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=== Picture references ===

Itt írjon a(z) ElephantCycle-ról/ről ...

The sexually active states of free-ranging male African elephants (Loxodonta africana)

- defining musth using endocrinology, physical signals, and behavior


Introduction


The African elephant, also called Loxodonta Africana is one of the largest living land mammals in the world, with a weight around four to seven tons and height up to three to four meters in an adult male elephant. Originally there are two subspecies found, Loxodonta Africana (Savanna elephant) and Loxodonta Africana cyclotis (Forest elephant). The African elephant are slightly larger than its Asian cousin and can be identified by their larger ears, the sloping forehead and two fingers at the tip of their trunk that is not present to the same extent in the Asian elephant (Ganswindt, 2004). As well as being the world's largest land mammal, they are one of the longest living animals with lifespan of about seventy years. These grey giants used to live all over Africa, but now their habitats are mainly limited to small areas of central and eastern Africa (Smith, 1995).

2005-tusker-musth-crop.jpg
Fig 1.
Musth secretion (wikimedia commons)

Musth

Musth is a periodic sexual condition in bull elephants. The word “musth” comes from the word “mast”, meaning intoxicated. This may refer to some of the main characteristics of this period like the intensely heightened aggressive behavior accompanied by the large rise in reproductive hormone secretion. The state of musth appears around three years after the young elephant reaches puberty, which will happen between the age of eight and fifteen. When entering sexual maturity, the musth occurs periodically once a year and is triggered by a testosterone boost (Poole 1987, 1989).






1024px-Addo_Elefants_Panorama.jpg
Fig 2.
African elephants (wikimedia commons)

















The behavioral aspect of musth


Competitive behavior

Male elephants face a very intense reproductive competition and they show a unique dominance pattern in which individual males repeatedly experience periods of both high and low dominance status. The musth period influences the male dominance status greatly, a male elephant in musth is always the dominant male compared to other non-musth males, regardless of their size and age. The reason for this phenomenon is presumably their highly enhanced aggression during this period (Poole, 1987, 1989). There is a known tendency for bulls to spread musth fluid on objects like tree trunks leaving it as a message of the animal's condition and state of musth, this actually avoids potentially costly fights with other males (Vehrencamp, 2001).To avoid altercations and fights male elephants in musth also decrease their association with other male elephants instinctively during this period. Mechanisms underlying these behaviors are still unknown. Elephants are not restricted to seasonal breeding; the seasonality of male musth periods reflects the pattern exhibited by females (Poole et al, 1987). During the rain period when the food is plentiful and most females come into estrus, the oldest, highest-ranking male will be the first one to enter musth (Poole, 1987). Consequently males enter musth asynchronously and dominance relationship between any two males can therefore potentially change each time they meet depending upon which, if either, male is in musth at that time (Poole, 1987, 1989).

Group dynamics

Males and females do not live together in permanent social groups. Females live in social groupings generally with their female relatives and calves (Archie et al, 2006), while males range independently of these female groups, joining them only occasionally for brief periods to travel and mate (Moss & Poole, 1983; Poole & Moss, 1989). They normally leave their natal families at around 14 years of age (Amboseli Elephant Research Project (AERP) long-term records). Newly independent young males may follow several different courses to social maturity. Some join up with small bull groups in a bull area and some choose to still stay in female areas moving from family to family. The young elephant will do this for a couple of years while maturing. When they reach about twenty years of age the male elephant will enter a highly dynamic world of changing sexual state, rank, behavior and associations (Poole, 1989). During the sexually inactive and non-musth periods males spend time alone or in the small groups of other males, where their interactions are relaxed and calm. During the active state of musth males leave their bull areas in search of estrus females, they are then likely to be found alone or in association with female groups (Poole, 1987).

Effects of age and musth on paternity success

There is a report done by the The Association for the Study of Animal Behavior (Mates, 2007) that shows the results of a genetic paternity analysis of a well-studied population of wild African elephants. The research is based on the paternity for 119 calves born over a 22-year period. The research clearly showed that for males in musth the paternity success increased significantly with age until the very oldest age classes, when it started to decline. During non-musth the male elephants experienced relatively constant, but low levels of paternity success. But it is important to note that adult males both in and out of musth, and of all ages are able to produce calves, this research just shows the relationship between musth, age and paternity success. In general, older males in musth had a markedly elevated paternity success compared with younger males. The prime age for an elephant is about 45 years of age, and under normal circumstances males probably do not father their first offspring until they are between 30-35 years old.

Physical and physiological changes aspects of musth


Elephant males in active state of musth go through several physical changes due to all the physiological changes that occur within the animal.

Temporal secretion

512px-Sekretausscheidung_zur_Musth.jpg
Fig 3.
Musth secretion (wikimedia commons)

Temporal gland is an apocrine sweat gland, uniquely possessed by elephants. The glands are located in the temporal fossa on each side of the head about midway between the eye and ear. Elephants in musth discharge a highly viscous secretion called temporin from the swollen temporal ducts. Temporin contains proteins, lipids (notably cholesterol), phenol and 4-methyl phenol, cresols and sesquiterpenes. This will appear as dark lines on the sides of the bulls face. The secretion is not unique to musth bulls since it can also be seen in females as well as youngsters, indicating a rise in adrenalin from the animals either being excited, nervous or angry. Still secretions from the temporal glands are one of the main physical characteristics seen in a bull during musth (Raman, 2003).

Urinary dribbling

Another characteristic of musth is the constant urine dribbling from penis staining the inside of the legs much darker than the rest of the body, and also the foreskin of the penis becomes white-greenish in color. This gives a way an unmistakable odor, a sort of sharp bitter smell (Rasmussen et al, 2002; Rasmussen and Greenwood, 2003). The elephant during musth can secrete huge amount of urine per day due to the constant urine dribbling, this further leads to increased water intake. In time the urine will turn more acidic and as a side effect it may lead to irritation in the skin of the hind limbs. Elephants can react to the pheromones released in urine and from the temporal glands by doing an action called flehmen. By using this action chemo sensory information is processed through both the extra ordinary olfactory system and the vomeronasal organ (VNO), which primarily detects airborne gaseous substances. This is a form for chemo signaling where bulls can communicate their state of musth to other males and potentially avoid altercations (Rasmussen et al, 1982, 1986; Perrin, 1995; Rasmussen and Greenwood, 2003).

Physical condition

A male enters musth at peak physical condition and they are highly aggressive during this period. Musth seems to be an energetically costly state to maintain; males lose a lot of weight and their physical condition visibly deteriorates as musth progresses. The reason for this presumably is because of the decreased foraging coupled with increased distance travelled in the search for females in estrus (Poole, 1982), and also the alterations occurring in the body homeostasis can be an influencing factor (Schulte and Rasmussen, 1999). The older males maintain the active state of musth for the longest time and subsequently they are the ones
that experience the largest deterioration (Poole, 1989).

Endocrinology of musth


During musth the elephant experiences both a physically and mentally stressful time. Stress, glucocorticoids and androgens that are produced in the organism show continuous changes and there is a rise and fall of testosterone, dihydrotestosterone and androstenedione (Yon L. et al, 2007). Musth is regulated by a complex process of hormonal secretion called hypothalamic–pituitary–gonad and –adrenal axis. In males, the production of GnRH, LH, and FSH are similar, but the effects of these hormones are different. FSH stimulates Sertoli cells to release androgen-binding protein, which promotes testosterone binding. LH binds to the Leydig cells, causing them to secrete testosterone. Testosterone is required for normal spermatogenesis and inhibits the hypothalamus. Inhibin is produced by the spermatogenic cells, which, also through inactivating activin, inhibits the hypothalamus. After puberty these hormones levels remain relatively constant.

pop-up text
Fig 4.
Hormonal changes

The musth period is divided on the basis of these hormonal changes in a pre-, main- and post-musth period (Wittemyer et al, 2007, Foley et al, 2001; Viljoen et al, 2008). Analysis of variance (ANOVA) and Bonferroni's multiple comparison test were used in order to study the hormonal changes during the different phases of musth (Watanabe et al, 2010). The hormones included and the hormonal changes during musth will be listed here below.

GnRH

Is a tropic peptide hormone produced in the arcuate nuclei of hypothalamus and stimulates the synthesis and secretion of the two gonadotropins FSH and LH, by the anterior pituitary gland. The characteristics of all releasing hormones and most striking in case of GnRH are the phenomenon of pulsative secretion. Under normal circumstances, GnRH is released in pulses at intervals of about 90 to 120 minutes. The neurons that secrete gonadotropin-releasing hormone have connections to an area of the brain known as the limbic system, which is heavily involved in the control of emotions and sexual activity (Utiger, 2010).

LH and FSH

Luteinizing hormone (LH) and follicle-stimulating hormone (FSH) are produced in the pituitary gland and secretion is regulated by signals from the hypothalamus (Kaewmanee et al, 2010). Results of variance (ANOVA) and Bonferroni's multiple comparison test showed a significant increase of LH concentration in blood serum four week before the musth began. These high levels were maintained for five weeks followed by a significant decrease to the baseline level when musth behavior was observed. By the findings of the increase in LH serum concentration in the pre-musth period it is suggested that it might stimulate secretion of testosterone and ir-inhibin and by this initiate the musth behavior. Throughout the year, the changes of FSH concentrations in serum followed the LH changes, however the changes of FSH were not as clear as that of the LH. Similar to LH, the FSH showed the highest concentration during the pre-musth stage and in the musth stage FSH showed higher concentration than during non-musth stage. Positive correlation between these two hormones was observed the whole period (Kaewmanee et al, 2010).

Testosterone and immunoreactive-inhibin

Testosterone is a steroid hormone, belonging to the group of androgens. In males it is mainly synthesized by Leydig cells in the testicles, but adrenal glands do also secrete it in smaller amounts. Testosterone synthesis is regulated by the hypothalamic-pituitary-testicular axis. Inhibin is a peptide hormone produced in the Sertoli cells which acts on the pituitary gland by limiting the secretion of FSH. Like testosterone, it is also under the control of hypothalamic-pituitary-testicular axis. There have been made two different experiments where changes in testosterone and ir-inhibin were observed from April to October. During musth there were positive correlations among testosterone, ir-inhibin and musth behaviour. During non-musth and pre-musth stages there were no significant differences in the concentration levels of testosterone. On the other hand the level of circulating ir-inhibin during pre-musth was significantly higher than during non-musth. Both testosterone and ir-inhibin showed highest concentration level during musth stage (Kaewmanee et al, 2010).

Glucocorticoid (GCM) and Epiandrosterone (EA)

Glucocorticoid hormone is steroid hormone synthesized from cholesterol in the adrenal cortex and stimulated by adrenocorticotropic hormone (ACTH). During musth there is a slight reduction of glucocorticoid level. Another steroid hormone called Epiandrosterone (EA), normally produced from the adrenal hormone DHEA, showed an increased level during musth (Ganswindt et al, 2003). There are many factors that affect GCM and AE concentrations, health problems are known to affect steroid levels, especially glucocorticoid output (Muenscher et al, 2009). Glucocorticoids and epiandrogens concentrations were compared during an experiment between four stages of musth, which includes: non-musth, pre-musth, musth and post-musth. The two different experiments used are called Kruskal–Wallis one-way and ANOVA, they use feaces in order to get the hormonal changes in these experiments. The relationship between pre-musth and post-musth of physical signs and changes in hormone levels can be determined by these experiments. Also the occurrence of periods of elevated EA and reduced GCM levels can be determined (Ganswindt et al, 2005).

The beginning and end of temporal gland swelling and secretion (TG/TGS), urine dribbling (UD) and reduced glucocorticoid levels in relation to the beginning and end of periods of elevated androgen levels are compared. The two diagrams show concentrations of EA and GCM representing data derived from fecal samples of six bulls. The diagrams represent the average hormone value of all individuals which showed either no physical signs, only TG/TGS, or TG/TGS and UD (Ganswindt et al, 2003).

1. EA concentrations.jpg
Fig 5.
EA concentrations

1. GCM concentrations.jpg
Fig 6.
GCM concentrations

  • Non musth – no signs
  • Pre-musth – only TG/TGS
  • Must- TG/TGS and UD
  • Post-musth – only TG/TGS

The diagram for epiandrosterone, the average EA value during non-musth present was about half that of the average EA level when animals showed pre-musth, about one third of the corresponding level when TGS and UD (musth) were present, and almost the same when bulls showed post-musth. EA levels differs significantly between the different musth stages. In contrast to EA levels, GCM levels were higher in non-musth bull, and reduction of the GCM levels can be observed in the other three conditions.





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Picture references

Krishnappa S Yathin, 2012,figure 1, http://commons.wikimedia.org/wiki/File:Sekretausscheidung_zur_Musth.JPG?uselang=sv

Hammer Julian, 2010, figure 2, http://commons.wikimedia.org/wiki/File:2005-tusker-musth-crop.jpg?uselang=sv

Masteraah, 2007, figure 3, http://commons.wikimedia.org/wiki/File:Addo_Elefants_Panorama.jpg?uselang=sv

Garðarsdóttir Dögg S., 2013, figure 4

Garðarsdóttir Dögg S., 2013, figure 5

Garðarsdóttir Dögg S., 2013, figure 6

ElephantCycle (last edited 2013-12-04 12:16:14 by 2475E)