Endocrine Correlates of Musth in Free-Ranging Asian Elephants (Elephas maximus) Determined by Non-Invasive Faecal Steroid Hormone Metabolite Measurements

The occurrence of musth, a period of elevated levels of androgens and heightened sexual activity, has been well documented for the male Asian elephant (Elephas maximus). However, the relationship between androgen-dependent musth and adrenocortical function in this species is unclear. The current study is the first assessment of testicular and adrenocortical function in free-ranging male Asian elephants by measuring levels of testosterone (androgen) and cortisol (glucocorticoid – a physiological indicator of stress) metabolites in faeces. During musth, males expectedly showed significant elevation in faecal testosterone metabolite levels. Interestingly, glucocorticoid metabolite concentrations remained unchanged between musth and non-musth periods. This observation is contrary to that observed with wild and captive African elephant bulls and captive Asian bull elephants. Our results show that musth may not necessarily represent a stressful condition in free-ranging male Asian elephants.     

The Social and Ecological Integration of Captive-Raised Adolescent Male African Elephants (Loxodonta africana) into a Wild Population

Background

A rapid rise in the number of captive African elephants (Loxodonta africana) used in the tourism industry in southern Africa and orphaned elephants in human care has led to concerns about their long-term management, particularly males. One solution is to release them into the wild at adolescence, when young males naturally leave their herd. However, this raises significant welfare concerns: little is known about how well released elephants integrate into wild populations and whether they pose a greater threat to humans than wild elephants. We document the release of three captive-raised adolescent male African elephants in the Okavango Delta, Botswana.

Methodology/Principal Findings

Despite having been part of a herd of working elephants for at least eight years, the three males progressively integrated into the complex fission-fusion society of wild bull elephants. In the three years following release, they showed no tendency to be closer to human habitation, and there were no significant differences between wild and captive-raised adolescent males in the total number of social interactions, size of ranges and habitat use. However, the captive-raised elephants sparred less and vocalised more, and spent more time alone and in smaller social groups. Thereafter the released elephants continued to expand their ranges and interact with both mixed-sex herds and males. One male was shot by farmers 94 months after release, along with ten wild elephants, on a ranch outside the protected area.

Conclusions/Significance

We show that captive-raised adolescent male elephants can integrate into a wild population. Long-term studies are required to determine the longevity, breeding success, and eventual fate of released male elephants, but we identified no significant short-term welfare problems for the released elephants or recipient population. Release of captive-raised mammals with complex social systems is a husbandry option that should be explored further.     

Frontalin: a chemical message of musth in Asian elephants (Elephas maximus)

Musth is an important male phenomenon affecting many aspects of elephant society including reproduction. During musth, the temporal gland secretions (as well as the urine and breath) of adult male Asian elephants (Elephas maximus) discharge a variety of malodorous compounds together with the bicyclic ketal, frontalin. In contrast, teenage male elephants in musth release a sweet-smelling exudate from their facial temporal gland. We recently demonstrated that the concentration of frontalin becomes increasingly evident as male elephants mature. In the present study, we demonstrate that behaviors exhibited towards frontalin are consistent and dependent on the sex, developmental stage and physiological status of the responding conspecific individual. To examine whether frontalin functions as a chemical signal, perhaps even a pheromone, we bioassayed older and younger adult males, and luteal- and follicular-phase and pregnant females for their chemosensory and behavioral responses to frontalin. Adult males were mostly indifferent to frontalin, whereas subadult males were highly reactive, often exhibiting repulsion or avoidance. Female chemosensory responses to frontalin varied with hormonal state. Females in the luteal phase demonstrated low frequencies of responses, whereas pregnant females responded significantly more frequently, with varied types of responses including those to the palatal pits. Females in the follicular phase were the most responsive and often demonstrated mating-related behaviors subsequent to high chemosensory responses to frontalin. Our evidence strongly suggests that frontalin, a well-studied pheromone in insects, also functions as a pheromone in the Asian elephant: it exhibits all of the determinants that define a pheromone and evidently conveys some of the messages underlying the phenomenon of musth.     

Physical, physiological, and behavioral correlates of musth in captive African elephants (Loxodonta africana)

Although musth in male African elephants (Loxodonta africana) is known to be associated with increased aggressiveness, urine dribbling (UD), temporal gland secretion (TGS), and elevated androgens, the temporal relationship between these changes has not been examined. Here, we describe the pattern of musth-related characteristics in 14 captive elephant bulls by combining long-term observations of physical and behavioral changes with physiological data on testicular and adrenal function. The length of musth periods was highly variable but according to our data set not related to age. Our data also confirm that musth is associated with elevated androgens and, in this respect, show that TGS and UD are downstream effects of this elevation, with TGS responding earlier and to lower androgen levels than UD. Because the majority of musth periods were associated with a decrease in glucocorticoid levels, our data also indicate that musth does not represent a physiological stress mediated by the hypothalamic-pituitary-adrenal axis. Furthermore, we demonstrate that the occurrence of musth is associated with increased aggression and that this is presumably androgen mediated because aggressive males had higher androgen levels. Collectively, the information generated contributes to a better understanding of what characterizes and initiates musth in captive African elephants and provides a basis for further studies designed to examine in more detail the factors regulating the intensity and duration of musth.     

The sexually active states of free-ranging male African elephants (Loxodonta africana): defining musth and non-musth using endocrinology, physical signals, and behavior

Musth in male African elephants, Loxodonta africana, is associated with increased aggressive behavior, continuous discharge of urine, copious secretions from the swollen temporal glands, and elevated androgen levels. During musth, bulls actively seek out and are preferred by estrous females although sexual activity is not restricted to the musth condition. The present study combines recently established methods of fecal hormone analysis with long-term observations on male-female associations as well as the presence and intensity of physical signals to provide a more detailed picture about the physical, physiological, and behavioral characteristics of different states of sexual activity in free-ranging African elephants. Based on quantitative shifts in individual bull association patterns, the presence of different physical signals, and significant differences in androgen levels, a total of three potential sub-categories for sexually active bulls could be established. The results demonstrate that elevations in androgen levels are only observed in sexually active animals showing temporal gland secretion and/or urine dribbling, but are not related to the age of the individual. Further, none of the sexually active states showed elevated glucocorticoid output indicating that musth does not represent an HPA-mediated stress condition. On the basis of these results, we suggest that the term "musth" should be exclusively used for the competitive state in sexually active male elephants and that the presence of urine dribbling should be the physical signal used for defining this state.     

Testosterone and dihydrotestosterone concentrations in elephant serum and temporal gland secretions

Serum and temporal gland secretions (TGS) were obtained from mature wild African (Loxodonta africana) and captive Asian elephants (Elephas maximus). Samples were obtained from five cows and eight bulls culled for management purposes in Kruger National Park, South Africa, and from four females and two males residing at the Washington Park Zoo, Portland, Oregon. Our purpose was to describe the levels of the androgens, testosterone (T), and dihydrotestosterone (DHT), and to correlate these observations with sex, species and behavioral status. Male-female differences in serum T were pronounced in the Asian species, whereas male and female concentrations overlapped in the African elephant serum. Serum T concentrations in African females were greater than in Asian females. Serum DHT reflected T levels, except that the striking elevation of testosterone in Asian bulls during musth was not paralleled by equal increases in DHT levels. A species difference observed among males was higher serum T levels in nonmusth Asian bulls (1.84-5.35 ng/ml) compared to the levels in African bulls (0.38-0.68 ng/ml), except for one dominant African bull (6.64 ng/ml). This single African value was still considerably lower than the serum T values of the Asian males during musth. These musth values were the highest serum androgen concentrations: T was between 19 and 40 ng/ml (average 26.10 ng/ml). The TSG values of T and DHT were much higher than serum levels except in the Asian female. T/DHT ratios in TGS were more similar than in serum. One dominant African bull had a T TGS value of 78 ng/ml, which was much higher than the rest of the African males or females, but considerably lower than as Asian bull in musth (547 ng/ml). It seems apparent that a change in androgen status as reflected in serum and TGS levels of T and DHT precedes or is concomitant with overt alteration in behavior in the Asian male. The temporal gland appears to actively concentrate androgens in both African males and females, but in the Asian male the gland secretes only during musth when the greatest concentration of both T and DHT were observed. The apparent difference in the degree of temporal gland secretory activity between the two species suggests a more specific communicative function within the Asian male.     

Urinary androstenedione and luteinizing hormone concentrations during musth in a mature African elephant

Musth has not been well documented in captive African elephants. A 37-year-old African bull elephant in the Kansas City Zoological Park was observed during periods of behavioral musth and non-musth. Androstenedione and luteinizing hormone (LH) concentrations in urine were measured by radioimmunoassay. Urinary androstenedione and LH levels were significantly higher in musth urine than in non-musth samples. A positive correlation (P > 0.001) existed between urinary LH and androstenedione concentrations. These results indicate that musth can occur in a zoo-maintained African elephant and that urinary androgen levels are elevated during musth, possibly as the result of LH stimulation of testicular steroidogenesis.     

Endocrine and behavioral changes in male African elephants: linking hormone changes to sexual state and reproductive tactics

Hormones play a crucial role in mediating genetic and environmental effects into morphological and behavioral phenotypes. In systems with alternative reproductive tactics (ART) shifts between tactics are hypothesized to be under proximate hormonal control. Most studies of the underlying endocrine changes behind ART have focused on fish and amphibians rather than mammals and few have investigated the potential interaction between different endocrine axes in regulating shifts between conditional dependent tactics. Using a combination of endocrine and behavioral data from male African elephants we expand on our previously published analysis and show that the initial increase in androgens predates the behavioral shifts associated with reproductively active periods, supporting the role of androgens in activating sexually active periods in males. A strong interactive effect between androgens and glucocorticoids was found to determine the presence or absence of temporal gland secretion and urine dribbling, signals associated with the competitive reproductive tactic of musth, with elevated glucocorticoids levels suppressing the occurrence of musth signals. In addition external environmental conditions affected hormone levels. The presence of receptive females resulted in elevated androgens in dominant musth males but increased glucocorticoids in subordinate non-musth males. The presented data on hormones, behavior and reproductive tactics strongly support an underlying endocrine mechanism for mediating the translation of intrinsic as well as extrinsic local conditions into the conditional dependent reproductive tactics in male elephants via interactions between the hypothalamic-pituitary-gonadal and -adrenal axes.     

Altered androstenedione to testosterone ratios and LH concentrations during musth in the captive male Asian elephant (Elephas maximus)

Greater concentrations of androstenedione than testosterone were usually present during periods of non-musth in plasma collected weekly for various periods up to 2 years in 8 male Asian elephants (4-35 years of age). For the 6 males that exhibited musth the androstenedione/testosterone ratio shifted greatly in favour of testosterone. The severity of musth was assessed weekly using a scale of 1 to 5 for each of 8 behavioural traits including urine dribbling, temporal gland secretion and aggression. A significant correlation (P less than 0.05) was noted between plasma testosterone concentrations and the musth score value in 5 of 6 musth episodes. Brief shifts in the ratio of two androgens when testosterone predominated (n = 106) were seen during the non-musth period in 3 of the males studied continuously for 2 years. In 82% of these instances, stimuli of a sexual or aggressive nature had occurred in the preceding 48 h (chi 2, P less than 0.01). A heterologous bovine assay was used to measure LH values in plasma collected every 15 min for 12 h. Increases in testosterone concentrations followed pulsatile increases in plasma LH concentrations during 7 non-musth periods in 4 animals. Apart from pulse frequency, increases in the variables describing pulsatile LH secretion were seen in 2 strong musth and 2 mild musth episodes compared to non-musth values. A strong musth, however, was characterized by a much greater increase in pulsatile testosterone secretion than was a mild musth and which may be a function of the duration of musth.     

Musth and urinary testosterone concentrations in the African elephant (Loxodonta africana)

Urine samples were obtained from free-ranging African elephants that were considered to be in and out of musth. Testosterone concentrations, measured by radioimmunoassay were significantly greater in males that were in or around the time of behavioural musth. This study supports a correlation between the observed behavioural characteristics of musth and urinary testosterone levels.     

Sexual segregation in habitat use by elephants in Chobe National Park, Botswana

We report on a study conducted on free‐ranging African elephants in the woodlands of northern Botswana. We compared bull groups and family units with regard to (1) their patterns of habitat use and (2) their ranging distances from perennial water sources. During the dry season, adult males frequented more habitat types than family units, whereas family units used a wider diversity of habitats than bulls during the wet season. Bulls roamed widely (>10 km) from perennial drinking water in the dry season, when family units congregated within 3.5 km of the rivers. During the wet season, when ephemeral pans were abundant, all elephant groups were found at intermediate distances (5 km) from the rivers. The spacing of elephants in the dry season is consistent with sexual segregation but we reject the hypothesis that this is an outcome of indirect competition for food, because our concurrent studies on elephant feeding ecology found no evidence for intraspecific competition. Instead, we propose that most adult male elephants space themselves to avoid conflict with musth bulls and roam widely in the dry season between discretely distributed feeding ‘hotspots’. The small proportion of males that are in musth remain close to family units to maximize mating opportunities, and family units are unable to range far from water in the dry season. This is due to (1) comparatively high rates of water turn‐over among juveniles and lactating cows and (2) the reduced mobility of neonates.     

Social associations and vocal communication in wild and captive male savannah elephants Loxodonta africana

相似文献   

The elephant population of Samburu and Buffalo Springs National Reserves, Kenya

A 21‐month individual identification project on the Samburu and Buffalo Springs National Reserves' elephant population was conducted between November 1997 and July 1999. The free ranging population, of at least 767 elephants, which relied heavily on areas outside the reserves, was individually identified. The numbers of elephants observed per day fluctuated but were greater during dry periods then wet. However, the sizes of aggregations were greater during wet periods. Preliminary investigation suggested that the population could be divided into two groups, which were designated resident and non‐resident family units. The groups comprised approximately equal numbers of cows and calves, but temporally had different reserve use patterns and calving peaks. The daily numbers of males and musth males were correlated with numbers of females. The reserves appeared to be a focal area for calving, indicating that the study area was of reproductive importance to the population. Demographic data indicated a female biased population sex ratio, with over twice the number of mature females to males. The observed sex skew was greatest for older age classes, and the density of musth bulls in the study area was low. The population was affected by poaching. Continued monitoring will assist conservation efforts by alerting authorities of major demographic or range use changes.     

Effects of rainfall, host demography, and musth on strongyle fecal egg counts in African elephants (Loxodonta africana) in Namibia

Wild African elephants (Loxodonta africana) are commonly infected with intestinal strongyle parasites. Our objective was to determine baseline fecal strongyle egg counts for elephants in the northeast region of Etosha National Park, Namibia and determine if these numbers were affected by annual rainfall, elephant demography (age of individuals and composition of groups), and hormonal state of males. We found that matriarchal family group members have significantly higher fecal egg counts than male elephants (bulls). Among family group members, strongyle egg counts increased with age, whereas among bulls, strongyle egg counts decreased with age. Years of higher rainfall were correlated with decreased numbers of strongyle eggs among bulls. Finally, bulls were not affected by their physiologic (hormonal) status (musth vs. nonmusth). These results suggest that infection by strongyle parasites in Namibian African elephants is a dynamic process affected by intrinsic and extrinsic factors including host demography and rainfall.     

Honest signalling through chemicals by elephants with applications for care and conservation

Chemical signals are difficult to fake because they are often directly associated with phenotype and physiological condition, and hence likely to be honest signals for intraspecific communication. Chemical signals may be modified after release by the sender or by the environment. The proximate and ultimate signal meanings are dependent not only on the condition of the sender, but also on the physiological status of the receiver. Understanding the relationships and linkage among signal modality, signal function and receiver response is an essential first step before using natural signals for animal care and conservation. Our studies on chemical communication in Asian and African elephants combine observational and experimental work in captive and wild settings to further this understanding. Recent discoveries of pheromones in Asian elephants and the biochemistry of these compounds provide strong evidence that such chemical signals are honest indicators of reproductive status. Chemically identifying the signals and verifying their functional context with statistically robust behavioural studies are essential aspects for understanding the communication system. Additionally, the investigative process of discovering, identifying and verifying the function of chemical signals among captive elephants offers safe and stimulating enrichments. The knowledge garnered from such studies has potential conservation benefits for managing wild elephant populations. A firm foundation of scientific information is required for successful behavioural investigations and applied conservation and enrichment components.     

Longitudinal study of haematological and biochemical constituents in blood of the Asian elephant (Elephas maximus)

1. Haematological parameters and biochemical analytes were determined in four elephants over a period of one year. 2. The haematological profile remained constant over time and was similar between animals. 3. Values for biochemical analytes were stable except for alkaline phosphatase, gamma glutamyl transferase and creatinine which rose during musth in male elephants. 4. The association of elevated enzyme levels with increased testosterone concentrations is discussed.     

Modeling population viability of captive elephants in Myanmar (Burma): implications for wild populations

Captive Asian elephants Elephas maximus , used as work animals, constitute up to 22–30% of remaining Asian elephants. Myanmar has the largest captive population worldwide (∼6000), maintained at this level for over a century. We used published demographic data to assess the viability of this captive population. We tested how this population can be self-sustained, how many elephants must be supplemented from the wild to maintain it, and what consequences live capture may have for Myanmar's wild population. Our results demonstrate that the current captive population is not self-sustaining because mortality is too high and birth rates are too low. Our models also suggest ∼100 elephants year⁻¹ have been captured in the wild to supplement the captive population. Such supplementation cannot be supported by a wild population of fewer than 4000 elephants. Given the most recent expert estimate of ∼2000 wild elephants remaining in Myanmar, a harvest of 100 elephants year⁻¹ could result in extinction of the wild population in 31 years. Continued live capture threatens the survival of wild and captive populations and must stop. In addition, captive breeding should be increased. These measures are essential to slow the decline and extinction of all of Myanmar's elephants.     

DEVELOPMENT OF DISPLAY BEHAVIOR IN YOUNG CAPTIVE BEARDED SEALS

In this study of the ontogeny of vocal behavior in captive bearded seals, Erignathus barbatus , (three males and three females), only males exhibited vocal displays. The onset of display behavior coincided with sexual maturity. Males exhibited three types of dive displays associated with the performance of vocalizations. Vocalizing individuals were frequently attended by another male that maintained passive muzzle contact with the vocalizing male. These interactions were non-aggressive and might play a role in the establishment of a social hierarchy or they might allow the attendee to obtain "near-field" vocal information from the displaying male. Captive males' vocalizations resembled those of males in the wild. However, display dives were shorter, and fewer vocalization types were documented among the captive males compared to bearded seals in the wild. The capacity of the captive males for producing well-formed, long calls with large frequency changes was also significantly less than for wild males. These capacities will likely develop further as the males grow older. Individual capacity for vocal production appears to develop gradually, showing plasticity in form development over time.     

Assessment of testicular endocrine function in captive African elephants by measurement of urinary and fecal androgens

Androgen measurements in urine and/or feces represent a potentially important tool for monitoring testicular endocrine function in the African elephant. To assess the feasibility of this approach, the aims of the present study were to: 1) examine the presence and relative abundance of immunoreactive testosterone (iT) and its 5α‐reduced 17‐oxometabolite epiandrosterone (iEA) in African elephant excreta, and 2) compare urine and fecal androgen profiles in animals of different ages and during the musth and non‐musth condition. Urine and fecal samples were collected over periods of up to 3 years from five bulls (ages 7–24 years) living in three mixed social groups. In parallel, indications of musth were recorded by keeper staff as an independent marker of male androgen status. Measurements of iT and iEA were carried out by enzymeimmunoassay (EIA) following methanolic extraction of hydrolyzed urine and lyophilized fecal powder. High‐pressure liquid chromatography (HPLC) of musth phase samples confirmed the presence of substantial quantities of testosterone (T) and epiandrosterone (EA) in both urine and feces. EA was predominant in feces, whereas T was more abundant in urine. In each male, the two androgen measures were significantly correlated (feces, r = 0.71–0.93, P < 0.0001; urine, r = 0.86–0.91, P < 0.0001), as were fecal and urinary concentrations of each of the two androgens measured (r = 0.35–0.77, P < 0.0001). Moreover, in the two oldest males that showed clear signs of musth, levels of iEA and iT were markedly elevated during musth compared to non‐musth periods (differences were significant for feces in both animals, but in urine only for one). Collectively, the data show that measurement of urinary and fecal androgens generates useful information on gonadal status in male African elephants, and as such should provide new opportunities to improve the management and welfare of bulls maintained in captivity, as well as to examine physiological correlates of reproductive function in free‐ranging animals. Zoo Biol 21:27–36, 2002. © 2002 Wiley‐Liss, Inc.     

Influence of age and gender on secretion of anti-Müllerian hormone in Asian (Elephas maximus) and African (Loxodonta africana) elephants

Anti-Müllerian hormone (AMH) secretion was studied in Asian and African elephants varying in age and reproductive status. Overall mean concentrations did not differ (P > 0.05) between species, but were markedly higher in male than female Asian elephants (31.01 ± 4.22 ng/mL and 0.19 ± 0.02 ng/mL, mean ± SEM) and African elephants (40.27 ± 3.18 ng/mL, 0.17 ± 0.04 ng/mL), respectively. Anti-Müllerian hormone secretion was not significantly affected by ovarian cyclicity status (cycling vs noncycling), but was higher (P < 0.05) in prepubertal (0.40 ± 0.10 ng/mL) than reproductive age (8-35 y; 0.18 ± 0.04 ng/mL) and aged (≥ 36 y; 0.16 ± 0.03 ng/mL) females. In males, AMH secretion was not significantly affected by musth status, but was age-related, with higher concentrations (P > 0.05) in prepubertal (49.08 ± 6.11 ng/mL) as compared to aged (≥36 y; 22.27 ± 5.82 ng/mL) bulls; concentrations in mature bulls (8-35 y; 37.01 ± 3.17 ng/mL) were similar to prepubertal and older bulls. We concluded that circulating AMH concentrations in elephants were similar between species and not affected by reproductive status; however, concentrations were significantly higher in males than females, and in younger animals. The diagnostic value of AMH to assess fertility status of individual elephants remains to be determined.