Male African Elephants Research Articles

Adolescence in male African elephants, Loxodonta africana, and the importance of sociality

The degree of sociality during an animal's life changes as it modulates its behaviour to reflect different life stages. Only a few species of mammal undergo a period of adolescence, but for these species it is probably one of their most important life stages. It is when individuals acquire skills and develop relationships that are of both immediate and long-term benefit to their survival and reproductive success, particularly in polygynous males in which sexual selection favours size and dominance. We collected focal and observational data on male African elephants in the Okavango Delta, Botswana, to assess behaviour and social interactions during adolescence. Adolescent males (10–15 and 16–20 years of age) were the most sociable age group, showing preferences for larger social groupings and being in closer proximity to other elephants; later adolescent males (ages 16–20) showed a tendency for higher social levels. Males of all ages preferred to have males ≥36 years of age as their nearest neighbour. We argue that this proximity to older males provides opportunities for males to learn from more experienced individuals. It has long been recognized that matriarchs are the repositories of social and ecological knowledge within elephant breeding herds: we suggest that mature males are reservoirs for such knowledge within bull society.

Risk and Ethical Concerns of Hunting Male Elephant: Behavioural and Physiological Assays of the Remaining Elephants

BackgroundHunting of male African elephants may pose ethical and risk concerns, particularly given their status as a charismatic species of high touristic value, yet which are capable of both killing people and damaging infrastructure.Methodology/Principal FindingsWe quantified the effect of hunts of male elephants on (1) risk of attack or damage (11 hunts), and (2) behavioural (movement dynamics) and physiological (stress hormone metabolite concentrations) responses (4 hunts) in Pilanesberg National Park. For eleven hunts, there were no subsequent attacks on people or infrastructure, and elephants did not break out of the fenced reserve. For three focal hunts, there was an initial flight response by bulls present at the hunting site, but their movements stabilised the day after the hunt event. Animals not present at the hunt (both bulls and herds) did not show movement responses. Physiologically, hunting elephant bulls increased faecal stress hormone levels (corticosterone metabolites) in both those bulls that were present at the hunts (for up to four days post-hunt) and in the broader bull and breeding herd population (for up to one month post-hunt).Conclusions/SignificanceAs all responses were relatively minor, hunting male elephants is ethically acceptable when considering effects on the remaining elephant population; however bulls should be hunted when alone. Hunting is feasible in relatively small enclosed reserves without major risk of attack, damage, or breakout. Physiological stress assays were more effective than behavioural responses in detecting effects of human intervention. Similar studies should evaluate intervention consequences, inform and improve best practice, and should be widely applied by management agencies.

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.

Age- and tactic-related paternity success in male African elephants

Information on age- and tactic-related paternity success is essential for understanding the lifetime reproductive strategy of males and constitutes an important component of the fitness trade-offs that shape the life-history traits of a species. The degree of reproductive skew impacts the genetic structure of a population and should be considered when developing conservation strategies for threatened species. The behavior and genetic structure of species with large reproductive skew may be disproportionately impacted by anthropogenic actions affecting reproductively dominant individuals. Our results on age- and tactic-specific paternity success in male African elephants are the first from a free-ranging population and demonstrate that paternity success increases dramatically with age, with the small number of older bulls in the competitive state of musth being the most successful sires. However, nonmusth males sired 20% of genotyped calves, and 60% of mature bulls (.20 years old) were estimated to have sired offspring during the 5-year study period. The 3 most successful males sired less than 20% of the genotyped offspring. Hence, contrary to prediction from behavior and life-history traits, reproduction was not heavily skewed compared with many other mammalian systems with a similar breeding system. Nevertheless, these results indicate that trophy hunting and ivory poaching, both of which target older bulls, may have substantial behavioral and genetic effects on elephant populations. In addition, these results are critical to the current debate on methods for managing and controlling increasing populations of this species. Key words: Eelephants, musth, paternity, reproductive strategy, skew, tactic. [Behav Ecol]

Age, musth and paternity success in wild male African elephants, Loxodonta africana

Male African elephants experience intense intrasexual selection in gaining access to oestrous females, who represent a very scarce and highly mobile resource. An unusual combination of behavioural and physiological traits in males probably reflects this intense selection pressure. Males show prolonged growth, growing throughout much or perhaps all of their long life span (ca. 60e65 years), and they show musth, a physiological and behavioural condition exclusive to elephants, which is manifested by bouts of elevated testosterone and aggression and heightened sexual activity. Most observed matings are by males over 35 years of age and in musth, suggesting that age and musth are both important factors contributing to male reproductive success. Here we report the results of a genetic paternity analysis of a well-studied population of wild African elephants. Patterns of paternity for 119 calves born over a 22-year period showed significant effects of both age and musth on paternity success. Among males in musth, paternity success increased significantly with age until the very oldest age classes, when it modestly declined. When not in musth, males experienced relatively constant, low levels of paternity success at all ages. Thus, despite the importance of both musth and age in determining male paternity success, adult males both in and out of musth, and of all ages, produced calves. In general, however, older males had markedly elevated paternity success compared with younger males, suggesting the possibility of sexual selection for longevity in this species.

Male African elephants, Loxodonta africana, can distinguish oestrous status via urinary signals

African elephants are a polygynous species that raise offspring in a matriarchal society. Unlike females, males disperse, spend time in male groups and search for mates when mature. Urinary chemical signals aid males in detecting reproductively active females. A preovulatory pheromone has been identified in Asian elephants, Elephas maximus, but has not yet been experimentally identified in African elephants. In this study, the goal was to determine whether adult captive male African elephants can distinguish between urine from conspecific females in luteal and periovulatory oestrous stages as an indication that a preovulatory pheromone is released in the urine. Urine was collected from seven different female African elephants during their luteal and periovulatory periods of oestrus. Bioassays were conducted with nine adult male elephants housed at six different facilities. Males were presented with the two urine types and a control sample once a day over 3 days to reduce sample novelty, which can result in misleadingly high responses. All males showed greater chemosensory responses to the periovulatory urine by trial 3 with the ability to distinguish the urines increasing over the 3 days. This is the first experimental behavioural evidence that African elephants release an oestrous pheromone in the urine. The ability of the captive male elephants to discern between the two urine types bolsters the hypothesis that there is a preovulatory pheromone in African elephants and encourages efforts to identify it.

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.

Acid-insoluble ash as a measure of dry matter digestibility in captive African elephants (Loxodonta africana)

There are limited data on the diet dry matter digestibility (DMD) of captive African elephants. Although the total fecal collection method is the standard for determining DMD, it is labor-intensive, time-consuming, and expensive. The acid-insoluble ash (AIA) marker technique has been used successfully to determine DMD in ruminants and monogastrics. The objective of this study was to assess how accurately the AIA marker technique could estimate the DMD of captive African elephants (Loxodonta africana). Three mature male African elephants at Disney's Animal Kingdom in Florida were used in this study. The animals were offered a Bermuda grass hay-based ration, and the total dry matter intake (DMI) and total fecal output were measured daily over a 7-day period to determine the total collection DMD. The feed ingredients and fecal samples were also analyzed for AIA. Although there were differences (P<0.05) in total DMI and total fecal outputs, the DMD values did not (P>0.05) differ (35.1±0.72 vs. 37.1±0.72 for total collection and AIA, respectively). There was a linear (y=0.9461x; R2=0.74) relationship between the total collection and AIA marker technique DMD values. These results suggest that AIA can be used to accurately estimate the DMD of captive African elephants. Zoo Biol 0:1–5, 2005. © 2005 Wiley-Liss, Inc.

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.

Non-invasive assessment of adrenocortical function in the male African elephant ( Loxodonta africana) and its relation to musth

Adult male elephants periodically show the phenomenon of musth, a condition associated with increased aggressiveness, restlessness, significant weight reduction and markedly elevated androgen levels. It has been suggested that musth-related behaviours are costly and that therefore musth may represent a form of physiological stress. In order to provide data on this largely unanswered question, the first aim of this study was to evaluate different assays for non-invasive assessment of adrenocortical function in the male African elephant by (i) characterizing the metabolism and excretion of [ 3H]cortisol ( 3H-C) and [ 14C]testosterone ( 14C-T) and (ii) using this information to evaluate the specificity of four antibodies for determination of excreted cortisol metabolites, particularly with respect to possible cross-reactions with androgen metabolites, and to assess their biological validity using an ACTH challenge test. Based on the methodology established, the second objective was to provide data on fecal cortisol metabolite concentrations in bulls during the musth and non-musth condition. 3H-C (1 mCi) and 14C-T (100 μCi) were injected simultaneously into a 16 year old male and all urine and feces collected for 30 and 86 h, respectively. The majority (82%) of cortisol metabolites was excreted into the urine, whereas testosterone metabolites were mainly (57%) excreted into the feces. Almost all radioactive metabolites recovered from urine were conjugated (86% 3H-C and 97% 14C-T). In contrast, 86% and >99% of the 3H-C and 14C-T metabolites recovered from feces consisted of unconjugated forms. HPLC separations indicated the presence of various metabolites of cortisol in both urine and feces, with cortisol being abundant in hydrolysed urine, but virtually absent in feces. Although all antibodies measured substantial amounts of immunoreactivity after HPLC separation of peak radioactive samples and detected an increase in glucocorticoid output following the ACTH challenge, only two (in feces against 3α,11-oxo-cortisol metabolites, measured by an 11-oxo-etiocholanolone-EIA and in urine against cortisol, measured by a cortisol-EIA) did not show substantial cross-reactivity with excreted 14C-T metabolites and could provide an acceptable degree of specificity for reliable assessment of glucocorticoid output from urine and feces. Based on these findings, concentrations of immunoreactive 3α,11-oxo-cortisol metabolites were determined in weekly fecal samples collected from four adult bulls over periods of 11–20 months to examine whether musth is associated with increased adrenal activity. Results showed that in each male levels of these cortisol metabolites were not elevated during periods of musth, suggesting that in the African elephant musth is generally not associated with marked elevations in glucocorticoid output. Given the complex nature of musth and the variety of factors that are likely to influence its manifestation, it is clear, however, that further studies, particularly on free-ranging animals, are needed before a possible relationship between musth and adrenal function can be resolved. This study also clearly illustrates the potential problems associated with cross-reacting metabolites of gonadal steroids in EIAs measuring glucocorticoid metabolites. This has to be taken into account when selecting assays and interpreting results of glucocorticoid metabolite analysis, not only for studies in the elephant but also in other species.

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

AbstractAndrogen 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 &lt; 0.0001; urine, r = 0.86–0.91, P &lt; 0.0001), as were fecal and urinary concentrations of each of the two androgens measured (r = 0.35–0.77, P &lt; 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.

Older bull elephants control young males.

Orphaned male adolescents go on killing sprees if mature males aren't around. Musth is a state of heightened sexual and aggressive activity in male elephants1,2. Between 1992 and 1997, young orphaned musth male African elephants (Loxodonta africana) that had been introduced to Pilanesberg, South Africa, killed more than 40 white rhinoceros (Ceratotherium simum). The killing ceased after six older male elephants were introduced from the relatively normal Kruger Park population. The deviant behaviour of the young Pilanesberg males was rectified by the consequent reduction in musth.

Chemical Profiles of Male African Elephants, Loxodonta africana: Physiological and Ecological Implications

This study reports concentrations of testosterone and dihydrotestosterone in both serum and temporal-gland secretions of male African elephants (Loxodonta africana), including ra­ diocollared elephants, and identifies a spectrum of volatile components in the temporal­ gland secretions. Androgens in the serum (testosterone and dihydrotestosterone) were mea­ sured in 111 adult male African elephants, ages 21-40 years, from two national parks in South Africa during several years and seasons. About one-fifth (18.6%) of these mature, male, African elephants exhibited dramatically increased concentrations of testosterone in serum characteristic of male Asian elephants during musth. In Kruger National Park, six radiocollared male African elephants, ages 25-35 years, were tracked and serially sampled for both serum and temporal-gland secretions during a 5-year period. Concentrations of testosterone in serum and temporal-gland secretions were elevated cyclically at times when typical musth behaviors, including aggression, were observed. This study reports the first chemical characterization of the volatile compounds of the temporal-gland secretions from male African elephants in musth. It reveals many similarities between the chemical con­ stituents of the temporal-gland secretions of these male African elephants and the com­ pounds identified in male Asian elephants. In addition, several compounds, not previously identified in temporal-gland secretions of African elephants, are described. Such chemical data support the behavioral observations by ourselves and other researchers that male Af­ rican elephants experience musth. Especially convincing are the concurrent hormonal and chemical data from the radiocollared males during episodic periods of behavioral musth. Implications of the incidence of musth in the past and present ecology of African elephants are discussed in view of the increasing compression within national parks.

Serum testosterone and musth in captive male African and Asian elephants

AbstractTestosterone concentrations in serum samples collected weekly over a 5‐year period from a young adult male Asian elephant (Elephas maximus) and a young adult male African forest elephant (Loxodonta africana cyclotis) were measured by radioimmunoassay. Testosterone profiles during this maturational period were compared between the two species and related to the occurrence of musth, a recurring physiological and behavioral condition exhibited by most mature Asian, and some African, bull elephants. Musth is characterized by secretion from the bull's temporal glands, dribbling urine, and increased aggression. Serum testosterone concentrations in the Asian bull were elevated substantially between April and September each year, coincident with the presence of temporal gland secretion, urine dribbling, and aggressive behavior. Testosterone levels from April through September averaged (± SEM) 41.2 ± 2.8 ng/ml, compared to 7.6 ± 1.0 ng/ml during the rest of the year. In contrast, the testosterone profile of the African bull showed greater variation and lower levels overall, the only pattern being a tendency for levels to be lowest from November to February (avg. 6.8 ± 1.5 vs. 10.3 ± 0.8 ng/ml during the rest of the year). Temporal gland secretion and other signs of musth were first observed in this bull in 1988, at age 17. While his testosterone profile did not show a pattern comparable to that in the Asian bull, average testosterone values were significantly greater in 1988 compared to previous years.The Asian bull showed sexual attention to preovulatory (estrous) cows whether in musth or not, and exposure to estrous cows did not appear to alter the highly consistent, annual pattern of musth as evidenced in temporal gland flow.

Plasma testosterone levels in relation to musth in the male African Elephant

A long-term study of the behaviour and ecology of the African elephant Loxodonta africana was begun in the Addo Elephant National Park in 1976. During the period June 1976 to March 1979 regular observations were made on all animals. Every individual elephant could be recognised (the population was less than 100 animals) and every individual was seen several times a month. From the start of the study records were kept of whether the temporal gland was secreting or not for every animal at every observation.

Observations on the Adrenal Gland of the African Elephant

Forty-nine female and 32 male African elephants (Loxodonta africana) were collected from July 1958 to May 1959 in Bunyoro District, Uganda. Reproductive status, body weight, and measurements were recorded and ages estimated. Gross morphology and histology of the adrenal gland are described: histology of the elephant adrenal corresponds with generalized descriptions for those of other eutherian mammals. the fetal cortex is well developed in an elephant 2 months of age, but gradually degenerates and is completely absorbed by the fourth year of postnatal life without giving rise to another transitory zone. No significant increase in relative adrenal weight related to Uganda's December-to-March dry season was detected. Relative adrenal weight of elephants is higher in females than males of comparable age, in immature males than mature males, and in immature females than nonpregnant or nonlactating females. Pronounced increase in relative adrenal weight is related to pregnancy and lactation.

Male reproductive organs of the African elephant, Loxodonta africana.

Summary. Results are presented of detailed dissections of the reproductive tracts of eight adult male African elephants and of one full-term male foetus, together with additional information obtained from the examination of a number of other bulls and cows. A notable feature of the elephant's tract is the absence of a pampini-form plexus, cremaster muscle and inguinal canal; this is consistent with the intra-abdominal location of the testes. The weight of the testes and the mean diameter of the seminiferous tubules appear to be related to the size and hence the age of the animal. Active spermatogenesis was observed in all the adult testes examined. Testosterone was isolated from the testes and identified by infra-red spectroscopy ; the testicular testosterone concentrations ranged from 3 to 490 μg/100 g testis and were apparently unrelated to season, age, behavioural status or vesicular fructose concentrations. The elephant has no anatomically distinct epididymis. The wolffian duct is highly convoluted and probably several hundred metres in length. Its caudal half has an unusual histological appearance, with a very folded and extremely vascular lamina propria. The ampullae are large glandular structures, opening into the ducts of the corresponding seminal vesicles. The seminal vesicles are large, thick-walled sacs that contain up to 350 ml of a watery secretion rich in fructose. The prostate varies in shape considerably between animals, being uni- or multilobular. The bulbo-urethral glands are large, and full of a highly viscous secretion. The penis has a well-developed corpus cavernosum penis and large paired levator penis muscles on its dorsal surface. The temporal gland is apocrine in nature, with a strongly smelling serous secretion. Its secretory activity appears to be unrelated to the reproductive status of the animal or the body temperature. The mean deep body temperature was found to be 36·8° C (range 36·2 to 37·5° C). Spermatozoa, recovered within 2 to 6 hours of death from the caudal end of the wolffian duct and the ampullae, were immotile, but could be partially activated by dilution with vesicular secretion. At least two of the elephants had had a retrograde ejaculation when they were shot, and in one instance motile spermatozoa were recovered from the bladder 6 hr after death.

Molariform Teeth of Male African Elephants in Relation to Age, Body Dimensions, and Growth

This paper is based upon the teeth, body dimensions and weights of 58 male elephants ( Loxodonta africana ) collected in Uganda and represents an attempt to relate dental status to approximate age as revealed by a hypothetical growth curve. The elephant bears a successional series of six molars in each half of each jaw during its potential life of about 70 years. Molars 1, 2, 3 and 6 can be readily identified. Molars 4 and 5 are sometimes difficult to identify, but satisfactory designations appear possible by reference to the body weight of the individual. The correlation coefficient between body weight and shoulder height is 0.99. This relationship, when compared with data from an elephant of known age, makes possible the construction of a growth curve. Comparisons of the tooth data with the growth curve reveal the approximate times that the teeth appear in an individual and also their subsequent periods of usage. By knowing the approximate longevity of each tooth, one can satisfactorily estimate the ages of individual animals.