Musth cases in two captive male Asian elephants (Elephas maximus) in Korea

Abstract

Importance

When male elephants reach sexual maturity, they exhibit excessive sexual behaviors called musths. The musth period is important in the management of elephant herds. However, the timing of the musth and the effect of musth elephants on non-musth elephants in Korea have not been clearly analyzed.

Case presentation

In our observations, one male elephant (Koshik), who had been alone with a female, was observed to be on musth from age 15, while another young male elephant (Udara), who joined the group later, was not observed to be on musth at age 15, moreover the male elephants that were found to be on musth earlier had a longer duration of musth after the introduction of the other male. Furthermore, we also found that Koshik’s testosterone levels increased approximately 200-fold during musth (the lowest level was 0.93 ng/mL) compared to before musth (the highest level was 214 ng/mL).

Conclusions and Relevance

We found that the duration and behavior of musth in captive male elephants were affected by the introduction of other growing male elephants.

INTRODUCTION

Asian elephants reach sexual maturity at 14–15 years for males and 15–16 years for females. In the wild, they often do not mate until their late teens or 20s [1,2]. Upon reaching adulthood, males exhibit hormonally driven behavior called musth, which lasts for weeks to months and includes behaviors such as aggression and urine dribbling behavior in response to elevated testosterone levels [1,3,4]. During musth, Asian and African elephants secrete various volatile substances, such as phenol and benzoic acid, from the temporal gland located in both cheeks, known as temporal gland secretion (TGS) (Supplementary Fig. 1) [5]. Similar aromatic compounds have also been detected in urine [6].

Nevertheless, no studies have been conducted on musth in male elephants in Korean zoos. Male elephants in musth can be unpredictable and aggressive, causing harm to keepers and other animals [7]. Thus, the urine of elephants in musth is sometimes distinguished from that of elephants no musths for safety and herd management [8].

The zoo in which the study was conducted included one female and two male elephants (15 and 34 years old). A 34-year-old male elephant exhibited musth behavior since the age of 15 years. Before the age of 25 years, musth lasted about 2–3 months, and after that, it lasted about 4–5 months. The male elephant of age 15 stayed with the female elephant during the day, and the males were separated at night. The team discussed their strategy for managing a full-blown musth if it developed after noticing musth-like symptoms and a small amount of discharge from the temporal gland when the male elephant was 13 years old. Given that elephants live in herds, hormonal changes can lead to changes in herd behavior. Thus, this study aimed to analyze the behavior and testosterone levels in the blood of two male elephants around the time of musth to understand the changes in the elephant herd.

CASE PRESENTATION

Hormone analysis

Blood was drawn one to three times per year for health checks. The 5 mL of blood was collected each time and transferred to tubes for heparinization, ethylenediaminetetraacetic acid and plain tubes. Blood in plain tubes was centrifuged at 1,008 × g for 5 min. Serum samples were sent to the NEODIN VetLab Laboratory (Korea) for testosterone testing. Enzyme immunoassays and radioimmunoassays have been used to measure testosterone in serum and feces in elephants, and all have been found to be useful [9,10]. Testosterone concentrations in the present study were measured by electrochemiluminescence immunoassay using the Elecsys testosterone II assay on the Cobas e 801 modular analyzer series (Roche Diagnostics, USA), which has not been used in elephants but has been applied in other animals [11]. Hematology and biochemistry results of the blood for health check showed no abnormalities in male elephants 1 and 2, but the alkaline phosphatase level of Udara was slightly higher than that of the reference regardless of time (Supplementary Data 1 and 2, Tables 1 and 2) [12,13].

Table 1. Testosterone levels in the blood of Koshik and Udara during musth season.

Elephants		20-Feb	21-Feb	21-Dec	22-Dec	23-Jan	23-Apr	23-May
Koshik
	Status	Non-musth	Intermusth	Non-musth	Non-musth	Non-musth	Premusth	Musth
	Testosterone (ng/mL)	0.96	7.54	1.58	1.2	0.93	15	214.00
Udara		17-May	-	-	-	-	23-Apr	24-Apr
	Status	Non-musth	-	-	-	-	Premusth	Musth
	Testosterone (ng/mL)	0.114	-	-	-	-	4	27.40

Table 2. Musth expression before 2023 in Koshik.

Year	Age	Start date	End date	Interval previous musth (days)
2005 (First)	15	3/11	4/30	-
2006	16	3/7	4/26	311
2007	17	2/28	5/9	307
2008	18	2/1	5/2	267
2010	19	3/3	5/11	671
		10/15	11/18	154
2011	20	6/1	8/8	228
2012	21	6/30	7/30	328
2013	22	5/11	7/15	286
2014	23	2/7	6/20	273
2015	24	2/7	7/2	233
2016	25	2/27	6/12	241
2017	26	3/3	7/24	265
2018	27	2/19	8/28	211
2019	28	2/10	8/11	167
2020	29	3/15	5/28	218
2021	30	2/26	5/6	275
2022	31	2/13	9/3	284
2023	32	2/28	8/17	178

RESULTS

Koshik has been observed with musth since 2005, when he was 15 years old. He has been observed every year, with no symptoms in 2009 and two musth episodes in 2010. Over 18 years of age, the average number of days with musth was 99, and the longest was 202 days. After the first month, the number of symptomatic days did not exceed 100 days until the ninth year. However, the 10th year after the first musth, starting in 2014, most symptomatic days exceeded 100 (Fig. 1). Table 1 shows that the onset of musths in Koshik was occurred between February and June, and when two musth episodes were observed in 2010, the second musth started in October (Supplementary Data 1 and 2, Supplementary Table 1) [10]. On average, the interval between the end of musth each year and the beginning of the following year was 277 days.

Fig. 1. Changes of musth duration before 2023 in Koshik. Before 2014, koshik was the only elephant in the herd, the number of symptomatic days did not exceed 100 days and since then, a male named Udara has been added to the herd, making it two males (Blue asterisk), and the symptomatic musth days exceeded 100.

Testosterone levels were low before and after musth, and when measured during musth, testosterone levels were nearly 200 times higher than before. The lowest level was 0.93 ng/mL, less than 1, before musth in February 2020, and the highest was 214 ng/mL during musth in May 2023 (Table 2).

DISCUSSION

One female and two male elephants were housed separately at the zoo. Koshik, who is 34 years old, was first observed to have musth at 15 years old, which lasted 52 days. In other Asian elephants in captivity, some of them were first observed with musth at 15 or 16 years of age, but most of them were over 20 years of age when they exhibited musth, indicating that Koshik was observed with musth at an earlier age than the others [10,14]. This is likely due to the presence of only one female elephant at the time of musth observation, good nutritional ecology, and the absence of other competing males.

Udara was introduced in 2013, and there were already a male and female elephant when he was introduced. Koshik was separated from the female elephant because of aggressive behavior during musth, and the female elephant and Udara have been together ever since. In 2023, at the age of 14, Udara had slightly elevated testosterone levels, a discharge in his temporal gland, and decreased appetite, which we thought was early musth. However, he did not exhibit aggressive behavior and was aware of Koshik and we determined that Koshik had full musth, but Udara had not yet had the exact full musth symptoms and behavioral changes [15]. We expected more changes when he reached 15 years of age in 2024 and kept him with the female elephant because he did not show any sexually mature behavior. However, if Udara shows aggressive behavior, it will be separated from the female elephant in 2025. Although the female elephant was not yet near the male Koshik, behavioral changes were observed between the two elephants. Therefore, elephant husbandry will have a critical time by 2024. Based on other examples of elephants in captivity and in the wild, Udara will be somewhat inhibited by Koshik rather than continuing to musth as strongly as he normally would, as Koshik is a mature adult of 30+ years old, is still in good health, is larger than the female elephant and Udara, and is visually and olfactorily influenced by each other [16,17].

Young male Asian elephants in the wild are usually observed living with females unless musth status is observed between males, indicating that they are still sexually immature [18]. As they get older, most male elephants become independent, especially when they are older. This is like the current situation in zoos. In several cases, male elephants exhibiting musth have shown a tendency to seek mixed-sex groups, which are believed to be a way of expressing themselves to females, thinking that they can outcompete younger males [17,18]. Given these examples, it is easy to infer that Koshik had a longer duration of musth which affected the expression of musth in Udara.

Musth for male elephants is a critical point in their management because they can be aggressive toward keepers or other elephants, which may lead to foot problems because of their aggressive behavior, or can be a safety hazard for workers [10,19]. Considering the timing of TGS and testosterone elevation in male elephants, as well as the expected onset of musth, it is imperative to limit high-calorie feed intake, ensure easy access to water for proper testosterone excretion, and minimize kidney issues. In addition, hazardous objects should be removed as males become more active [20].

Various strategies have been used to manage male elephants during musth, especially in Southeast Asia where tourism is prevalent. These may include controlled feeding or separation to safeguard visitors [20]. Gonadotropin releasing hormone (GnRH) vaccines have been recently used to delay or prevent the onset of musth [3,21]. However, it has not been effective in all male elephants, and when testosterone levels were already elevated; therefore, it does not fully guarantee the safety of workers and other elephants [7,21].

This study aimed to review the case of Koshik, who was first observed to have musth symptoms, and to establish a proactive response to Udara, who developed musth symptoms, as well as future directions for herd management. Considering the transient effectiveness of GnRH vaccines and tranquilizers, such as xylazine, during musth in male elephants, and the potential for stress and stereotypical behaviors resulting from animal separation, it is imperative to prioritize herd cohesion during periods deemed safe [10]. There are some limitations to this study. The study was conducted on only two male elephants, and despite the characteristics of elephants living in groups, there are only three elephants in the zoo. therefore, the stimulation between the animals may have been somewhat insufficient to elicit various changes in behavior. in addition, musth was determined through blood changes and aggressive behavior, but additional data such as urine and changes in feed and drinking water intake were not available.

Furthermore, research on musth is needed as a basis for understanding how bull elephants express themselves and reproduce successfully in herds, and there is a lack of data on how musth changes with age and in the wild. We believe this study can help us observe the developmental process of male elephants in wild elephant herds [22].

Further research should include the relationship between male elephants in other zoos, the effects of migration on musth, and confirmation of urine extracts. despite these limitations, we believe that this study is valuable as a basis for the management of captive elephants in various aspects, including the relationship between keepers and elephants and the development of relationships among elephants. Further research is necessary to understand the relationship between keepers and elephants during musth and the mechanism by which stressors vary with the time of union and affect animal health and safety.

SUPPLEMENTARY MATERIALS

Supplementary Data 1

Blood and hormone analysis

Supplementary Data 2

Measuring the musth period and musth criteria

Supplementary Table 1

Hematology and chemistry data of Koshik and Udara

Supplementary Fig. 1

Discharge from the temporal gland (yellow asterisk) of Koshik