Endocrinological correlates of male bimaturism in wild Bornean orangutans

Abstract

Among primates, orangutans are unique in having pronounced male bimaturism leading to two fully adult morphs that differ in both physical appearance and behavior. While unflanged males have a female-like appearance, flanged males have the full suite of secondary sexual characteristics, including cheek flanges and a large throat sac. So far, hormonal correlates of arrested development in unflanged males and the expression of secondary sexual characteristics in flanged males have only been studied in zoo-housed individuals. In this study, we investigated fecal androgen and glucocorticoid metabolites as hormonal correlates of male bimaturism in 17 wild adult Bornean orangutans (Pongo pygmaeus) in Central Kalimantan, Indonesia. We predicted and found higher androgen levels in flanged males compared to unflanged males, probably due to ongoing strong competition among flanged males who meet too infrequently to establish a clear linear dominance hierarchy. Furthermore, we found no difference in fecal glucocorticoid metabolite concentrations between flanged and unflanged males, indicating that social stress is unlikely to explain arrested development in unflanged wild orangutans. The only actively developing male in our study showed significantly higher androgen levels during the period of development than later as a fully flanged male. This supports earlier findings from zoo studies that elevated androgen levels are associated with the development of secondary sexual characteristics.

Testosterone and reproductive effort in male primates

“…These include sifakas (Brockman et al 2001, Kraus et al 1999), white-faced capuchins (Schoof et al 2014, 2016), gray-cheeked mangabeys (Arelt et al 2011), long-tailed macaques (Girard-Buttoz et al 2015), mandrills ( Mandrillus sphinx : Setchell et al 2008, Wickings & Dixson 1992), mountain gorillas (Robbins & Czekala 1997), and orangutans (Marty et al 2015). In these species, high-ranking males are generally able to monopolize estrous females, particularly during the periovulatory period.…”

“…Adult male orangutans exhibit two morphs, only one of which possesses the suite of secondary sexual characteristics that includes projecting cheek pads, a throat pouch, long hair, and a musky odor (Knott & Kahlenbeg 2007). These dominant males exhibit higher androgen levels than undeveloped males, but further details are not available (Marty et al 2015). Sifaka males also exhibit two morphs – one with a dark chest stain that is associated with sternal gland activity and scent marking, and one with a clean chest.…”

“…In male chimpanzees, however, mean monthly testosterone levels correlated with mean monthly rates of pant-hooting, and diurnal patterns of pant-hooting paralleled those of testosterone production (Fedurek et al 2016). Comparable data are not available from orangutans, but in that species loud calls are only produced by dominant, flanged males (Mitani 1985), who maintain higher androgen levels than unflanged males (Marty et al 2015). Harem-holding gelada baboon males give loud calls during competitive displays against bachelor males.…”

The dark side of the red ape: male-mediated lethal female competition in Bornean orangutans

“…Moreover, changes in his facial features as well as behavior suggest that he was already in the process of growing flanges (by August 2015 he had fully developed flanges) (cf. Dunkel et al 2013;Marty et al 2015). Over the years, Ekko was often observed in association with resident females, (during 31.5% of 534 hours of focal follow hours on Ekko since 2003), including Sidony.…”

A Review of Hormone Analysis on Primate Ecology

“…。しかし，尿は排泄後に時間が経 過すると乾燥して回収できなかったり，排尿場所によっ ては全く回収ができない場合がある。そのため，より 採取が容易な糞を用いた研究が，その後 1990 年頃から 飼育下および野生下で発表されるようになった (Lasley and Kirkpatrick, 1991;Wasser et al, 1988;Ziegler et al, 1989) 。雌の性ホルモン(特に種特異性のない性ステロ イドホルモン)濃度を分析することで，春機発動(繁 殖能力の発現開始) ，発情期(排卵期) ，妊娠の有無， 陰部腫脹との関係などが明らかにされてきた (Carroll et al, 1990;Curtis et al, 2000;Dahl et al, 1987;Heistermann et al, 1996;Kinoshita et al, 2017;Shimizu, 2005;Shimizu et al, 2003) Fourie et al, 2016) Fairbanks et al, 2011;Henley et al, 2013;Vliegenthart et al, 2016;Yamanashi et al, 2013) (Maggioncalda et al, 1999;Marty et al, 2015) ，その間に成長ホルモンの濃度も上昇 することが確認されている (Maggioncalda et al, 2000) 。 ただし，野生オランウータンにおける遺伝解析により， アンフランジ(フランジがない)雄でも子の父親になっ ていることが確認されており (Goossens et al, 2006) (Prudom et al, 2007;Roberts et al, 2001;Soltis et al, 2005;Ziegler and Snowdon, 2000;Ziegler et al, 1996) (Woods, 1975) Pettitt et al, 2007) 。糞中の水分含量が高いと，より一層細菌による 代謝は活発になる (Palme, 2005 (Khan et al, 2002;Palme, 2005;Pettitt et al, 2007;Woods, 1975 (Kinoshita et al, 2016) 。オランウータンやチンパンジーにおいて， 有機溶媒を用いてフィルターペーパーからホルモンを 抽出し分析に成功している研究例もある (Seraphin et al, 2008;Shideler et al, 1995;Thompson and Knott, 2008) 。 このように，調査地の状況に合わせてどのような保存 方法をとるべきかについても，予備実験で確認してお くことが重要である。また，近年は「Field-Friendly 法」 として，保存過程を経ずに野外で直接サンプルからホ ルモンを抽出し実験室に抽出物を持ち帰って分析して い る 例 も あ る (Nugr...…”