Published in Primates 42:15-25 (2001)
MINNA J HSU, National Sun Yat-sen University
GOVINDASAMY AGORAMOORTHY, National Pingtung University of Science & Technology
JIN-FU LIN, Shri-Pu Junior High School
ABSTRACT. The birth season of Formosan macaque, M. cyclopis during our study started in February and ended in August with a peak in the second half of April and the first half of May. The average birth rate was 82% ± 21 for 114 females with four years of breeding records. Our study reports that a time span of one year between births can be considered as the norm for the wild M. cyclopis. Of the 288 inter-birth intervals (IBI), 88.5% showed a one-year interval (mean 364 ± SD 29 days); 11% showed two-year interval (727 ± 36 days); and 1% (2 females) had 3-year interval (range 1030-1040 days). The IBI for females that had infant loss within 6 months of life were the shortest. But there was no significant difference from that of females that had stillbirth (p>0.9) and infant that survived for first 6 months of life (p>0.06). However, among 255 cases of 1-year IBI, stillbirth or following infant loss within 6 months of life did significantly shorten IBI for 10 days (F 1, 253 = 5.74, p<0.05).
Key words: reproduction, birth rate, conception, infant mortality, Macaca cyclopis
Running head: Birth interval and seasonality in free-ranging Macaca cyclopis
INTRODUCTION
In primates, prolonged lactation prevents pregnancy mainly by inhibiting the return of ovulation. Postpartum endocrine changes in apes and monkeys appear to be similar to those found in humans (FRAWLEY et al., 1983; NADLER et al., 1981). Lactation infertility was reported to be a mechanism selected to achieve adequate spacing between successive births and hence to avoid maternal overburdening. This mechanism is also affected by maternal nutrition and hence allows mothers to space births flexibly according to their capacity for feeding infants (FRISCH, 1978). In recent years, the reproductive parameters of primates stimulated interest among zoologists to evaluate the interpretations of sexual selection theory (FEDIGAN, 1983; HARCOURT, 1987; DIXSON, 1998) and birth seasonality (COZZOLINO et al. 1992, BITETTI & JANSON, 2000).
Among the 19 extant species of the Macaca genus, M. cyclopis, is one of the least known. It is endemic to the island of Taiwan (area 36,000 km2). It is listed as Vulnerable in the IUCN Red List of Threatened Animals (1996) and protected by Taiwan's Wildlife Conservation Law (WCL, 1989). It is distributed in a wide range of elevation (30-3300 m) occupying a variety of habitats. Previous studies for more than a decade on this species were focused on field surveys to estimate the status and distribution (DIEN, 1985; MASUI et al., 1986; TANAKA, 1986; KAWAMURA et al. 1991; LEE & LIN, 1991, 1995). Reproductive parameters such as sexual skin and vaginal desquamation changes during the menstrual cycle, time of ovulation and gestation period for M. cyclopis have been thoroughly studied in a laboratory condition by PENG et al. (1973). They indicated that the birth season was from March to June, based on 48 wild caught pregnant monkeys that gave birth in the laboratory from 1965-1969. Long-term data on the reproductive parameters for M. cyclopis in the field are limited to a single monthly census and observations of two troops with a maximum size of 29 individuals (WU & LIN, 1992, 1993).
We have been monitoring several habituated troops of free-ranging Formosan macaques that live in the lowland rainforest habitat at Mt. Longevity, southern Taiwan since July 1993 to record data on ecology and population dynamics. In addition to the occurrence of twins (HSU et al., 2000), we examine for the first time the birth seasonality and duration of inter-birth intervals (IBIs) in more than a hundred female Formosan macaques from 16 troops over a period of four years. We also assess correlates of maternal age on births, and the influence of lactation status on females' reproductive activities.
MATERIALS AND METHODS
STUDY SITE
Mt. Longevity is located in Kaohsiung City adjacent to the Taiwan Strait. It is about 5 km long and 2.5 km wide, an area of about 1116 ha with a peak of 354m (22°39'N, 120°15'E). A topographic field map was used to estimate the total area used by all macaque troops that includes several uplifted coral reefs, undulating hillocks and valleys. Due to long-term effects of water penetration in hills, strange shapes of stones and steep valleys have been formed and these combined with natural lowland rainforest habitat provide safe roosting areas for the macaques. The floras of Mt. Longevity include 209 species in 72 families and 164 genera. The habitat and succession of plant communities follow the pattern of distinct wet and dry season that is similar to the Kenting national park (WU & LIN, 1992). According to the records of the Central Weather Bureau of Kaohsiung, average annual precipitation (1996-1999) was 2106 (SD ± 716) mm. Rainfall was concentrated from June to August as the wet season with monthly average above 360 mm (Fig 1). The dry season started from October and ended in March with monthly average rainfalls below or near 40 mm. The average monthly temperature was the lowest in January (19.8 ℃) and highest in July (29.2 ℃).
DATA COLLECTION AND ANALYSIS
A field study to investigate the population of Formosan macaques that inhabit Mt. Longevity began in July 1993. Data presented in this paper are limited to the systematic census of 7-16 habituated macaque troops on a weekly basis between 1 December 1994 and 31 December 1999. During the February-August period of each year, adult females in these troops were monitored for 4-days per week to reliably record birth data. Identification of individuals was based on their natural marks and body characteristics using video and photographic documentation. Kin relations and age of study animals were known from long-term genealogical record compiled by the authors (unpublished data). About 50% of troops (eight troops) receive small amount of food from people on an irregular basis (usually on weekends and holidays) while other troops still remain wild with minimal contact from tourists. Among the later, two troops did not have observations long enough to calculate their IBI. In general, tourists have been discouraged to feed monkeys.
We used scan sampling and ad libitum sampling (ALTMANN, 1974) to record data on mating behaviors during troop encounters. Gestation length was calculated between the date of birth and the last successful copulation seen, and we limited the range of 142-175 days according to PENG et al. (1973) to avoid wrong calculation because of missing mating behaviors. However, for some females without accurate copulation records, conception time was backdated from birth, assuming a gestation length of 162 days (PENG et al. 1973). Conception rates were calculated as the proportion of females that gave birth to a surviving infant (in each month) during the previous birth season who gave birth during the next breeding season. Average conception rates were calculated from 1996 to 1998. For average IBIs of multiparous or primiparous females, we first calculated the mean IBI per female, and then calculated the average IBI per category.
We used various test programs from SAS (1989). The effect of food provisioning or troop identity on average IBI of females was tested through ANOVA. Waller-Duncan tests were also used for the average IBI of 14 troops. A series of Spearman rank correlation coefficients was calculated to investigate the correlation of precipitation with monthly number of birth lags in time (0-12 months). Various General Linear Models were used to test associations between successful rearing of infants and maternal condition, age or troop identity. Number of live births per year was calculated as number of infants that survive till weaning divided by the number of years of observation on the respective focal female. The number of infant deaths per year was calculated as the number of infants that died before weaning divided by the number of years of data for the respective focal female. In both cases, the number of live births per year or the number of infant deaths per year was used as the dependent variables, and the age of mother and troop type as the independent variables.
RESULTS
SYNCHRONY AND BIRTH SEASON
Infant births in Formosan Macaques at Mt. Longevity were highly synchronized. The birth season started in February and ended in August with a peak during mid-April to mid-May (Fig. 1, 2A, 2B). A total of 475 births were recorded from 211 females in 16 troops. Among them, five pairs were twins. Majority (91.5%) of infants were born over a period of 2.5 months, between April 1 and June 15, with a peak of 52% births between April 16 and May 15. The average birth rate was 82% ± 21 per year per female for 114 females with four years breeding records.
The average gestation length was 163 (SD ± 8) days (n=98), and a majority of females conceived during November. Among 141 females, copulation occurred in an average of 175 ± 26 days (range 87 to 253 days) after their previous date of birth. However, in 118 females, an average of 41 ± 27 days were counted between their first mating and actual dates of conception. Although mating activities of Formosan macaques started in early September and mostly ended in late January annually, we found the conception period extended from September till next February.
Monthly precipitation had significant and positive correlation with number of births at 10-11 months of time lags (Fig. 3) and conceptions with 4-5 months' lag. Those were the only significant correlation consistent throughout the study period. The maximum Spearman's rank correlation coefficient occurred at ten (1996, 1998 and 1999, n=12, p<0.005) or eleven (1997, p<0.001) months lag of birth in time.
INTER-BIRTH INTERVAL (IBI)
The frequency distribution of the total of 288 samples of IBIs from 144 females was separated into three clusters (Fig. 4). However, 67 other females gave birth once during the 4-year study period and did not contribute any IBI samples. The average length of these 288 intervals between successive births was 408 days. The variability was large (standard deviation of 128 days and a range from 270 to 1040 days; Table 1) mainly due to a combination of 1-year, 2-year and 3-year intervals. Of the 288 IBIs, a vast majority (88.5%) occurred in the range from 270 to 488 days and the average length of these 1-year intervals was 364 ± 29 days. Of the remaining IBIs, 31 cases that accounted for 10.8% were 2-year intervals with an average of 727 ± 36 days (range 662 - 825 days). However, two IBIs (0.7%) were 3-year interval with an average of 1035 ± 7 days (range 1030-1040 days).
We did not find any significant effect in terms of human contact or provision in shorting the IBI of females (F 1, 142 = 0.25, p>0.62). Troop identity also did not play a significant role on the average length of IBI (F 13, 130 = 1.34, p>0.20). However, we found significant difference in the shortest average IBI (333 ± 52 days from troop Aa, n=4) and the longest average IBI (542 ± 224 days from troop E, n=9), and both troops had frequent contact with human.
IBI AND PARTURITION
The IBI following the birth of the first infant of primiparous females was not significantly different from that after the birth of the second infant of multiparous females (F 35, 105 = 1.14, p>0.59). The majority of primiparous females gave birth at 5 years old (67%, n=79); 14% gave birth at 6 years old, 10% at 4 years old. We also found 9% (n=7) primiparous females who gave birth when they were 7-9 years old. Among these primiparous females, 81.5% of them had one-year IBI with 365 ±19 days after their first births, and rest had two-year intervals or above. The average IBI of primiparous females was 404 ± 112 days, while IBI of 106 multiparous females was 408 ± 105 days. Maternal age was not positively correlated with mean IBI of multiparous females ((p>0.15), but old adult females (10+ years) had the tendency to give birth during early or late birth season. Only 23 births occurred in Feb-March and July-August. 22 births of them were from multiparous females, especially those that lost infants in the previous year contributed 64% of early births. None of the primiparous females gave birth before April. The earliest birth was recorded on 17 February 1999, 150 days after her last recorded copulation. Another old female delivered an infant on 28 February 1997. Only two births were recorded from two old adults in the early August (Fig 2B), and the latest birth recorded was on 12 August 1998.
IBI AND INFANT DEATH
About 22% infants died within the first year of life, and 10% infants died within the first week of their life in which 66% were stillbirth. The majority of deaths occurred within the first week of life (45.7%, n=105), and another 17% deaths occurred before the infants reached one-month old. The peak of infant deaths occurred in May (mean 31.4% ± 12.2) and June (mean 18.6% ± 9.7). We witnessed two accidental deaths when two male infants aged 42 and 59 days, slipped off from trees and landed on rocks during the rainy days of June.
Variation among these IBIs could not be significantly explained by maternal age (F1, 284 = 3.19, p>0.07), neither previous stillbirths, infant losses within 6 months of life, nor infants surviving to their first 6 months of life (F2, 284 = 1.90, p>0.15). The average maternal age at birth for stillbirths was not significantly older than for live births (F1, 286 = 0.57, p>0.4, Table 1). However, the variability among the number of infant survived per year for females was significantly explained by troops’ identity (F15, 204 = 3.53, p<0.001), but not related to maternal age (F1, 204 = 2.22, p>0.1). The highest infant mortality rate occurred in troop Aa (mean 80.0% ± 27.4, n=5).
The IBIs for females that had infant loss within 6 months of life were the shortest, which did not differ from IBI following stillbirth (F1, 63 = 0.01, p>0.9) or from IBI following infant surviving for first 6 months of life (F1, 275 = 3.31, p>0.07). However, among 255 cases of 1-year IBI, combining stillbirth or following infant loss within 6 months of life did significantly reduce IBI by 10 days (F 1, 253 = 5.74, p<0.05) compared to those following infant surviving for first 6 months of life (Table 2). The average 1-year IBI of females that had stillbirth or infant loss within 6 months of life was 356 ± 35 days (n=61).
The conception rates of females with surviving infants were a function of the dates of their deliveries in the previous birth season (Table 3). The conception rates were higher for females that gave birth to infants in the early part of the previous birth season than for females that had a late birth. Moreover, the conception rates of females that gave birth in previous July and August were zero. These results indicate that timing of the birth excluded the reproductive outcome of the mothers during the following year.
The females who came into estrus earlier were usually multiparous females without pregnancy or with stillbirth or dead infants in the previous year. Only three females more than 10 years old were observed to mate before September but none of them conceived during that time. Among them, the first one did not give birth in 1998, while the second had a stillbirth in April 22, but both were seen in estrous and mated on June 22 and July 29 1998 respectively. But none delivered any infant during 1999. The third one didn’t give birth during 1998, mated on Aug. 21 1998, but only delivered an infant on 22 July 1999 as a result of copulation in February.
DISCUSSION
The birth seasonality demonstrated in our results indicated that seasonal variation in environmental cues and social interaction was crucial to time the reproductive activity of the animals and provide the biological rhythm. Births of M. cyclopis during our study are consistent with the wild caught females that were pregnant during their capture later delivered infants in the laboratory only between March and June (PENG et al. 1973). Both indicated over 90% births within three month period, highly synchronized in a much narrow range than the previous field report (75%, WU & LIN, 1992). The birth peak in our study occurred 10-11 months after peak precipitation, compared to 8-10 months lag in Kenting (WU & LIN, 1992). Heavy rains cause infant deaths, and therefore it is crucial to deliver infants before the wet season. Our study site has distinct dry and wet seasons and the birth peak of M. cyclopis coincides when the availability and diversity of natural food resources starts to increase in May, just before the rainy season (June to August) (Lin and Hsu, unpublished data). On the other hand, successful conceptions or artificial insemination of socially isolated M. cyclopis (except during mating with an adult male for 5 days) could be obtained throughout the year with the exception of July in laboratory controlled environment (PENG et al. 1973). But in a recent study from the New England Regional Primate Research Center, 41% of births in M. cyclopis were recorded within three months (March to May) from females that lived in social groups (PETTO et al., 1995). Even without proximate factors for food availability and/or changes of photoperiod, M. cyclopis in captivity was reported to be the most strongly seasonal in breeding compare to M. mulatta, M. fascicularis and M. arctoides (PETTO et al., 1995). Furthermore, shift in birth timing has been influenced by altitude with combination of food availability and daily temperature changes in M. thibetana (ZHAO 1994). It would be interesting to examine the patterns of birth seasonality in M. cyclopis in different parts of Taiwan with variations in altitudes and/or raining patterns.
The average birth rate over the four birth seasons (83%) is similar to that of many of rhesus macaque troops (DRICKAMER, 1974; WOLFE, 1986) but higher than that of provisioned and wild troops of Japanese macaques (27-54%, TAKAHATA et al., 1998). Our findings concluded that one year between births can be considered the norm for the wild M. cyclopis in contrast to 2 years for the closely related M. fuscata in the wild (TAKAHATA et al., 1998). The mean IBI and percentage of one-year interval was very similar to M. sylvanus (408.7 days and 88.4%, PAUL & THOMMEN 1984). The majority IBI of M. cyclopis (88.5%) fell into the 1-year interval category, but mean IBI of primiparous was similar to that of multiparous females, which was different with a previous report (WU & LIN, 1992). However, in cases involving old adult females, the birth interval was longer, and fell into 3-year interval category or even longer. Although the average IBI in our study was 13.4 months, shorter than that of 15.4 months of live birth in this species (in 8 females, WU & LIN, 1992), our study included stillbirths (7%), and deaths shortly after birth, which are easy to miss in most field studies. According to HENDRIE et al. (1996), live birth rate was 83.4% in M. mulatta and prenatal mortality (abortion plus stillbirths) accounted for 13-22% in M. mulatta and 18% in M. fascicularis of confirmed pregnancy, which was similar to 16% prenatal mortality in M. cyclopis (PENG et al. 1973). Therefore, IBI of live birth should be longer than IBI including stillbirth. However, one adult female M. cyclopis in the wild was reported to produce an offspring each year for six successive years (WU & LIN, 1992).
Although few mating activities of Formosan macaques occurred outside of mating season (September to next February), females either went through spontaneous pregnancy losses or did not conceive during that time. They might have undergone a phase of amenorrhea as reported in M. mulatta (KEVERNE & MICHAEL 1970) or postpartum sterility that lasts at least until the beginning of the next mating season.
Females of many non-seasonal species may renew their sexual activity shortly after the death of the infant and thus reduce their length of birth interval (DIXSON, 1998). It has been reported among seasonally breeding closely related macaques such as M. fuscata and M. mulatta, that females that lost their infants within six months of life had dramatically shorter IBIs compared to females with surviving infants (TAKAHATA et al., 1998; RAWLINS & KESSLER, 1986). Infant loss has a great impact on shortening IBI for species with year-round breeding (ALTMANN, et al., 1978) and for seasonally breeding species with a normal IBI of two years (TANAKA et al., 1970; SCUCCHI, 1984), but not for species with IBI of one year (PAUL & THOMMEN 1984). Although stillbirth, or infant loss within 6 months of life, shortened 1-year IBI on average for 10 days in this study, only giving birth in the late season (July and August) dramatically prevented females from conceiving in the coming mating season.
The occurrence of abortions and stillbirths among captive and recently captured macaques was reported to be high (VALERIO et al., 1969) and appeared to be associated with physical, social or environmental stress. For example, wild-caught or imported M. cyclopis had 31% (22 out of 72) abortions or stillbirths which is higher than the 16% in laboratory mating colonies (PENG et al., 1973). However, free-ranging M. mulatta at Cayo Santiago with constant food provision had an incidence of abortions or stillbirths of 3.8% (RAWLINS & KESSLER, 1986), which is relative to the other rates, about the same as that of 7% in the present study. The shortest average IBI as well as the highest infant mortality rate had occurred in troop Aa, which was a new branch troop formed as a result of fission in May-June 1997. Our study indicates that social stress associated with adult male replacements and/or fission might have influenced the prenatal and infant mortality that further reduced 1-year IBI of females.
Acknowledgements. The field research on Formosan macaques at Mt. Longevity has been partially supported by the National Science Council through a research grant awarded to G. AGORAMOORTHY and M.J. HSU (NSC 88-2313-B-020-023). We thank C. M. Crockett, R. I. M. Dunbar, H. Takahashi, and other anonymous reviewers for critically reviewing earlier drafts of the paper.
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Authors' Names and Addresses: MINNA J HSU, Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung, Taiwan, Republic of China; GOVINDASAMY AGORAMOORTHY, Department of Wildlife Conservation, National Pingtung University of Science and Technology, Taiwan, Republic of China, and S.M. Govindasamy Nayakkar Memorial Foundation, Thenpathy 609111, Tamilnadu State, India; and JIN-FU
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