Captive breeding

Last updated
USFWS staff with two red wolf pups bred in captivity Red wolf pups - captive breeding.jpg
USFWS staff with two red wolf pups bred in captivity

Captive breeding, also known as captive propagation, is the process of keeping plants or animals in controlled environments, such as wildlife reserves, zoos, botanic gardens, and other conservation facilities. It is sometimes employed to help species that are being threatened by the effects of human activities such as climate change, habitat loss, fragmentation, overhunting or fishing, pollution, predation, disease, and parasitism. [1]

Contents

For many species, relatively little is known about the conditions needed for successful breeding. Information about a species' reproductive biology may be critical to the success of a captive breeding program. [2] [3] [4] In some cases a captive breeding program can save a species from extinction, [5] but for success, breeders must consider many factors—including genetic, ecological, behavioral, and ethical issues. Most successful attempts involve the cooperation and coordination of many institutions. The efforts put into captive breeding can aid in education about conservation because species in captivity are closer to the public than their wild conspecifics. [6] These accomplishments from the continued breeding of species for generations in captivity is also aided by extensive research efforts ex-situ and in-situ. [6]

History

The Arabian Oryx is one of the first animals reintroduced via a captive breeding program. Arabian oryx (oryx leucoryx).jpg
The Arabian Oryx is one of the first animals reintroduced via a captive breeding program.

Captive breeding techniques began with the first human domestication of animals such as goats, and plants like wheat, at least 10,000 years ago. [7] These practices were expanded with the rise of the first zoos, which started as royal menageries such as the one at Hierakonpolis, capital in the Predynastic Period of Egypt. [8]

The first actual captive breeding programs were only started in the 1960s. These programs, such as the Arabian Oryx breeding program from the Phoenix Zoo in 1962, were aimed at the reintroduction of these species into the wild. [9] These programs expanded under The Endangered Species Act of 1973 of the Nixon Administration which focused on protecting endangered species and their habitats to preserve biodiversity. [10] Since then, research and conservation have been housed in zoos, such as the Institute for Conservation Research at the San Diego Zoo founded in 1975 and expanded in 2009, [11] which have contributed to the successful conservation efforts of species such as the Hawaiian Crow. [12]

Coordination

The breeding of species of conservation concern is coordinated by cooperative breeding programs containing international studbooks and coordinators, who evaluate the roles of individual animals and institutions from a global or regional perspective. These studbooks contain information on birth date, gender, location, and lineage (if known), which helps determine survival and reproduction rates, number of founders of the population, and inbreeding coefficients. [13] A species coordinator reviews the information in studbooks and determines a breeding strategy that would produce most advantageous offspring.

If two compatible animals are found at different zoos, the animals may be transported for mating, but this is stressful, which could in turn make mating less likely. However, this is still a popular breeding method among European zoological organizations. [14] Artificial fertilization (by shipping semen) is another option, but male animals can experience stress during semen collection, and the same goes for females during the artificial insemination procedure. Furthermore, this approach yields lower-quality semen, because shipping requires extending the life of the sperm for the transit time.

There are regional programmes for the conservation of endangered species:

Challenges

Genetics

The objective of many captive populations is to hold similar levels of genetic diversity to what is found in wild populations. As captive populations are usually small and maintained in artificial environments, genetics factors such as adaptation, inbreeding and loss of diversity can be a major concern.

Domestication adaptations

Adaptive differences between plant and animal populations arise due to variations in environmental pressures. In the case of captive breeding prior to reintroduction into the wild, it is possible for species to evolve to adapt to the captive environment, rather than their natural environment. [15] Reintroducing a plant or animal to an environment dissimilar to the one they were originally from can cause fixation of traits that may not be suited for that environment leaving the individual disadvantaged. Selection intensity, initial genetic diversity, and effective population size can impact how much the species adapts to its captive environment. [16] Modeling works indicate that the duration of the programs (i.e., time from the foundation of the captive population to the last release event) is an important determinant of reintroduction success. Success is maximized for intermediate project duration allowing the release of a sufficient number of individuals, while minimizing the number of generations undergoing relaxed selection in captivity. [17] Can be minimized by reducing the number of generations in captivity, minimizing selection for captive adaptations by creating environment similar to natural environment and maximizing the number of immigrants from wild populations. [18]

Genetic diversity

One consequence of small captive population size is the increased impact of genetic drift, where genes have the potential to fix or disappear completely by chance, thereby reducing genetic diversity. Other factors that can impact genetic diversity in a captive population are bottlenecks and initial population size. Bottlenecks, such as rapid decline in the population or a small initial population impacts genetic diversity. Loss can be minimized by establishing a population with a large enough number of founders to genetically represent the wild population, maximize population size, maximize ratio of effective population size to actual population size, and minimize the number of generations in captivity. [17]

Inbreeding

Inbreeding is when organisms mate with closely related individuals, lowering heterozygosity in a population. Although inbreeding can be relatively common, when it results in a reduction in fitness it is known as inbreeding depression. The detrimental effects of inbreeding depression are especially prevalent in smaller populations and can therefore be extensive in captive populations. [19] To make these populations the most viable, it is important to monitor and reduce the effects of deleterious allele expression caused by inbreeding depression and to restore genetic diversity. [19] Comparing inbred populations against non-inbred or less-inbred populations can help determine the extent of detrimental effects if any are present. [20] Closely monitoring the possibility of inbreeding within the captive bred population is also key to the success of reintroduction into the species' native habitat.

The Speke's Gazelle was the focus of a captive breeding program centered on determining the effect of selection on reducing genetic load. Speke's Gazelle.jpg
The Speke's Gazelle was the focus of a captive breeding program centered on determining the effect of selection on reducing genetic load.
Outbreeding

Outbreeding is when organisms mate with unrelated individuals, increasing heterozygosity in a population. Although new diversity is often beneficial, if there are large genetic differences between the two individuals it can result in outbreeding depression. This is a reduction in fitness, similar to that of inbreeding depression, but arises from a number of different mechanisms, including taxonomic issues, chromosomal differences, sexual incompatibility, or adaptive differences between the individuals. [21] A common cause is chromosomal ploidy differences and hybridization between individuals leading to sterility. The best example is in the orangutan, which, prior to taxonomic revisions in the 1980s would be commonly mated in captive populations producing hybrid orangutans with lower fitness. [22] If chromosomal ploidy is ignored during reintroduction, restoration efforts would fail due to sterile hybrids in the wild. If there are large genetic differences between individuals originally from distant populations, those individuals should only be bred in circumstances where no other mates exist.

Behavior changes

Captive breeding can contribute to changes in behavior in animals that have been reintroduced to the wild. Released animals are commonly less capable of hunting or foraging for food, which leads to starvation, possibly because the young animals spent the critical learning period in captivity. Released animals often display more risk-taking behavior and fail to avoid predators. [23] Golden lion tamarin mothers often die in the wild before having offspring because they cannot climb and forage. This leads to continuing population declines despite reintroduction as the species are unable to produce viable offspring. Training can improve anti-predator skills, but its effectiveness varies. [24] [25]

Salmon bred in captivity have shown similar declines in caution and are killed by predators when young. However, salmon that were reared in an enriched environment with natural prey showed less risk-taking behaviors and were more likely to survive. [26]

A study on mice has found that after captive breeding had been in place for multiple generations and these mice were "released" to breed with wild mice, that the captive-born mice bred amongst themselves instead of with the wild mice. This suggests that captive breeding may affect mating preferences, and has implications for the success of a reintroduction program. [27]

Chatham Island Black Robin on Rangatira Island, New Zealand. Black Robin on Rangatira Island.jpg
Chatham Island Black Robin on Rangatira Island, New Zealand.

Human mediated recovery of species can unintentionally promote maladaptive behaviors in wild populations. In 1980 the number of wild Chatham Island Black Robins was reduced to a single mating pair. Intense management of populations helped the population recover and by 1998 there were 200 individuals. During recovery scientists observed "rim laying" an egg laying habit where individuals laid eggs on the rim of the nest instead of the center. Rim laid eggs never hatched. To combat this land managers pushed the egg to the center of the nest, which greatly increased reproduction. However, by allowing this maladaptive trait to persist, over half the population were now rim layers. Genetic studies found that this was an autosomal dominant mendelian trait that was selected for due to human intervention. [28]

Another challenge presented to captive breeding is an attempt to establish multi-partner mating systems in captive populations. It can be difficult to replicate the circumstances surrounding multiple mate systems and allow it to occur naturally in captivity due to limited housing space and lack of information. When brought into captivity, there is no guarantee that a pair of animals will pair bond or that all the members of a population will participate in breeding. Throughout facilities, there is limited housing space so allowing for mate choice may establish genetic issues in the population. A lack of information surrounding the effects of mating systems on captive populations can also present issues when attempting to breed. These mating systems are not always fully understood and the effects captivity may have on them cannot be known until they are studied in greater capacity.

Successes

A cheetah at the De Wildt Cheetah and Wildlife Centre. Cheetah at De Wildt Cheetah Farm, Hartbeespoort, North West Province (6253206366).jpg
A cheetah at the De Wildt Cheetah and Wildlife Centre.
King cheetah, a variety of cheetah with a rare mutation at De Wildt Cheetah and Wildlife Centre King cheetah, De Wildt Cheetah Research Centre (South Africa).jpg
King cheetah, a variety of cheetah with a rare mutation at De Wildt Cheetah and Wildlife Centre

The Phoenix Zoo had an Arabian Oryx breeding program in 1962. They were able to successfully breed over 200 individuals from a lineage of only 9 original founders. Members from this founding population were then sent to many other facilities worldwide, and many breeding herds were established. In 1982, the first of the population was reintroduced back into Oman, and over the next two decades, their population increased over time and was able to successfully reestablish in native regions. Arabian Oryx have now been reintroduced into areas such as Saudi Arabia, Oman, and Israel and they now number 1,100, showing a recovery thanks to captive breeding efforts. [29]

The De Wildt Cheetah and Wildlife Centre, established in South Africa in 1971, has a cheetah captive breeding program. Between 1975 and 2005, 242 litters were born with a total of 785 cubs. The survival rate of cubs was 71.3% for the first twelve months and 66.2% for older cubs, validating the fact that cheetahs can be bred successfully (and their endangerment decreased). It also indicated that failure in other breeding habitats may be due to "poor" sperm morphology. [30]

Przewalski's horse, the only horse species never to have been domesticated, was recovered from the brink of extinction by a captive breeding program, and successfully reintroduced in the 1990s to the Mongolia, with more than 750 wild roaming Przewalski's horses as of 2020. [31]

The Galápagos tortoise population, once reaching as low in population as 12 remaining individuals, as of 2014 was recovered to more than 2000 by a captive breeding program. [32] [33] A further 8 tortoise species were supported by captive breeding programs in the island chain. [33]

Wild Tasmanian devils have declined by 90% due to a transmissible cancer called Devil Facial Tumor Disease. [34] A captive insurance population program was started, but the captive breeding rates as of 2012 were lower than they needed to be. Keeley, Fanson, Masters, and McGreevy (2012) sought to "increase our understanding of the estrous cycle of the devil and elucidate potential causes of failed male-female pairings" by examining temporal patterns of fecal progestogen and corticosterone metabolite concentrations. They found that the majority of unsuccessful females were captive-born, suggesting that if the species' survival depended solely on captive breeding, the population would probably disappear. [35]

In 2010, the Oregon Zoo found that Columbia Basin pygmy rabbit pairings based on familiarity and preferences resulted in a significant increase in breeding success. [36]

In 2019, researchers trying to breed captive American paddlefish and Russian sturgeon separately inadvertently bred sturddlefish - a hybrid fish between the two fish. [37]

Research

Captive breeding can also be a research tool to understand the reproductive physiology and reproductive behaviors of species. In order to successfully breed animals, there must be an understanding of their mating systems, their reproductive physiology, and behavior or mating rituals. Through captive breeding programs, these factors can be measured in a finite setting and the results can be interpreted and used to aid in ex-situ and in-situ conservation. Through a greater understanding of these systems, captive breeding efforts can have greater success when attempting to reproduce a species. A lot of research about elephant reproductive physiology and estrus cycles has been conducted in captivity and a greater understanding of how these factors play into breeding attempts can be established. [38] Behavioral research quantifies the effects of how estrus plays a role in the herds behaviors and how this effects the bulls of a herd. [39] This research can help facilities monitor for behavior changes in their herd and conduct successful breeding attempts through this understanding. Research helps with better understanding these physiological systems which in turn helps increase successful breeding attempts and allows for more generations to be brought up in captivity.

Not only does physiological research aid in captive breeding attempts, but multi-generational research is also another important research tool that is conducted on different species and genetic changes can be tracked through different lineages brought up in captivity. Genetic changes throughout a specific lineage can help provide breeding recommendations and allow for genetic diversity within a captive population to remain high. Studbooks are an important resource that contains records of species lineages to track all of the data throughout breeding histories to allow facilities to understand the genetic history of an individual, the births and deaths of involved in the captive breeding of a certain species, and the parentage of certain individual animals. [40] These studbooks come from years of effort of conducting research involving captive breeding programs, which allows facilities view the history surrounding certain individuals and then work together to evaluate the best plan of action to increase breeding success and genetic diversity within certain species populations in captivity. This genetic record keeping is also used in order to understand phylogeny and to better understand fitness changes that may occur over generations in captive populations. [40] This form of record keeping helps aid in research surrounding population genetics in order to evaluate the best method to sustain high genetic variation within captive populations.

Research conducted on captive breeding populations is also important when creating SAFE's and SSP's for a certain species. Studies in behavior are important when developing captive breeding programs because they allow facilities to understand an animals response to captivity and allows facilities to adapt proper housing conditions for the animals. [41] Populations that are currently being propagated in captivity are very important research tools for understanding how to carry out successful propagation of a certain species. [41] This research allows the knowledge to be passed on to more facilities allowing for more breeding programs to be developed in order to increase the genetic diversity of captive populations. The research conducted on breeding populations is also an important gateway into understanding other aspects of an animal such as social dynamics, nutrition and diet requirements, and demographics to allow for captive populations to prosper. [41]

Methods used

Every known individual of the California condor population has been captured and then bred using research from microsatellite regions in their genome. Californian Condor 50 MC.jpg
Every known individual of the California condor population has been captured and then bred using research from microsatellite regions in their genome.

To found a captive breeding population with adequate genetic diversity, breeders usually select individuals from different source populations—ideally, at least 20-30 individuals. Founding populations for captive breeding programs have often had fewer individuals than ideal because of their threatened state, leaving them more susceptible to challenges such as inbreeding depression. [42]

To overcome challenges of captive breeding such as adaptive differences, loss of genetic diversity, inbreeding depression, and outbreeding depression and get desired results, captive breeding programs use many monitoring methods. Artificial insemination is used to produce the desired offspring from individuals who do not mate naturally to reduce effects of mating closely related individuals such as inbreeding. [42] Methods as seen in panda pornography allow programs to mate chosen individuals by encouraging mating behavior. [43] A concern in captive breeding is to minimize the effects of breeding closely related individuals, microsatellite regions from an organism's genome can be used to determine amounts of relationship among founders to minimize relatedness and pick the most distant individuals to breed. [42] This method has successfully been used in the captive breeding of the California condor and the Guam rail. The maximum avoidance of inbreeding (MAI) scheme allows control at a group level rather than an individual level by rotating individuals between groups to avoid inbreeding. [42]

Facilities can use intensive housing compared to group housing to allow for easier reproductive success and create more genetic diversity within a population. Intensive housing is when a species is forced into monogamy so only two individuals mate with each other, compared to group housing where the entire population is kept in the same space to try and replicate multi-partner breeding systems. When using intensive housing and forcing monogamy to take place, it is seen that inbreeding is lowered and a greater genetic diversity results. [44] Intensive housing efforts were used with Tasmanian Devil populations in captivity compared to allowing for group mate choice. [44] This helped increase the populations reproductive success in captivity and saw less inbreeding depression within the population. [44] Using intensive housing to help establish a genetically healthy population in captivity can allow facilities to further increase conservation efforts of a species and combat genetic issues that may arise in the captive population.

New technologies

Assisted reproduction technology (ART): Artificial insemination

Getting captive wild animals to breed naturally can be a difficult task. Giant pandas for example lose interest in mating once they are captured, and female giant pandas only experience estrus once a year, which only lasts for 48 to 72 hours. [45] Many researchers have turned to artificial insemination in an attempt to increase the populations of endangered animals. It may be used for many reasons, including to overcome physical breeding difficulties, to allow a male to inseminate a much larger number of females, to control the paternity of offspring, and to avoid injury incurred during natural mating. [46] It also creates more genetically diverse captive populations, enabling captive facilities to easily share genetic material with each other without the need to move animals. Scientist of the Justus-Liebig-University of Giessen, Germany, from the working group of Michael Lierz, developed a novel technique for semen collection and artificial insemination in parrots producing the world's first macaw by assisted reproduction. [47]

Cryopreservation

Animal species can be preserved in gene banks, which consist of a cryogenic facilities used to store live sperm, eggs, or embryos in ultracold conditions. The Zoological Society of San Diego has established a "frozen zoo" to store frozen tissue from the world's rarest and most endangered species samples using cryopreservation techniques. At present, there has been more than 355 species, including mammals, reptiles, and birds. Cryopreservation can be performed as oocyte cryopreservation before fertilization, or as embryo cryopreservation after fertilization. Cryogenically preserved specimens can potentially be used to revive breeds that are endangered or extinct, for breed improvement, crossbreeding, research and development. This method can be used for virtually indefinite storage of material without deterioration over a much greater time-period relative to all other methods of ex situ conservation. However, cryo-conservation can be an expensive strategy and requires long term hygienic and economic commitment for germplasms to remain viable. Cryo-conservation can also face unique challenges based on the species, as some species have a reduced survival rate of frozen germplasm, [48] but cryobiology is a field of active research and many studies concerning plants are underway.

An example of the use of cryoconservation to prevent the extinction of a livestock breed is the case of the Hungarian Grey cattle, or Magya Szurke. Hungarian Grey cattle were once a dominant breed in southeastern Europe with a population of 4.9 million head in 1884. They were mainly used for draft power and meat. However, the population had decreased to 280,000 head by the end of World War II and eventually reached the low population of 187 females and 6 males from 1965 to 1970. [49] The breed's decreased use was due primarily to the mechanization of agriculture and the adoption of major breeds, which yield higher milk production. [50] The Hungarian government launched a project to preserve the breed, as it possesses valuable traits, such as stamina, calving ease, disease resistance, and easy adaptation to a variety of climates. The government program included various conservation strategies, including the cryopreservation of semen and embryos. [49] The Hungarian government's conservation effort brought the population up to 10,310 in 2012, which shows significant improvement using cryoconservation. [51]

Cloning

The best current cloning techniques have an average success rate of 9.4 percent, [52] when working with familiar species such as mice, while cloning wild animals is usually less than 1 percent successful. [53] In 2001, a cow named Bessie gave birth to a cloned Asian gaur, an endangered species, but the calf died after two days. In 2003, a banteng was successfully cloned, followed by three African wildcats from a thawed frozen embryo. These successes provided hope that similar techniques (using surrogate mothers of another species) might be used to clone extinct species. Anticipating this possibility, tissue samples from the last bucardo (Pyrenean ibex) were frozen in liquid nitrogen immediately after it died in 2000. Researchers are also considering cloning endangered species such as the giant panda and cheetah. However, cloning of animals is opposed by animal-groups due to the number of cloned animals that suffer from malformations before they die. [54]

Interspecific pregnancy

A potential technique for aiding in reproduction of endangered species is interspecific pregnancy, implanting embryos of an endangered species into the womb of a female of a related species, carrying it to term. [55] It has been used for the Spanish Ibex [56] and Houbara bustard. [57]

Conservation education

Captive breeding is an important tool used in modern education of conservation issues because it provides a framework for how we care about species and allows institutions to show the beauty that is contained in our natural environment. These practices of captive breeding can be used to explain the function of the modern-day facilities and their importance in conservation. Through continued breeding efforts populations can continue to be displayed in closer proximity to the public and their role in conservation can be explained. These explanations help show a side of the world many people will not engage with because conservation is not something that is inherently known about, it must be shown and taught to others to raise awareness of the issues around the globe. By allowing people to view these species in captivity, it allows facilities to explain the issues they face in the wild and advocate for the conservation of these species and their natural habitats. [58]

Institutions focus efforts on large charismatic species, such as elephants, giraffes, rhinos etc., because these draw more visitors to institutions and garner more attention from the public. [58]  While a lot of these charismatic megafauna do draw more attention than other species, we can still use captive breeding programs and facilities involving other species to educate the public about a broader range of issues. Bristol Zoo Gardens in the United Kingdom has maintained a species of medicinal leech (Hirudo medicinalis) in their facility to use as an education exhibit. [59] Leeches normally have a negative connotation surrounded by them but they have been used as an important tool in medicine. The display at Bristol Zoo Gardens provides an educational piece and tells the story of a woman who sold leeches to the locals around her for medicinal purposes. [59] This display advocates for a smaller species that would not normally be covered by facilities, but they are well maintained in this facility and are active conservation of the species is being done because of its significance around humans and in the environment. Facilities can use captive breeding for a number of possibilities, such as educating the populace about captive breeding which provides conservation advocacy and a maintenance of these populations helps make the conservation issues surrounding the species more prevalent in the minds of the general public.

Ethical considerations

With successes, captive-breeding programs have proven successful throughout history. Notable examples include the American black-footed ferret; in 1986, a dwindling wild population of only 18 was eventually raised to 500. A Middle-Eastern antelope, the Arabian oryx was hunted over centuries, reducing their population by the late 1960s to merely eleven living animals; not wanting to lose such a symbolic animal of the Middle East, these individuals were rescued and donated by King Saud to the Phoenix Zoo, the San Diego Zoo and their (at the time) newly developed, 1,800-acre (730 ha) Wild Animal Park, prior to his death in 1969. [60] From these actions, those eleven oryx were successfully bred from the brink of extinction, and would go on to be re-released in the deserts of Jordan, Oman, Bahrain, United Arab Emirates and Qatar. Starting in 1980, the first animals were set free. Currently, the wild animals number around 1,000 individuals, with a further 6,000-7,000 in zoos and breeding centres internationally. [61]

While captive breeding can be an ideal solution for preventing endangered animals from facing serious threats of extinction there are still reasons why these programs can occasionally do more harm than good. Some detrimental effects include delays in understanding optimal conditions required for reproduction, failure to reach self-sustaining levels or provide sufficient stock for release, loss of genetic diversity due to inbreeding, and poor success in reintroductions despite available captive-bred young. [62] Although it has been proven that captive breeding programs have yielded negative genetic effects in decreasing the fitness of captive-bred organisms, there is no direct evidence to show that this negative effect also decreases the overall fitness of their wild-born descendants. [63]

It has been argued that animals should be released from captivity programs for four main reasons: a lack of sufficient space due to overly successful breeding programs, closure of facilities due to financial reasons, pressure from animal rights advocacy groups, and to aid the conservation of endangered species. [64] Additionally, there are many ethical complications to reintroducing animals born in captivity back into the wild. For example, when scientists were reintroducing a rare species of toad back into the Mallorcan wild in 1993, a potentially deadly fungus that could kill frogs and toads was unintentionally introduced. [65] It is also important to maintain the organism's original habitat, or replicate that specific habitat for species survival.

There are ethical issues surrounding if a species truly needs human intervention and if the resources going toward the captive breeding of these species cannot be allocated to other areas. Some populations may not need intervention because they were never extinction-prone in the first place such as the peregrine falcon. [66] The population of peregrine falcons had a crash in the 1950s and 1960s due to the effect of pesticides on egg production and species survival, causing a decline in the population. Many facilities at the time in the U.S. and in European countries brought in peregrine falcons in order to help their declining population and establish a steady population through captive breeding. It was later shown through research conducted on the reproductive success of Peregrine Falcons and an analysis of their population that human intervention was not necessary in order for the population to recover and reach a steady point of equilibrium. This raises the question of should efforts on captive breeding and population establishment be done with human intervention or should efforts be carried out to prevent the source of the issue. The efforts and finances used to help bring about new Peregrine Falcon populations could have been used to prevent some level of pollution or to help breeding effort for extinction-prone species who truly need intervention.

See also

Related Research Articles

<span class="mw-page-title-main">Inbreeding</span> Reproduction by closely related organisms

Inbreeding is the production of offspring from the mating or breeding of individuals or organisms that are closely related genetically. By analogy, the term is used in human reproduction, but more commonly refers to the genetic disorders and other consequences that may arise from expression of deleterious recessive traits resulting from incestuous sexual relationships and consanguinity. Animals avoid inbreeding only rarely.

<span class="mw-page-title-main">Przewalski's horse</span> Subspecies of mammal

Przewalski's horse, also called the takhi, Mongolian wild horse or Dzungarian horse, is a rare and endangered horse originally native to the steppes of Central Asia. It is named after the Russian geographer and explorer Nikolay Przhevalsky. Once extinct in the wild, since the 1990s it has been reintroduced to its native habitat in Mongolia in the Khustain Nuruu National Park, Takhin Tal Nature Reserve, and Khomiin Tal, as well as several other locales in Central Asia and Eastern Europe.

<i>Ex situ</i> conservation Preservation of plants or animals outside their natural habitats

Ex situ conservation is the process of protecting an endangered species, variety, or breed of plant or animal outside its natural habitat. For example, by removing part of the population from a threatened habitat and placing it in a new location, an artificial environment which is similar to the natural habitat of the respective animal and within the care of humans, such as a zoological park or wildlife sanctuary. The degree to which humans control or modify the natural dynamics of the managed population varies widely, and this may include alteration of living environments, reproductive patterns, access to resources, and protection from predation and mortality.

<span class="mw-page-title-main">Population bottleneck</span> Effects of a sharp reduction in numbers on the diversity and robustness of a population

A population bottleneck or genetic bottleneck is a sharp reduction in the size of a population due to environmental events such as famines, earthquakes, floods, fires, disease, and droughts; or human activities such as genocide, speciocide, widespread violence or intentional culling. Such events can reduce the variation in the gene pool of a population; thereafter, a smaller population, with a smaller genetic diversity, remains to pass on genes to future generations of offspring. Genetic diversity remains lower, increasing only when gene flow from another population occurs or very slowly increasing with time as random mutations occur. This results in a reduction in the robustness of the population and in its ability to adapt to and survive selecting environmental changes, such as climate change or a shift in available resources. Alternatively, if survivors of the bottleneck are the individuals with the greatest genetic fitness, the frequency of the fitter genes within the gene pool is increased, while the pool itself is reduced.

<span class="mw-page-title-main">Hawaiian crow</span> Species of bird in the crow family

The Hawaiian crow or ʻalalā is a species of bird in the crow family, Corvidae, that is currently extinct in the wild, though reintroduction programs are underway. It is about the size of the carrion crow at 48–50 cm (19–20 in) in length, but with more rounded wings and a much thicker bill. It has soft, brownish-black plumage and long, bristly throat feathers; the feet, legs, and bill are black. Today, the Hawaiian crow is considered the most endangered of the family Corvidae. They are recorded to have lived up to 18 years in the wild, and 28 years in captivity. Some Native Hawaiians consider the Hawaiian crow an ʻaumakua.

<span class="mw-page-title-main">Black-footed ferret</span> Species of carnivore

The Black-footed ferret, also known as the American polecat or prairie dog hunter, is a species of mustelid native to central North America.

<span class="mw-page-title-main">Père David's deer</span> Species of mammals native to China

The Père David's deer, also known as the milu or elaphure, is a species of deer native to the subtropical river valleys of China. It grazes mainly on grass and aquatic plants. It is the only extant member of the genus Elaphurus. Some experts suggest demoting Elaphurus to a subgenus of Cervus. Based on genetic comparisons, Père David's deer is closely related to Eld's deer.

<span class="mw-page-title-main">Species reintroduction</span> Wildlife conservation technique

Species reintroduction is the deliberate release of a species into the wild, from captivity or other areas where the organism is capable of survival. The goal of species reintroduction is to establish a healthy, genetically diverse, self-sustaining population to an area where it has been extirpated, or to augment an existing population. Species that may be eligible for reintroduction are typically threatened or endangered in the wild. However, reintroduction of a species can also be for pest control; for example, wolves being reintroduced to a wild area to curb an overpopulation of deer. Because reintroduction may involve returning native species to localities where they had been extirpated, some prefer the term "reestablishment".

<span class="mw-page-title-main">Golden lion tamarin</span> Species of New World monkey

The golden lion tamarin, also known as the golden marmoset, is a small New World monkey of the family Callitrichidae. Endemic to the Atlantic coastal forests of Brazil, the golden lion tamarin is an endangered species. The range for wild individuals is spread across four places along southeastern Brazil, with a recent census estimating 3,200 individuals left in the wild and a captive population maintaining about 490 individuals among 150 zoos.

<span class="mw-page-title-main">Conservation genetics</span> Interdisciplinary study of extinction avoidance

Conservation genetics is an interdisciplinary subfield of population genetics that aims to understand the dynamics of genes in a population for the purpose of natural resource management, conservation of genetic diversity, and the prevention of species extinction. Scientists involved in conservation genetics come from a variety of fields including population genetics, research in natural resource management, molecular ecology, molecular biology, evolutionary biology, and systematics. The genetic diversity within species is one of the three fundamental components of biodiversity, so it is an important consideration in the wider field of conservation biology.

<span class="mw-page-title-main">Chinese crocodile lizard</span> Species of lizard

The Chinese crocodile lizard is a semiaquatic anguimorph lizard found only in cool forests in southeastern China and northeastern Vietnam. The Chinese crocodile lizard spends much of its time in shallow water or in overhanging branches and vegetation, where it hunts its prey of insects, snails, tadpoles, and worms. Individuals in captivity may be fed baby mice. A rare and little-studied lizard, it is listed in CITES Appendix II, which regulates international trade of specimens. This is the only species in the monotypic genus Shinisaurus. It is the only living member of Shinisauria, a clade of lizards whose fossil record extends back to the Early Cretaceous, over 120 million years ago.

<span class="mw-page-title-main">Wyoming toad</span> Species of amphibian

The Wyoming toad, also known commonly as Baxter's toad, is a species of toad in the family Bufonidae. The Wyoming toad is an extremely rare amphibian that exists only in captivity and within Mortenson Lake National Wildlife Refuge in Wyoming in the United States. The Wyoming toad was listed as an endangered species in 1984, and listed as extinct in the wild since 1991. As with black-footed ferrets at the Tom Thorne and Beth Williams Wildlife Research Center at Sybille in Wheatland, Wyoming, the effort to save the Wyoming toad has been a cooperative effort among state and federal agencies and private landowners. The Wyoming toad was common from the 1950s through the early 1970s, but its distribution was limited to the Laramie Basin in Albany County. The population crashed around 1975 and was extremely low by 1980. The Wyoming toad was federally listed as endangered in January 1984. To prevent extinction, a captive-breeding program began in 1989 at the Thorne Williams Unit that produced enough offspring in its first few years to supply seven zoos, and in 1998 the Saratoga National Fish Hatchery received captive-breeding stock. Nearly 46,000 offspring were produced at the Thorne Williams Unit from 1995 until 2006, when the remaining captive stock was moved to the Red Buttes Environmental Biology Laboratory south of Laramie, and then released back into the wild. Before the sharp declines occurred, this toad had been originally classified as Bufo hemiophrys baxteri, a subspecies of the Canadian toad, by Kenneth Raymond Porter in 1968.

<span class="mw-page-title-main">Dama gazelle</span> Species of mammal

The dama gazelle, also known as the addra gazelle or mhorr gazelle, is a species of gazelle. It lives in Africa, in the Sahara desert and the Sahel. A critically endangered species, it has disappeared from most of its former range due to overhunting and habitat loss, and natural populations only remain in Chad, Mali, and Niger. Its habitat includes grassland, shrubland, semi-deserts, open savanna and mountain plateaus. Its diet includes shrubs, herbs, grasses, leaves, shoots, and fruit.

<span class="mw-page-title-main">Cheetah Conservation Fund</span> Non-profit organisation based in Namibia

The Cheetah Conservation Fund is a research and lobby institution in Namibia concerned with the study and sustenance of the country's cheetah population, the largest and healthiest in the world. Its Research and Education Centre is located 44 kilometres (27 mi) east of Otjiwarongo. The CCF was founded in 1990 by conservation biologist Laurie Marker who won the 2010 Tyler Prize for her efforts in Namibia.

<span class="mw-page-title-main">Species translocation</span> Human relocation of plants or animals

Translocation is the human action of moving an organism from one area and releasing it in another. In terms of wildlife conservation, its objective is to improve the conservation status of the translocated organism or to restore the function and processes of the ecosystem the organism is entering.

Genetic erosion is a process where the limited gene pool of an endangered species diminishes even more when reproductive individuals die off before reproducing with others in their endangered low population. The term is sometimes used in a narrow sense, such as when describing the loss of particular alleles or genes, as well as being used more broadly, as when referring to the loss of a phenotype or whole species.

A frozen zoo is a storage facility in which genetic materials taken from animals are stored at very low temperatures (−196 °C) in tanks of liquid nitrogen. Material preserved in this way can be stored indefinitely and used for artificial insemination, in vitro fertilization, embryo transfer, and cloning. There are a few frozen zoos across the world that implement this technology for conservation efforts. Several different species have been introduced to this technology, including the Pyrenean ibex, Black-footed ferret, and potentially the white rhinoceros.

The EAZA Ex-situ Programme (EEP) is a population management and conservation programme by European Association of Zoos and Aquaria (EAZA) for wild animals living in European zoos. The programme was formerly known as the European Endangered Species Programme.

<span class="mw-page-title-main">Persian fallow deer</span> Species of deer

The Persian fallow deer is a deer species once native to all of the Middle East, but currently only living in Iran and Israel. It was reintroduced in Israel. It has been listed as endangered on the IUCN Red List since 2008. After a captive breeding program, the population has rebounded from only a handful of deer in the 1960s to over a thousand individuals.

<span class="mw-page-title-main">Conservation behavior</span>

Conservation behavior is the interdisciplinary field about how animal behavior can assist in the conservation of biodiversity. It encompasses proximate and ultimate causes of behavior and incorporates disciplines including genetics, physiology, behavioral ecology, and evolution.

References

  1. Holt, W. V; Pickard, A. R; Prather, R. S (2004). "Wildlife conservation and reproductive cloning". Reproduction. 127 (3): 317–24. doi: 10.1530/rep.1.00074 . PMID   15016951.
  2. Comizzoli, Pierre (3 August 2022). "The importance of understanding wildlife sex". Knowable Magazine . Annual Reviews. doi: 10.1146/knowable-080222-1 . Retrieved 10 August 2022.
  3. Holt, William V.; Comizzoli, Pierre (15 February 2022). "Opportunities and Limitations for Reproductive Science in Species Conservation". Annual Review of Animal Biosciences . 10 (1). Annual Reviews: 491–511. doi: 10.1146/annurev-animal-013120-030858 . ISSN   2165-8102. PMID   34699258. S2CID   240000205.
  4. Fraser, Dylan J (2008). "How well can captive breeding programs conserve biodiversity? A review of salmonids". Evolutionary Applications . 1 (4): 535–86. Bibcode:2008EvApp...1..535F. doi:10.1111/j.1752-4571.2008.00036.x. PMC   3352391 . PMID   25567798.
  5. Pain, Stephanie (8 October 2019). "An amphibious rescue mission". Knowable Magazine . Annual Reviews. doi: 10.1146/knowable-100819-1 . S2CID   213331727 . Retrieved 10 August 2022.
  6. 1 2 Ralls, Katherine; Ballou, Jonathan D. (2013-01-01), "Captive Breeding and Reintroduction", in Levin, Simon A (ed.), Encyclopedia of Biodiversity (Second Edition), Waltham: Academic Press, pp. 662–667, doi:10.1016/b978-0-12-384719-5.00268-9, ISBN   978-0-12-384720-1 , retrieved 2023-09-11
  7. "domestication". National Geographic . National Geographic Society. 2011-01-21. Retrieved 2018-05-12.
  8. "The World's First Zoo | JSTOR Daily". JSTOR Daily. 2015-11-12. Retrieved 2018-05-12.
  9. "The Loneliest Animals | Captive Breeding Success Stories | Nature | PBS". Nature. 2009-04-01. Retrieved 2018-05-12.
  10. "Detailed Discussion of the Laws Affecting Zoos | Animal Legal & Historical Center". www.animallaw.info. Retrieved 2018-05-12.
  11. "Biological Research Institute at the Zoological Society of San Diego". International Zoo Yearbook. 3 (1): 126–127. 2008-06-28. doi:10.1111/j.1748-1090.1962.tb03439.x. ISSN   0074-9664.
  12. "'Alala". San Diego Zoo Institute for Conservation Research. 2015-09-18. Retrieved 2018-06-06.
  13. "Captive Breeding Populations". Smithsonian Conservation Biology Institute . Archived from the original on 2010-06-12.
  14. European Association of Zoos and Aquaria (2015-02-05). "EEPs and ESBs". Archived from the original on 2015-02-05.
  15. Christie, Mark R.; Marine, Melanie L.; French, Rod A.; Blouin, Michael S. (2012-01-03). "Genetic adaptation to captivity can occur in a single generation". Proceedings of the National Academy of Sciences. 109 (1): 238–242. Bibcode:2012PNAS..109..238C. doi: 10.1073/pnas.1111073109 . ISSN   0027-8424. PMC   3252900 . PMID   22184236.
  16. Frankham, Richard (2008). "Genetic adaptation to captivity in species conservation programs". Molecular Ecology . 17 (1): 325–33. Bibcode:2008MolEc..17..325F. doi:10.1111/j.1365-294X.2007.03399.x. PMID   18173504. S2CID   8550230.
  17. 1 2 Robert, Alexandre (2009). "Captive breeding genetics and reintroduction success". Biological Conservation. 142 (12): 2915–22. Bibcode:2009BCons.142.2915R. doi:10.1016/j.biocon.2009.07.016.
  18. Frankham, Richard; Ballou, J D; Briscoe, David A (2010). Introduction to conservation genetics (2nd ed.). Cambridge: Cambridge University Press. ISBN   978-0-521-87847-0. OCLC   268793768.
  19. 1 2 Kalinowski, Steven T. (2018). "Inbreeding Depression in the Speke's Gazelle Captive Breeding Program". Conservation Biology. 14 (5): 1375–1384. doi:10.1046/j.1523-1739.2000.98209.x. S2CID   84562666.
  20. Grueber, Catherine E. (2015). "Impacts of early viability selection on management if inbreeding and genetic diversity in conservation". Molecular Ecology. 24 (8): 962–1083. Bibcode:2015MolEc..24.1645G. doi: 10.1111/mec.13141 . PMID   25735639.
  21. Frankham, Richard (2011). "Predicting the Probability of Outbreeding Depression". Conservation Biology. 25 (3): 465–475. Bibcode:2011ConBi..25..465F. doi: 10.1111/j.1523-1739.2011.01662.x . PMID   21486369. S2CID   14824257.
  22. Palmer, Alexandra; Sommer, Volker; Msindai, Josephine Nadezda (June 2021). "Hybrid apes in the Anthropocene: Burden or asset for conservation?". People and Nature. 3 (3): 573–586. Bibcode:2021PeoNa...3..573P. doi:10.1002/pan3.10214. ISSN   2575-8314. PMC   8581989 . PMID   34805779.
  23. McPhee, M. Elsbeth (2003). "Generations in captivity increases behavioral variance: considerations for captive breeding and reintroduction programs" (PDF). Biological Conservation. 115: 71–77. doi:10.1016/s0006-3207(03)00095-8.
  24. Beck BB, Kleiman DG, Dietz JM, Castro I, Carvalho C, Martins A, Rettberg-Beck B (1991). "Losses and Reproduction in Reintroduced Golden Lion Tamarins Leontopithecus rosalia". Dodo . 27. Jersey Wildlife Preservation Trust: 50–61.
  25. Griffin AS, Blumstein DT, Evans CS (2000). "Training Captive Bred or Translocated animals to avoid predators". Conservation Biology. 14 (5): 1317–326. Bibcode:2000ConBi..14.1317G. doi:10.1046/j.1523-1739.2000.99326.x. S2CID   31440651.
  26. Roberts, L.J.; Taylor, J.; Garcia De Leaniz, C. (2011-07-01). "Environmental enrichment reduces maladaptive risk-taking behavior in salmon reared for conservation". Biological Conservation. 144 (7): 1972–1979. Bibcode:2011BCons.144.1972R. doi:10.1016/j.biocon.2011.04.017. ISSN   0006-3207.
  27. Slade B, Parrott ML, Paproth A, Magrath MJ, Gillespie GR, Jessop TS (November 2014). "Assortative mating among animals of captive and wild origin following experimental conservation releases". Biology Letters. 10 (11): 20140656. doi:10.1098/rsbl.2014.0656. PMC   4261860 . PMID   25411380.
  28. Massaro, Melanie; Sainudiin, Raazesh; Merton, Don; Briskie, James V.; Poole, Anthony M.; Hale, Marie L. (2013-12-09). "Human-Assisted Spread of a Maladaptive Behavior in a Critically Endangered Bird". PLOS ONE. 8 (12): e79066. Bibcode:2013PLoSO...879066M. doi: 10.1371/journal.pone.0079066 . ISSN   1932-6203. PMC   3857173 . PMID   24348992.
  29. Tsui, Sherman (2023-08-16). "Breeding Programmes For Endangered Species: Do They Really Help?". Earth.Org. Retrieved 2023-10-15.
  30. Bertschinger, HJ; Meltzer, DGA; Van Dyk, A (2008). "Captive Breeding of Cheetahs in South Africa 30—Years of Data from the de Wildt Cheetah and Wildlife Centre". Reproduction in Domestic Animals. 43: 66–73. doi: 10.1111/j.1439-0531.2008.01144.x . PMID   18638106.
  31. Nuwer, Rachel (2020-09-12). "Extinction Is Not Inevitable. These Species Were Saved". The New York Times. ISSN   0362-4331 . Retrieved 2020-09-17.
  32. Captive breeding program helps save tortoises species, 2014-10-30, retrieved 2020-09-17
  33. 1 2 "Tortoise Breeding and Rearing Programs". Galapagos Conservancy, Inc. Retrieved 2020-09-17.
  34. Rehmeyer, Julie (March 31, 2014). "Fatal Cancer Threatens Tasmanian Devil Populations". Discover .
  35. Keeley, T; o'Brien, J.K; Fanson, B.G; Masters, K; McGreevy, P.D (2012). "The reproductive cycle of the Tasmanian devil (Sarcophilus harrisii) and factors associated with reproductive success in captivity". General and Comparative Endocrinology. 176 (2): 182–91. doi:10.1016/j.ygcen.2012.01.011. PMID   22306283.
  36. "Love is in the hare: Zoo explores pygmy rabbit 'love connection'". The Oregon Zoo. KVAL. February 14, 2013.
  37. Káldy, Jenő; Mozsár, Attila; Fazekas, Gyöngyvér; Farkas, Móni; Fazekas, Dorottya Lilla; Fazekas, Georgina Lea; Goda, Katalin; Gyöngy, Zsuzsanna; Kovács, Balázs; Semmens, Kenneth; Bercsényi, Miklós; Molnár, Mariann; Patakiné Várkonyi, Eszter (6 July 2020). "Hybridization of Russian Sturgeon (Acipenser gueldenstaedtii, Brandt and Ratzeberg, 1833) and American Paddlefish (Polyodon spathula, Walbaum 1792) and Evaluation of Their Progeny". Genes. 11 (7): 753. doi: 10.3390/genes11070753 . PMC   7397225 . PMID   32640744.
  38. Smith;Hutchins, Brandie;Michael (January–June 2000). "The Value of Captive Breeding Programmes to Field Conservation: Elephants as an Example". Pachyderm. 28: 101–109. doi:10.69649/pachyderm.v28i1.1003. S2CID   82449818.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  39. Ortolani, Alessia; Leong, Kirsten; Graham, Laura; Savage, Anne (July 2005). "Behavioral indices of estrus in a group of captive African elephants (Loxodonta africana)". Zoo Biology. 24 (4): 311–329. doi:10.1002/zoo.20053. ISSN   0733-3188.
  40. 1 2 Farquharson, Katherine A.; Hogg, Carolyn J.; Grueber, Catherine E. (2021-05-24). "Offspring survival changes over generations of captive breeding". Nature Communications. 12 (1): 3045. Bibcode:2021NatCo..12.3045F. doi:10.1038/s41467-021-22631-0. ISSN   2041-1723. PMC   8144597 . PMID   34031378.
  41. 1 2 3 Eisenberg, J. F.; Kleiman, Devra G. (January 1977). "The usefulness of behaviour studies in developing captive breeding programmes for mammals". International Zoo Yearbook. 17 (1): 81–89. doi:10.1111/j.1748-1090.1977.tb00871.x. ISSN   0074-9664.
  42. 1 2 3 4 Frankham, Richard (2010). Introduction to Conservation Genetics . Cambridge University Press. Kindle Edition. United Kingdom: Cambridge University Press. ISBN   978-0-521-87847-0.
  43. Gray, Denis D. (2006-11-23). "Pandas Getting New View of Mating Ritual". The Washington Post and Times-Herald. ISSN   0190-8286 . Retrieved 2018-05-12.
  44. 1 2 3 Asa, C. S.; Traylor-Holzer, K.; Lacy, R. C. (January 2011). "Can conservation-breeding programmes be improved by incorporating mate choice?: Mate Choice, and Genetic and Demographic Management". International Zoo Yearbook. 45 (1): 203–212. doi:10.1111/j.1748-1090.2010.00123.x.
  45. "Giant Panda Undergoes Artificial Insemination Procedure at the San Diego Zoo". Zoonooz. 2015-03-11.
  46. "Artificial Insemination of the Mare". Equine Artificial Insemination.
  47. Pomeroy, Ross (June 24, 2013). "Finally: A Way to Collect Semen from Parrots". Real Clear Science.
  48. "Cryoconservation of Animal Genetic Resources". www.fao.org. Retrieved 2018-04-30.
  49. 1 2 Solti L, Crichton EG, Loskutoff N, Cseh S (2000-02-01). Economic and ecological importance of indigenous livestock and the application of assisted reproduction to their preservation. Vol. 53.
  50. "WWF". wwf.hu. Retrieved 2018-04-30.
  51. "Domestic Animal Diversity Information System (DAD-IS) | Food and Agriculture Organization of the United Nations". www.fao.org. Retrieved 2018-04-30.
  52. Ono T, Li C, Mizutani E, Terashita Y, Yamagata K, Wakayama T (December 2010). "Inhibition of class IIb histone deacetylase significantly improves cloning efficiency in mice". Biology of Reproduction. 83 (6): 929–37. doi: 10.1095/biolreprod.110.085282 . PMID   20686182.
  53. Jabr, Ferris. "Will Cloning Ever Save Endangered Animals?". Scientific American. Retrieved 2018-04-30.
  54. "Are cloned animals safe to eat?". The Week . 30 November 2010.
  55. Niasari-Naslaji A, Nikjou D, Skidmore JA, Moghiseh A, Mostafaey M, Razavi K, Moosavi-Movahedi AA (2009-01-29). "Interspecies embryo transfer in camelids: the birth of the first Bactrian camel calves (Camelus bactrianus) from dromedary camels (Camelus dromedarius)". Reproduction, Fertility and Development. 21 (2): 333–337. doi:10.1071/RD08140. ISSN   1448-5990. PMID   19210924. S2CID   20825507.
  56. Wang, Xichao; Dai, Bojie; Duan, Enkui; Chen, Dayuan (2001). "Advances in interspecific pregnancy". Chinese Science Bulletin. 46 (21): 1772–8. Bibcode:2001ChSBu..46.1772W. doi:10.1007/BF02900547. S2CID   84433057.
  57. Wernery U, Liu C, Baskar V, Guerineche Z, Khazanehdari KA, Saleem S, Kinne J, Wernery R, Griffin DK, Chang IK (December 2010). "Primordial germ cell-mediated chimera technology produces viable pure-line Houbara bustard offspring: potential for repopulating an endangered species". PLOS ONE. 5 (12): e15824. Bibcode:2010PLoSO...515824W. doi: 10.1371/journal.pone.0015824 . PMC   3012116 . PMID   21209914.
  58. 1 2 Cohn, Jeffrey P. (May 1988). "Captive Breeding for Conservation". BioScience. 38 (5): 312–316. doi:10.2307/1310732. ISSN   0006-3568. JSTOR   1310732.
  59. 1 2 Spencer, W.; Jones, G. (July 2007). "The captive breeding and educational display of the Medicinal leech Hirudo medicinalis (Linnaeus 1758) at Bristol Zoo Gardens". International Zoo Yearbook. 41 (1): 138–144. doi:10.1111/j.1748-1090.2007.00005.x.
  60. Tony Perry (5 July 2011). "Arabian Oryx, a comeback story". Los Angeles Times. Retrieved 15 October 2022.
  61. "Is Breeding Endangered Species in Captivity the Right Way to Go?". Pacific Standard. Retrieved 2018-04-30.
  62. Dolman, Paul M; Collar, Nigel J; Scotland, Keith M; Burnside, Robert. J (2015). "Ark or park: The need to predict relative effectiveness ofex situandin situconservation before attempting captive breeding" (PDF). Journal of Applied Ecology. 52 (4): 841–50. Bibcode:2015JApEc..52..841D. doi: 10.1111/1365-2664.12449 .
  63. Araki, H; Cooper, B; Blouin, M. S (2009). "Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild". Biology Letters. 5 (5): 621–4. doi:10.1098/rsbl.2009.0315. PMC   2781957 . PMID   19515651.
  64. Waples KA, Stagoll CS (1997). "Ethical Issues in the Release of Animals from Captivity". BioScience. 47 (2): 115–121. doi: 10.2307/1313022 . JSTOR   1313022.
  65. "Captive Breeding Introduced Infectious Disease To Mallorcan Amphibians". ScienceDaily. Retrieved 2018-04-30.
  66. Rahbek, Carsten (1993-08-01). "Captive breeding—a useful tool in the preservation of biodiversity?". Biodiversity & Conservation. 2 (4): 426–437. Bibcode:1993BiCon...2..426R. doi:10.1007/BF00114044. ISSN   1572-9710. S2CID   19536156.