This is a common situation for many captive-bred species that have often experienced rapid declines related directly or indirectly to human activities. In theory, a well-managed captive breeding program implementing a number of procedures e. There is consequently a consensus that the more these effects are reduced in a captive breeding program see Table 2 , and the larger the N e , the more successful that captive breeding program will be at maintaining genetic diversity Frankham et al.
One relevant question to ask is, how many generations can N e of typical salmonid captive breeding programs maintain genetic diversity? Frankham et al. In reality, the goal of any captive breeding program should be perhaps to conserve as much genetic diversity as possible. Relationships between genetic diversity and population viability are also complex and likely vary between species and populations within species Tallmon et al.
Indeed, there is at least one report of a successful introduction of salmonid populations into previously unoccupied habitat despite limited genetic diversity and low N e Koskinen et al. Consequently, the present review applies the aforementioned yardsticks cautiously and with these points in mind when interpreting results from empirical or theoretical studies on salmonids. In reality and, like many other organisms, salmonids have overlapping generations in which individuals from several different-year classes might contribute to a population's gene pool annually.
However, relative to species from which historical modeling of overlapping generations was derived Felsenstein ; Hill , many salmonids also differed because they die after breeding. This is the case for semelparous Pacific salmon Oncorhynchus spp. Waples discussed how such a characteristic causes a complete turnover in the breeding population each year rather than the gradual transition of most overlapping generation models. In other words, short-term genetic change in many salmonids is more a function of the effective number of breeders per year, N b , and not generational N e Waples Waples simulated the loss of heterozygosity and allelic diversity that might be accrued over years in isolated salmonid populations with N b of 24, 50, and , under a Wright-Fisher model with random mating and separate sexes.
For a salmonid with a 4-year generation time, these N b values would translate into generational N e values of roughly , , and Such greater losses of allelic diversity relative to heterozygosity are consistent with a wide body of theory e. Thus, the model also suggested that a smaller N b 24—50 might be reasonably tolerated in captive breeding programs for shorter time periods than years e.
Encouragingly, there are means by which to reduce the rate of loss of genetic diversity based on the theoretical considerations outlined above e. Ideally though, it is better to start with as large a founder captive population as possible Allendorf and Ryman ; Frankham et al.
One simple and widely recognized approach is to ensure that each individual contributes exactly the same number of progeny to the next generation. Assuming that, for example, an individual of one sex is bred with a single individual of the opposite sex, equalized family sizes from these matings yield a rate of of inbreeding and genetic drift that is roughly half those generated from random contributions of parents in an idealized population Wright ; Wang In other words, equalization of family sizes effectively doubles N e relative to a randomly mated population.
The few experimental tests carried out on this topic with fruitflies have supported theoretical predictions Borlase et al. For instance, Rodriguez-Ramilo et al. With respect to salmonids, more recently instated captive breeding programs, such as live-gene banking programs of Atlantic salmon, attempt to balance sex ratios and equalize family sizes not only within captivity but also at the time of release into the wild O'Reilly and Doyle ; P.
Live-gene banking programs also attempt to recover at least one offspring per spawned adult repeatedly at each spawning, in each spawning year, and at each sampling event to maximize the retention of genetic diversity of individuals P.
Another more sophisticated and recommended approach is to use pedigree or molecular genetic marker data to minimize mean inbreeding or kinship coancestry coefficients between parents before generating every new captive generation Ballou and Lacy ; Caballero and Toro , ; Fernandez et al.
Salmonid spawnings based on minimizing mean kinship are now being carried out in a number of captive breeding programs e. Currently, however, little empirical research in salmonids or other taxa has been conducted to assess to what degree genetic diversity can be more effectively retained with these additional measures relative to theoretical expectations, in terms of their long-term effectiveness. For instance, over four generations and constant population size, Montgomery et al. Namely, the reuse of under-represented individuals in successive generations would allow them to make greater genetic contributions to successive captive generations Montgomery et al.
Finally, it is worth noting that some measures for minimizing kinship require detailed pedigree information e. One potential caveat of strategies that minimize kinship is that they often assume captive broodstock founders are unrelated and not inbred Rudnick and Lacy , although with DNA techniques, it is now possible to at least estimate founder relationships Gautschi et al.
If founders are related or inbred, maximizing N e by equaling the genetic contributions of captive breeders will only exacerbate the effects caused by a nonrepresentative sampling of the ancestral gene pool within the captive broodstock Ebanhard ; Doyle et al. This is important to consider in many salmonids for two reasons. First, related family members within populations may not be distributed randomly at various stages of the life cycle Hansen et al.
Second, sampling collections for captive broodstock purposes may be restricted in time and spatial coverage Herbinger et al. Recent modeling suggests that while the potential benefits from knowing founder relationships probably vary on a case-by-case basis, minimizing kinship within a captive broodstook under traditional founder assumptions could still generate near optimal results Rudnick and Lacy Yet, Doyle et al.
Notably, using relatedness estimates based on DNA markers and minimum kinship analyses, Doyle et al. Relative to random subsets of breeders of equal size, preferentially-mated subsets of breeders had a lower mean coancestry and they generated an offspring gene pool with greater heterozygosity and allelic diversity Doyle et al. Because of their high polymorphism, microsatellite loci currently represent the most widely used DNA technologies to detect whether losses of genetic diversity have occurred within captive breeding programs.
Where available, the rate of loss of genetic diversity per generation is noted. Program type: S, supplementation; C, captive-breeding; H, harvest augmentation. H e , expected heterozygosity; A , mean numbers of alleles per locus uncorrected across studies for sample size ; G , number of generations in captivity; NA, not available.
Several points and caveats of the studies in Table 4 are worth noting that might make generalities difficult with respect to what constitute typical N b and N e values in salmonid captive broodstocks. In the case of supplementation programs, information was often lacking on whether broodstocks were being supplemented each generation with wild-caught individuals, or whether they were being entirely regenerated from previous generations of the captive broodstock isolated from the wild.
Second, it is uncertain in some cases whether a loss of genetic diversity might be attributable to low captive N e or whether it was related to captive founder effects, because levels of genetic diversity in the captive broodstock were compared to those of the wild population and not to the initial founding captive broodstock. These differences may affect interpretations of the rate at which genetic diversity is lost over time in captive broodstocks. Third, details were lacking in many programs to assess what types of procedures were employed to minimize reductions in N e in the hatchery, so the results may not always be directly applicable to current captive breeding programs Table 1 adopting procedures in Table 2.
Fourth, N b and N e were estimated from different methods, and in particular cases, some of the underlying assumptions of these methods were violated Table 4.
Similarly, N b and N e point estimates in some cases had fairly wide confidence intervals, and many had no confidence intervals at all Table 4. Fraser et al. Finally, conversions of N b estimates to a generational N e estimate assumed that each year's breeding population contributed equally to the next generation regardless of the number of breeders Waples , a.
Assuming that these estimates reflect true values, only crude generalities can be made regarding the capacity of salmonid captive breeding programs to conserve genetic diversity. Interestingly, in only one captive population Oulujoki was a statistically significant reduction in heterozygosity and allelic richness detected Table 4. For example, in two of six captive populations where data on the rate of loss of genetic diversity per generation existed, a loss of 4. The above discussion has dealt with cases where populations have become extirpated or nearly extirpated from the wild.
In such cases most, if not all, remaining population members are involved in captive breeding. These are relevant cases to consider in the context of the capacity of captive breeding programs to conserve genetic diversity.
Nevertheless, during the process towards successful reintroduction into the wild, at some point there will be both wild and captive-reared components to the population. Likewise, when a wild population is experiencing drastic declines and a decision is made to prevent its extinction by supplementing the wild population with captive-reared individuals, the population will comprise these same two components.
Ryman and Laikre modeled the potential increase or reduction in N e even if N of the population is increased , and thus the potential for the rate of loss of genetic diversity to be diminished or magnified, that might occur when captive-reared individuals are released into a wild population over a single generation.
In particular, Ryman and Laikre focused on how captive releases might lead to a reduction in N e. Among other things, the model assumed discrete generations, that captive-reared and wild fish had equal probabilities of breeding in the wild, and that the number of offspring produced by either wild or captive breeder components was distributed binomially. For salmonids, such assumptions are likely violated in many cases Waples ; Wang and Ryman ; see below.
Nevertheless, the model made an important conclusion. For situations where the wild population was small, and thus, most likely to go extinct, supplementation with captive-reared fish could especially lead to a serious reduction of genetic diversity of the overall population through a reduction of N e Ryman and Laikre This concern was also most prominent when only a few captive-reared individuals were used in attempts to recover populations Ryman and Laikre On a positive note, however, in perhaps the only detailed salmonid captive breeding program to effectively apply the Ryman and Laikre method, supplementation does not appear to have reduced genetic diversity in a small, wild population, and it perhaps increased N e Hedrick et al.
For instance, Hedrick et al. Estimation of N b in this study made several assumptions; most notably that survival and return of released captive-reared individuals were random. Nevertheless, using genotypic pedigree information to examine the representation of different captive-reared families in returning breeders, Hedrick et al. The results implied that if N b of the wild population had not been increased with a captive-rearing component, it had at least not been greatly reduced Hedrick et al.
Importantly, this program attempted to equalize the contributions of captive breeders by breeding each male and female as evenly as possible and by releasing the captive offspring generated from different families as evenly as possible Hedrick and Hedgecock ; Hedrick et al. More recent models and simulations have evaluated under what conditions supplementing a wild population over multiple generations could be either beneficial or detrimental, in terms of increasing or reducing N e , and related effects such as the rate of inbreeding and genetic drift Waples and Do ; Wang and Ryman ; Duchesne and Bernatchez Both Wang and Ryman and Duchesne and Bernatchez found that supplementation did not result in either substantial reductions in N e or increases in inbreeding under certain conditions.
For instance, in species where the variance in family size in the wild component was much larger than binomial variance as may be common in salmonids, e. In some circumstances, family size variance in the captive component might even be manipulated i. In addition, Duchesne and Bernatchez found that scenarios, where the rate of inbreeding with supplementation either remained stable or declined relative to a control of no supplementation , were generally those involving a larger than smaller captive N.
Nevertheless, the outcomes generated by these models often changed considerably depending on the demographic scenario employed or the underlying assumptions. Wang and Ryman found that supplementation could only increase N and N e if the increase in N was substantial and continuous, in which case, elevated rates of inbreeding and genetic drift could ensue.
The boost in N e over multiple generations was in part due to the increase in N which compensated for the effects of the enlarged variance in the genetic contributions between individuals in the whole population that arose from initial supplementation Wang and Ryman For the early stages of many captive breeding programs, however, such continual census size increase scenarios may be too optimistic Waples and Do ; Duchesne and Bernatchez Similarly, this model did not explore how declining populations could affect genetic diversity outcomes Wang and Ryman , which is another realistic situation in which decisions to initiate captive breeding programs are based.
Additionally, and particularly for smaller populations, initial supplementation in the first couple of generations could be detrimental to wild N e , given the negative demographic effect of sampling the wild population to generate a captive broodstock.
Just to potentially overcome such an initial setback, captive rearing and successful supplementation i. Finally, neither Wang and Ryman nor Duchesne and Bernatchez examined how reduced reproductive success in captive-reared individuals see below could affect genetic diversity outcomes in supplemented populations. Collectively, few generalizations can be currently made with respect to scenarios wherein both captive and wild components are involved in the i supplementation of a severely declining population or ii reintroduction of an extirpated one.
The outcomes of supplementation are difficult to predict based on current modeling, empirical tests of the predictions of these models are very limited, and outcomes may be specific to particular captive breeding programs Waples ; Duchesne and Bernatchez ; Naish et al. While empirical and theoretical studies both suggest that most salmonid captive breeding programs can maintain genetic diversity over several captive generations, considerable uncertainty remains with respect to the capability of many programs to maintain genetic diversity over the longer-term.
In part, this is because many of the procedures for maintaining captive N e Table 2 have only been implemented recently in most salmonid captive breeding programs, often after considerable time had passed since the programs were initiated.
Thus, the apparent low N e in some captive broodstocks might easily be avoided today through the use of such procedures. On the other hand, despite the plethora of procedures available to reduce the loss of genetic diversity in captivity through the maintenance of N e Table 2 , few have been systematically evaluated for long-term effectiveness.
In any event, the varying N b and N e estimates of different broodstocks in Table 4 suggest that the capacity of captive breeding programs to maintain genetic diversity in endangered salmonids will likely be case-specific.
Standing levels of neutral genetic diversity may not be a good correlate of quantitative genetic diversity Reed and Frankham , and the level of either can depend on many factors other than population size Willi et al. Recent studies suggest that, on average, quantitative genetic variation may not be lost within small populations as rapidly as neutral genetic diversity, but that levels of quantitative genetic variation can be highly variable among small populations Willi et al.
Similarly, putatively neutral microsatellite loci are located in parts of the genome that are not subject to natural selection. As a result, allelic characteristics at these loci they may have little or no relationship to survival and fitness, and they tell us nothing about genetic changes at quantitative traits that might be occurring in the captive environment Reed and Frankham ; McKay and Latta Consequently, even if levels of neutral genetic diversity can be sufficiently maintained in captivity, caution must be exercised in interpreting such data for risk assessment and the ability of captive breeding programs to maintain fitness, a subject treated in detail in the next section.
A lengthy, two-sided debate surrounds the use of harvest augmentation, supplementation and captive breeding programs to either increase salmonid harvest levels, give a demographic boost to declining, at-risk populations, or to recover endangered salmonid populations, respectively.
The debate is especially contentious with respect to whether or not hatchery- or captive-rearing, in general, can maintain attributes other than genetic diversity, namely fitness. A first predominant perspective argues that hatchery- or captive-rearing has negative impacts on the long-term persistence and fitness of wild salmonids. Under this view, hatchery- or captive-rearing leads to unavoidable genetic changes within hatchery-raised salmonids, chiefly through domestication selection Box 1.
Domestication selection results in a fitness reduction when hatchery- or captive-reared fish are then introduced into the wild and breed with wild fish. Such domestication selection can be reduced Table 2 , but it cannot be eliminated entirely Hindar et al. Theoretical work also suggests that domestication selection in the hatchery could have significant fitness consequences for a wild population in the case of supplementation programs, even if local, wild-born fish are used to generate hatchery fish each generation Lynch and O'Hely ; Ford ; Reisenbichler et al.
A corollary to this perspective is that hatchery programs, particularly hatchery augmentation and supplementation programs which have been the main focus of the debate, generally fail in their objective of maintaining fitness and of contributing to the natural productivity of wild salmonid populations Reisenbichler and Rubin ; Fleming and Petersson ; Reisenbichler et al.
A second and alternative perspective argues that hatchery- or captive-rearing of salmonids can maintain fitness within populations and play an important role in the supplementation of declining or recovery of endangered salmonid populations Brannon et al.
A corollary to this perspective is that the genetic risks associated with hatchery- or captive-rearing have been overstated. First, proponents of this view argue that, aside from theoretical studies on these genetic risks, the purported long-term effects of hatchery- or captive-rearing have little or no empirical basis Incerpi ; Rensel ; Brannon et al.
Second, in many cases, apparent effects on wild populations have not been differentiated from the effect of management decisions involving the misuse of the hatchery fish Campton ; Rensel ; Brannon et al. Most notably, in many instances, hatchery fish from nonlocal rather than local source populations Box 1 were stocked into large geographic regions without consideration that they may not have been adapted to those areas Brannon et al.
To objectively evaluate the comparative strength of these divergent perspectives in the context of salmonid captive breeding programs, the evidence for each one must firstly be carefully sifted and presented see Appendix 1 for details of the literature search. Particularly relevant are hatchery- or captive-rearing programs where i wild-born broodstock parents of hatchery fish are collected from a local river each generation, large numbers of their offspring are raised under captive conditions for a period of time, then released into the same local river, and where ii the lifetime fitness performance of the returning hatchery-born adults or their wild-born offspring versus wild adults can be directly evaluated in the wild.
Under these conditions, one can most legitimately address the likelihood that current captive breeding procedures involving hatcheries will conserve fitness within populations.
Table 5 summarizes 30 laboratory studies that evaluated whether hatchery-rearing resulted in genetic changes in hatchery relative to wild salmonids. This list of studies by no means should be viewed as exhaustive as undoubtedly, some other studies have been inadvertently overlooked.
The studies in Table 5 were not carried out in the wild, so they only address the potential for genetic changes incurred from captive breeding to have negative impacts on the persistence and adaptability of wild salmonids.
Additionally, many of these studies have been based on traditional supplementation practices see Table 1 ; footnotes of Table 5 and not necessarily on current captive breeding program procedures.
Laboratory studies that have provided evidence for genetic changes or that found no evidence of genetic changes in phenotypic traits between hatchery-reared and wild populations of salmonid fishes. Hatchery and wild populations were compared under common environmental conditions, unless otherwise noted. Of the 30 studies comparing hatchery and wild fish in Table 5 , only five compared hatchery fish derived from the same local population as the wild fish, and without confounding environmental and genetic differences or some degree of intentional artificial selection in the hatchery, which is not a typical element of captive breeding programs see Table 5 footnotes.
Of these five studies, three compared traits in hatchery and wild salmonids after one generation of captive breeding Dahl et al. Despite ample statistical power, only small, albeit significant, genetic differences were detected in two of three studies. Most significantly was a 2. In another study, trait differences that had been detected under hatchery conditions were not found when comparing hatchery and wild fish in the wild Dahl et al.
The other two studies compared traits in hatchery and wild salmonids after four to six generations of captive rearing Johnsson et al. Genetic differences were detected in three of four trait comparisons for juvenile growth rate and antipredator response.
Finally, as expected, clear genetic differences between hatchery and wild fish were also detected when hatchery fish were nonlocal or had experienced intentional selection Table 5. Table 6 summarizes 20 studies that have directly evaluated the fitness performance of hatchery and wild salmonid fishes in the wild, with one additional study comparing fitness between fish with different degrees of captive-rearing Carofinno et al. Again, this list of studies by no means should be viewed as exhaustive as undoubtedly, some other studies have been inadvertently overlooked.
Likewise, many of these studies have been based on common supplementation practices rather than current captive breeding procedures see Table 1 ; footnotes of Table 6. Field studies within natural environments that have evaluated the fitness performance of hatchery and wild salmonid fishes.
G , number of hatchery generations as in Table 5. Of these 20 studies comparing hatchery and wild fish in Table 6 , nine compared hatchery fish derived from the same local population as the wild fish. Of these nine studies, three detected survival differences between hatchery and wild fish Reisenbichler and McIntyre ; Unwin ; Araki et al. However, the lifetime performance of second generation hatchery and wild fish in Reisenbichler and McIntyre differed in only two of four stream comparisons where hatchery fish survival was lower , and the Unwin study was confounded by rearing hatchery fish for 8—12 months in captivity before release into the wild from Brannon et al.
In addition, all studies finding no survival differences must be considered with caution because i hatchery fish were larger than wild fish when released into the wild Rhodes and Quinn ; Bohlin et al. On the other hand, unanimously, hatchery fish had inferior fitness when they were nonlocal or had been under intentional selection Table 6.
To date, Araki et al. Based on steelhead trout Oncorhynchus mykiss , the program used wild-born broodstock parents of hatchery fish that were collected each generation and from which more numbers of offspring were raised in a hatchery for a period of time before being released into the same local river as 1-year old, juvenile smolts.
For a single generation, Araki et al. Consistent with what would be expected if captive breeding programs use local broodstock and minimize the time that individuals are kept in captivity, the authors found i no differences in reproductive success between local hatchery fish and wild fish, ii no differences in reproductive success between local hatchery-wild crosses and wild-wild crosses, but iii lower reproductive success in nonlocal hatchery fish relative to wild fish.
The results were therefore encouraging because they suggested that short-term captive-rearing programs of one generation might be capable of generating fish with quasi-equal fitness to that of wild fish. Still, Araki et al. The study also could not rule out the possibility that initial differences in rearing environments between the local hatchery and wild fish affected the former's fitness performance in the wild Araki et al.
Araki et al. The two chief results of the study were as follows. Second, relative to pure wild fish with no history of captive-rearing, and born and returning from sea in the same years a replication of Araki et al. The results of Araki et al. However, confidence intervals around point estimates of reproductive success were large in both Araki et al. This might account for the conflicting conclusions regarding whether one generation of captive-rearing leads to or does not lead to a loss of fitness in the wild.
If anadromous, hatchery-reared fish generate a greater proportion of nonanadromous offspring than anadromous wild fish, or vice-versa, then the relative fitness of hatchery-reared anadromous fish relative to wild fish in these studies would have been underestimated or overestimated, respectively.
Second, steelhead are often raised in hatcheries for a whole year to achieve a body size conducive to smoltifying which will increase survival chances in the wild Araki et al. We may expect differences in the survival rates of offspring of wild-born parents vs. Therefore, we ran a second analysis as above but excluding all offspring with either one or both wild-born parents i. Three of the species in our dataset typically give birth to only one offspring and would be unlikely to drive any differences between the extended dataset relative to our main analysis Supplementary Fig.
Results of the extended dataset model were used to qualitatively check that our random selection of independent litters did not unintentionally bias the dataset, by comparing parameter estimates between the two approaches. Qualitative inferences were the same as in our main analysis Supplementary Table 2a , Fig.
We selected one of the independent litter sampling subsets that was representative of the five sets of results to further investigate trends across species Supplementary Fig. We fitted separate random-slope models for each predictor to estimate species-level effects, where the main effect is interpreted as the mean across all species, and the random component quantifies the amount of variation in that slope among species.
For example, while the main effect may suggest a negative relationship between dam age at breeding and offspring survival over all species, the effect of dam age may vary between species. Random-slope models were fitted from the global model, as model averaging cannot provide random slope estimates. No parameters were dropped from the top model set with model averaging Supplementary Table 3 , so we do not expect the random slopes models to differ substantially if estimation after model selection was possible.
We also investigated phylogenetic signal by estimating lambda using the random slope estimates for each of the parameters of interest aside from sire age for which a random slope model did not converge. Further information on research design is available in the Nature Research Reporting Summary linked to this article. Data underlying this analysis is available as Supplementary Data 1. All figures can be reproduced using this data and the available code. Custom R code underlying this study is available as Supplementary Code 1.
All figures can be recreated using this code. McGowan, P. IUCN guidelines for determining when and how ex situ management should be used in species conservation. Article Google Scholar. Conde, D. An emerging role of zoos to conserve biodiversity. Science , — Lacy, R. Columbia Univ. Press, Frankham, R.
Genetic adaptation to captivity in species conservation programs. Jule, K. The effects of captive experience on reintroduction survival in carnivores: a review and analysis. Araki, H. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Evolution of Peromyscus leucopus mice in response to a captive environment. PLOS One 8 , e Milot, E. Reduced fitness of Atlantic salmon released in the wild after one generation of captive breeding.
Where are we in conservation genetics and where do we need to go? Williams, S. Minimizing genetic adaptation in captive breeding programs: a review.
Christie, M. A single generation of domestication heritably alters the expression of hundreds of genes. Farquharson, K. A meta-analysis of birth-origin effects on reproduction in diverse captive environments. Genetic adaptation to captivity can occur in a single generation. Natl Acad. USA , — Matos, M. Maternal effects can inflate rate of adaptation to captivity. USA , e Grueber, C. Inbreeding depression accumulation across life-history stages of the endangered takahe. Harrisson, K. Lifetime fitness costs of inbreeding and being inbred in a critically endangered bird.
Boakes, E. An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity 98 , — Kennedy, E. Severe inbreeding depression and no evidence of purging in an extremely inbred wild species - the Chatham Island black robin. Evolution 68 , — Introduction to Conservation Genetics 2nd edn, Cambridge Univ. Hedrick, P. Inbreeding depression in conservation biology.
Fa, J. Zoos have yet to unveil their full conservation potential. Martin, T. Mammal and bird species held in zoos are less endemic and less threatened than their close relatives not held in zoos. Fisher, D. The comparative method in conservation biology. Trends Ecol. Data gaps and opportunities for comparative and conservation biology. Species Charlesworth, D. The genetics of inbreeding depression. Packer, C. Reproductive cessation in female mammals. Nature , — Pedigree analysis reveals a generational decline in reproductive success of captive Tasmanian devil Sarcophilus harrisii : implications for captive management of threatened species.
Hammerly, S. A pedigree gone bad: increased offspring survival after using DNA-based relatedness to minimize inbreeding in a captive population. Woodworth, L. Rapid genetic deterioration in captive populations: causes and conservation implications. Fraser, D. Population correlates of rapid captive-induced maladaptation in a wild fish. Modeling problems in conservation genetics using captive Drosophila populations: rapid genetic adaptation to captivity.
Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Mason, G. Plastic animals in cages: behavioural flexibility and responses to captivity. Courtney Jones, S. What role does heritability play in transgenerational phenotypic responses to captivity? Implications for managing captive populations. Kokko, H. Oxford Univ. Impacts of early viability selection on management of inbreeding and genetic diversity in conservation.
Wells, J. Commentary: paternal and maternal influences on offspring phenotype: the same, only different. Int J. Calkins, E. Factors influencing reproductive success and litter size in captive island foxes. Species-survival plans coordinate with zoos around the world to bring species together for breeding that ensures genetic diversity. The audio, illustrations, photos, and videos are credited beneath the media asset, except for promotional images, which generally link to another page that contains the media credit.
The Rights Holder for media is the person or group credited. For information on user permissions, please read our Terms of Service. If you have questions about how to cite anything on our website in your project or classroom presentation, please contact your teacher. They will best know the preferred format.
When you reach out to them, you will need the page title, URL, and the date you accessed the resource. If a media asset is downloadable, a download button appears in the corner of the media viewer. If no button appears, you cannot download or save the media. Text on this page is printable and can be used according to our Terms of Service. Any interactives on this page can only be played while you are visiting our website. You cannot download interactives. Students discuss endangered and threatened species and learn about captive-breeding programs.
Students complete a case study for one species in a captive-breeding program and evaluate the effectiveness of the program. Ever since humans began living in agricultural communities, farmers have sought to breed crops that produce higher yields, are more resilient, and taste better. Williams, P. In Hymenoptera and biodiversity. Wilson, E. In Earth ' Changing geographic perspectives J. De, Blij Harm, ed. Download references. You can also search for this author in PubMed Google Scholar.
Reprints and Permissions. Rahbek, C. Captive breeding—a useful tool in the preservation of biodiversity?. Biodivers Conserv 2, — Download citation. Received : 06 September Revised : 08 February Accepted : 08 February Issue Date : August Anyone you share the following link with will be able to read this content:. Sorry, a shareable link is not currently available for this article. Provided by the Springer Nature SharedIt content-sharing initiative. Skip to main content. Search SpringerLink Search.
References Ackery, P. Google Scholar Ashton, P. Google Scholar Benirschke, K. Google Scholar Bibby, C. Google Scholar Bloch, H. Google Scholar Brush, S. Google Scholar Burke, R. Google Scholar Cade, T. Google Scholar Cohn, J. Google Scholar Collar, N. Google Scholar Collins, N. Google Scholar Corbet, G. Google Scholar DeBlieu, J. Google Scholar Diamond, J. Google Scholar Dodd, C. Google Scholar Erwin, T. Google Scholar Faith, D.
Google Scholar Fitter, R. Google Scholar Franklin, J. Google Scholar Frost, D. Google Scholar Gilpin, M. Google Scholar Griffith, B. Google Scholar Halliday, T. Google Scholar Hammond, P. Google Scholar Hearne, J. Google Scholar Henderson, D. Google Scholar Hodkinson, I. Google Scholar Howard, R.
Google Scholar Humphries, C. Google Scholar Imboden, C.
0コメント