Differential energy budget and monopolization potential of harem holders and bachelors in hanuman langurs (Semnopithecus entellus) Preliminary results.код для вставкиСкачать
American Journal of Primatology 55:57–63 (2001) Differential Energy Budget and Monopolization Potential of Harem Holders and Bachelors in Hanuman Langurs (Semnopithecus entellus): Preliminary Results OLIVER SCHÜLKE* Abteilung Verhaltensforschung und Ökologie, Deutsches Primatenzentrum, Göttingen, Germany The demographic structure in the Hanuman langur (Semnopithecus entellus) population of Jodhpur is extreme, in that some single males monopolize harems with, on average, 25 adult females. It has been proposed that extratroop males, which live in all-male bands, inhabit lowquality habitats and suffer from reduced food provisioning and longer daily travel distances. To compare the resulting energetic consequences for harem holders and bachelors, I estimated their gross energy intake and daily energetic expenditures. This analysis revealed no clear-cut differences between the two classes of males in time spent feeding on provisioned food, daily path length, gross energy intake, and energy expenditure. Due to the small sample size and other limitations of the study design, the hypothesis under investigation can not be evaluated conclusively. The preliminary results suggest, however, that energy budgets of harem holders and bachelors do not differ markedly. The importance of direct ecological pressures to males for our understanding of variation in group composition is highlighted. Am. J. Primatol. 55:57–63, 2001. © 2001 Wiley-Liss, Inc. Key words: number of males; energy budget; harem; all-male band; food provisioning; Semnopithecus entellus INTRODUCTION Variation in the number of males in primate groups is thought to be determined mainly by two factors: the degree of estrus synchrony among females, and female group size [reviewed in Nunn, 1999]. In general, this holds also for Hanuman langurs (Semnopithecus entellus). Groups with more than 12 females generally contain more than one male [Newton, 1988] and one-male groups are common where female receptive periods are spread throughout the year [Srivastava & Dunbar, 1996]. Thus, the langur population of Jodhpur (Rajasthan/ India) is exceptional with respect to their extremely large bisexual groups comprised of a single adult male and, on average, 25 females. Surplus males (bachelors) are living in all-male bands (AMBs). Based on the observations that food Contract grant sponsor: Indian Council for Cultural Relationships. *Correspondence to: Oliver Schülke, Abteilung Verhaltensforschung und Ökologie, Deutsches Primatenzentrum, Kellnerweg 4, 37077 Göttingen, Germany. E-mail: email@example.com Received 31 July 1998; revision accepted 7 June 2001 © 2001 Wiley-Liss, Inc. 58 / Schülke provisioning is centered on harems and that AMBs have larger home ranges and longer travel distances, Rajpurohit et al.  and Sommer [1996, as cited in Pereira, 1998] picked up an earlier suggestion by Sugiyama et al. , who proposed that AMBs are forced into low-quality habitats by bisexual groups. According to Sugiyama et al. , poor habitat quality makes bachelors suffer more from energy stress compared to males in harems. Extremely divergent energy budgets of harem holders and bachelors may explain why single males are capable of monopolizing large groups of females. This paper addresses this hypothesis by comparing the energy budgets of harem holders and bachelors. METHODS In 1996, a total of 1,514 Hanuman langurs were living in 30 bisexual groups, which were all organized as harems (Mohnot, Rajpurohit, and Chhangani, unpublished census data). The average group size of harems was 46 (8–128); average female group size was 25 (5–73). In addition, 136 bachelors (94 adults) lived in at least 11 AMBs, with a mean band size of 10 (3–33). The study area around Jodhpur has been described by Vogel . The four harem holders of the bisexual groups of Bhadreshwar (B28, 42), Kadamkandi-West (B27, 19), Kailana I (B19, 9) and Sidhnath-Temple (B24, 25) were selected as focal animals (letter/ number codes refer to designations of earlier studies, and adult group size). Four bachelors from the two AMBs, Chopasani (AMB 11, 2) and Soothla (AMB 9, 5), were observed, including the only two adults of Chopasani and two mid-ranking males (male #1 and male #5) from Soothla. All focal animals were approximately the same age. From October 1996 through January 1997, I observed each focal male continuously throughout his activity period from before dawn (6:15 AM) until after dusk (6:30 PM) on four consecutive days. I conducted instantaneous recording (30-sec intervals) of positional and feeding behavior [Martin & Bateson, 1993]. An attempt was made to sample bite rates for every male for every food item by counting the number of bites, complete items (e.g., whole leaf or fruit) or handfuls ingested during 10 independent 30-sec intervals. Daily path length was measured with a pace counter during observations or on the following day. Plant samples were collected for later identification at the Botanical Institute of the JNV University of Jodhpur (Dr. Sundaramoorthy) and at the Central Arid Zone Research Institute (CAZRI; Dr. B.K. Dutta) for chemical analysis (see below) and in order to obtain the dry weight (SICO POPULAR® SB1 balance) of one “bite” on an item-specific basis. Phytochemical analyses were performed on 88 food items at the German Primate Center, Göttingen, using methods described elsewhere [Heiduck, 1997]. Calculation of energy content was based on the concentrations of nutrients per gram dry weight by the following factors: 16.7 kJ/g for carbohydrates and proteins, and 37.6 kJ/g for lipids [Janson et al., 1986]. Daily gross energy intake was calculated by multiplying the energy content of each particular food item with the corresponding bite rate, bite weight, and daily feeding time [Rhine & Flaningon, 1978]. Since bite rate was not measured for every male for every item he ever fed on, I calculated an average bite rate across all males for every item. Daily energetic costs K were calculated using Equation 1 [Coelho, 1974]: K = [B1*(24–P)] + L + ΣAi  where K = daily energy expenditure (kJ/day); B1 = basal metabolic rate per hour (kJ/h) [Kleiber, 1961]; P = activity period of the individual (h); L = energy expen- Differential Energy Budget of Langurs / 59 diture due to locomotion (kJ); and Ai = energy expenditure due to behavior i performed during activity period (kJ). Energetic costs of locomotion L were calculated as the costs of moving the individual’s body mass over a measured distance [Coelho, 1974]. I assumed the body mass of all focal males to be 18.1 kg (SD: 0.74 kg, range 17.0–19.0 kg), the average body mass of five adult males weighed by Sommer . For daily energetic costs Ai associated with a specific nonlocomotor behavior, i values from the literature were used [Coelho et al., 1976]. For comparisons between bachelors and harem holders I used one value per male (mean value of 4 days of observation) for a Mann-Whitney U-test. The statistical power of the test, however, is small due to small sample size, and in order to present the data in more detail, means and standard deviations are given along with the medians. RESULTS Habitat quality in terms of abundance of provisioned food could not be compared directly, because patterns of provisioning varied markedly. Harems were provisioned daily by one to 19 persons with high-quality food, such as wheat preparations, fruit, vegetables, and sweets, near their sleeping site. In contrast, bachelors had to move into human settlements and beg for food. Bachelors initiated the act of provisioning and were fed individually rather than as a group. As a consequence, and contrary to the predicted pattern, the average time a male spent feeding on provisioned food did not differ markedly between harem holders and bachelors (NHH = NBA = 4, HH: median = 7.9% activity time, mean ± SD = 8.3 ± 2,7, range = 5.7–11.5%, BA: median = 5.2% activity time, mean ± SD = 5.3 ± 1.3, range = 4.0–6.9%; one-tailed MWU: U = 3, Z = –1.44; 0.05 < P < 0.1). Rajpurohit  found that one AMB had longer daily travel distances than one harem, and concluded that bachelors have higher energy expenditures than harem holders. My data did not support this prediction (NHH = NBA = 4, HH: median = 2.7 km, mean ± SD = 2.7 ± 1.0, range = 1.5–4.0, BA: median = 3.0 km, mean ± SD = 3.4 ± 1.5, range = 2.1–5.3; one-tailed MWU: U = 7.0, Z = –0.29, n.s.). Rajpurohit , however, measured the movement of the entire group, whereas I measured individual movements. Because the energy consequences of daily activities are the focus of this paper, the latter measure should be preferred here. It seems noteworthy, however, that bachelors often moved 5–6 km per day, which was rare for harem holders. On all of these days bachelors left the exclusive part of their home range to visit harems. On their way bachelors crossed open shrub-savanna with low food abundance, and after arriving at the harems they rarely got a share from the provisioned food because the harem holder kept them away from the feeding females. In the evening bachelors usually returned to the exclusive areas of their home range (median of the mean daily path length of three bachelors when visiting = 5.4 km, mean ± SD = 5.5 ± 0.2, range = 5.7– 5.3). On the other hand, whenever bachelors stayed away from harems they never moved farther than 3.5 km on a single day (median of the means of three bachelors = 1.8 km, mean ± SD = 1.7 ± 0.4) and approached humans to beg successfully for food several times a day. Visiting harems therefore may entail the doubled costs of higher energy expenditure (visit: median of the means of three bachelors = 3.7 kJ*103/day, mean ± SD = 3.7 ± 0.04 vs. stay: median = 3.5, mean ± SD = 3.5 ± 0.07) and lower energy intake (visit: median of the three means = 5.5 kJ*103/ day, mean ± SD = 5.2 ± 0.6 vs. stay: median = 9.5, mean ± SD = 10.0 ± 3.6). However, more data on the distribution of visits is needed to investigate this point in detail. 60 / Schülke Fig. 1. Individual gross energy intake plotted against energy expenditure for four harem holders (open points: B28: Bhadreshwar; B27: Kadamkandi-West; B19: Kailana I, B24: Sidhnath-Temple) and four bachelors (filled points: AMB11: Chopasani males #1 and #2; AMB 9: Soothla males #1 and #5) on four days, each. Daily gross energy intakes did not differ between harem holders and bachelors (Fig. 1; NHH = NBA = 4, HH: median = 10.2 kJ*103/d, mean ± SD = 10.3 ± 4.0, BA median = 8.3, mean ± SD = 7.9 ± 1.9, one-tailed MWU: U = 4.0, Z = –1.16, n.s.). Although medians of mean daily gross energy intake point in the predicted direction, samples of harem holders and bachelors overlapped to such an extent that no statistical difference was detected. In contrast to the prediction, the total daily energetic costs of harem holders (median = 3.6 kJ*103/d, mean ± SD = 3.6 ± 1.3) were not significantly lower than those of bachelors (median = 3.6 kJ*103/d, mean ± SD = 3.6 ± 1.1; one-tailed MWU: U = 8.0, Z = 0.0, n.s.), which may be due to small sample size. Daily energy budgets were not balanced in the sense that high energy expenditure was compensated for by high energy intake on the same day (Fig. 1). DISCUSSION Variation in primate group composition is generally viewed from the females’ perspective. Ecological settings are thought to determine the distribution of fertile females in time and space, which both result in a certain level of monopolizability of females [Nunn, 1999]. The influence of ecology on males and the role of males in shaping primate social systems are often neglected but should be emphasized [Pereira et al., 2000]. The present study investigated the influence of two such ecological parameters, namely distribution of provisioned food and homerange size, on differential competitive abilities among males. In contrast to the expected pattern, the presented data revealed no clear tendencies for differences between males living in harems and males from AMBs. Differences in habitat quality, namely food provisioning, did not translate into differences in feeding times for provisioned food or daily energy intakes in the present sample. Bach- Differential Energy Budget of Langurs / 61 elors could have compensated for low food abundance by longer search times and travel distances. But neither daily path length nor daily energy expenditure differed markedly between the two classes of males. Sugiyama et al.’s  suggestion that AMBs are forced into low-quality habitats by harem groups and consequently suffer from energy disadvantages was not supported, but small sample size definitely preludes a final evaluation of the hypothesis. The failure to detect significant differences between these two classes of males may be due to a number of factors. First, this study used bachelors of intermediate rank, rather than only AMB alpha males, who alone are in direct competition over leadership in bisexual troops. Second, only a small proportion of the entire population was included in the analysis. Bachelors from other AMBs probably experience harsher conditions than the males sampled in this study, which worked against the hypotheses under investigation. Third, the data presented here are restricted to the winter season, thereby missing the period of food shortage for langurs at Jodhpur. However, if bachelors face higher costs in summer, the frequency of harem holder replacements by bachelors should drop during or after the summer, which is not the case [Sommer & Rajpurohit, 1989]. Hence, seasonality in natural food and water abundance does not seem to affect harem holders and bachelors differentially. Fourth, interindividual differences in body mass may have influenced the males’ energy budgets differentially. And finally, the calculation of daily gross energy intake was based on average ingestion rates, rather than individual rates. This is potentially problematic, because male classes may differ in feeding speed. With these potential limitations, a final conclusion concerning potential differences in energy budgets between harem holders and bachelors must await additional data from year-round observation, individually measured body weights, and a larger number of males, which should then be analyzed in a multivariate approach. A detailed investigation of langur male energy budgets should include the comparison of days when AMBs visit harems and days when bachelors stay in the exclusive areas of their home range. It is possible that bachelors experience energy stress when visiting harems because they have to pass long distances and get less natural and provisioned food. On the other hand, bachelors have the opportunity to restore energy by reducing costs for traveling, and to gain energy from more frequent food provisioning, when they stay away from the harems. Therefore, the frequency of harem visits will be decisive for a bachelor’s overall energy budget. Moreover, the frequency of visits is closely related to what Moore  suggested to be responsible for variation in group structure among Hanuman langur populations: intruder pressure. Moore  proposed that intruder pressure is most importantly influenced by population density. However, it is the density and distribution of bisexual groups—not population density—that is decisive, if the number of groups that a male regularly encounters is of interest. Population density is moderate at Jodhpur [Newton, 1988], but the group density of 0.4/km2 [Vogel, 1988] is very low compared to other sites (1.3/km2 Ramnagar [Borries, 2000]; 1.8/km2 Kanha [Newton, 1988]; and 1.6/km2 Rajaji [Laws & Vonder Haar Laws, 1984]). In addition, the distribution of bisexual groups at Jodhpur is clumped around man-made water resources and temples. Thus, compared to other sites, distances between patches of harems are extremely long, and the number of bachelors visiting a harem should be low. This may favor the formation of onemale groups. The core of this argument again stresses the importance of direct ecological pressures on extragroup males for progress with our understanding of the variation in primate group composition. 62 / Schülke ACKNOWLEDGMENTS C. Borries and A. Koenig provided invaluable help and guided me through all phases of my work. I thank S.M. Mohnot for his kind cooperation; S.M. Mohnot, L.S. Rajpurohit, and A.K. Chhangani for their permission to use unpublished census data; and B.K. Dutta and Sundaramoorthy for identification of plant samples. I feel deeply indebted to L.S. Rajpurohit for guidance and encouragement. I thank J. Ganzhorn for his hospitality and for making it possible to analyze my plant samples at the DPZ; J. Ostner and V. Sommer for numerous discussions; and P.M. Kappeler, W. Dittus, and four anonymous reviewers for valuable comments on earlier drafts of this paper. REFERENCES Borries C. 2000. Male dispersal and mating season influxes in Hanuman langurs living in multi-male groups. In: Kappler PM, editor. Primate males. Kappeler PM, editor. Cambridge: Cambridge University Press. p 146–158. Coelho AM. 1974. Socio-bioenergetics and sexual dimorphism in primates. Primates 15:263–269. Coelho AM, Bramblett CA, Quick LB, Bramblett SS. 1976. Resource availability and population density in primates: a sociobioenergetic analysis of the energy budgets of Guatemalan howler and spider monkeys. Primates 17:63–80. Heiduck S. 1997. Food choice in masked titi monkeys (Callicebus personatus melanochir): selectivity or opportunism? Int J Primatol 18:487–502. Janson CH, Stiles EW, White DW. 1986. Selection on plant fruiting traits by brown capuchin monkeys: a multivariate approach. In: Estrada A, Flemming TH, editor. Frugivores and seed dispersal. Dordrecht: Dr W Junk Publishers. p 83–92. Kleiber M. 1961. Fire of life: an introduction to animal energetics. New York: John Wiley Publications. Laws JW, Vonder Haar Laws J. 1984. Social interactions among adult male langurs (Presbytis entellus) at Rajaji Wildlife Sanctuary. Int J Primatol 5:31–50. Martin P, Bateson P. 1993. Measuring behaviour. Cambridge: Cambridge University Press. p. 84–100. Moore J. 1999. Population density, social pathology, and behavioral ecology. Primates 40:1–22. Newton PN. 1988. The variable social organization of Hanuman langurs (Presbytis entellus), infanticide, and the monopolization of females. Int J Primatol 9:59–77. Nunn C. 1999. The number of males in primate groups: a comparative test of the socioecological model. Behav Ecol Sociobiol 46:1–13. Pereira ME. 1998. One male, two males, three males, more. Evol Anthropol 7:39–45. Pereira ME, Clutton-Brock TH, Kappeler PM. 2000. Understanding male primates. In: Kappeler PM, editor. Primate males. Cambridge: Cambridge University Press. p 271–277. Rajpurohit LS. 1994. The comparison of day journey lengths for bisexual troop and male band in Hanuman langurs (Presbytis entellus) around Jodhpur (India). Cheetal 33:33–36. Rajpurohit LS, Sommer V, Mohnot, SM. 1995. Wanderers between harems and bachelor bands: male Hanuman langurs (Presbytis entellus) at Jodhpur in Rajasthan. Behaviour 132:255–299. Rhine RJ, Flaningon M. 1978. An empirical comparison of one-zero, focal animal, and instantaneous methods of sampling spontaneous primate social behavior. Primates 19:353–361. Sommer V. 1985. Weibliche und männliche Reproduktionsstrategien der Hanuman Languren (Presbytis entellus) von Jodhpur, Rajasthan/ Indien [dissertation]. Göttingen: University of Göttingen. Sommer V, Rajpurohit LS. 1989. Male reproductive success in harem troops of Hanuman langurs (Presbytis entellus). Int J Primatol 10:293–317. Sommer V. 1996. Heilige Egoisten: Die Soziobiologie indischer Tempelaffen. München: Beck. Srivastava A, Dunbar RIM. 1996. The mating system of Hanuman langurs: a problem in optimal foraging. Behav Ecol Sociobiol 39:219–226. Differential Energy Budget of Langurs / 63 Sugiyama Y, Yoshiba K, Parthasarathy MD. 1965. Home range, mating season, male group and intertroop relations in Hanuman langurs (Presbytis entellus). Primates 6:73–106. Vogel C. 1988. Sociobiology of Hanuman langurs (Presbytis entellus): introduction into the Jodhpur field project. Hum Evol 3:217–226.