Endocrine Correlates of Puberty in Female Asian Elephants (Elephas Maximus) at the Pinnawala Elephant Orphanage, Sri Lanka Samanthi Mendis1,2, Niromi K
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Mendis et al. BMC Zoology (2017) 2:1 DOI 10.1186/s40850-016-0012-8 BMC Zoology RESEARCHARTICLE Open Access Endocrine correlates of puberty in female Asian elephants (Elephas maximus) at the Pinnawala elephant orphanage, Sri Lanka Samanthi Mendis1,2, Niromi K. Jayasekera1*, Rajapakshalage C. Rajapakse3 and Janine L. Brown4 Abstract Background: Previous studies have established ovarian cycle characteristics of adult Asian elephants using progestagen analyses, but little work has been done on young elephants to determine age at puberty. Demographic studies of wild Asian elephants suggest females give birth at about 12–18 years of age (conceiving at 10–16 years of age based on a 2-year gestation). However, there are a few examples of zoo elephants giving birth at only 5–6 years of age, so they would have started cycling much earlier. This study was carried out at the Pinnawela Elephant Orphanage (PEO) in Sri Lanka, where a herd of >80 captive elephants breeds successfully, resulting in a unique opportunity to monitor hormones and document initiation of ovarian cyclicity in young females, thus contributing to the normative reproductive database for this species. Results: We measured serum progestagens in samples collected every 10 days for 18 – 24 months from 11 females (3.5–15 years of age), and found six (5.5 – 12 years of age) already were cycling at study onset. Four females started cycling during the study at 4.5, 5.5, 7.5 and 15 years of age. There were no quantitative or qualitative differences between the first pubertal luteal phase and those of subsequent cycles. Of the 46 ovarian cycles observed, 78% were associated with clear behavioral signs of estrus (heightened bull attentiveness, and willingness of females to be mounted) during the late non-luteal period when progestagens were low. The average body weight at puberty was ~48% of that of adult female elephants at PEO. Conclusions: Asian elephants under human care, including under semi-captive conditions, may reach puberty earlier than those in the wild, perhaps due to better nutrition and reaching a body weight capable of supporting reproductive activity at a younger age. Thus, facilities with bulls need to carefully manage elephants to avoid accidental pregnancies in young females that may be too small to safely carry a pregnancy to term. Keywords: Elephant, Estrus, Ovarian cycle, Progestagens, Puberty Background longest estrous cycle of any land mammal, ranging between Ovarian cycle activity in elephants is easily determined 13 and 17 weeks, with a 3 to 6-week follicular phase and 7 by weekly or bi-weekly progestagen analyses of serum, to 12-week luteal phase [4, 5]. By contrast, substantially less urine or feces [1–3]. A properly maintained record of is known about aspects of reproductive function in ‘domes- progestagen data is key to determining the reproductive ticated’ Asian elephants in range countries. Despite their capacity of individual animals, as well as allowing proper being managed under human care for thousands of years, planning and timing of breeding, and accurate pregnancy few captive populations are self-sustaining [6]. Today, with diagnosis [4]. A substantial endocrine database related to the exception of Myanmar, it is illegal to capture wild Asian ovarian cycle characteristics now exists for Asian elephants, elephants for any purpose; thus, to sustain this important particularly those in western zoos [3]. Elephants have the cultural heritage, successful captive breeding programs are essential, and could benefit by a thorough understand- * Correspondence: [email protected]; [email protected] ing of basic biological functioning, including age at 1Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine and Animal Science, University of Peradeniya, Peradeniya, Sri Lanka puberty onset [4]. Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Mendis et al. BMC Zoology (2017) 2:1 Page 2 of 6 From observational data, Asian elephants begin repro- elephants at the PEO to determine pubertal status. Changes ducing at around 12–18 years of age in the wild [7, 8]. In in body weight also were examined in relation to age and North American zoos, the average age at first conception ovarian cycle activity. Such information could help improve based on studbook data is 16.9 years [9]. Logging the on going breeding program at PEO, and also provide elephants of Myanmar show low fecundity up to about information to captive facilities globally on how to best 13 years of age, followed by a rapid increase to a peak at manage young elephants for maximal reproductive success. 19 years of age [10]. There are examples of captive births occurring at much younger ages, however, raising ques- Methods tions about when females actually reach puberty and are Animals and sample collection capable of reproduction. For example, the Asian elephant The PEO is open to the public and located in the wet-zone, studbook in the U.S. lists two zoo births in females less mid-country region of Sri Lanka (92 m elevation). It than 7 years of age [11]. We also have preliminary consists of 11 hectares with sheds for night accommoda- hormone data in Asian elephants showing initiation of tion, a grassland area with a large water hole, and access to ovarian cyclicity at 6, 7 and 8 years of age [4, 5]. Unfortu- the adjacent Maha Oya river. Elephants are not tamed and nately, few facilities collect samples for hormone monitor- are managed under semi-captive conditions as a group ing before 8 years of age, so it is unclear how common it comprising adult females and male/female calves, which is for females to start cycling that young. are allowed full social interactions throughout the day. Of the ~4000 Asian elephants in Sri Lanka, about 300 are Adult females are chained overnight from approximately maintained in captivity, mostly at temples or held by private 1600 – 0800 h; calves under 4 years of age are untethered owners [12]. The largest captive population in Sri Lanka is and stay in close proximity. Females and young bulls (<8– at the Pinnawala Elephant Orphanage (PEO), managed by 10 years of age) are walked as a group to the river (<1 km) the Department of National Zoological Gardens, which is a for bathing twice a day (at 1000 and 1400 h) for 2 h each, rare exception in having not only a sustaining, but also a and fed a mixture of browse, supplemented with local growing population [13, 14]. The PEO began as an elephant fruits. A full time veterinarian is onsite, and individual re- orphanage in 1975 with five baby elephants. Today it is a cords of health and reproductive events are maintained on successful captive breeding center with a current popula- all elephants, starting at birth or arrival at PEO. This study tion of over 80 elephants, including 45 that were born at was approved by the Animal Care and Use Committee at the orphanage; there now are three generations of ele- the Peradeniya University, Kandy, Sri Lanka, and Conserva- phants at PEO [14]. Thus, this facility provided a unique tion & Research Center/National Zoological Park Animal opportunity to study hormonal changes in young elephant Care and Use Committee (#06-20). females, at or near the time of puberty. The aim of this Eleven female elephants at PEO were evaluated and are study was to analyze serum progestagens in young Asian described in Table 1. All calves of wild origin were brought Table 1 Summary of the age and origin of female elephants utilized in this study, and mean (± SEM) estrous cycle characteristics and serum progestagen concentrations Female Date of Age at Onset Captive or Number Luteal Phase Follicular Phase Total Cycle Baseline Luteal Peak Birth and End of Wild Born of Cycles Length (days) Length (days) Length (days) Progestagens Progestagens Study (years) (ng/ml) (ng/ml) Tikiri ~Sep 2002 3.0 – 4.5 Wild 0 0.63 Mali* ~ Nov 2001 3.2 – 5.0 Wild 4 55.1 ± 6.8a 24.2 ± 6.5 90.0 ± 1.7a 0.73 2.25 ± 0.12c Maya* ~Jan 2000 4.0 – 5.8 Wild 4 79.0 ± 4.2b,c 25.3 ± 9.5 104.3 ± 13.5b 0.55 3.26 ± 0.50d Uthpala Aug 1999 5.5 – 7.5 Captive 7 78.3 ± 7.1b,c 33.4 ± 2.8 114.6 ± 6.0c 0.34 0.94 ± 0.10a Ashokamala* Aug 1999 6.5 – 8.3 Captive 4 78.0 ± 3.4b,c 28.3 ± 0.8 109.3 ± 2.8c 0.20 0.89 ± 0.15a Surangi ~Dec 1997 7.0 – 9.2 Wild 7 76.9 ± 2.8b,c 29.0 ± 3.2 104.8 ± 4.5b,c 0.76 2.06 ± 0.20c Supamali** ~Jun 1997 7.3 – 9.1 Wild 2 69.5 ± 3.3a,b 28.5 ± 3.3 98.0 ± 1.0a,b 0.50 2.23 ± 0.04c Meena** ~Nov 1997 8.3 – 10.3 Wild 3 77.7 ± 2.8b,c 35.0 ± 8.3 112.7 ± 5.6c 0.52 2.01 ± 0.27c Sandali ~Jul 1993 11.6 – 13.6 Wild 7 65.7 ± 5.9a,b 27.0 ± 5.2 88.5 ± 5.7a 0.43 1.28 ± 0.16b Kanthi ~Aug 1992 12.8 – 14.8 Wild 6 82.3 ± 6.3c 31.0 ± 2.0 113.3 ± 6.2c 1.70 4.71 ± 0.17e Manika* ~1990 14.3 – 16.2 Wild 3 83.7 ± 10.9c 33.7 ± 2.1 117.3 ± 12.6c 1.13 3.43 ± 0.25e Overall Mean 74.6 ± 2.8 30.6 ± 1.1 105.3 ± 3.2 0.68 ± 0.13 2.31 ± 0.38 *Exhibited first estrous cycle during the study period **Females conceived during study period a,b,c,d,eValues within column differ (P < 0.05) Mendis et al.