WILD FELIDS

Seasonality and Cyclicity

The wild feline population consists of about 36 different species all of which vary slightly in their reproductive cycle. All species of wild felines are considered to be seasonally polyestrous (2). It has been found that each species may vary in response to photoperiod length and a breeding program may need to be adjusted according to recommendations for each species (2). The average estrous cycle for a wild feline varies within a 2-4 week interval where estrus can last 3-10 days (2). Typically these animals are considered to be induced ovulators. This means that upon mating, neurotransmitters are released into the bloodstream which will subsequently trigger the release of GnRH and an LH surge to result in ovulation. It has been found that in addition, some of these species may also be spontaneous ovulators in certain environments (10). A spontaneous ovulator is one that will ovulate naturally in response to hormones in the body with no external cause. Some of these species can exhibit either form of ovulation (spontaneous and induced) which is greatly affected by their environment (2). Refer to Table 1 for the primary form of ovulation in specific wild felid populations. 

Species

Spontaneous Ovulator

Induced Ovulator

Lion

X

 

Clouded Leopard

X

 

Pallas’ Cat

X

 

Leopard

X

 

Fishing Cat

X

 

Margay

X

 

Tiger

 

X

Cheetah

 

X

Puma

 

X

Snow Leopard

 

X

Tigrina

 

X

Ocelet

 

X

Domestic Cat

 

X

Table 1: This table demonstrates the ovulation types of several known species of wild felid


It is important to determine the effect of seasonality and the type of ovulation to help with conservation of these animals.  Most of the 36 species of wild felids are endangered or threatened and persevering these animals are of a top priority.  By determining these characteristics it could be determined what reproductive problems exist and how best to fix them.  This could also help with developing more effective reproductive techniques for an individual species of wild felid.  Along with this it could also be found what the best method of contraceptive would be for each species so that there would be no inbreeding in the preserved animals.  Mostly this technology would be used though zoos for breeding programs and conservation. 

To demine the seasonality of wild felids, a non invasive method was used, so as not to disturb the animals.  This method is fecal steroid analysis.  It was found that surges of fecal estrogens distinguish between estrous and anestrous periods (2).  It has also been found in some species that fecal progestins are increased during estrogen surges as well (2).

In addition, studies have also been conducted concerning the seasonal variation in semen characteristics in captive populations (3, 7, 8).  It has been found that there is no difference in fecal androgen concentration between spring, summer, autumn and winter in the jaguar, margay, and tigrina (7, 8).  A peak in androgen concentration was observed during the wet season for the jaguar and in the summer for the ocelot (7,8).  A peak in average sperm production has been noticed in the summer months for the ocelot, tigrina and margay (7).  The margay has been found to be lacking spines on the penis, which are key to induced ovulation in the domestic cat, suggesting that this wild feline may be a spontaneous ovulator (7).  Sperm motility was not found to be affected by season in the ocelot, but was observed to be higher in winter for the tigrina and higher in the spring for the margay (7).  Only a minimal difference in sperm morphology between seasons was found in the tigrina and margay (7).  The ocelot was observed to have decreased sperm morphology in the winter (7).  All these findings suggest that the male tigrina, ocelot, jaguar and margay are capable of breeding all year round (7, 8). Young animals may be monitored throughout their life to assess sperm quality and overall breeding soundness (see Figure 1).


Much of the information that is currently known about the seasonality of wild felids is based off what is known about the more extensively researched domestic cat.  Research on the domestic cat has shown that photoperiod is important in seasonality (2).  In naturally fluctuating light periods the domestic cat is polyestrous (2).  This can be changed due to artificial light; domestic cats will cycle year round if kept under 12-14 hours of light daily (2).  Based off this knowledge, similar findings have been found for various species of wild felids (2).  The element that is activated by light is melatonin (2).  With increased light there is increased melatonin and therefore, cyclicity is promoted.  This is proven though giving injections of melatonin and cyclicity continuing (2).  Various wild felids are more influenced by this phenomenon than others (2).  The tiger, clouded leopard, Pallas’ cat, and snow leopard are all strongly polyestrous (2).  However, lions, leopards, pumas, and fishing cats are not influenced by seasonality (2).  Those that are polyestrous respond to an increase in photoperiod with an increase in fecal estrogen (2).

To increase the number in these species, captive breeding programs have been using hormone regulation to manipulate and maintain wild felid cycles.  This is done through regulation with contraceptives.  In contrast hormones can also be used for assisted reproductive techniques.  When these techniques are used in captive breeding programs conditions should be highly monitored due to the reproductive effects of grouping these animals together.  To have successful results, hormone regulations are the key component and should be researched in depth for each species (10).

Captive Breeding Programs
There are a number of growing concerns for the fecundity of wild endangered populations throughout the world.  Some reproductive concerns for wild felids include a limited gene pool leading to infertility, inbreeding and an increased mortality rate of young (6, 16).  One study noted when small wild felids were housed in groups larger than a pair they were not likely to reproduce successfully (5).  Also, a husbandry style involving zookeepers talking to and interacting with these animals were more likely to result in offspring (5).  However, forty-two percent of all pairings failed to produce offspring (5).  Most wild felids mate frequently during estrus which has led to the assumption that they are induced ovulators (2).  Recent research has now suggested that this is not the case (2).

Housing and management play major roles in the reproductive success of wild felids.  A sudden transition to “long days” can stimulate premature follicular steroidogenesis (2).  For example, the Pallas’ cat has had ovarian activity stimulated when moved to an outdoor exhibit (2).  Ovarian activity was also stimulated during an artificial increase in photoperiod, which resulted in an increase in fecal estrogen during the seasonal increase in photoperiod with no breeding success (2).  The following year, these same animals were not subjected to an artificial increase in photoperiod and were able to attain conception (2).  This suggests that each wild felid species must be carefully maintained in normal seasonal photoperiods to achieve reproductive success.

There is a need to assess levels of genetic variation to avoid inbreeding in recovering populations that are increasing in number to ensure heterozygosity within the captive population (6).  This implies an important role that captive breeding programs may play in preserving genetic diversity of endangered species.  The level of genetic variation in some species is much lower, for example in kotiya leopards, than in other big cat species (6).  In some circumstances, knowledge about wild felid temperament may also be a useful tool to optimize captive reproduction and to increase success of reintroduction to the wild (4).  Natural, sexual and artificial selection in wild and captive populations can cause permanent shifts in temperament, reducing the diversity of temperament that may be critical to reintroduction success (4).  In the lion and leopard, a period of nonmating has been known to induce an increase in progestins which is more common in females that are housed together (2).  Other spontaneous ovulations have occurred in single-housed wild felids, such as, the clouded leopard, margay and fishing cat (2).

Cheetahs (Acinonyx jubatus) suffer from unusually high juvenile mortality and decreased fecundity in captivity due to genetic monomorphism (16).  The mortality of young from related parents has been found to be higher than the mortality of young from unrelated parents (16).  This may be due largely as result of intrinsic causes (stillbirths and congenital defects) that may have a genetic basis or it may be due to different management practices between facilities (16).  Housing and enforced social living could also be a factor that is suppressing reproductive activity in the cheetah (2).  Cheetahs have been found to have periods of alternating estrous cyclicity in some types of group housing (2).  This proposes that reproductive success of wild felids species largely depends on management and maintenance of these species in captivity (2, 5).

Inbreeding depression in the cheetah may still occur in the captive population and deleterious recessive alleles are being segregated which may be a cause of decreased fecundity (16).  Acinonyx jubatus has an average of 3.6 cubs per litter, which is higher than all except 2 of 29 species examined in one study (16).  This may represent a life history adaptation to counteract high juvenile mortality from predation by lions and hyenas (16).

Being able to understand the uniqueness of carnivore reproduction will greatly contribute to species management and conservation.  A key factor in obtaining reproductive success is in knowing the cycle of each of the wild felid species (2).  Whether it is seasonal, induced, or spontaneous, each species must be observed individually. 

Currently, a large-scale frozen repository of 225 sperm from 150 wild-caught cheetahs in Africa will become useful for infusing new genes into ex situ populations (3).  This form of assisted breeding is interesting because the cheetah has poor natural mating in captivity, with only 25% of all adult females having ever reproduced in the current North American population (3).  From the new sperm bank it has been observed that overall seminal quality improves in cheetahs older than 2 years and remains at a relatively sustained quality through adult-hood, up to 10 years of age (3). Male cheetahs also show no seasonality in sperm output or quality (3).  No seasonality has been observed in male tigrinas, margays or jaguars concerning fecal androgen concentration (7, 8).  Recently, advanced cheetah embryos (morula ⁄ blastocyst) have been produced by in vitro fertilization, an approach that could eventually allow transport of the combined male ⁄ female genome of the cheetah between continents (3).

Example of Reproductive Behaviors
The age of sexual maturity in lions is between two and three years old. At maturity, the males go off in search of a pride of their own and the females usually will remain in the same pride. However, some females may leave the pride or be kicked out. These females become known as nomadic lions; they will eventually mate and raise families.

The mating style is about the same for any other wild felid. In most prides, females enter estrous and conceive around the same time as other females in the pride. Female lions can come into heat at anytime; however, there tend to be peak periods depending on location. A typical female will be in estrus for 4-8 days. If the female does not become pregnant, the estrus cycle will repeat in about 90 days (15).

The mating begins with growling, pawing and even biting. When the female is ready for intercourse, she lies down, and the male mounts her. Most females will mate with more than one male during her estrus; this can result in cubs with different fathers.

Contraception
Contraceptives are becoming much more widely used in wild felids.  Contraceptives use different hormones to manipulate and control the cyclicity of wild felids.   Seasonality and the type of ovulator are taken into account when determining what kind of contraceptive should be used.  There have been different contraceptives that have come into favor and used through time.  The reason for change in the contraceptives used is due to the increased knowledge that has been gained about various species’ seasonality and the long term effects of the contraceptives.  

One way to affect the cyclicity of lions is to remove the lion cubs soon after birth; this is a practice that is often put in action by zoos (17).  Once the cubs are removed, the lionesses will come into heat and reconceive much sooner (17).  This can happen as quickly as within the first month after parturition.  For this reason many zoos and parks use contraceptives to control breeding (see Figure 2) (17).  Zoos are also under the observation of the Association of Zoos and Aquariums (AZA) (17).  The AZA keeps records of the breeding animals to ensure that there is no inbreeding of the animals and that the best genetics is used to maintain the healthiest animals (17). 

lions

Figure 2: Contraceptives can be used to control breeding at zoos where males and females are housed together.


One such contraceptive that has been in used in some research studies is the use of long-acting biocompatible deslorelin implants.  This study looked at adult free-ranging lionesses in Kruger National Park (1).  The data found from this study has been shown to be both safe and effective at controlling reproduction (1).  One such implant used was Suprelorin (Peptech Animal Health, Sydney) which has been specifically formulated to deliver long-term release of deslorelin (1).  Deslorelin is a GnRH agonist which down regulates luteinizing hormone (LH) and follicle-stimulating hormone (FSH).  The overall result is thus, the down regulation of ovarian function (1). 

Another contraceptive that is used in zoos and parks for lions is Melengesterol acetate (MGA) (9).  This type of contraceptive has been used extensively.  They are silastic implants that are placed subcutaneously or intramuscularly in the lion (9).  They deliver sufficient concentration of MGA for two years which prevent pregnancy (9).  MGA is now starting to fall out of favor due to the fact that prolonged exposure to MGA has been associated with endometrial hyperplasia and pyometra (9).

Another popular contraceptive used in lions is Depo Provera.  It is a hormone injection that will typically be given every two months (17).  Depo Provera contains synthetic progesterone.  The shot will stop the ovaries form releasing eggs and causes the cervical mucus to thicken.  At the present time, Depo Provera is the easiest to reverse without any complications making it the favorite of many vets (17).  In one particular zoo, the North Eastern Wisconsin (NEW) zoo, this is the method of choice (17).  The veterinarian working with the lion population is Dr. Tracy Gilbert (17).  Dr. Gilbert has chosen to use Depo Provera shots as contraception because of the ease of reversibility and ease of application (17).  For this to be applied, the animals do not need to be sedated unlike the implanted contraceptives (17). 

Through examining controceptives there are several chioces for wild felids. In looking at these options it is important to keep in mind the benefits and side effects of each. In particular, the ease of managment should be kept in mind for future breeding goals.

Assisted Reproductive Techniques

Many of the 36 species of wild felines are becoming endangered so certain steps are being taken in zoos to protect these species. Captive breeding programs are using new research to help prevent inbreeding in these small populations. By using the knowledge known about the individual species’ seasonality and the use of hormone therapy, assisted reproductive techniques can be applied to help these struggling populations. It is foremost to understand whether the animal is exclusively an induced ovulator or if it may be a spontaneous ovulator (10). Being familiar with the species is important to tailor a hormone therapy program to be able to time ovulation. In the case of many species it is most difficult to work with spontaneous ovulators because they are rarer and would then require more of a hormone work-up for artificial insemination (AI) or in vitro fertilization (IVF) (10).

Seasonality can also play a large role in when the manager of the population may decide to perform these techniques. The likelihood of success will depend on the whether the animal needs to be under lights and if so for how long during the day (2). All these contributing factors need to be taken into consideration when using assisted reproductive techniques. Advancements in these technologies can be applied to the female and male which include semen collection, AI, in vitro production, intra cytoplasmic sperm injection (ICSI) and cryopreservation (11). The use of assisted reproductive technology is studied with the domestic cat as the model for the wild felid population (11). It is necessary to remember that through the use of the technologies the hope is to protect the genetic diversity and prevent the extinction of these species.

Applying reproductive techniques to the male can be of particular importance to enhance the success of fertility in the female when using AI or in vitro production. It has been found in some males of the wild felid species that there is poor sperm quality (12). Though ejaculated sperm can be used for AI, it has been found that epididymal spermatozoa involves less characterization and penetrates the oocyte much quicker (14).  The preferred method for collection in male felids is through electroejaculation and particular caution should be taken when administering certain drugs, such as anesthetics, to these males to prevent harm to the sperm (14). Once collected, cryopreservation can be used as a method to preserve sperm to assist in building genetic diversity in cryo banks (14).  At a young age in these animals the opporturnity may arise where a physical exam can be coupled with other procedures that require anesthesia (17). These physical exams may allow these animals to be considered as sires for future breeding progams (see Figure 3).


In female wild felines, artificial insemination can be used to help develop better breeding in captive breeding populations, especially in zoos. The cryopreserved sperm can be used with laparoscopy to deposit the semen into the uterus and has shown to successfully produce viable embryos (12). This method of an assisted reproductive technique is favored over embryo transfer and in vitro fertilization in captive breeding programs because it is less intensive (12). It is important to be well knowledgeable in the seasonality of their cycle and how hormones should be regulated. Use of artificial insemination is more successful in those with high reproductive fitness, so further research should be completed within each specific species to get the best results (10). Reproductive fitness declines at a certain age and it may be sooner than researchers believe (10). If it is at an earlier age, those animals should be bred sooner in captive breeding programs rather than later.

Another reproductive technique being researched in wild felids is in vitro production. However, this is not being used as extensively in captive breeding programs currently because it mostly has shown irregular results with only some success in living offspring (10). To utilize any reproductive techniques on the female, hormones need to be highly regulated and exogenous gonadatropins may need to be given (10). However, the improper dosages are a major contributor to poor oocyte quality (10). The hormones lead to high estrogen concentration and excessive progesterone concentrations which disrupt the oocytes natural environment too much (10). With a poor starting material it is difficult to obtain highly successful results. In general, they have found that it is best to recover in vivo matured oocytes and fertilize them in vitro. Due to poor sperm quality, it is suggested to use ICSI for in vitro fertilization to obtain the best results that can then be transferred to a synchronized recipient (12). Embryo transfer in wild felines also has limited success in most of the species. There has been a success in four of the species and they suggest that when 5 embryos were transferred there was a 0-50% success in pregnancy (10). The variable percentage of pregnancy is from the variability in synchronization of the recipients of the embryos (10).

References

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