids and apes should be further investigated to understand the genetic and developmental bases of polythelia and its relationship with twinning. This may shed light on questions of Figure 2. Number and proportion of adult females with supernumerary nipples in 18 social groups of Formosan macaques at Mt. Longevity, Taiwan. CORRESPONDENCE 276 CURRENT SCIENCE, VOL. 90, NO. 3, 10 FEBRUARY 2006 Table 1. Twin births and adult females/their offspring with polythelia among wild Formosan macaques at Mt. Longevity, Taiwan between 2001 and 2005 Troop Other births Offspring with name ID no. N Date of birth Sex Outcome (year/sex)* supernumerary nipples B 12 3 16 April 2003 M, F M died < 3 days 2000 F, 2002 M, 2004 F Yes (2, 3) F 10 2 1 August 2005 F, F 1 died < 4 days 2000 F, 2002 M died < 6 months, 2003 F, 2004 M No I 12 2 13 April 2002 M, M 1 died < 2 week 2000 F, 2001 F, 2003 M, 2004 M No Kc 5 0 12 June and M, M 1 died < 6 weeks 2000 M, 2002 F, 2003 M, 2004 F Yes (2) 26 June 2001 N, Number of supernumerary nipples. *Birth records of 2000 were pooled from unpublished data. fundamental interest, such as fluctuating asymmetry and primate trend to single births. It is not easy though to observe polythelia in the often arboreal and furry, nonhuman primates under field conditions due to visibility problems. Field biologists have to approach their subjects in close quarters to carefully observe the presence of polythelia. Countries like India where monkeys such as the bonnet macaque, rhesus macaque and Hanuman langur coexist with people in rural and urban areas, may provide better opportunity for such closer scrutiny. This ultimately may result in understanding the population genetics and fitness consequences of both phenomena, as well as the intriguing relationship amongst multiple births, polythelia and the potential correlation of urogenital anomaly. 1. Gould, G. M. and Pyle, W. L., Anomalies and Curiosities of Medicine, Julian Press, New York, 1962. 2. Geoffroy-Saint-Hilaire, I., Historie generale et particuliere des anomalies de l’himme et les animaux, vol. 1, J.B. Bailliere, Paris, 1832. 3. Darwin, C., The Descent of Man, John, Murray, London, 1871. 4. Schmidt, H., Eur. J. Pediatr., 1998, 157, 821–823. 5. Rahbar, F., Clin. Pediatr., 1982, 21, 46–47. 6. Rajaratnam, K., Kumar, P. D. and Sahasranam, K. V., Am. J. Cardiol., 2000, 86, 695–697. 7. Casey, H. D., Chasan, P. E. and Chick, L. R., Ann. Plastic Surg., 1996, 36, 101– 104. 8. Urbani, C. E. and Betti, R., Int. J. Dermatol., 1996, 35, 349–352. 9. Grossl, N. A., South Med. J., 2000, 93, 29–32. 10. Hsu, M. J., Moore, J., Lin, J. F. and Agoramoorthy, G., Am. J. Primatol., 2000, 52, 199–205. MINNA J. HSU1 JIN-FU LIN2 TAI-JUNG LIN3 GOVINDASAMY AGORAMOORTHY3,* 1Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung 804, Taiwan 2 Shi-Pu Junior High School, Kaohsiung 840, Taiwan 3Department of Pharmacy, Tajen University, Yanpu, Pingtung 907, Taiwan *e-mail: agoram@mail.nsysu.edu.tw Plight of higher education and our helplessness to act One would like to agree and appreciate the commentary by Lakhotia1 about the plight of universities in our country in highlighting the prevailing conditions in teaching and research, faculty, facilities, funds, admissions, appointments, administration and also suggestions for possible improvements. A lot has been said in the past about publications and journals too. All this is too well known, particularly to those scientists who matter for shaping the policy of higher education and research. Sometime back, one of the top scientists of the country publicly expressed his anguish over the prevailing poor scientific status of universities in the country, and implying thereby his helplessness to do anything about it. The basic question is: if the physician has diagnosed the illness rightly, why does he not administer the medicine? Unless such things are highlighted, how are they going to be improved? Lakhotia1 has rightly suggested restrictions for Master’s and Ph D degrees. If one wants to improve the situation, this is perhaps the first thing to be done. The big question is: Can we close down so many PG colleges which have sprung up in remote corners of the country? Will our political system permit this? Another farreaching suggestions is contractual appointments of teachers. Would we permit an altogether different service condition in isolation from elite services? UGC made this recommendation about three years ago, but so far no university has adopted the scheme. Lakhotia has not dealt with the factors affecting the standard of education in the universities. It is the government policy of liberalization of education which has literally reduced education to a commodity so that thousands of private professional and basic sciences colleges have been started throughout the country. How can one expect any standard and excellence from such institutions? Given the existing circumstances, what little can a common scientist do? Thirty years ago when I was appointed as head of the Department of Chemistry

 American Journal of Primatology 52:199–205 (2000) © 2000 Wiley-Liss, Inc. BRIEF REPORTS High Incidence of Supernumerary Nipples and Twins in Formosan Macaques (Macaca cyclopis) at Mt. Longevity, Taiwan MINNA J. HSU1 , JIM MOORE2*, JIN FU LIN3 , AND GOVINDASAMY AGORAMOORTHY4 1 Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung, Taiwan 2 Department of Anthropology, University of California at San Diego, La Jolla, California 3 Shi-Pu Junior High School, Kaohsiung, Taiwan 4 S.M. Govindasamy Nayakkar Memorial Foundation, Thenpathy, Tamilnadu State, India A population of Formosan macaques at Mt. Longevity exhibits an unusually high incidence of supernumerary nipples (polythelia: between 1–6 accessory nipples and/or areolae on 33% of adults), as well as a high rate of twinning (about 1% of births). The coexistence of these unusual traits suggests a connection, which is further supported by a tendency for mothers of twins to have accessory nipples and for twins to be born in troops with high incidence of polythelia. Am. J. Primatol. 52:199–205, 2000. © 2000 Wiley-Liss, Inc. Key words: polythelia; twin; development; founder; Macaca cyclopis; Taiwan INTRODUCTION The Formosan macaque (Macaca cyclopis) evolved from a rhesus macaque (M. mulatta) ancestor when they became isolated on the island of Taiwan [Hoelzer & Melnick, 1996]. At present they are restricted to coastal rainforests in the south and mountainous forests in the east. They are considered Threatened and are fully protected, though some poaching does continue (personal observations). Although field surveys have been conducted to determine their status and distribution [Lee & Lin, 1991], little is known about their population ecology, reproductive parameters, and social behavior. Social behavior and troop size data are limited to a single troop studied in Kenting [Wu & Lin, 1992; Wu & Lin, 1993]. We have been monitoring 16 troops of Formosan macaques at Mt. Longevity, southern Taiwan, since 1993 [Hsu & Agoramoorthy, 1999; Hsu et al., 2000]. In this work, we present data on the occurrence of supernumerary nipples among these monkeys and discuss them in light of the unusually high rate of twinning at this site. Contract grant sponsor: National Science Council, Republic of China; Contract grant number: 88- 2313-B-020-023. *Correspondence to: Jim Moore, Department of Anthropology, University of California–San Diego, La Jolla, CA 92093-0532. E-mail: jjmoore@ucsd.edu Received 5 June 2000; revision accepted 14 September 2000 200 / Hsu et al. METHODS The study population of about 790 monkeys occupies Mt. Longevity, a 1,116 ha protected area covered with tropical lowland rainforest, located within the city limits of Kaohsiung. Observations began in January 1995, and currently 16 troops are monitored on a regular basis. Subjects mentioned in this work are individually known. Kin relations and ages were verified from genealogical records compiled by the authors (unpublished). Troop compositions and polythelia prevalences reported here are from July 1999. Troops are monitored at least three times per week during the birth season and twin births were inferred by the presence of two neonates nursing from a single female who continues to care for both. It is possible but highly unlikely that some “twins” could represent permanent neonatal adoptions; it is somewhat more likely that perinatal death of a twin might not be detected. Because observation conditions are good, and these potential problems bias results in opposite directions, we believe our reported twinning rate is very close to the actual one. The term polythelia covers a range of eight types, from morphologically and functionally normal extra breasts (type 1) to “polythelia pilosa,” a patch of hair only [Leung & Robson, 1989]. All are associated with histologically identifiable glandular tissue [Camacho & Gonzalez-Campora, 1998]. Animals were visually inspected without restraint for presence of supernumerary nipples or areolae (types 5–7). Without capture, distinguishing small nipples from areolae is difficult, and they are not differentiated here. Polythelia can be difficult to detect within the fur (especially on males), and we included only individuals for whom we were confident supernumerary nipples/areolae would have been detected if present. Both the color and prominence of supernumerary nipples/areolae are hormone-dependent, and they may not appear prior to puberty [Grossl, 2000; Zuckerman, 1935]. Because of this the sample is restricted to adults. Statistical analyses were performed using StatView (version 4.5). RESULTS Supernumerary Nipples Eighty-nine of 211 females (42.2%) and 20 of 117 males (17.1%) possess between 1–6 accessory nipples or areolae (Tables I and II; Fig. 1). Nursing from accessory nipples has never been observed. Since polythelia is less visible on males, the sex difference may be partially artifactual, although we were aware of this possible bias and attempted to avoid it (see Methods section). Among humans, the commonest form is a single accessory nipple, but here 63.9 % of cases exhibit two or more; the commonest pattern is two bilaterally symmetric nipples above the normal pair (52.3% of cases). All extra nipples observed occur roughly along the mammary line(s). Nipple/areola number is asymmetric in 43.1 % of individuals. There is no left-right bias in asymmetry (right side with more nipples than left, 23; left > right, 22; contra reports of a left-side bias in non-humans [Hartman, 1927]), but females appear more likely to be asymmetric (females: 48 symmetric, 41 asymmetric; males 16 and 4, respectively; P < 0.06, chi-square with Yates correction for continuity). The prevalence of polythelia among adult females varied from 8% to 90% across troops (mean 39% ± 21%, n = 16 troops); in only four troops was the prevalence over 50%. For males, prevalence ranged from 0–75% (mean 20% ± 19%), with only one troop with more than 50%. Prevalence across troops among males and females was correlated (P < 0.05) but this was due almost entirely to high Supernumerary Nipples in Formosan Macaques / 201 TABLE I. Adult Females With Supernumerary Nipples Among Free-Ranging Formosan Macaques at Mt. Longevity, Taiwan Total of females Total no. of Number of with supernumerary Troop adult females supernumerary nipples nipples in troop name in troop 1 2 3 4 5 6 (N, %) A 10 1 2 0 0 0 0 3 30.0% Ba 17 7 0 1 2 0 0 10 58.8% C 17 1 7 0 0 0 0 8 47.1% Da 10 2 3 0 0 0 0 5 50.0% E 10 0 2 0 1 0 0 3 30.0% Fa 17 2 3 1 0 0 0 6 35.3% G 17 3 4 0 0 0 0 7 41.2% Aa 5 0 1 0 0 0 0 1 20.0% I a 15 4 4 0 0 0 0 8 53.3% J 14 2 1 0 0 0 0 3 21.4% Ka 26 8 7 2 0 0 0 17 65.4% Ia 8 0 1 0 0 0 0 1 12.5% M 10 1 1 1 0 0 0 3 30.0% N 11 1 1 0 1 0 0 3 27.3% O 13 0 1 0 0 0 0 1 7.7% Iba 11 3 6 0 0 0 1 10 90.9% Total 211 35 44 5 4 0 1 89 42.2% % 100.00 16.6 20.9 2.4 1.9 0.0 0.5 42.2 a Indicates troops in which twins occurred. TABLE II. Adult Males With Supernumerary Nipples Among Free-Ranging Formosan Macaques at Mt. Longevity, Taiwan Total of males Total no. of Number of with supernumerary Troop adult males supernumerary nipples nipples in troop name in troop 1 2 3 4 (N, %) A 7 0 0 0 0 00 B 11 0 3 0 1 4 36.4 C 10 2 0 0 0 2 20 D 8 0 1 0 0 1 12.5 E 3 0 0 0 0 00 F 11 1 1 0 0 2 18.2 G 9 0 0 0 0 00 Aa 4 0 1 0 0 1 25 I 6 0 1 0 0 1 16.7 J 9 0 1 0 0 1 11.1 K 10 0 1 0 0 1 10 Ia 3 0 1 0 0 1 33.3 M 3 0 1 0 0 1 33.3 N 9 0 1 0 0 1 11.1 O 10 0 1 0 0 1 10 Ib 4 1 1 1 0 3 75 Total 117 4 14 1 1 20 17.1 % 100 3.4 12.0 0.9 0.9 17.1 202 / Hsu et al. Fig. 1. Adult female Formosan macaque at Mt. Longevity with two symmetric pairs of supernumerary nipples/areolae. Supernumerary Nipples in Formosan Macaques / 203 prevalence in Troop Ib (10 of 11 females, 3 of 4 males) and may be spurious. Future research at the site will address this issue. Twins Six pairs of twins (11 live births) have been observed since 1996, out of 596 births (1.01%, or 0.84% for 5 sets of live births only) (Table III) [Hsu et al., 2000]. Both twins survived past 36 months in two cases, and both died within one week in one case. One of the infants (female 6) died after being carried for three days by a juvenile aunt, and presumably died of starvation. The cause of death is unknown in the other cases. Co-Occurrence of Polythelia and Twinning All six of the females who produced twins have supernumerary nipples. This is more than twice the overall prevalence (Fisher exact probability P = 0.005) and suggests a link between polythelia and multiple births. This is further supported by an association between incidence of polythelia in troops and presence of twinning: the six troops in which twins were born had the highest incidences of polythelia (Table I; Mann-Whitney U-Test, U = 2.0, n = 6, 10, P < 0.01). DISCUSSION Polythelia among monkeys and apes is occasionally commented upon (e.g., “Several (of > 1,000 rhesus) have one or two non-functional supernumerary nipples” [Koford et al., 1966]) but there has been little quantitative work on patterns and incidence [see Buss & Hamner III, 1971; Schultz, 1956]. With three exceptions, previous reports of incidence have been in the range of about 1–5%, similar to that reported for humans [Grossl, 2000; Schultz, 1948]. The exceptions are a report by Thorington et al. [1979], who found supernumerary nipples on five of 13 immobilized male red howlers (Alouatta seniculus); a statement by Itani et al. [1963] that among Japanese macaques “[i]n T-troop of Shodoshima ... nearly half of females there had extra nipples (Itani and others, unpublished)”; and a report by Zuckerman [1935] that three of 12 adult female chacma baboons he shot had extra nipples. The Mt. Longevity Formosan macaque population has more individuals with polythelia than have to date been reported for all nonhuman primates combined. TABLE III. Twin Births at Mt. Longevity Troop ID # N Birthdate Sex Outcome Other births I 8 2 5/11/96 F, F Survive 97F, 98M, 99M I a 17 2 5/11/96 F, M Survive 97-, 98M died < 2 mos, 99M D 6 1 4/5/98 F, F 1 died < 1 month 96F, 97M, 99F K 11 1 5/4/98 M, M 1 died < 1 month 96M, 97M died < 1 day, 99M B 2 2 5/15/99 & F F dead < 1 day, 96F, 97M, 98M stillbirth 5/24/99 M M dead < 1 week F 8 1 3/17/00 & ? Abortion 96F, 97F, 98F died at 2 mos 5/11/00 M (accidental), 99F died < 3 mos a Female F.I.17 moved to Ib when this new troop formed in October, 1998. # N, no of supernumerary nipples. 204 / Hsu et al. Most supernumerary nipples result from a failure to terminate mammary bud development, consistent with over- or underexpression of Hox genes [Schmidt, 1998]. They occur in 1–5% of humans, are usually asymmetrically expressed, and are associated with increased risk for urogenital malignancies. The nature of possible causal relationships between gene defects, polythelia, and urogenital disease is unknown [Casey et al., 1996; Urbani & Betti, 1996]. It is hoped that ongoing studies at Mt. Longevity can elucidate such possible biomedically relevant associations in Taiwanese macaques. Polythelia is anecdotally linked to multiple births in humans. Confirmatory data are lacking [Leung & Robson, 1989], however, and the connection is currently thought to be spurious [Grossl, 2000]. Our data suggest that the connection merits reevaluation. Twins appear to be rare among macaques. At Cayo Santiago the rate is under 0.1% [Koford et al., 1966; Rawlins & Kessler, 1986]. Hendrickx and Nelson [1971] give rates ranging from about 0.2–1% for several macaque and baboon colonies; the higher rates either include abortions and stillbirths or have n < 100. In their largest sample, two twin live-births were recorded among 838 rhesus (0.2%). Schultz [1956] has argued that the rate of twinning is similar in humans and nonhuman primates (about 1%), but this is based on aggregating nonhuman taxa, and the rate for macaques in his data is about 0.3%. The rate at Mt. Longevity is apparently between 3–10+ times greater than that of other macaques. The cause(s) of the high incidences of twinning and polythelia at this site is unknown, but founder effect and/or inbreeding in an isolated population are obvious possibilities. A high rate of twinning is reported for an island population of mouflon founded by a single pair [Boussès & Réale, 1998], and the troop-specific high incidences of polythelia reported by Itani et al. [1963] and Zuckerman [1935] also suggest a matrilineal founder effect. This is the first report in any nonhuman showing a clear association between the phenomena. Ongoing noninvasive studies of the Mt. Longevity macaques should help to elucidate the population genetics and fitness consequences of both phenomena, as well as to study the relationship between multiple births, polythelia, and (potentially) urogenital abnormalities. ACKNOWLEDGMENTS Partial funding for the ongoing field research on Formosan macaques at Mt. Longevity has been provided by the Republic of China’s National Science Council through a research grant (NSC 88-2313-B-020-023) awarded to G. Agoramoorthy and M.J. Hsu. Thanks to Jasmine Tan for her assistance. REFERENCES Boussès P, Réale D. 1998. Biology of twinning and origin of an unusually high twinning rate in an insular mouflon population. Z Säugetierkunde 63:147–153. Buss DH, Hamner III J. 1971. Supernumerary nipples in the baboon (Papio cynocephalus). Folia Primatol 16:153–158. Camacho F, Gonzalez-Campora R. 1998. Polythelia pilosa: a particular form of accessory mammary tissue. Dermatology 196:295–298. Casey HD, Chasan PE, Chick LR. 1996. Familial polythelia without associated anomalies. Ann Plast Surg 36:101–104. Grossl NA. 2000. Supernumerary breast tissue: historical perspectives and clinical features. South Medi J 93:29–32. Hartman CG. 1927. A case of supernumerary nipple in Macacus rhesus, with remarks upon the biology of polymastia and polythelia. J Mamm 8:96–106. Hendrickx AG, Nelson VG. 1971. Reproductive failure. In: Hafez ESE, editor. Comparative reproduction of nonhuman Supernumerary Nipples in Formosan Macaques / 205 primates. Springfield, IL: Charles C. Thomas. p 403–425. Hoelzer GA, Melnick DJ. 1996. Evolutionary relationship of the macaques. In: Fa JE, Lindburg DG, editors. Evolution and ecology of the macaque societies. Cambridge: Cambridge University Press. p 3–19. Hsu MJ, Agoramoorthy G. 1999. Population dynamics and male leader tenures among Formosan macaques at Mt. Longevity, Taiwan. Am. J. Primatol. 49:63–64. Hsu MJ, Lin J-F, Agoramoorthy G. 2000. Occurrence of twins in wild Formosan macaques, Macaca cyclopis, at Mt. Longevity, Taiwan. Folia Primatol 71:154–156. Itani J, Tokuda K, Furuya Y, Kano K, Shin Y. 1963. The social construction of natural troops of Japanese monkeys in Takasakiyama. Primates 4:1–42. Koford CB, Farber PA, Windle WF. 1966. Twins and teratisms in rhesus monkeys. Folia Primatol 4:221–226. Lee LL, Lin YS. 1991. Status of Formosan macaques in Taiwan. In: Ehara A, Kimura T, Takenaka O, Iwamoto M, editors. Primatology today. Amsterdam: Elsevier. p 33–36. Leung AKC, Robson WLM. 1989. Polythelia. Int J Dermatol 28:429–433. Rawlins RG, Kessler MJ. 1986. Demography of the free-ranging Cayo Santiago macaques (1976–1983). In: Rawlins RG, Kessler MJ, editors. The Cayo Santiago macaques: history, behavior and biology. Albany: SUNY Press. p 47–72. Schmidt H. 1998. Supernumerary nipples: prevalence, size, sex and side predilection— a prospective clinical study. Eur J Pediatr 157:821–823. Schultz AH. 1948. The number of young at a birth and the number of nipples in primates. Am J Phys Anthropol 6n.s.:1–23. Schultz AH. 1956. The occurrence and frequency of pathological and teratological conditions and of twinning among non-human primates. Primatologia 1:965–1014. Thorington Jr RW, Rudran R, Mack D. 1979. Sexual dimorphism of Alouatta seniculus and observations on capture techniques. In: Eisenberg JF, editor. Vertebrate ecology in the northern neotropics. Washington, DC: Smithsonian Institution Press. p 97–106. Urbani CE, Betti R. 1996. Accessory mammary tissue associated with congenital and hereditary nephrourinary malformations. Int J Dermatol 35:349–352. Wu HY, Lin YS. 1992. Life history variables of wild troops of Formosan macaques (Macaca cyclopis) in Kenting, Taiwan. Primates 33:85–97. Wu HY, Lin YS. 1993. Seasonal variation of the activity and range use patterns of a wild troop of Formosan macaque in Kenting, Taiwan. Bull Inst Zool 32:242–252. Zuckerman S. 1935. Supernumerary nipples in monkeys. J Mammal 16:229–230.

 

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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