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Understanding the Role of Semiochemicals on the Reproductive Behaviour of Cheetahs (Acinonyx jubatus)—A Review

Simple Summary
This review aims to provide an in-depth overview of the reproductive physiology and behaviour of cheetahs (Acinonyx jubatus). Specifically, it focuses on the role that pheromones (a class of semiochemicals) play by directly affecting the reproductive (e.g., precopulatory and copulatory) behaviour. Furthermore, it aims to critically analyze current research and provide new insights on study areas needing further investigation. It is clear, for instance, that further research is necessary to investigate the role of semiochemicals in the reproductive behaviour of cheetahs in order to rectify the current behavioural difficulties experienced when breeding younger females. This, in turn, would aid in improving captive breeding and the prevention of asymmetric reproductive aging.

Abstract
The cheetah species (Acinonyx jubatus) is currently listed as vulnerable according to the International Union for Conservation of Nature (IUCN). Captive breeding has long since been used as a method of conservation of the species, with the aim to produce a healthy, strong population of cheetahs with an increased genetic variety when compared to their wild counterparts. This would then increase the likelihood of survivability once released into protected areas. Unfortunately, breeding females have been reported to be difficult due to the age of these animals. Older females are less fertile, have more difficult parturition, and are susceptible to asymmetric reproductive aging whereas younger females tend to show a significantly lower frequency of mating behaviour than that of older females, which negatively affects breeding introductions, and therefore mating. Nonetheless, the experience from breeding methods used in some breeding centres in South Africa and the Netherlands, which also rely on the role that semiochemicals play in breeding, proves that cheetahs can be bred successfully in captivity. This review aims to give the reader an in-depth overview of cheetahs’ reproductive physiology and behaviour, focusing on the role that pheromones play in this species. Furthermore, it aims to provide new insight into the use of semiochemicals to improve conservation strategies through captive breeding.

1. Introduction
With less than 7100 cheetahs left in the world [1] and an overall classification as “vulnerable with a decreasing population trend” [2], the cheetah is one of many species in need of conservation efforts [1]. During the last ice age, the cheetah species almost went extinct [3] and experienced a “population bottleneck” that led to reduced genetic diversity, followed by high levels of inbreeding [4]. As reported by Frankham [5], the International Union for Conservation of Nature (IUCN) considers genetic diversity as “one of the three levels of biodiversity requiring conservation”. Therefore, captive breeding aims to create a captive population that would act as a vital genetic reservoir in the case of another sudden, unforeseen loss of wild populations [6]. Besides the fact that reproduction is a crucial part in ensuring the conservation and survival of a species [7], the main aim of captive breeding is to produce a population of cheetahs with a higher genetic variety when compared to their wild counterparts. This has become a necessity in creating a sustainable, healthy population of cheetahs that would survive after possible reintroduction into protected wild areas [8,9]. Therefore, studies focusing on increasing natural reproduction in supervised populations are crucial to obtaining a self-sustainable cheetah population.
Research advancement in animal behaviour related to reproduction, raising of offspring, breeding, and communication, including that of chemical communication (the predominant form of interaction between many organisms) [10], is crucial for the conservation of numerous endangered animals [11].
Cheetahs rely on their advanced olfactory systems for chemical communication [12] which contributes largely to regulating animal behaviour [13], including sexual receptivity [10]. Chemical communication occurs through volatile chemical signals and/or non-volatile chemical signals. The former is generally fixed by lipids, released into the air, and detected as an odour, whereas non-volatile chemical signals are transferred to the vomeronasal organ of an animal’s olfactory system [14,15]. The odours that are released bind to corresponding receptors on the sensory neurons to stimulate a response; thus, the shape and structure of the chemical compounds are important in the discrimination of different odours [12]. The release and reception of chemical signals (semiochemicals) from one animal to another is involved in a very intricate system from initial detection to final response [16] and contributes largely to regulating animal behaviour [13], including sexual receptivity [10].
Therefore, this review aims to provide the reader with an overview of the cheetah’s characteristics and, in particular, on its reproductive behaviour focusing on the role that semiochemicals play in this species. Furthermore, it aims to provide new insight into the use of semiochemicals to improve conservation strategies through captive breeding.
2. The Cheetah
Well-known for its speed, the cheetah (Acinonyx jubatus) is a medium-sized feline and the only member of its genus [17]. In the past, the cheetah could be found throughout Asia and Africa. Today, however, they can only be found in Iran and sub-Saharan Africa in grassland and savannah habitats, with larger populations in areas with an abundance of prey and a large stretch of land [12].
In the 1900s, the cheetah population was composed of over 100,000 individuals worldwide. Today, less than 7100 cheetahs are left [1], with a 76% loss in Africa and a reduction of the Asian population to very small numbers [6]. The Asian population is therefore listed as critically endangered [6] and the overall cheetah population is listed as vulnerable with a decreasing population trend [2]. The decreasing trend emphasizes the need for more effort in conserving the species [6].

2.1. Threats

Some of the leading causes relating to the endangerment of many wild cat species, including tigers and leopards, are the disturbance humans have on the environment [18,19,20], along with harmful human activities such as poaching and climate change [11,17]. With regards to cheetahs, the increasing human population and, therefore, the utilization of more land for activities such as farming [21] has led to the fragmentation or total loss of habitat [17] and has resulted in a total loss of 91% of historic range since the 1900s [1]. Competition, therefore, arises between farmers and cheetahs, where cheetahs are killed because they are perceived as pests and a threat to livestock [12,22].

As an intermediate predator, a cheetah faces a great deal of competition from larger predators [23]. Unfortunately, with cheetahs being built solely for speed there is the disadvantage of insufficient physical strength to protect its offspring, territories, and prey from stronger predators, predominantly lions and hyenas [24,25,26,27]. Therefore, a decline in habitat would cause an increase in the abundance of these predators in certain areas, thus causing cheetahs to avoid specially protected areas that serve as a refuge for most large predators [12].

2.2. Possible Reasons for Population Decline

Generally, felids have small litter sizes (1–5 with an average of 3) because females usually have no aid from males or other females in hunting, providing and caring for their young, and later teaching their offspring how to hunt [25]; in contrast, cheetahs have large litter sizes (1–8 with an average of 4) [22,27], with low birth weights (approximately 380–700 g) [27] and high growth rates. These traits, along with the swift return to oestrus after the loss of an unweaned litter of cubs, have been speculated to have evolved as a response to the high mortality rate of cheetah cubs in order to increase survival rate [23].

Studies evaluating cub mortality and possible causes, showed that the most common causes of death were predation [23,28], abandonment [23] starvation and injury [28]. Unfortunately, cheetah cub survival in predator-free, unprotected areas, is not much greater than in protected areas containing large predators [28] because cheetahs inhabiting unprotected areas are more prone to human conflict, including the illegal pet trade [22].

In captivity, the highest amount of cub deaths is attributed to bad mothering ability [29]. In the wild, the ability to find and obtain prey plays a primary role in the abandonment of cubs by their mothers [23]. In captivity, however, it could be speculated that a contributing factor most likely responsible for the high cub mortality could be related to the mother’s genetics.

Several studies have proved that mothering ability is a genetically linked trait, and it is essentially related to the rate of offspring survival before weaning [30,31,32,33,34]. While it is possible to select for good mothering ability in a captive breeding program, selective breeding is difficult for species with a low genetic diversity [35].

Cheetahs population is said to have undergone a genetic bottleneck that severely reduced genetic diversity [36], followed by constant inbreeding [4]. It has been known for a long time that inbreeding reduces survival and reproduction in a species, including mothering ability, sperm production, and adult and juvenile survival [5].

2.3. Reproductive Characteristics

Female cheetahs reach sexual maturity at 20–24 months of age [1] and have a considerably short oestrous cycle if compared to those of other large felids, which lasts 20–30 days [24]; in fact, the duration of the oestrous cycle is between 7–21 days, with oestrus lasting between 2–6 days on average and inter-oestrous periods lasting for 13.9 ± 0.7 days [17,37].

Cheetahs are induced ovulators [9], meaning that frequent copulation contributes in maintaining high levels of oestrogen, and, in combination with the low levels of progesterone, stimulates the anterior pituitary to release luteinizing hormone (LH) and trigger ovulation [38,39,40,41,42].

Female cheetahs are also polyoestrous; therefore, oestrus and breeding occur throughout the year [9,12,24]. In the wild, however, it has been seen that females “decide” when it is the right time to come on oestrus [12] and are therefore thought of as being seasonally polyoestrous [22]. In captive breeding facilities, with no environmental pressure, reproduction and oestrous onset can occur at any time throughout the year [6]. At 6 years of age, females reach maximum reproductive capability, which continues until they are 8 years old and declines thereafter [22].

Unfortunately, female cheetahs are susceptible to asymmetric reproductive aging (ARP); therefore, the older a female is when she has her first litter, the shorter her reproductive lifespan will be. This occurs due to continuous oestrous cycling, where the fluctuating levels of oestrogen cause the reproductive organs to age at a faster rate [8]. Failure to reproduce after a long period of not reproducing is observed in a wide variety of species [43]. In female cheetahs it has been observed that although older cheetahs produced less recoverable oocytes and ovarian follicles, the quality of the gametes and function of the ovaries were unexpectedly normal. The main factor being the cause of infertility in older cheetahs was seen to be uterine integrity, with endometrial hyperplasia seen in 50% of the females considered to be in their “prime” years (e.g. best years fo reproduction; 6–8 years) and in more than 85% of the older females (9–15 years) [44]. These results are similar to that of another study with 23 species of felids that had been exposed to progestins for at least 6 months, which is believed to have stimulated the endometrial epithelial cells to start differentiating [45].

This rapid aging process can be prevented by breeding females when they are still young adults [8], which would also increase their chances of being able to reproduce for the rest of their reproductive lifespan [43].

2.4. Reproductive Behaviour

Although cheetah females display characteristic feline oestrus behaviour, there is a large amount of variability between individuals [9]. The periods in which a female cheetah will accept a male to mate with her is also very short, difficult to identify or lacking [46]. A few authors have hypothesized this as “silent” oestrus [47,48,49]. In captive breeding programs, silent oestrus is seen in younger, more inexperienced females. Therefore, even though an active male can still detect a female on oestrus by her scent, if she does not display oestrus behaviour, he will not be able to find her [50].

According to Wielebnowski and Brown [9], in cheetahs, the increased frequency of certain behaviours is correlated with increasing concentrations of faecal oestradiol and, therefore, to oestrus. In this study, they classified seven females as breeders, four as non-breeders, and three as undetermined. The breeders had all previously given birth and were older than the age of 6 years. The non-breeders were younger than 4 years and had never bred before, despite being introduced to two different males more than 15 times. The undetermined group consisted of one 2-year-old female and two 5-year-old females who had never been introduced to a male. Although this study had few limitations (females were usually housed together; they were under different management systems; the undetermined group was classified as non-breeders during data analyses), it did have interesting results. Based on their observations, in fact, the behaviours “rub”, “object sniff”, “roll”, “urine-spray” and “meow-chirp” (refer to Wielebnowski and Brown [9] for definitions) significantly correlated in a positive manner with increases in oestradiol concentrations; all females of varying ages showed typical feline oestrous behaviour; there was a significant difference in age and breeding status with regards to the frequency of oestrous behaviour displayed, where non-breeders and younger females showed significantly less characteristic oestrous behaviour. Based on their results, the researchers concluded (i) that oestrus could not be regarded as silent since all ages displayed oestrous behaviour; (ii) the frequency of oestrous behaviour displayed increased with age; and (iii) age and experience are the two main factors that influence the frequency of oestrous behaviour.

Based on the results and conclusions of this study, the following assumption can be made: Since all non-breeders were under 4 years of age (breeders were over 6 years of age) and had all been previously introduced to males (>15 introductions) with no success, it can be assumed that even though mating behaviour is displayed by younger females, if the frequency is not enough, mating will not occur.

Whereas the above study proved that female cheetahs do show characteristic feline oestrous behaviour, it also proved the variation between individuals regarding the frequency and type of behaviour displayed by each female. This is different from other felids, where the sequence of behavioural changes is displayed in a foreseeable manner during oestrus [6]. In a captive breeding setting, the sequence displayed by each individual would need to be analysed in order to determine the oestrous state, which is difficult and time-consuming [6].

3. The Physiology of Olfaction

3.1. The Main Versus the Vomeronasal (Accessory) Olfactory System

All mammals possess a main and an accessory (vomeronasal) olfactory system besides bats, marine mammals, and humans [51,52]. These systems contain sensory neurons that are necessary to detect semiochemicals and, therefore, scent-marks [11]. Both systems are astonishingly consistent in all species of mammals, and although there are structural differences, there are also similarities in how each system functions [12,53]. The olfactory and vomeronasal receptors are very different from each other with regards to their primary structures and location [11,16]. The receptors from each system are only able to detect certain categories of compounds [51]. For example, volatile compounds are generally detected by the olfactory system via the nasal epithelium, whereas non-volatile compounds are said to be detected by the vomeronasal organ, which is located in the nasal septum [54,55]. Although the neural pathways of each system do run parallel to each other [55], the olfactory receptors transmit signals to the main olfactory bulb, and the vomeronasal receptors transmit signals to the accessory olfactory bulb [14,53]. Both neural pathways from each system, however, are involved in managing behavioural and endocrine responses [56].

In terms of detection and response to pheromones, previous misconceptions included the fact that the vomeronasal system detected only pheromones, whereas the main olfactory system could not [53]. This is not true as some pheromones utilize the vomeronasal system while others utilize the main olfactory system [16]. Furthermore, some semiochemicals can be detected by both olfactory systems [53].

Another misconception was that the main olfactory system initiated general reproductive behaviour and the vomeronasal system moderated specific behavioural signals relevant to each sex [57]. Both olfactory systems do coincide with each other [16]. In fact, although reduced, a neuroendocrine reaction in response to certain pheromones is still seen after the removal of the vomeronasal organ [55]. For example, the mating stance, which is a behavioural response to the steroidal pheromone, androstenone, was not affected after blocking the vomeronasal duct. Only in immature mammals that do not possess a functional vomeronasal organ, reproductive behaviour is affected [16].

3.2. The Main Olfactory System

The arrangement of the olfactory system is similar across species with regards to how the olfactory receptors function, the physiological activity thereafter, as well as the arrangement of the olfactory central nervous system [58]. Although the main olfactory epithelium generally detects volatile compounds [54], detection of non-volatile compounds occurs when an animal expresses behaviour that consists of direct physical contact [56].

The two kinds of receptors in the main olfactory epithelium are known as the olfactory receptors and the trace amine-associated receptors [11]. In rats, the suckling pheromone triggers a particular segment of the main olfactory bulb [57]. This pathway is also involved in the identification of the opposite sex [16]. The fact that both pheromones and common odours can influence the neuroendocrine system [57] is most likely due to the fact that the olfactory epithelium also contains a group of receptors dedicated to detecting pheromones [59]. These receptors are otherwise known as V1R-positive and are, in fact, a type of vomeronasal receptor [56], which means that the detection of pheromones is not a specific function of the vomeronasal system [53].

3.3. The Vomeronasal (Accessory) Olfactory System

The vomeronasal system is generally believed to be the main detector of semiochemicals, especially pheromones [56], and can detect chemical compounds of both high and low volatility [51]. Detection of pheromones via the vomeronasal system plays a large role in reproduction through the influence of sexual behaviour, as well as hormone levels involved with reproduction [55]. The vomeronasal organ, or otherwise known as the organ of Jacobson [12], is where the detection of chemical compounds occurs [60]. Cats transport non-volatile semiochemicals, such as steroid conjugates and proteins, to the vomeronasal organ by using the flehmen grimace [61]. Flehmen is a behavioural response where the lower jaw opens halfway while the cat pauses and breathes steadily [62]. The flehmen response to a scent mark seems to be universal amongst all felids, including the cheetah, domestic cat, tiger, and lion [61,63,64,65]. It is used to analyse urine [51], although males tend to show this reaction at a higher rate than females [64].

The vomeronasal organ is found in most terrestrial mammals [16], apart from bats and some species of primates. It is a tubular structure that is found in between the oral and nasal cavities [51], consisting of two sacs filled with fluid that forms an opening at only one end [12]. The vomeronasal receptors are the V1r receptors [53] and V2r receptors [66].

3.4. The Link to Olfaction and Hormone Release

The connection between the gonadotropin-releasing hormone (GnRH) and olfactory systems, as well as between mediation of sexual behavioural/hormonal responses is very intricate [16]. The GnRH neurons are ultimately the main drivers of reproductive status. They have been identified to possess bidirectional connections with neurons involved in odour and pheromone processing, such as in the olfactory cortex, medial amygdala, and posterocortical amygdalar nucleus, thus proving that signals are received from both the vomeronasal and olfactory system [55]. This connection of neurons is generally referred to as the “hypothamalmic-pituitary-gonadal axis” [16]. Noradrenaline and serotonin levels also act as an indication of the psychological state of the animal and thus affect the reproductive endocrinology and behaviour of the animal [57]. GnRH neurons, therefore, influence the endocrinology of the animal in correlation with the psychological state of the animal [55]. Since the GnRH neurons are involved in bidirectional connections with neurons from the olfactory systems [55], semiochemicals and scent-marking would, therefore, play a role in reproduction and the endocrinology of the animal as well.

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