Donkey breeding behavior with an emphasis on the Pêga breed

Introduction

The world donkey population is estimated at 50 million animals. Brazil has approximately 1.5 million mules and donkeys living under domesticated conditions. Donkeys are bred in many countries and in some, there is particular interest in using donkey jacks for mule (Equus mulus) production via both in-hand natural mating and artificial insemination. Breeding by artificial insemination has gained popularity, but in most mule farms breeding by in-hand natural mating is the predominant breeding system [1]. Mules and donkeys are in demand in rural areas due to their physical strength, disease resistance, endurance and ability to withstand heavy workloads. Worldwide, mules are used in herding cattle, traction, western sports and dressage, as well as for pleasure, pets and pack animals [2].

The Pêga donkey, a large (130 - 155 cm) saddle-type asinine, is a particularly valuable Brazilian breed which has been selectively bred and improved for over two hundred years and is popular in many Brazilian states for the production of outstanding saddle-type mules. The Pêga breed was initially created in the Minas Gerais state by a Catholic priest, Father Manoel Maria Torquato de Almeida, who visualized the potential of this animal as a saddle-type donkey as well as an excellent mule producer. After his initial efforts his family continued his work on selection, and the Pêga donkey has become the most popular breed in almost all Brazilian states as well as in some other countries in South America such as Bolivia, Paraguay and Colombia [3].

Five to ten years ago the Pêga donkey was considered to be endangered; however, since then, the breed has gained significant popularity for production of dressage-type mules [2]. Currently the Brazilian Association of Pêga Donkey Breeders (ABCJ Pêga) has approximately 2,000 breeder members spread throughout Brazil with approximately 20,000 mules and donkeys registered [3].

Brazil has the largest commercial cattle population (~ 210 million) in the world, approximately 80% of which are beef cattle. At least 100 million of those beef cattle are herded using mules that are bred from light saddle mares by Brazilian saddle-type jacks. The typical Brazilian beef farm is characterized by expansive pasture area, as well as large herds of Zebu cattle. In the majority of those farms, cattle production is only possible with mule work because the farms cover such large areas in tropically high temperatures and either extremely dry or humid conditions. Such weather conditions favor infectious and parasitic diseases, so usually horses present several clinical problems and thus cannot perform herding activities at the same level as mules. Mules are used for work with cattle typically 30 - 36 hours/week, covering an average distance of 15 - 25 km/day. Under such conditions, mules are outstanding for this type of work and remain healthy with less care than horses (Canisso, unpublished personal experience).

Production of mules to supply Brazilian beef farms usually takes place on the farms themselves or in specialized stud farms located far away from the major areas of beef cattle production. The beef farmers typically keep a small herd (80 - 200 broodmares) of crossbred mares (generally Quarter Horse mixed with Brazilian saddle-type horse breeds) and 1 to 5 donkey jacks as sires. For both the specialized breeding operations and the beef farm mule breeders, the Pêga breed or Pêga type donkey jacks predominate. The donkey jacks are produced mainly in the Southwest region, especially in the states of Minas Gerais and São Paulo in small stud farms (20 - 150 donkey dams). At 1.5 - 3 years of age the donkeys are sold to serve as sires on beef cattle farms or specialized mule breeding farms. Pêga breed donkey jacks have high monetary value (from U.S.$ 4,000 to $50,000), and so are used for breeding well into old age; in Brazil, they are bred well beyond age 20 (Canisso, unpublished personal experience).

The breeding management of donkeys under intensive conditions is considered challenging because of their peculiar reproductive behavior [2,4]. Thus, efforts to manage donkeys by considering and accommodating key elements of their natural behavior to the extent possible in the domestic condition, has greatly improved breeding efficiency. Therefore, the aim of this chapter is to describe the natural sexual behavior of donkeys and the authors’ experiences with an emphasis on the domestic breeding system currently used in Brazil.

Figure 1. Mules (offspring from Quarter Horse-type horse mares and Pêga donkey-type), in a beef farm, located in the Mato Grosso state, Northern Brazil. Note a group of Zebu beef cows in the background (Courtesy of Rodrigo Cervi, DVM, Cuiaba, MT, Brazil).

Figure 2. A group of herding mules in a beef farm, located in the Mato Grosso state, Northern Brazil. Note the disposition of the mules; the animals are trained to organize themselves in a side-by-side line-up along the perimeter of a paddock, to facilitate catching by the cowboys and to avoid fighting between animals (Courtesy of Rodrigo Cervi, DVM, Cuiaba, MT, Brazil).

Jack Sexual Behavior

Asinine natural reproductive organization differs from that of equines. Domestic donkey jacks are territorial, non-harem breeders and usually do not display herding behavior, either with jennies or horse mares [4,5]. In contrast, horse stallions are non-territorial, harem breeders that display herding behavior [6]. If kept at pasture, the jack spends most of his time within a specific area, his territory, which normally contains a good source of water, shade and grass [4,7].

Under natural mating conditions the jack will approach the jenny as she enters his territory, or alternately, is sought out by the jenny when she is in estrus. Once interest has been established, the donkey jack begins to tease the jenny; such teasing includes loud vocalization, flehmen response and sniffing the jenny’s perineal area, inguinal region, hind legs and ventral abdomen as well as voided urine or vaginal fluids on the ground. Other teasing behavior includes rolling in the soil and mouth clapping, which is often followed by mounting without an erection. Mounting without erection occurs on average at least once per mating episode, whether using natural or in-hand mating, or during semen collection [2,4,5,7,8]. Usually young, less experienced jacks are slower breeders compared to older jacks and have been reported under certain circumstances to have twice the number of mounts, without erection, as adult jacks [2]. After teasing, the jack may retreat somewhat and remain at a distance from the jenny, during which time an erection is achieved. Typically the erection is initiated a few minutes after retreat while the jack may appear uninterested, grazing and gazing around, although penile movements known as masturbation may occur. Usually within another few minutes the jack returns to the jenny and teasing resumes, culminating in successful copulation [4,8]. The duration of teasing before copulation is highly variable among donkey jacks and among mating episodes of individual jacks [2,4].

The territorial nature of donkeys is of particular importance in breeding management of jacks. Our experience [4] suggests that a shorter latency to a full erection results if breeding or semen collection is always conducted in the same location, likely because this more closely simulates the donkey’s natural territorial behavior. As a territorial breeder the donkey is easily distracted by potential threats or intruders in its environment, especially the sight or sound of another donkey which triggers defensive behavior [4]. Finally, breeding is usually more efficient when the environment is quiet, ideally with the same familiar handlers, away from other donkeys, and with minimal traffic of animals, agricultural machines or other distractions [4,9].

Under in-hand mating or semen collection, we have observed that as a rule, before donkey jacks achieve a sustained full erection, they present the following sequence of behavior: 1) a few seconds of quietness (reduced movements and reduced alertness to the environment, females, and handlers); 2) tail elevation at the ischium level; 3) almost simultaneously, penis extrusion and emission of transparent white secretion; 4) partial erection through to a progressive full erection; 5) masturbation (penis movements against the abdomen) and then 6) ejaculatory mounting. During semen collection or natural mating, if the donkey jack does not achieve stage 5) often the mount is unsuccessful. If the donkey is left undisturbed and allowed to progress to stage 5), then mounting with ejaculation is usually achieved (Canisso, unpublished personal experience).

Knowing this pre-copulatory behavioral progression for jacks to achieve the erection and mount readiness is useful for workers involved in semen collection or in-hand natural mating of jacks. For instance, when the collector or handlers notice the sequence described above until stage 5, the artificial vagina can be held in-hand ready to collect semen. Understanding of the typical progression enables patience, appreciation of progress, and anticipation and preparedness for the mount. Bearing that in mind, the jack can be well guided by the handler to perform the mount.

Jenny Sexual Behavior

Domestic jennies and some species of wild donkeys, if kept in large pastures, live in migratory groups which are attracted to the jack’s territory when seeking water and feed [5,10]. They remain there while in estrus, during which time they are courted and mated by the donkey jacks [7]. Traditionally, donkey stud farms keep the jacks isolated in all-male yards and the donkey dams in paddocks away from the males. Jennies are well known to be difficult to contain within agricultural enclosures. This is especially the case when in estrus, as they work at seeking out the donkey jacks (Canisso, unpublished personal experience). This behavior is highly undesirable on Brazilian stud farms [4].

The sexual behavior of jennies is distinct in several aspects from that of horse mares [11]. Jennies play a more dynamic role in courtship than mares. Likely due primarily to this difference, jacks are naturally reluctant to breed mares [4,7]. Jennies’ solicitous behavior includes frequently approaching the jack, ears back against the neck, typical loud vocalization, mouth clapping, rhythmic eversion of the clitoris, urination in small amounts, and the mounting stance. Estrous jennies congregate into sexually active groups in which intensive heterosexual behaviors are displayed, such as mounting each other, similar to female-female mounting in bovids. This particular sexual interaction of jennies is important for jack stimulation [5]. Under intense breeding programs when such stimulation is not provided, outcomes are likely to be poor for in-hand natural mating or semen collection using jennies and especially when using mares.

Crossbreeding

The differences between donkeys and horses in sexual behavior is likely to be in part responsible for reduced sexual interest and response typically shown by jacks toward mares, and vice versa [4,5,7]. As a result, there are several challenges that practitioners face when crossbreeding horse mares and donkey jacks. The difference in height as well as the fact that most mares do not accept jacks’ approach offer distinct disadvantages for the jack. Generally, less than 40% of estrous mares display receptive or solicitous behavior to donkey jacks despite being confirmed as estrous in response to a stallion [12]. Even though mares generally become increasingly accepting of jacks to which they have been bred, free-range breeding remains challenging and usually for the most part unsuccessful. Those mares that accept the jack usually present only discreet signs of estrus, which appears to reduce the interest and sexual response of the jack. On most mule stud farms the presence of donkey jennies is considered to be disruptive because they interfere with the sexual behavior of jacks to mares and are more difficult to contain.

In a recent study [2], the behavior of horse mares used as mount females for semen collection from donkey jacks was evaluated. At the time of use, all mares were confirmed to be in estrus upon exposure to a horse stallion and by acceptance of the jack’s approach. Good acceptance of the donkey jack by the mare was characterized by showing estrus signs in the presence of the jack, and by not kicking or excessively moving when the jack teased or mounted her. A lesser number of mares displayed additional signs of estrus such as exposure of the clitoral area, even though in many of these mares it was quite discreet. In a smaller number of mares, this was accompanied by passing of a small volume of urine.

In the same study [2], the behavior of jacks when presented to a mare during semen collection was evaluated. Although no mouth clapping was shown by any jacks, other normal sexual behavior was observed in all jacks, including rolling in soil, vocalization (at the introduction of the donkey jack to the horse mare) and sniffing the mare’s perineal area, inguinal region, hind legs and ventral abdomen, as well as the ground.

Several strategies have been applied to overcome the differences in sexual behavior of horses and donkeys. Usually Brazilian donkey breeders keep young jacks and fillies together from weaning to two years of age. During this period, all physical, visual, and auditory contact with jennies is avoided. If jacks are only bred with fillies from puberty onward, they appear to become attracted to horse mares and conditioned to mate them. It appears that if a donkey achieves puberty with mares as the only available females, throughout life the jack is more likely to respond with greater interest to horse mares than to donkey jennies [4,7].

Mule Sexual Behavior

Generally if the female mule shows estrus, it is similar to that of horse mares. In addition, female mules often will copulate with either horse stallions and donkey jacks, although the impression is that female mules are more attracted to horse stallions than to donkey jacks. This may be because horse stallions tend to be more vocal than donkey jacks in the presence of female mules. Again the impression is that female mules, like horse mares, seem to display more intense estrus. Estrus when shown by mules includes winking the clitoris, expelling urine in small amounts, but not clapping the mouth nor seeking out the stallion as intensely as donkey jennies do with donkey jacks. Female mules may show estrus in a cyclical manner or year-round, or may be persistently anestrous. Persistent estrus is considered highly unacceptable, especially for sport mules as well as for cattle-herding animals (Canisso, unpublished personal experience).

Currently, the most popular mule sport is Western Brazilian dressage. In this modality, mules are required to be naturally comfortable for riding and to demonstrate good compliance with directional commands of the rider. Female mules are more prized for dressage than male mules, based on popular superstition that the females bring the best luck and are better for riding. Persistent estrus is currently a serious problem for female sport mules, especially during mule competitions when horse stallions are present (Canisso, unpublished personal experience).

The male mule presents behavior that is more similar to that of horse stallions than that of donkey jacks. Male mules are well known in rural areas to present strong stallion-like behavior that makes them highly undesirable if not gelded. Normally, under Brazilian farm conditions they are gelded between 1.5 and 2.5 years of age. Usually male mules are attracted to horse mares and not with the same intensity to donkey jennies (Canisso, unpublished personal experience).

Hinnies (offsprings of a horse stallion and donkey jenny) are an uncommon occurrence. Since the fertility of horse stallion semen in donkey jennies is remarkably low and there is a high incidence of early embryonic death [13], the authors have not seen as many hinnies as mules. The behavior of hinnies that has been observed, is more similar to that of donkeys than that of horses. This is likely the reason why hinnies are highly undesirable in rural areas as working animals, although the best dressage animal in Brazil in 2008 was a gelded male hinny (Canisso, unpublished personal experience).

Breeding Management of Donkeys

It is not the aim of this chapter to review the breeding management of donkeys in great detail; for more information on the subject, readers are encouraged to consult reports published elsewhere [4,14]. However, here is a brief overview of the breeding strategies that have been successfully applied in the breeding management of jacks.

The first method aims to facilitate expression of several typical elements of the donkey courtship. Initially, the jack is allowed to tease the restrained mare, and is allowed to mount without a full erection. Then the jack is kept at a distance but within sight of the mare until a full erection is reached. The initial teasing, mounting without an erection and observation of the mare from a distance while gaining an erection mimics the jacks’ natural sexual behavior. Additionally, estrous jennies can be placed in a separate pen to improve the jack’s response and to train young jacks to breed mares. As soon as the jack learns to mount mares, the goal is to remove the jennies from sight (Figure 3).

Figure 3. An illustration of a breeding system used for semen collection or for in-hand natural mating of donkeys. On the right is a restrained mare deep in estrus, in the center is the donkey presenting full erection, kept at a distance (4 - 6 m) from and gazing at the estrus mare, and in the background to the left are two estrous jennies within visual contact of the jack thus emulating the natural system and encouraging sexual behavior in the jack. This drawing was presented and published in the proceedings of the 55th Annual Convention of the American Association of Equine Practitioners, Las Vegas, Canisso et al. [15].

The personal experience of the authors [4], suggests that during breeding, donkeys usually bite and grasp onto the mare’s mane more aggressively than is typical of horse stallions, resulting in excessive movement and kicking by the mare which then leads to the jack loosing erection and focus during breeding. The use of a rustic Brazilian stock restrains the lateral movement of the mare and prevents kicking. In addition, differences in height can be accommodated by adjusting the pitch of the ground.

A third breeding strategy involves the use of a horse mare, a horse stallion and a donkey jack. In this system, the horse mare teased by a horse stallion will display intense estrus, and the donkey jack near the mare will respond to the mare. This method is quite useful for training mature jacks to start breeding mares and also to encourage jacks with low libido to breed mares (Figure 4).

Figure 4. A drawing to illustrate a stimulatory breeding system that can be used in training non-conditioned juvenile or elderly donkeys to mate with mares, or for adult donkeys with low libido that are required to breed mares. On the left the donkey jack being trained is allowed to approach the perineal area of the estrous mare (center), which is restrained and held between a double fence. On the right is a stallion, which is used to elicit estrus that in turn will encourage sexual response in the jack. This drawing was presented and published in the proceedings of the 55th Annual Convention of the American Association of Equine Practitioners, [15].

An alternative method for extremely territorial jacks is to turn an estrous mare with the jack in a small paddock or its stall. In addition, an estrous jenny can be placed nearby and then taken away from the jack. As a result, often the jack will mount the mare and then the clinician can enter the paddock/stall to collect the semen. However, the use of this strategy increases the risk of injuries such as kicks and bites to both the horse mare and the donkey jack.

Figure 5. A drawing to illustrate part of the typical donkey jack sexual behavior evident when a jack is turned out freely in a small paddock or a mare in deep estrus (trained to mate with jacks) is placed in the donkey’s stall. The donkey, with full erection, approaches an estrous mare that is presenting typical passive behavior (top); the donkey jack may mount the mare, laterally (middle); successful copulation (bottom). This drawing was presented and published in the proceedings of the 55th Annual Convention of the American Association of Equine Practitioners [15].

Final Considerations

In summary, donkeys’ natural sexual behavior differs considerably from that of horses. Mules’ sexual behavior is generally more similar to that of horses than donkey behavior. Knowledge of the natural sexual behavior of donkeys is useful for implementing strategies to increase the efficiency of in-hand breeding of donkeys. Strategies that simulate the jack’s natural behavior maximize the efficiency and success of the breeding program.