A Surge-Like Increase in Luteinizing Hormone Preceding Musth in a Captive Bull African Elephant (Loxodonta africana)

Abstract

ABSTRACT. This study was conducted to determine the correlation between reproductive hormones and musth in a male African elephant. Changes in circulating luteinizing hormone (LH), follicle stimulating hormone (FSH), testosterone and immunoreactive (ir-) inhibin and the degree of musth were evaluated for 4 years. LH increased 4 weeks before musth began. The highest concentrations of testosterone and ir-inhibin were observed from April to October. There were positive correlations among testosterone, ir-inhibin and musth behavior. These findings suggested that the surge-like LH in the pre-musth period might stimulate secretion of testosterone and ir-inhibin and thus initiate the musth behavior. This study also suggested that the high LH level before musth might be a useful biomarker for the beginning of the musth season.KEY WORDS: African elephant, inhibin, luteinizing hormone, musth, testosterone.J. Vet. Med. Sci. 73(3): 379-383, 2011 Musth is a unique phenomenon that occurs either annually or semiannually in adult male African (Loxodonta africana) [7,16,17] and Asian (Elephas maximus) elephants [5,11]. During musth, male elephants have elevated levels of androgens, especially androstenedione and testosterone [1,6,7,10,15,18,20,21,24]. Musth bulls were reported to have elevated levels of luteinizing hormone (LH) in both African [1] and Asian [15] species. Secretory patterns of follicle stimulating hormone (FSH) and immunoreactive (ir-) inhibin in male elephants have never been reported before. In captivity, both African and Asian bulls in musth exhibit aggression towards their mahouts or handlers [5,10,20], which is extremely dangerous for zoo staff, veterinarians and researchers who manage breeding programs. Thus, our understanding of markers for prediction of musth needs to be improved. The objective of this study was to investigate secretion of reproductive hormones associated with musth characteristics in a male African elephant in Japan.A male African elephant named "Tamao" (Fig. 1A) was studied for 4 years, from 33 to 37 years of age. It was housed at the Tama Zoological Park, Hino City, Tokyo, Japan, together with 4 female African elephants. All elephants were housed outside during the daytime (0900 hr-1600 hr) and inside the building at night throughout the year. Blood samples were collected weekly between 0800 hr and 0900 hr from an ear vein without anesthesia. The samples were centrifuged, and sera were stored at -20C until hormonal analysis. The appearance of characteristic behavioral and physical changes was recorded daily during the 4-year period. The bull elephant was classified as being in musth when one or a combination of the following behavior and/or physical changes were continuously (for more than 3 days per week) observed: increased aggressive behavior, temporal gland secretion (TGS; Fig. 1B) and urine dribbling (UD; Fig. 1B) as described previously [3]. Since TGS can occur in African bulls under stress or social excitation, TGS was considered as an indicator of musth only if it occurred ...

Secretory Pattern of Inhibin During Estrous Cycle and Pregnancy in African (Loxodonta africana) and Asian (Elephas maximus) Elephants

“…Previous reports have shown that the serum inhibin levels were parallel with progesterone throughout the estrous cycle in Asian elephants [Brown et al, ; Kaewmanee et al, ]. Kaewmanee et al demonstrated that the immunolocalization of inhibin α, βA, and βB subunits were detected in both granulosa cells of antral follicles and luteal cells in the ovary of an Asian elephant [Kaewmanee et al, ]. These findings strongly suggested that CLs and follicles were the source of circulating inhibin during the estrous cycle in the Asian elephants.…”

“…The serum concentrations of ir‐inhibin were determined by RIA based on the bovine inhibin RIA previously described [Kaewmanee et al, , ; Hamada et al, ], using antisera against bovine inhibin (TNDH‐1, Laboratory of Veterinary Physiology, Tokyo University of Agriculture and Technology) and bovine 32 kDa inhibin for both iodination and standard, respectively. Since inhibin antiserum (TNDH‐1) cross‐reacts with 26 kDa α monomer [Kaneko et al, ; Medan et al, ] inhibin are referred to as immunoreactive (ir‐) inhibin.…”

Immunohistochemical localization of inhibin/activin subunits in adult Asian elephant (<i>Elephas maximus</i>) testes

“…Although research regarding the role of inhibin in both African and Asian female elephants has been previously reported [ 7 , 13 , 24 ], only males in the African species have been studied [ 8 , 12 ]. The present study determined the immunolocalization of inhibin/activin subunits in the testes of adult male Asian elephants.…”

“…Moreover, the inhibin secretory pattern in male African elephants has been previously reported by Kaewmanee et al . [ 8 ], who found that the level of circulating immunoreactive (ir)-inhibin in male African elephants was correlated with the degree of musth and testosterone level, with the latter being higher in the musth than in the pre- and non-musth stages. The authors suggest that the increasing level of (ir)-inhibin and testosterone during the musth stage resulted from the stimulation of high luteinizing hormone (LH) and FSH during the pre-musth stage [ 8 ].…”

Differential testosterone response to GnRH-induced LH release before and after musth in adult Asian elephant (Elephas maximus) bulls

“…Frequent sampling of Asian elephant bulls has further demonstrated that pulses of testosterone closely follow those of LH (w1 pulse/ 3 hours) [13]. In a long-term study (4 years) of one African bull, serum LH increased about 4 weeks before the onset of musth and was maintained for approximately 5 weeks and was considered likely to be responsible for triggering the rise in testosterone [14]. The temporal relationship between aggressive behaviors and androgen production during musth suggests that the two are linked although the regulatory mechanisms are unknown.…”