Assessment of dominance hierarchy through urine scent marking and its chemical constituents in male blackbuck Antelope cervicapra, a critically endangered species
Introduction
Many ungulates are socially characterized by well-defined stable dominance hierarchies (Cassinello, 1995, Cote, 2000, Freeman et al., 2004, Roden et al., 2005) which often determines the first or the best access to food, social interactions, and choice of mate (Roden et al., 2005, Hemelrijik et al., 2008). The hierarchical position of an individual is influenced by various factors including age (Bison bison: Maher and Byers, 1987, Robitaille and Prescott, 1993), body weight (Gazella dama: Cassinello and Pieters, 2000), both age and body weight (Bison bison: Roden et al., 2005), aggressiveness (Oreamnos americanus: Cote, 2000; Capra hircus: Barroso et al., 2000; Loxodonta africana: Ganswindt et al., 2005), androgen level (Pupu puda: Barto et al., 1998; Elaphurus davidianus: Li et al., 2004; Pan troglodytes: Muller and Wrangham, 2004) and dominance hierarchy is characterized by scent marking/production (Lemur catta: Kappeler, 1990; Mus domesticus: Hurst, 1990; Oreotragus oreotragus: Roberts and Dunbar, 2000; Propithecus uerreauxi uerreauxi: Lewis, 2005; Equus Caballus: Kimura, 2001; Meriones unguiculatus: Shimozuru et al., 2006).
Typically urinary scent marking involves deposition of social pheromones to elicit response from a conspecific (Ewer, 1968, Bowyer et al., 1994, Hoffman et al., 2010). Scent marking behaviours of many ungulates have been described (Gosling, 1985, Bowyer et al., 1994); urine and scent glands are the major sources of the odors (Roberts and Dunbar, 2000, Gosling and Roberts, 2001, Lewis, 2005). Major functions of urinary scent marking are defense of territory and resources, advertisement of social status, regulation of social relationships, mate attraction, and advertisement of reproductive condition (Halpin, 1986, Penn and Potts, 1998, Smith et al., 2001, Brennan and Kendrick, 2006).
In many ungulates urinary scent marking behaviour not only mediates aggressive interactions between males but also facilitates male–female interactions. For example, odors of urinary scent marking help to establish the territory of dominant male and also to keep the other males away from its territory (Thomsons's gazelles, Gazella Thomson: Estes, 1967; Blackbuck, Antelope cervicapra: David, 1973). In ungulates like bontebok, Damaliscus dorcas dorcas (Schaller, 1967), springbok, Antidorces marsupialis (David, 1973) and wildebeest, Connochaetes taurinus (Estes, 1969) urinary scent marking directs other males as part of a ritualized challenge. Urinary scent marking in North American elk, Cervus elaphus primarily influences the dominance interactions between adult males and the urinary pheromones might advertise the physical condition of males (McCullough, 1969, Bowyer and Kitchen, 1987). Male urine excreted during rut has a strong, pungent and unique odor which relays information an dominance hierarchy to conspecifics (Miquelle, 1991) indicating the urine of males may possess critically important components required in establishing territory and/to attract females.
Urinary constituents of a few ungulates have been characterized, but the biological role of urinary scent marking is yet to be investigated. For example, the red deer urine consisted mainly that derivative of carboxylic acids and some aromatic compounds (Bakke and Figenschou, 1990). Volatile substances identified in the urine of white-tailed deer comprise alcohol, aldehyde, furan, ketone, nitrite, alkene, alkane, thiol ester, disulfide, aromatic ether, ketal and amine classes of compounds (Miller et al., 1998). The preselection of candidate substances has further resulted in successful characterization of a few biological urinary pheromones in various zoo animals, farm animals and rodents. For example, urine of Asian female elephants in estrus contain high concentration of a volatile (Z)-7-dodecen-1-yl acetate compound which function as a sex pheromone stimulating male sexual behaviour (Rasmussen et al., 1997). In addition, the estrus-specific urinary volatile, 1-iodoundecane may function as bull attractant (Rameshkumar and Archunan, 2002). The male mice urinary pheromones like 2-sec-butyl-dihydrothiazole and dehydro-exo-brevicomin were active in eliciting inter-male aggression (Novotny et al., 1985a), attractiveness to females (Jemiolo et al., 1985), and estrus synchronization (Jemiolo et al., 1986). Another urinary volatile compound 2,5-dimethylpyrazine delivered from grouped adult females, delayed sexual maturation among young female mice (Novotny et al., 1985b). The urinary compounds and putative pheromones of dominant and subordinate male blackbucks are yet to be identified.
The Indian Blackbuck, A. cervicapra is territorial and generally lives in herds 30–100 individuals. The regulation of its social life depends to a large extent on chemical communication as reflected by its various odoriferous skin glands and other sources of chemical signals. Each group has a territory within which a linear dominance hierarchy is formed by means of aggression interactions. Previous study has demonstrated that the Indian Blackbucks scent mark their territory with urine and preorbital glands (David, 1973, Manimozhi, 1996, Rajagopal and Archunan, 2008, Rajagopal et al., 2010). We tested the hypothesis that there were differences in the frequency of scent urination and its chemical composition in dominant male before, during and after the dominance hierarchy period when compared with that of bachelor male. The study is a first step in understanding the potential role of urine marking in the dominance hierarchy of Indian Blackbuck.
Section snippets
Study area
This study was conducted in the conservation and breeding centre of Arignar Anna Zoological Park (AAZP) (13°16′S and 79°54′E at an altitude of MSL+ 10–100 m), Vandalur, Chennai, South India. Chennai has the distinction of being the first zoo in India, started in 1855. In 1976, the zoo was moved to the Vandalur Reserve Forest comprising, an area of about 510 ha near Chennai. The habitat of AAZP is considered a tropical evergreen scrub, a degraded forest mostly consisting of thorny bushes. The
Duration of dominancy or leadership period
Among the 14 adult male Blackbuck observed under the semi-natural captive conditions, 9 were found to have established dominance hierarchy during the study period from June 2007 to December 2008. In the beginning the animal number 4 (14th June to 17th July 2007) exhibited dominance and took over the other males followed by animal numbers 5, 8, 6, 1, 11, 14, 12 and 10, respectively (Table 2). Animal number 14 showed the longest duration of leadership in the same enclosure for 210 days from 4th
Discussion
The frequency of urine marking by the dominant male during hierarchy formation period (p < 0.001) is higher when compared to before and after the hierarchy period as compared to bachelor males. The result is in agreement with earlier investigations, which have described that the dominant male urine scent marking behaviour (i.e. odor) may adversely affect the fighting ability, suppressing the social and sexual behaviour of subordinate males in several species like pine vole, Microtus pinetoram (
Acknowledgements
The authors thank Prof. B.V. Burger, Department of Chemistry, University of Stellenbosh, South Africa, for encouragement and suggestion, Prof. P.Govindarajalu, for critically sign through the manuscript and the Chief Wildlife Warden and the Director of the AAZP, Vandalur, Chennai, for granting permission to carry out this study. The authors are indebted to Dr K. Senthilkumar (Veterinary Assistant Surgeon) and Dr Pathan Nazrulla Khan (Zoo Veterinarian) of the AAZP for their help in collection of
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